Male Mating Strategies within a Shifting
Competitive Landscape: Performance and
Phenotypic Correlates of Mate Guarding
Success
by
Megan McPhee
A thesis submitted in conformity with the requirements
for the degree of Master of Science
Ecology and Evolutionary Biology
© Copyright by Megan McPhee 2015
ii
MALE MATING STRATEGIES WITHIN A SHIFTING COMPETITIVE
LANDSCAPE: PERFORMANCE AND PHENOTYPIC CORRELATES OF
MATE GUARDING SUCCESS
Master of Science
2015
Megan McPhee
Ecology and Evolutionary Biology
University of Toronto Scarborough
Mate-guarding males who limit access of rivals to females may be likewise preferred by
females, or their mating advantage may lie only in excluding opponents. In the jumping spider
Phidippus clarus, males guard immature females, mating once females synchronously moult. To
investigate factors contributing to mate guarding success in the field, we compared the
morphology, competitive and courtship success of guarding and non-guarding males collected
throughout their season. Guarders were larger than roamers only during the time when females
moult, and also demonstrated both higher fighting and courtship success independent of size-
related advantages. Thus, high levels of male-male competition during female moult implicates
male-male contests in determining mate-guarding success. Given the proposed significance of
mate guarding to male fitness, heritability of traits related to competitive ability and guarding
may explain the observed correspondence between sexual selection via female choice and male-
male competition.
iii
ACKNOWLEDGMENTS I would like to express extreme gratitude to my co-supervisors, Prof. Maydianne C.B.
Andrade and Prof. Andrew C. Mason, for helping me to follow a dream since childhood and a
passion since adulthood, while providing both the support and freedom in which to do so. Their
direction, expertise and passion for the scientific method were indeed invaluable to me.
I would also like to thank my committee members Prof. Darryl T. Gwynne and Dr.
Kenneth Welch for their input and direction, as well as my funding source NSERC for the
CGSM Scholarship they bestowed upon me. I greatly appreciation the advice and support of all
members of the Andrade and Mason lab, as well as to the students, faculty and staff at UTSC. A
special thanks is owed to Terrence Chang for his ceaseless enthusiasm for our topics of research
and to my parents who were the first to support my scientific endeavors, both intellectually and
financially.
iv
TABLE OF CONTENTS
ACKNOWLEDGMENTS ............................................................................................................................... v
List of Figures ........................................................................................................................................... vi
List of Tables ............................................................................................................................................ vi
Abstract ......................................................................................................................................................... ii
Chapter One: General Introduction ............................................................................................................... 1
Chapter two: Male mating strategies in response to a shifting competitive landscape: A field study .......... 8
Introduction ............................................................................................................................................... 8
Methods .................................................................................................................................................. 14
Research Sites ..................................................................................................................................... 14
Surveying and Collection .................................................................................................................... 14
Morphological Measurements ............................................................................................................. 17
Statistical Analyses ............................................................................................................................. 17
Results ..................................................................................................................................................... 20
Population Structure ............................................................................................................................ 20
Male Size and Guarding Success across the Reproductive Season .................................................... 24
Discussion ............................................................................................................................................... 29
Chapter Three: Male courtship and fighting performance as a function of guarding status ....................... 38
Introduction ............................................................................................................................................. 38
Methods .................................................................................................................................................. 43
P. clarus reproductive behaviour ........................................................................................................ 43
Collection and Housing ....................................................................................................................... 44
Signal Recording ................................................................................................................................. 45
Courtship Trials .................................................................................................................................. 45
Competition Trials .............................................................................................................................. 46
Signal Analysis ................................................................................................................................... 48
Statistical Analyses ............................................................................................................................. 49
Courtship Outcome and Signal Characteristics Related to Status ....................................................... 50
Contest Outcome and Male Characteristics Related to Status ............................................................ 50
Results ..................................................................................................................................................... 51
Courtship Trials and Signal Characteristics Related to Male Status ................................................... 51
Contest Outcome and Signal Characteristics Related to Male Status ................................................. 56
Focal-Male Model: .............................................................................................................................. 60
Discussion ............................................................................................................................................... 63
v
Guarding Male Courtship Success ...................................................................................................... 63
Guarding Male Contest Success ......................................................................................................... 65
Chapter 4: General Conclusion ................................................................................................................... 70
References .................................................................................................................................................. 72
vi
List of Figures Fig. 1. 1. Male Phidippus clarus ................................................................................................................... 9
Fig. 1. 2. Female Phidippus clarus ............................................................................................................... 9
Fig. 2. 1. Field Site Map ............................................................................................................................. 23
Fig. 2. 2. Number and status of males and females collected across the season ......................................... 27
Fig. 2. 3. Proportion of collected males found guarding or roaming across the season .............................. 28
Fig. 2. 4. Male status as a logistic function of body size ............................................................................ 31
Fig. 2. 5. Average body size of guarders and roamers across the season ................................................... 33
Fig. 3. 1. Courtship success as a logistic function of vibration rate for guarders and roamers ................... 59
Fig. 3. 2. Relationship between male body size and courtship vibration rate ............................................. 60
Fig. 3. 3. Contest success for guarders as a logistic function of vibration rate ........................................... 64
Fig. 3. 4. Relationship between body size and aggressive vibration rate .................................................... 67
List of Tables Table 2. 1 PC1 Factor Loadings.................................................................................................................. 24
Table 2. 2. Analysis of predictors of field status ........................................................................................ 30
Table 3. 1. Analysis of courtship outcomes ................................................................................................ 58
Table 3. 2. Both-male analysis of contest outcomes: Relative ................................................................... 62
Table 3. 3. Both-male analysis of contest outcomes: Relative ................................................................... 63
Table 3. 4. Focal-male analysis of contest outcomes: Absolute ................................................................. 66
Table 3. 5. Focal-male analysis of contest outcomes: Relative .................................................................. 66
1
CHAPTER ONE: GENERAL INTRODUCTION
As first acknowledged by Darwin (1859, 1871), sexual selection can shape the evolution
of male and female traits through the effects of two mechanisms; male-male competition and
female mate choice. Empirical and theoretical research on sexual selection since then has tended
to study these processes independently, emphasizing the role of one or the other in the evolution
of traits (Hunt, Breuker, Sadowski, & Moore, 2009). However, male-male competition and
female mate choice rarely occur in isolation (Wong & Candolin, 2005), and their interaction will
influence the outcome of these processes in nature, and thus their evolutionary consequences.
The net effect of competition and choice will partly depend on whether these processes occur
simultaneously or sequentially, and whether the traits that confer success in each process are
convergent or divergent.
In many species, males attempt to limit access of rival males to females (competition) by
guarding. In these cases, competition and choice may occur sequentially, and this temporal
separation between fighting and mating attempts can provide an ideal opportunity to study the
roles of male-male competition and mate-choice on the evolution of mating strategies. Although
mate guarding is common across the animal kingdom (Andersson, 1982) and has been the focus
of various theoretical and empirical studies (e.g. Grafen & Ridley, 1983; Härdling, Kokko, &
Elwood, 2004; Komdeur, 2001; Mathews, 2003), the relative importance of the interaction
between choice and competition in the evolution of guarding has remained a topic of debate
(Estrada, Yildizhan, Schulz, & Gilbert, 2010).
In this thesis, I seek to understand the ecological and physiological factors involved in sexual
selection and how these affect the evolution of guarding strategies of males. To do this, I use a
2
combination of field and laboratory studies to test hypotheses about mate-guarding in the
jumping spider Phidippus clarus (Araneae: Salticidae). P. clarus shows pre-copulatory mate
guarding during a temporally restricted reproductive season (June, July and August) with
relatively synchronous female maturation (Hoefler & Jakob, 2006). This species is found in old
field habitats across temperate North America where it makes use of the upper portions of woody
or herbaceous plants for retreats and nests (Hill, 2014). In June, roaming adult males seek out
and cohabit with immature (final instar) females which nest within silken retreats constructed in
rolled leaves (Hoefler & Jakob, 2006). During their final instar, females build a thick silk
envelope inside the retreat, and apparently do not leave until they moult (pers obs).
Protandry results in a male-biased operational sex ratio during this period of the mating
season, when males compete for opportunities to guard. Males prefer larger females and large
males have an advantage in competition, so the outcome is that males and females pair
assortatively by size (Hoefler 2007). Following a synchronous female moult period (~3 days,
Hoefler & Jakob, 2006) the operational sex ratio shifts to even, and guarding males attempt to
mate with newly-matured females. Guarding males are found on or near the nest, in close
proximity to females. Near the moulting period, males move inside the silk retreat and court
females. After moulting and mating, adult females spend time foraging outside of their nest
during the day (Hoefler & Jakob, 2006; pers obs). It has been suggested that during this period,
guarding no longer occurs, and male mating success will depend on encountering and persuading
previously-mated females to copulate (female receptivity decreases after guarding and mating,
Elias et al 2014; Sivalinghem et al., 2010, Elias et al 2011). Laboratory studies have shown
mature females are capable of mating multiply, however it is unclear how often this occurs in
nature. Although there have been no sperm competition studies in jumping spiders (Schneider &
3
Andrade 2011), first male sperm precedence is the most likely outcome of polyandry since the
morphology of their genitalia is such that the first sperm to enter would be the first to exit at
fertiliization (Elgar 1998). Moreover, first-male sperm precedence is expected to impose strong
selection for protandry and pre-copulatory mate guarding, as seen in P. clarus.
P. clarus males produce variable multi-modal signals (visual and vibrational) that are
important in competition and courtship. As is characteristic of all jumping spiders, P. clarus
possesses a remarkable visual acuity that is important in both prey capture (Li, Jackson, & Lim,
2003) and reproduction (Clark & Morjan, 2001) and males have striking, sexually dimorphic
visual ornaments which are utilized in complex courtship displays and during inter-male
competition (Fig. 1.1, 1.2; Crane, 1949; Jackson, 1982). In P. clarus, in addition to the bright red
colouration of the abdomen, males have enlarged, black forelegs ornamented with black tufts in
contrast to the more cryptic brown and orange females (Figure 1). The forelegs are outstretched
during ritualized competition between males, and are an indicator of size, but they may also be
used directly for grappling when contests escalate to physical combat (Elias et al., 2008). In
addition to visual displays, like some other recently studied salticids, P. clarus males produce
several different types of vibratory signals in both inter- and intra-sexual contexts. Thus, when
guarding males are challenged by rivals, the competitors engage in aggressive, stereotyped visual
and vibratory signalling (Elias et al., 2008; Kasumovic, Elias, Sivalinghem, Mason, & Andrade,
2010). The vibratory signals directed at competitors compared are distinct from those directed at
adult females during courtship and signal features are correlated with success in mating and in
inter-male competition (Elias, Kasumovic, Punzalan, Andrade, & Mason, 2008; Elias,
Sivalinghem, Mason, Andrade, & Kasumovic, 2010; Sivalinghem, Kasumovic, Mason, Andrade,
& Elias, 2010). Guarding males perform intricate courtship displays involving both visual and
4
vibratory signals prior to copulation (Sivalinghem et al., 2010). In addition, recent work shows
that males also direct vibratory signals to immature females during guarding, and these may
affect female receptivity later (Elias, Sivalinghem, Mason, Andrade, & Kasumovic, 2014).
Fig. 1. 1. Male Phidippus clarus. The male is marked (blue paint on abdomen) for individual
identification (see Chapter 3). Image courtesy of Ken Jones.
Fig. 1. 2. Female Phidippus clarus. Image courtesy of Ken Jones.
5
The seasonal shifts in the importance of male-male competition and female choice that occur
across the breeding season make P. clarus an ideal system to investigate how mate-guarding may
translate to mating success for males within a variable environment. Here I assess phenotypic
correlates of performance and fitness in males as a function of their status in the field (successful
guarder or not), and examine how this is reflected in the characteristics of signals and signalling
behaviour, particularly as the competitive environment and sex ratio shift during the mating
season.
In Chapter two, I report the results of a field survey on a natural population of P. clarus
across the mating season. I used collection data to document the phenology and occurrence of
mate guarding, and compare the phenotype of successful guarders to males that are not guarding
(roamers). Larger males are more likely to win fights (Elias et al., 2008; Hoefler, 2007;
Kasumovic, Elias, Punzalan, Mason, & Andrade, 2009; Kasumovic, Mason, Andrade, & Elias,
2011), but the relative size of guarders and roamers may change over time because (1) larger
males commence guarding when females are most reproductively valuable (i.e., near the
female’s moult date, the takeover hypothesis) or (2) successive fights act as a progressively more
restrictive filter on male traits as the female moult date approaches and male motivation to fight
increases (the fight effort hypothesis). I tested a common prediction of both of these
hypotheses—that the most extreme difference in the phenotypic traits of guarders and roamers
would occur near the time of the female’s moult date, when females are most reproductively
valuable to males. While previous work documented the competitive advantage of larger males
(Elias et al., 2008; Hoefler, 2007; Kasumovic, Elias, Punzalan, Mason, & Andrade, 2009;
Kasumovic, Mason, Andrade, & Elias, 2011), it is not clear whether this translates into guarders
being larger than roamers in nature. This is an important point because it has also been shown
6
that competition in P. clarus is mediated by advantages of residents (i.e., males that are already
guarding) over intruders (i.e., roamers) and by a ‘winner’ effect whereby males that have won
previous competitions are more likely to win again compared to males that had previously lost
(Kasumovic et al., 2009, 2010, 2011). Thus it is unclear how to extrapolate from staged
laboratory contexts to field dynamics.
In Chapter Three, I tested whether males differed in their competitive ability or courtship
success as a function of their status as ‘guarders’ or ‘roamers’. In this chapter, I staged
competitive contests between males collected as roamers and guarders in the field. I tested
whether factors other than the relative size of males in these roles (quantified in Chapter Two)
determined guarding status and fight performance (Elias et al., 2008; Hoefler, 2007; Kasumovic
et al., 2009, 2011). I was particularly interested in the effect of variation in behavioural and
aggressive signalling traits of guarders compared to roamers. In this chapter, I also tested
whether courtship success was predicted by the same traits as competitive success. I paired
individual males with unmated females and compared courtship performance and intersexual
signals of guarders and roamers. While previous laboratory work has identified male traits
important in male-male competition and female mate choice respectively, empirical evidence on
how these traits are related to mate-guarding success in nature is lacking.
By assessing seasonal variation in male traits involved in successful mate-guarding and
identifying how these and other traits are related to competitive success and female preferences, I
aim to link the current body of lab-based research in P. clarus to natural phenology and
population dynamics. Features of the mating system and natural history of this species suggest it
could be an ideal model for examining evolutionary consequences of interactions between the
7
multiple mechanisms of sexual selection, particularly as they are linked to variation in the
environment.
8
CHAPTER TWO: MALE MATING STRATEGIES IN RESPONSE TO A
SHIFTING COMPETITIVE LANDSCAPE: A FIELD STUDY
Introduction
Mate-guarding is expected to evolve as a male mating strategy when the paternity
benefits outweigh the time and energy costs associated with guarding (Bel-Venner & Venner,
2006; Komdeur, 2001). Costs include forgoing other possible mating opportunities (Birkhead &
Møller, 1992; G. A. Parker, 1974), restricted feeding during guarding (Alberts, Altmann, &
Wilson, 1996; Girard-Buttoz et al., 2014; Komdeur, 2001; Prenter, Elwood, & Taylor, 2006;
Sparkes, Keogh, & Pary, 1996), energetic or injury costs of agonistic interactions with rival
males (Galimberti, Sanvito, Braschi, & Boitani, 2007; Plaistow, Bollache, & Cezilly, 2003),
higher predation risks (Cooper, 1999; Fahey & Elgar, 1997), and any additional energy
requirements of maintaining close proximity to females (Adams & Greenwood, 1983; Wilcox,
1984) including mate-guarding courtship (Elias et al., 2014). Despite the costs, mate guarding
has evolved in many different taxa where it may manifest as (pre-copulatory) guarding of
subadult or adult potential mates or as post-copulatory guarding of mates; with both forms of
guarding being important in terms of sexual selection on males (Danielsson, 2001; Ward, 1988).
Pre-copulatory guarding entails the additional risk that a guarding male may invest significant
energy and time, and yet end up losing out completely on any reproductive benefits if evicted by
a rival (Bel-Venner & Venner, 2006) or rejected by the female he is guarding (Chuang-Dobbs,
Webster, & Holmes, 2001; Elias et al., 2014; Huffard, Caldwell, & Boneka, 2010; G. A. Parker,
1974; Watson, 1990).
The type of mate-guarding to occur depends primarily on species-specific life history
traits and population dynamics related to reproduction. Post-copulatory guarding of females
9
(after insemination is secured), is predicted in species with longer windows of receptivity or
fertility (Harts & Kokko, 2013), and/or last-male sperm precedence (Holdsworth & Morse,
2000). On the other hand, pre-copulatory guarding typically occurs when acquiring the first
mating with a female has crucial fitness benefits for a male due to restricted periods of
receptivity and/or first male sperm precedence. This form of mate guarding is more likely to
evolve when males can predict female receptivity and when monopolization of females prior to
this time is feasible (Austad, 1982; Clutton-Brock, 1989; G. A. Parker, 1974; Yamamura, 1987).
Despite the additional risk inherent in pre-copulatory mate-guarding, this alternate guarding
tactic has been documented in a wide range of taxa, including mammals (Schubert, Schradin,
Rödel, Pillay, & Ribble, 2009), fish (Morbey, 2002), frogs (Yamamura, 1987), crustaceans
(Bauer & Abdalla, 2001; Cornet, Luquet, & Bollache, 2012; Härdling et al., 2004; Jormalainen,
1998; Plaistow et al., 2003; Wada, Tanaka, & Goshima, 1999), insects (Arakaki et al., 2004;
Estrada et al., 2010), and spiders (Bel-Venner & Venner, 2006; Bridge, Elwood, & Dick, 2000;
Holdsworth & Morse, 2000; Robert R. Jackson, 1986).
Here, I focus on pre-copulatory mate guarding, which is particularly interesting when
males guard immature females. In this case, the maximum possible reproductive gains of
guarding remain constant while the risk of losing those benefits decreases continuously as
females approach sexual maturity, since the time in which take-overs can occur and the energetic
expenditure needed to survive until female maturation decrease with time. Thus it is predicted
that mate guarding should become increasingly profitable as the window of female
receptivity/maturity approaches (Elwood & Dick, 1990; Grafen & Ridley, 1983; G. A. Parker,
1974; Watson, 1990). Results from previous arthropod studies have been consistent with this
prediction, demonstrating that guarding often occurs close to the onset of female sexual
10
receptivity (Cornet et al., 2012; Mathews, 2003), when the time left prior to maturation and
likelihood of a take-over before mating is at its lowest.
The time during a female’s cycle when guarding would be adaptive for a given male will
depend, however, on each male’s competitive ability as this will impact the likelihood of a take-
over, and thus the risks associated with mate guarding (Grafen & Ridley, 1983; Härdling et al.,
2004; G. A. Parker, 1974). Male phenotype (including size) may also affect the likelihood that
the female will accept the male once she is receptive and thus the likelihood of a payoff from
guarding effort (Iyengar & Starks, 2008). Therefore for a searching male that encounters an
immature female, the decision of whether or not to guard will depend on the female’s status
(alone or guarded), developmental stage (likely time to maturity), the likelihood that the female
will accept the male as a mate, and the likelihood that the male could defend against rivals until
she matures within the current competitive environment (Bel-Venner & Venner, 2006; G. A.
Parker, 1974). Male competitive ability, and thus the likelihood of successful guarding, will
often vary with male phenotype and resource holding potential (the capacity of an animal to
defend a resource through an escalated fight against an opponent, RHP; Alonso-Alvarez,
Doutrelant, & Sorci, 2004; Caldwell & Dingle, 1979; Hack, Thompson, & Fernandes, 1997;
Parker, 1974; Simmons, 1986). Among the traits related to competitive ability, male size is
commonly favoured by precopulatory sexual selection (mediated by both competition and
choice; Andersson, 1994; Bonduriansky & Rowe, 2003; Dodson & Schwaab, 2001). A size-
advantage may be especially likely in systems where males compete directly for access to
immature females (Grafen & Ridley, 1983), and several studies have shown that larger males are
at an advantage in obtaining guarding positions (Berrill & Arsenault, 1984; Donaldson &
Adams, 1989; Elgar, De Crespigny, & Ramamurthy, 2003; Johnsen, Lifjeld, & Krokene, 2003;
11
Poirier, Whittingham, & Dunn, 2004) and more specifically in both making takeovers and
resisting such attempts by rival males (Bel-Venner & Venner, 2006; Ward, 1983).
Decisions about when to guard and how much energy to invest in guarding have been the
subject of considerable theoretical work. The takeover hypothesis, first modeled by Grafen &
Ridley (1983) frames mate-guarding as a male decision-making problem, and predicts that when
1) males compete directly for females, 2) guarding is costly to males, and 3) takeovers are
frequent, a size-advantage will allow larger males to start guarding later, when females are closer
to their moult dates. . This and related models were developed with reference to the mate-
guarding crustacean Gammarus pulex where empirical work shows males prefer females closest
to moult (Birkhead & Clarkson, 1980). Despite strong evidence for large male advantages in
male-male competition and size-assortative pairing close to female moult (Cornet et al., 2012;
Jormalainen, 1998; Plaistow et al., 2003), other studies show thatG. pulex males tend to start
guarding females earlier than smaller males (Cornet et al., 2012; Elwood & Dick, 1990; Ward,
1983). The failure to support ‘takeover’ predictions in this species has been attributed to the
relative rarity of takeovers and the low cost of guarding for large males (Elwood & Dick, 1990).
However, empirical evidence in support of the ‘takeover’ hypothesis has been found in the orb-
weaving spider Zygiella x-notata, where experimental studies have shown that 1) direct male-
male competition drives positive selection on guarding male size and, 2) that larger males opt to
guard females closer to their moult date than smaller males (Bel-Venner & Venner, 2006).
However, temporal changes in male phenotypic traits related to mate guarding success
may also be influenced by the outcome of continuous intrasexual competition. The ‘fight effort’
hypothesis proposes that increased male fighting effort for guarding positions is expected as
females approach moult and their reproductive value increases. When all males are highly
12
motivated to fight for high-value females, larger males will usually win. Consistent with this
idea, theory predicts increasingly intense and frequent male-male contests as the female’s moult
approaches (Elwood & Dick, 1990; Härdling et al., 2004). These two hypotheses operate via
different mechanisms (male choice versus direct intrasexual competition) yet both may operate
simultaneously. Despite empirical and theoretical evidence for both the takeover hypothesis and
the fight effort hypothesis, tests of the predicted temporal patterns in male traits influencing
guarding success in nature remain rare.
Here I studied seasonal variation in the phenotype of successful mate-guarding males in a
field population of Phidippus clarus. P. clarus is protrandrous and shows pre-copulatory mate
guarding during a 3-month reproductive season with relatively synchronous female maturation
(Hoefler & Jakob, 2006, Chapter one). These features make P. clarus an ideal taxon to
investigate the temporal predictions of the takeover and fight effort hypotheses. In June, roaming
adult males seek out and cohabit with subadult (final instar) females which nest within silken
retreats constructed in rolled leaves (Hoefler & Jakob, 2006). During cohabitation, males attempt
to repel potential rivals. Lab-based contests suggest males will have higher success if they are
relatively large and heavy (Elias, Sivalinghem, et al., 2010; Hoefler, 2007), and if they locate
females before rivals due to resident and winner effects (Kasumovic et al., 2009, 2011). The
advantage of larger males in contests in combination with a demonstrated male preference for
larger, more fecund females has been implicated in size-assortative cohabitation pairings
observed near female moult-dates in the field (Hoefler, 2007).
Independent of seasonal variation in the benefits of guarding, the intensity of male-male
competition may also change over the course of the breeding season since the sex ratio shifts
from male-biased to even after females moult (Elias, Andrade, & Kasumovic, 2011; Hoefler,
13
2007, 2008; Kasumovic et al., 2010). Since adult females spend time foraging during the day
after moulting (Hoefler & Jakob, 2006; per obs), it has been suggested that male mating success
following the females’ moult may be most strongly dependent on female choice-driven courtship
success (Elias, Sivalinghem, et al., 2010; Sivalinghem et al., 2010). A second goal of this study
was to assess temporal patterns in female occupation of retreats through the season, particularly
with respect to the pre-moult, compared to post-moult, period.
To date, no study has assessed whether male body size underlies cohabitation success in
nature in P. clarus. Furthermore, it is unknown whether there are temporal patterns in the relative
size of guarding males across the season matching those which would be predicted by the
takeover and fight effort hypotheses in this species. Consequently, the objective of this study was
to determine phenotypic correlates of male mate guarding success in P. clarus to test common
predictions of these two hypotheses. I performed a field survey and collection experiment on a
natural population of P. clarus, recording the occurrences of guarding and collecting both
guarding and roaming males throughout the breeding season and assessing size differences
between the two groups. I predicted that males found guarding would be on average larger than
males found roaming, and that this disparity would be greatest immediately preceding and during
the period of synchronous female moult, when the expected male fitness value of cohabitation is
highest. This study would be one of the few tests of predictions made by both the takeover and
fight effort hypotheses in nature, and provide insight into the selective processes involved in the
evolution of male mating tactics within the context of shifting population dynamics.
14
Methods
Research Sites
All field work was conducted throughout the summer months of 2014 in four old fields
(Fig. 2.1) dominated by a variety of grasses and common milkweed (Asclepias syriaca) within
the University of Toronto’s Koeffler Scientific Reserve in Joker’s Hill, King City, ON, Canada
(44° 03’ N, 79° 29’ W). Fields ranged in size from 16 x 50 to 48 x 43 m (Fig. 2.1) and were 10 -
150 m apart. Males were collected from fields 2, 3, and 4 only (Fig. 2.1). Field 1 was susceptible
to flooding and not suitable for regular collection of males, so this field was used exclusively to
collect females for behavioural experiments (Chapter two). The distance between the fields and
(in the case of field 4) borders of dispersion-limiting habitat (forest and a stream) is likely to
have reduced movement of males from one field to the other. However, it is unlikely that overall
population size was significantly affected through my continuous sampling of males within each
field as every collection field was contiguous with other old fields containing similar vegetation,
in which P. clarus have been observed (MCBA pers comm) which could thus serve as a source
for additional males (and see Results).
Surveying and Collection
Artificial retreat tubes (retreats) were constructed using 1.9 cm diameter rubber tubes cut
to be 3.8 cm long and attached at one end of 1.5 m bamboo poles (Backyard X-Scapes).
Artificial retreats were used in order to be able to consistently locate cohabiting pairs since
previous research has demonstrated that P. clarus readily creates retreats within tubing (Hoefler
& Jakob, 2006). The translucent tubing used in this study was covered in opaque duct tape to
make retreats more attractive to retreating females. Before the start of the growing season (April
27, 2015), poles were inserted into the ground at each field in approximately 3 x 3 m grids so
15
that retreats were ~1 m above ground. All retreats were marked with labelled flagging tape for
identification.
Of the four field sites, a field was designated for the collection of virgin females early in
the season for future use in mating and competition trials (field 1=66 retreats, Chapter two),
whereas the remaining three were designated for collection of guarding and roaming adult males
(field 2, n =100 retreats; field 3 n =80; field 4 n=80).
Retreats were surveyed on a bi-weekly basis for P. clarus emergence and retreat
colonization, starting on May 17, 2014. The first immature individuals (females and males were
indistinguishable by eye) were found on June 5, 2014. Following this date, retreats were checked
for occupancy 2 – 3 times a week between 1000 and 1400 hours, and the presence of either
immature females or males occupying marked retreats was recorded. After the first observation
of a cohabiting pair (June 23, 2015), we commenced collections. During each collection day, we
collected all males found cohabiting with immature females in retreats, collected any males
found roaming away from retreats on the same day, and noted the presence and development
stage of any females found in retreats. For all males, the date, status (roaming or guarding), field
location, and associated retreats (for guarders) were recorded. Mature males are readily
recognized given their distinct colouration, foreleg ornaments, and enlarged pedipalps (Hill,
2014). Females that were being guarded by collected males were left in retreats to maximize the
opportunity for male competitive processes to take place between collection days. The
developmental stage (immature or adult) of females was determined based on morphology,
colouration, and size (Hill, 2014). Once collected, all spiders were transported back to the lab for
morphological measuring. We ceased surveys on July 19th 2015 when all females were sexually
16
mature and many had produced egg sacs, and males were no longer being found regularly in the
field (males are relatively short-lived).
Our collection inevitably altered the number of males in our focal fields on our collection
days. Given that P. clarus is common and found throughout the 350 ha field station, it is unlikely
that collection would deplete the local population. We would expect dispersal of males into
fields continuously during this period. If dispersal was not sufficient to counteract the effects of
collection however, given that we did not collect females, our methods would have led to a
progressive shift in the sex ratio such that it would become more female-biased than an
undisturbed population as the mating season progressed. Since lower densities of males would
lead to a decrease in competition-based sexual selection on males over time (Andersson & Iwasa,
1996), it would tend to make it less likely that our predictions from the takeover and fight effort
hypotheses would be supported. Our test of these hypotheses is thus conservative given our
methods.
It is also possible that collecting males would lead to a depletion of males of a particular
size class as the season progressed. For example, this might occur if males mature over weeks
and first-maturing males are either larger (e.g. Neumann & Schneider, 2015; Schneider, 1997) or
smaller than males that mature later (e.g. Uhl, Schmitt, Schäfer, & Blanckenhorn, 2004). This is
not likely to affect our test of the takeover hypothesis since we are comparing guarders and
roamers collected in the same time interval. We nevertheless use our data to test for such an
effect by examining the average size and numbers of males (both guarders and roamers) as a
function of collection date.
17
Morphological Measurements
Spiders were maintained on regular feeding and watering schedules (see Chapter two for
details) until they died, at which time they were preserved in 70% ethanol. After their death, all
males were dissected and digitally photographed (Nikon Digital Camera DXM 1200) using a
Zeiss microscope (Stemi 2000C) and NIS-Elements imaging software (v. 4.0, Nikon). Once
captured, photographs were measured to scale using ImageJ software (Schneider, Rasband, &
Eliceiri, 2012). We measured various aspects of body size, including cephalothorax dimensions
(width and length), the length of the different segments of the leg, as well as the distance
between the two front legs at the coxa on the ventral surface (Table 1). We also measured the
width of the tibial brush, which is a foreleg ornament that may be important in inter-male
signaling of size. We were unable to take measurements of body mass, as survey of all fields and
collection of males was time and labour-intensive, and the large number of individuals collected
made timely weighing unfeasible. However, male size and mass were significantly correlated in
other studies (Sivalinghem et al., 2010).
Statistical Analyses
We used a principle components analysis to reduce potentially correlated morphological
variables into fewer metrics of male body size (Table 1). The first principle component (PC1 –
‘body size’) explained 83.8% of the phenotypic variation seen within the dataset, and had
positive loadings for all measurements, with the heaviest loading on femur, tibia and metatarsus
length, tibial brush and cephalothorax dimensions. As all other components represented an
equally small quantity of phenotypic variation relative to the first (< 10%). Factor scores from
PC1 were used as the single body size index in all further analyses.
18
Fig. 2. 1 Google earth image of the region of the University of Toronto’s Koeffler Scientific
Reserve at Joker’s Hill (King City, ON, Canada, 44° 03’ N, 79° 29’ W) where the study was
conducted. Artificial retreats were placed in each of the 4 outlined fields in a grid to facilitate
regular surveys and collections. Females were collected from retreats in field 1 for studies
described in Chapter two and guarding and roaming males were collected from fields 2-4.
19
Table 2.1. Factor loadings for the first principle component of morphological variables measured
on Phidippus clarus males collected from a field population throughout the breeding season. All
variables loaded most heavily and relatively equally on PC1, thus supporting the use of PC1 as
the single male-size-related phenotypic variable.
PC1
Cephalothorax Width 0.391
Cephalothorax Length 0.343
Coxa length 0.146
Trochanter length 0.116
Femur 0.434
Patella 0.271
Tibia 0.437
Metatarsus 0.314
Tarsus 0.125
Ventral Coxal Gap 0.119
Tibial Brush 0.336
20
To determine whether male body size predicted guarding success, I used backwards
stepwise logistic regression models with male’s collection status (guarding or roaming) as the
categorical response variable. The model included collection field, body size, and collection date
index as predictors. Collection dates were pooled into early-, mid-, and late-season based on our
observed timings of male and female maturation. Early-season (June 23rd – June 29th) was
categorized as the time from first observation of mature males in the field to the date just prior to
the first observation of a mature female. Mid-season (June 30th – July 8th) encompassed the
period of female moulting (from 0 to 100% of observed females mature), and late-season (July
10th – July 18th) was categorized as all collection dates after all females were mature.
Finally, to determine whether there were overall changes in the body size of males
collected as the season progressed a generalized linear mixed model with a gamma error
distribution was used with collection date index as a fixed effect and collection field as a random
factor. Post hoc Tukey’s tests were performed to isolate the cause of any resulting significant
differences in male size across the different periods of the season.
All statistical analyses were performed using R (R Core Team, 2014) or SPSS (v. 23).
Results
Population Structure
Females
While the average occupancy of artificial retreats across the season ranged between 9%
and 21.5% in different fields, occupancy reached 70% on some days, indicating that the artificial
retreats could be readily located and provided suitable retreats for females and males. The
earliest mature cohabiting female was identified on June 30th, while the first mature female
observed roaming (not in a retreat) was found on July 2nd. By July 10th, all females found either
21
in retreats or roaming were mature (Fig. 2.2A). I observed a population-wide female moult
period of 10 days, which is consistent with results from other field studies on different wild
populations of P. clarus (Hoefler & Jakob, 2006).
Males
Confirming protandry in this species, 50% of males observed in the field were mature by
June 20th, 10 days prior to the first mature female appearing. The first instances of cohabitation
were recorded on June 23rd, when 100% of males observed in the population were mature (Fig
2.2B).
Anecdotally, we observed instances of an additional male found on the outside of retreat
tubes of cohabiting pairs, rapid guarder replacement after removal of original resident males, and
males engaging in physical combat next to a retreating female, which in some cases, resulted in
male mortality. Observed copulations only occurred within retreats between cohabiting pairs.
Mate guarding
Although not reported in previous studies, we also observed that mate guarding persisted
past the female moult period, with a relatively high number of males guarding retreating mature
females while other mature females were freely roaming and foraging (Fig 2.2B, Fig. 2.2). Males
were found copulating with females as late at July 16th, and females had laid and were guarding
egg sacs as early as July 14th. The number of cohabitating pairs peaked around June 30th,
coinciding with the start of the female moult period (Fig. 2.2). By July 19th, no cohabiting pairs
were found and roaming adult males were rare while we continued to find mature roaming
females until we ceased our surveys (July 23rd 2015).
22
Fig. 2. 2. Number of P. clarus females (A) and males (B) found in a field population throughout
the breeding season (2014) that were immature (grey) or mature (black) and were found either
inside or on a retreat (circles) or roaming on vegetation away from a retreat (diamonds).
23
Fig. 2. 3. Proportion of males collected guarding females (white bars) or roaming (black bars) at
three periods during the P. clarus breeding season, where females are immature in the Early-
season (June 23-29), are moulting or recently-moulted during the Mid-season (June30-July10)
and are all sexually mature during the Late-season (July 11-18). With approximately equal
sampling effort within each collection period, roaming males were more prevalent than guarding
males early-season than mid- and late-season, however this was not significant (χ2=3.6273, p=
0.1631, df=2). Cohabiting pairs were most prevalent during mid-season, when more than 60% of
males were guarding (also see Fig. 2.2), but guarding remained common through late-season.
Early- and mid-season males guarded immature females, whereas late-season males guarded
mature females.
n=24
n=99 n=88
n=38
n=92 n=82
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
Early-season Mid-season Late-season
Pro
port
ion c
oll
ecte
d
Guarders
Roamers
24
Male Size and Guarding Success across the Reproductive Season
Logistic regression analysis using all collection data revealed that larger males were more
likely than smaller males to be found guarding females, however this effect was driven by
differences in the size of guarders and roamers during the peak season (mid-season x status,
β=0.383, p=0.0004; Fig. 2.4, Fig. 2.5, Table 2). Relative to early in the season, late-season males
were more likely to be guarders than roamers (β=0.736, p=0.037, Table 2). The best model for
these data (Table 2.2) also included male size independent of season and collection fields as
main effects, however neither of these variables was significant. A Hosmer-Lemeshow goodness
of fit test for the final model showed no evidence of poor fit (χ2=7.084, df = 8, p = 0.528).
25
Table 2. 2. Summary of final logistic regression model with variables predicting the status of
Phidippus clarus males (roaming or guarding) in a field population.
Variables in Full model Final Model1 variables with Post-hoc tests
Male Size Wald1 = 2.912, df = 1
β=-0.02, p=0.808
Time of Season Wald1 = 4.355, df = 2, p = 0.113
Early vs. Mid: β=0.574, p=0.101
Early vs. Late: β=0.736, p=0.037*
Collection Field Wald1 = 7.630, df = 3, p = 0.054
Field2= β=-0.595, p=0.278
Field3= β=0.166, p=0.745
Field4= β=0.289, p=0.583
Size x Season Wald1 = 13.197, df = 2, p = 0.001
Early vs. Mid= β=0.383, p=0.0004*
Early vs. Late= β=0.143, p=0.191 1Omnibus test of model coefficients, χ2 = 25.27, df = 8, p < 0.001 *Significant at an α=0.05 significance level
26
Fig. 2. 4. Male status (guarder vs. roamer) was a logistic function of male body size index (1st
principle component of body size measurements, Table 2.1). Larger males were more likely to be
guarding than small males (p<0.0001, n = 434).
27
I also tested whether the size of collected males (pooled across status) changed over the
season (Fig. 2.5, grey columns). It is clear that the size of males was related to the period when
they were collected overall (F2,420= 10.353, p< 0.001). However, while early-season males (n =
62) were smaller than males collected in the mid (n = 190, Tukey’s p < 0.001) or late season (n =
170, Tukey’s p < 0.001), there was no difference in the average size of males collected at mid
compared to late season (Tukey’s p = 0.994) despite the continued collection of many (mid: n =
99; late: n = 88) guarding males as the season progressed.
28
Fig. 2. 5. Average body size (PC1) of guarding (white bars), roaming (black bars) and pooled
(grey bars) males across the P. clarus breeding season. Males were significantly smaller early in
the season (Tukey’s, p < 0.05) and guarding males were significantly larger than their roaming
counterparts during mid-season (β = 0.383, df = 2, p = 0.0004). The average size of males did not
significantly change from mid- to late- season (Tukey’s, p > 0.05). Within early- and late-season,
guarding and roaming males where not significantly different in size from one another. (β =
0.143, df = 2, p = 0.191).
-2.5
-2
-1.5
-1
-0.5
0
0.5
1
1.5
Early-season Mid-season Late-SeasonM
ale
Siz
e (P
C1)
29
Discussion Phidippus clarus has a relatively intense mating season with protandrous males guarding
immature females, all of which become mature within a 10 day period (Fig. 2.2). Thus the
expected payoff to males from guarding increases from early to mid-season. As predicted by
both the takeover and fight effort hypothesis, I found that guarder males in the field were
significantly larger in body size than their roaming counterparts, but only during mid-season,
immediately prior to and during female moult (Fig. 2.5), even though guarding was observed
throughout the mating season (Fig. 2.2, 2.5). During the early and late season, size differences
between roamers and guarders were not significant despite the large samples of collected males
(and thus, high power). This change in the characteristics of guarding males apparently occurs in
the context of a general seasonal shift in male size. I found evidence that early-season P. clarus
males were in general smaller than males found later in the season (Fig. 2.5). An average
increase in male size with the progression of the season is likely to be the consequence of a
trade-off between body size at maturation and developmental timing, where late-maturing, and
therefore larger males appear in the pool of available males later in the season (Prenter et al.,
2006; Schneider, 1997). This phenomenon however, cannot explain differences observed in male
size between guarding and roaming males at any given time in the season. Thus, it is likely that a
size disparity between guarders and roamers during female moult is the result of elevated sexual
selection on males as it relates to precopulatory mate-guarding.
Given the phenology of P. clarus (Hoefler & Jakob, 2006, Fig. 2.2), theory related to
male mating strategies (Elwood & Dick, 1990; Grafen & Ridley, 1983; Härdling et al., 2004)
predicts that mid-season would represent the period in which precopulatory guarding offers the
greatest benefit with the least cost. Guarding a female immediately prior to her final moult
minimizes opportunities for rival males to make take-overs before the female is receptive and
30
likewise requires the smallest investment in time and energy. Consequently, in conjunction with
synchronous female maturation, this dynamic should result in strong positive selection on traits
related to successful guarding around this period. Consistent with this, I observed direct male-
male contests, takeovers, and high male densities in the field. Studies on other species also
support this idea, as male-male competition has been implicated as the driving force for selection
on guarding males, favouring larger size in the period leading up to female receptivity in
Metellina segmentata (a species with an analogous mating systems to P. clarus; Prenter, Elwood,
& Montgomery, 2003). Field experiments on several orb-weaving spider species (M. mengeii
and Zigenilli x-notata) have confirmed that the advantage of large males in precopulatory
guarding is related to male-male contests, with larger males being better able to perform take-
overs of already-guarded females (Bel-Venner & Venner, 2006; Bridge et al., 2000).
Furthermore, takeovers resulting from a series of male-male conflicts have likewise been
implicated as the cause of a steady increase in the fighting ability of sequential guarders in the
sierra dome spider (Watson, 1990). As fighting ability has been linked to male body size in P.
clarus, an equivalent increase in fighting intensity is expected to be accompanied by an increase
in the size of guarders relative to roamers in the time approaching the female moult. Lab-based
experiments demonstrating size and weight advantages in male-male contests in P. clarus (Elias
et al., 2008; Hoefler, 2007; Kasumovic et al., 2009, 2010, 2011; Sivalinghem et al., 2010),
further support male-male contests as a likely mechanism for the mid-season mate-guarding size-
advantage.
As suggested by the takeover hypothesis, larger, late-developing P. clarus males may opt
to start guarding later when females are nearest their final moult and thus most valuable. Such a
mechanism would explain the observed size-difference between guarders and roamers mid-
31
season, since the resulting influx of large, competitively superior males into the pool of
perspective guarders would result in the replacement of smaller, early-developing guarding
males who had already started guarding. The absence of the size differential early in the season,
when selection for guarding is relaxed, is also consistent with this hypothesis. Guarding males
found during this time were just as small as roaming males, and male size overall was smaller
than later in the season. Small males may be unlikely to achieve takeovers of paired females later
in the season, but if they are present early in the season, they can begin guarding immature
females before larger males become established (Fig 2.2). By securing early ownership
advantages (Kasumovic et al., 2011), small males may maximize their chance of overcoming
size-disadvantages when challenged by larger, later-maturing males, and thus have the best
chance at defending their position until females moult. Early-season conditions for P. clarus may
be mirrored in the experiment performed by Bel-Venner & Venner (2006), where removal of
direct male-male competition resulted in smaller Z. x-notata males successfully guarding the
webs of females.
The evolution of protandry in this species may be due to selection for early development
arising from the advantage of reaching and establishing residency with valuable virgin females
prior to maturity. However, protandry is expected only if the benefits of early maturation
outweigh selection for large body size, which requires longer development (Maklakov, Bilde, &
Lubin, 2004; Schneider, 1997; Uhl et al., 2004). My results support the idea that this trade-off
may differ for different males. The existence of early-maturing males suggests that opting to
guard early may have some degree of reproductive payoff for inferior males that may be unable
to acquire larger body sizes. Thus the presence of a size differential between guarders and
roamers at the mid- but not early-season is consistent with alternative guarding duration
32
decisions by males based on guarding costs and their own relative competitive abilities, as
described by the takeover hypothesis.
However, there is also support in this study for the fight effort hypothesis, with
intensified male aggression and fighting occurring when guarding offers the highest reproductive
value for males (Enquist & Leimar, 1990; Hurd, 2006; Maynard Smith & Parker, 1976). Males
fighting harder for guarding status near the female’s moult would be expected to result in both an
increased frequency and intensity of size-determined male-male contests and ultimately generate
a size difference between successful and unsuccessful guarders in the absence of alternative male
decision making. Studies of other species have shown male preference for more reproductively
valuable females, be it related to time to maturity (Birkhead & Clarkson, 1980; Mathews, 2003)
or female body size (~fecundity; Bel-Venner & Venner, 2006; Cornet et al., 2012; Lawrence,
1986). Furthermore, empirical and theoretical evidence show increased fighting effort in
response to high resource values (Clutton-Brock, 1989; Enquist & Leimar, 1990; Sigurjónsdóttir
& Parker, 1981) and associations between the rate of turnovers and female value (Bel-Venner,
Dray, Allainé, Menu, & Venner, 2008). Since P. clarus males show preference for larger females
that are closer to moulting (Hoefler, 2008), males may also be more motivated to fight over
guarding these preferred females. An increased turnover rate as a consequence of this intensified
fighting would lead to increases in the size difference between guarders and roamers, particularly
since any successful intruding male is expected to be larger, with higher RHP than the resident
male. Although not measured here, heightened male motivation has been shown to lead to an
increased likelihood of escalation to physical combat (Brown, Chimenti, & Siebert, 2007;
Brown, Smith, Moskalik, & Gabriel, 2006; Nosil, 2002; Simmons, 1986; Tachon, Murray, Gray,
& Cade, 1999) and therefore in a heavier reliance on size-related RHP asymmetries in
33
determining guarding success. However, the absence of a size difference between roamers and
guarders early and late in the season is also consistent with fight effort hypothesis. By this
mechanism, the lower resource value of guarding positions over immature females far from
moult or already-mated females would drastically lower male fighting effort for these positions
and thusly uncouple guarding success from the outcomes of RHP-determined fights.
Since female choice also favours large males (Elias, Sivalinghem, et al., 2010;
Sivalinghem et al., 2010), there exists the additional potential for a size difference between
successful and unsuccessful guarders to be the result of females rejecting and rebuffing potential
guarders based on size (Elias, Botero, Andrade, Mason, & Kasumovic, 2010). Since lab-based
experiments have shown that guarding males experience high mating success if allowed to guard
until female maturation (Elias et al., 2014), selection could act on females to become more
aggressive towards less preferred guarders as females approach their final moult. Although
mature females are large and capable of potentially lethal aggression (Elias, Botero, et al., 2010),
immature females are smaller than most mature males, have relatively small legs, and are not
generally observed to be aggressive (pers obs). I argue that these characteristics, in addition to
the immature female’s position --tightly enclosed within a silken retreat-- make it unlikely that
immature females are capable of effectively fighting adult males. While precopulatory female
choice may be acting in more subtle ways than all-out eviction, the effects of male choice and/or
male-male competition during the period of cohabitation are likely to be primary determinants of
mate-guarding success. Since previous research has focused largely on sexual selection in males
with regards to pre-copulatory mate-guarding however, more research is needed in order to fully
investigate this possibility.
34
Since a goal of this research is to address potential mechanisms involved in determining
mate-guarding success within natural populations of P. clarus, it is important to note that
continuous sampling across the breeding season allows for the potential for collection itself to
alter the population structure and thus the competitive and selective environments under study
here. However, equal sampling effort (time spent searching) the consistent prevalence of both
guarders and roamers in large numbers late into the season when accrued sampling effects would
become a concern (Fig 2.5), indicate that any artefact would likely affect roaming and guarding
males equally. Evidence of a size disparity between guarding and roaming males within mid-
season, against a background of an overall increase in average male size (Fig 2.5) further
suggests that population densities and/or dispersal of males between local populations was
sufficient to maintain the variation in size that would be necessary to detect competitive
processes throughout the entire season. Had the consistent removal of guarding males exhausted
the pool of available large males, the average size of guarding males would be expected to
decrease over time. This not being the case, it is unlikely that collection itself significantly
altered natural conditions.
Although guarding males were larger on average than roaming males late in the season,
this difference was not significant. Previous studies have suggested that late in the season,
mature P. clarus females roam and forage during the day (Hoefler & Jakob, 2006; Sivalinghem
et al., 2010), which is consistent with the lack of strong selection on the size of guarding males
observed in this study (Fig 2.3). However, in contrast to previous reports, I observed males
cohabiting with mature females in retreats well after the period of synchronous female moulting.
Cohabitation with mature females often indicates postcopulatory mate guarding in arthropods
(Calbacho-Rosa, Córdoba-Aguilar, & Peretti, 2010), however extended postcopulatory guarding
35
in P. clarus is unlikely given the tendency for mature females to forage away from the retreat
(Hoefler & Jakob, 2006), and the prediction (based on comparisons to other taxa and protandry)
of male sperm precedence (Hoefler, 2007). I observed pairs copulating as well as cohabiting
beyond the synchronous period of female moult, and since spiders in this study were not marked,
it is therefore possible that these observations represent males mating multiply with the same
female, rather than novel pairings. Studies demonstrating decreased receptivity of mated and
guarded female P. clarus exposed these females to novel males rather than the male with which
they had experience (Elias et al., 2014; Sivalinghem et al., 2010). Thus it is possible that females
maintain receptivity with preferred guarding males, therefore making males found copulating
with females late into the season targets of both inter- and intrasexual selection. Superior males
may stand a better chance of acquiring additional paternity by attempting another mating with
their guarded female, rather than risking locating another, potentially less receptive mated female
found roaming. Evaluating these possibilities will require additional information (rather than just
inferences) about sperm limitation and use patterns in P. clarus, and the number of egg sacs
females are likely to produce in a mating season, as these will determine the value of repeated
copulation with the same female for males (Andrade & Banta, 2002; Wedell, Gage, & Parker,
2002). Regardless of these uncertainties, these observations highlight the importance of female
receptivity patterns, and suggest the potential for both male and female choice to be acting
simultaneously on male reproductive success related to mate-guarding.
However, observations of late-season copulation may also represent males mating with
newly-encountered, mated females. If this is the case, then males can accrue additional
reproductive success during the late-season, and this is not exclusively tied to success in
precopulatory mate-guarding. It has previously been proposed that selection on males following
36
female maturity is primarily determined by female choice directed at courtship display traits
(Hoefler, 2007), which may result in a late-season size-advantage for both cohabiting and
roaming males. This may thus explain the similarity in average body size found between these
two groups during this period in this study (Fig 2.5). The opportunity for males to find and court
additional mated females late in the season is anecdotally supported by my observation of high
densities of mature roaming female (pers obs). Additional longitudinal studies that focus on
female phenology and reproduction are necessary to understand the importance of these
observations.
In conclusion, here I show that male body size is positively correlated with mate guarding
success, but only in the period immediately surrounding the female moult in P. clarus. As male
size in this species has been associated with competitive ability, this pattern fits a common
prediction of the takeover and fight effort hypotheses. Consistent with both these hypotheses,
size differences between guarding and roaming males possibly reflect alternative male decision-
making based on guarding durations and/or heightened levels of male fighting effort in
accordance with the increasing reproductive value of mate guarding. Moreover, relaxed selection
on guarding males early and late in the season, as suggested by the lack of a significant size
difference between guarders and roamers, further emphasizes the importance of female patterns
of receptivity as it relates to the cost and benefits of guarding as a male mating strategy. Mate-
guarding early in the season requires more investment of time and energy, so males may not be
as motivated to obtain guarding positions at this time, and/or large males may mature and
attempt to guard only when females are close to moulting. Similarly relaxed selection on traits
related to successful guarding in the late-season may arise because of alternative opportunities
for copulations with previously-mated females found roaming. While it is difficult to distinguish
37
between the male takeover and fight effort models, these two hypotheses are not necessarily
mutually exclusive, as they are predicted under similar conditions, and are influenced by similar
factors. Here, evidence in support of common predictions nonetheless highlights the importance
of temporal variation in intra- and inter-sexual selection in the evolution of male mating tactics
within natural populations.
38
CHAPTER THREE: MALE COURTSHIP AND FIGHTING
PERFORMANCE AS A FUNCTION OF GUARDING STATUS
Introduction Mate-guarding, an attempt to limit mating access of rival males to females, can depend
on the outcomes in male-male contests (e.g. Benton, 1992; Dodson & Schwaab, 2001; Huffard et
al., 2010). The ability to acquire and defend a resource (in this case, a female), known as
resource holding potential (RHP; G. A. Parker, 1974a), is expected to be correlated with male’s
competitive ability. Body size is often used as a proxy for RHP and fighting ability in various
taxa, since size is often positively correlated with competitive success (Austad, 1983;
Christenson & Goist, 1979; Dodson & Beck, 1993; Hack et al., 1997; R.R. Jackson & Cooper,
1991; Suter & Keiley, 1984; Tedore & Johnsen, 2014). It has likewise been shown that
opponents assess signals of RHP produced by their competitors, either as direct signals, such as
size (Andersson, 1976; Clutton-Brock, Albon, Gibson, & Guinness, 1979; Davies & Halliday,
1979; Turner & Huntingford, 1986)) or indirect ones, such as components of bird songs (DuBois,
Nowicki, & Searcy, 2011; Illes, Hall, & Vehrencamp, 2006), push-up displays in lizards (Van
Dyk, Taylor, & Evans, 2007), and dominant frequencies of frog calls (Bee, Perrill, & Owen,
1999). Game theoretical models predict that relative and self-assessment strategies will evolve
where the likelihood of persisting in a contest is based on information about RHP and the costs
and benefits of winning or losing for each male (G. A. Parker, 1974). Some circumstances, such
as unavoidable receiver error or low costs of being deceived, may lead to the evolution of
unreliable signals of RHP (Gardner & Morris, 1989; Wiley, 1994). However, in systems where
bluffing has significant costs (e.g. physical injury), signals should evolve to convey accurate
information about an individual’s RHP (Maynard Smith & Parker, 1976). It is thus expected that
successful mate-guarding males will be those with higher RHP, and that these males will thus be
39
more likely to win fights either through actual fighting ability or through successfully conveying
information about their fighting ability or motivation to their opponents (Johnstone & Norris,
1993; Vehrencamp, 2000).
Pre-copulatory mate-guarding will increase male fitness only if successful guarders
achieve copulation. The most direct way mate guarding leads to increased mating success is by
preventing other males from mating with females. However if a male’s ability to defend a female
is also correlated with overall male viability (or other female-fitness enhancing traits), mate-
guarding males may also experience higher courtship success through being preferred by
females. In this case, in addition to preventing other males from courting/mating with females,
guarding males may have a higher likelihood of copulating if given the opportunity to court.
Females may thus indirectly benefit if successfully guarding males tend to be of superior genetic
quality (Andersson & Simmons, 2006; Benton, 1992; Härdling et al., 2004; Kokko, Jennions, &
Brooks, 2006; Mead & Arnold, 2004; Prenter et al., 2003). However, females may also pay a
cost of restricted access to preferred mates if males who typically guard successfully do not
possess traits favoured by female choice (Jormalainen, 1998). When mating with a dominant
male comes at a substantial cost to a female (e.g. Petersson, Järvi, Olsén, Mayer, & Hedenskog,
1999; Sih, Lauer, & Krupa, 2002), competition-driven mate-guarding may thus result in sexual
conflict (Wong & Candolin, 2005).
The degree to which mate guarding ensures a high quality mate or limits a female’s capacity
to mate with preferred males depends on the association between male traits providing females
with fitness benefits and those providing males with competitive advantages in gaining access to
females (Wong & Candolin, 2005). When the same traits are used for assessment of genetic
quality by females and of fighting ability by contesting opponents, male-male competition can
40
often benefit a female by having a mate-sorting effect in line with female choice (Review in
Berglund, Bisazza, & Pilastro, 1996). While exceptions have been documented (e.g. Howard,
Moorman, & Whiteman, 1997; McCauley, 1982; Petersson, Järvi, Olsén, Mayer, & Hedenskog,
1999), a large male mating advantage via competitive exclusion is often reinforced by female
preference (Reviewed in Hunt et al., 2009).
In the mating system of the jumping spider Phidippus clarus in which precopulatory mate
guarding has evolved, mature males guard retreating immature females from rival males up until
a period of synchronous female moult. Males able to defend females through male-male contests,
involving stereotyped visual and vibratory signals and escalation to physical combat, secure the
opportunity to court and mate with virgin females.
Laboratory experiments with P. clarus have shown that females favour larger (heavier), more
actively vibrating males (Sivalinghem et al., 2010), and such males are more likely to win fights
(Elias et al., 2008; Elias, Sivalinghem, et al., 2010). However, it is also clear that fight dynamics
can be complex, and may not entirely depend on male morphology (Hofmann & Schildberger,
2001). For example, Watson (1990) found that when size differences between sierra dome spider
males (Linyphia litigiosa: Linyphiidae) are less than 20%, contest outcomes are more likely
determined by vigor or persistence. It has also been suggested that willingness to fight
contributes non-trivially to contest outcomes for opponents with RHP-assymmetries (Hofmann
& Schildberger, 2001). Specific to P. clarus, an advantage of males holding guarding positions
over introduced males in fights (‘ownership’ advantages; Kasumovic et al., 2011) has been
demonstrated to outweigh a positive effect of size on the outcome of fights between males
(Hoefler, 2007; Elias et al., 2008). The result is that guarding males may be able to defeat larger
rivals in individual fights. These fights however, may be escalated and costly, particularly if a
41
rival is relatively large (Kasumovic et al., 2011). Moreover, there are both ‘winner’ and ‘loser’
effects in this species which affect the fighting performance of males as a function of their
success in previous contests (although size has a stronger influence on contest outcomes
(Kasumovic et al., 2009, 2010). There is evidence in other taxa that ‘winner’ or ‘loser’ effects
may also extend to male courtship behaviour and success following fights (Amorim & Almada,
2005).
Due to the synchrony of female maturation in P. clarus, selection via male-male competition
(fighting rival males for guarding positions) and female mate choice (female being receptive to
courtship) is expected to occur sequentially, where the first round of selection via competition
occurs distinctly before selection via female mate choice. The first competition-based bout of
selection on males is expected to be relatively strong, since the overall reproductive success of
males unable to acquire the opportunity to court a virgin female through guarding may be
drastically limited (Hunt et al., 2009). Nevertheless, selection via female mate choice may be
likewise strong in P. clarus since mature females are larger than males and can be highly
aggressive and potentially lethal to males (pers obs), thus making coercive mating unlikely. It is
therefore possible that a successfully guarding male that is not favoured by females could be
chased off or killed by his prospective mate once she matures, creating an opening for other,
more female-choice friendly males. A review by Hunt et al. (2009) found that opposing selection
was more likely to occur when mechanisms operate sequentially, therefore it cannot be assumed
that competitive success is equivalent to mating success and that guarding males are also
favoured by female choice. The reinforcing or opposing relationship between male-male
competition and female choice may have significant implications for the operation of sexual
42
selection on P. clarus as it relates to overall male fitness and thus the evolution of mating
strategies.
Instead of mating advantages purely by competitive exclusion, successfully guarding males
in this species may possess traits that are also preferred by females, and thus experience higher
average courtship success rates given the opportunity to court a mature virgin female (Elias et
al., 2014; Jormalainen, 1998; Neff & Svensson, 2013; D. J. Parker & Vahed, 2010). Regardless
of the specific mechanism, recent laboratory research in P. clarus has shown that indeed
guarding males experience high mating rates with their guarded females (Elias et al., 2014),
reinforcing that mate guarding in this species offers crucial reproductive benefits for males
despite the significant costs associated with this strategy. Indeed, the direct costs associated with
precopulatory mate-guarding may be mitigated if female mate choice reinforces selection via
male-male competition and thus offers indirect benefits for males successful in this strategy. The
fitness gain for successful guarders may be further enhanced by decreased receptivity of mated
and cohabited females to other males (Sivalinghem et al. 2010; Elias et al 2014), and the
synchronous nature of the female maturation period.
While laboratory arena-based male-male contests have shown that larger, heavier and
more actively signalling males tend to win fights, laboratory studies to date have not examined
male performance as a function of their guarding status in the field, so it remains unclear how
selection operates via guarding and female choice in natural populations. This is critical because,
for example, how these winner and loser effects, and strong resident advantages play out in
natural contexts is unclear (Hsu, Earley, & Wolf, 2006). Given the proposed importance of mate-
guarding for male reproductive success as a means to secure access to virgin females, the
objective of this study is to assess the influence of male status in the field on performance within
43
the context of male-male competition and female mate choice. Here I ask whether successfully
guarding males possess traits in addition to size and weight which contribute to RHP and mate
guarding success in nature. Additionally, I hypothesize that successfully guarding males are of
higher genetic quality and will be favoured by female preference. Consequently, I predict that
successful guarders will be more likely to win staged contests against roaming males in part due
to non-size related traits that would give guarding males additional advantages in a highly
competitive environment against rivals possessing similar RHP. I further predict that guarding
males will experience higher courtship success than non-guarders (hereafter “roaming males”)
through correlations between traits favoured by mate guarding and mating success. To test these
predictions I examined the outcome of staged mating opportunities and inter-male competition as
a function of naturally-determined male status (guarder or roamer). This study aims to
investigate the consequences of sexual selection related to mate guarding on male traits
associated with performance in male-male contests and courtship.
Methods
P. clarus reproductive behaviour
Courtship behaviour in P. clarus progresses in a predictable sequence (Hoefler, 2008).
After orientating towards a female, the male elevates its body above the substrate through leg
extension, then proceeds to raise and extend its first pair of (ornamented) legs horizontally. He
then waves these legs vertically in unison, along with an abdominal tremulation, while moving in
a typical jumping spider “zig-zag” motion (Forster, 1982) to slowly approach the female. As the
male approaches, an unreceptive female may raise her body from the substrate by straightening
44
her legs and produce aggressive vibrations with her front legs extended horizontally and fangs
exposed. If the male continues to approach while the female is aggressively displaying, she will
often strike the male with her legs or fangs. However, if a female becomes receptive to a
courting male, she will drop her body to the substrate and retract all of her legs. As this occurs,
the male will extend his front legs and touch the female’s cephalothorax several times while
producing vibrations similar in frequency to the initial vibrations but of longer duration. After
several touches, the male proceeds to mount the female, and if left uninterrupted, will turn her
abdomen to the side so he may insert a pedipalp into one of her two genital openings.
Collection and Housing
All spiders were collected from the University of Toronto’s Koffler Scientific reserve at
Joker’s Hill (see chapter 1 for details). During surveys of fields between June 5th and 23rd 2015,
penultimate-instar virgin females were collected from a field not utilized in other studies (Field
1, figure 2.1; Chapter two). Guarding and roaming males were collected throughout the mating
season as outlined in Chapter 2. Once in the lab, all collected males and females were transferred
into individual AMAC plastic cages (5.87 x 5.87 x 7.78 cm), with opaque dividers to maintain
visual isolation between individuals. Spiders were housed on a light:dark 12 hr cycle at 24 C.
Each cage contained a paper tube, to serve as a retreat, and a tree twig for sensory stimulation in
order to minimize the behavioural effects of lab housing (Carducci & Jakob, 2000). Spiders were
provided with water ad libitum via Eppendorf tubes filled with water and plugged with cotton,
and fed a small cricket (1/4 inch Acheta domesticus) twice weekly. Water tubes were replaced
when empty and cricket carcasses were removed every other week. Cages were checked daily
and the death of any spiders were recorded.
45
Signal Recording
Substrate-borne vibrations produced by males during courtship or male-male contests
were recorded using a Laser Doppler Vibrometer (LDV; Polytec OFV 3001 controller, OFV 511
sensor head) attached to a translation stage (Newport model 421), a procedure used successfully
in several studies of this species (Sivalinghem et al., 2010, Elias et al., 2008). Measured signals
were recorded on a digital VCR (Sony DVCAM DSR-20 digital VCR, 48,1000 kHz sampling
rate, Sony, New York, NY) before being analyzed by Raven Pro 1.4 audio software
(Bioacoustics Research Program, 2011). Small pieces of reflective tape (1 mm2) were placed on
the stretched nylon base of the experimental arena to be measurement points for the LDV.
Courtship Trials
Roaming (nR=37) and guarding (nG=38) males were randomly chosen for single-male
courtship trials (ntotal=75) through a random number generator. As there were not enough virgin
females to use a different female for every trial, females (n = 23) were used multiple times. To
limit the effect of successive trials on female behaviour, no female was used more than once a
day, and females were prevented from mating, and so remained virgins throughout the trials. All
experimental spiders were fed 1 – 2 days before the trial to ensure that hunger did not affect
courtship or aggressive behaviour. The experimental arena was made of nylon stretched over a
needlepoint frame with a transparent acetate plastic wall and an open top. The inside top of the
walls were covered in petroleum jelly to prevent spiders from climbing out. The inside was
cleaned with 70% ethanol between trials to remove any chemicals and silk laid down by previous
spiders. Females and males were both weighed before and after trials using an Ohaus Explorer
balance. Male size was measured post-trial, after males had died on their own as described in
chapter 1.
46
To start a trial, a female was placed in the arena and left to acclimate for 3 minutes before
a male was introduced. An individual male was then added to the arena and both were allowed to
interact freely. Along with LDV recordings, trials were recorded using a video camera recorder
(HANDYCAM®NEX-VG10; Sony e-mount lens SEL18200; 44.1 kHz audio sampling rate).
Males were left in the arena until the male began to mount the female, after the female
receptivity display (contracted legs), or until 10 minutes had elapsed from male introduction. A
10 minute cut-off was used, as has been used in previous lab studies with P. clarus (Elias,
Sivalinghem, et al., 2010; Sivalinghem et al., 2010) since males usually initiate interactions
relatively soon after visually detecting a female (mean latency to courtship initiation = 2.3 min).
Furthermore, males that did not successfully court within 10 minutes tended to either court for
only a small number of bouts or had females continuously aggressively display and strike at
them, either scenario suggesting that courtship was unlikely to be successful if trials were
continued past 10 minutes. After a male began mounting, spiders were separated using a camel-
hair paintbrush and returned to their original cages. Females were given a fresh cricket after
every trial to minimize any potential energetic costs of courtship and therefore reduce (though
potentially not fully removing) the influence courtship experience may have on receptivity in
subsequent trials. Individual females were introduced to males of different status in a random
order (i.e. first and subsequent experiences with a guarder or roamer randomly assigned), and no
female was used more than once per day to further limit the effect of experience.
Competition Trials
To investigate male-male competition, I followed a similar protocol to the courtship
trials, except that two similarly-sized males of opposite status (males collected as guarders or
roamers) were introduced simultaneously to the arena which already contained a virgin female
47
introduced 3 minutes earlier (to remove any resident-advantage, e.g., Kasumovic et al., 2011).
All males used in male-male contests were completely naïve within the laboratory context,
having not been previously used in courtship or competition trials (to avoid effects of courtship
experience, Hoefler, 2008, and winner and loser effects, Kasumovic et al., 2010). To prohibit
direct involvement in male-male interactions, females were placed under a small petri dish.
Females could nevertheless transmit visual and vibratory cues that might evoke competitive
behaviours. Females’ chemical cues were also present since females were allowed to roam freely
in the arena for 3 minutes prior to trials. As game theory predicts (Enquist & Leimar, 1990;
Hurd, 2006; Maynard Smith & Parker, 1976), and empirical studies have shown that males
compete more intensely for highly receptive females (i.e. high resource values; Austad, 1983;
Enquist & Leimar, 1987; Riechert, 1979; Wells, 1988) stimulus females (n= 6 virgin females)
were chosen based on demonstrated high receptivity (never aggressively displayed and accepted
mating attempts from at least one male) in the previous courtship trials. Since females were not
able to directly interact with males, and thus remained virgins, the same female was used in up to
12 consecutive trials. Before each trial, a small amount of nontoxic fluorescent paint was applied
to the dorsal abdominal surface of gently restrained males for identification, using a camel-hair
paintbrush. Males were allowed to interact freely during trials. Typically, males would orient
towards each after being released into the arena. Trials were terminated (1) after 10 minutes if
there were no interactions, or (2) after an interaction that was followed by one male turning 180°
to face away from an opponent and moving away in an apparent attempt to flee. An interaction
was defined as a period during which males were oriented towards each other, involving visual
(front legs raised) and/or vibratory (abdominal tremulations), and often the movement of one
male towards the second male.
48
Signal Analysis
Through analysis of recorded video and laser Doppler vibrometry (LDV), features of
male behaviour and signal displays were measured.
For courtship trials, this included active courtship duration, courtship outcome and
vibration rate (both aggressive- and courtship-type). The start of courtship was defined as the
time when the male initiated some form of courtship display (visual and vibratory or just visual)
while oriented towards the female. The active courtship duration was measured as the total
(summed) time a male spent actively displaying (visual and/or vibratory) while oriented towards
the female throughout the trial. This measure did not include periods of latency between bouts of
displaying where male and female interactions completely stopped. Courtship outcome was
categorized as successful if females displayed a receptivity posture (legs retracted) and
unsuccessful otherwise. Mean pulse durations were calculated from the pulse durations of a
randomly chosen subset (n=5) of recorded vibration pulses and vibration rate was measured as
the total number of pulses divided by courtship time. Signals were qualitatively categorized as
courtship or aggressive signals according to published descriptions (Elias et al., 2008;
Sivalinghem et al., 2010), and separate analyses were performed if both signals were produced in
a single trial. Courtship vibrations are longer in duration and are produced concurrently with a
vertical movements of the first legs (mean duration= 0.71 s) whereas aggressive-type vibrations
occur while the legs are maintained in an elevated position and tend to be of higher amplitude
and much shorter (mean duration=0.11 s), often happening in bouts of 2 or 3.
For competition trials, I scored contest outcome (whether the guarder or roamer
retreated/lost), degree of escalation (occurrence of physical combat), fight initiator (whether
guarding or roaming male was the first to display in a given interaction), active fight duration
49
(summed duration of all displays and/or physical combat) and vibration types and rates for each
male. A retreat, and therefore loss, was scored as when a male turned away from an opponent
following aggressive displays on the part of either males and attempted to run in the other
direction. Average vibration rate calculations were only made when it was clear which spider
was signalling (i.e., overlapping signals were not analyzed). The measurement of an interaction
between males commenced with the first display (visual or vibratory) from at least one male.
Statistical Analyses
Male morphological measurements included in our analyses were (1) composite measures
of male body calculated using principle components analysis (PC1 scores, see Chapter one
methods) and (2) male body condition. To obtain a measure of body condition for males that
incorporated mass, residual values for each male from a significant linear regression of male size
and mass were obtained (Jakob, Marshall, & Uetz, 1996; F1,164= 403.9, p=2..2e-16).
Backwards logistic regression analyses were performed to examine predictors of
courtship and contest success in relation to male status (roaming or guarding). Analysis began
with a complete model that included all measured variables and putative interaction effects that
were determined a priori based on the literature on this species (Table 3.1, Table 3.2). Model
selection involved sequentially dropping the least informative variable in successive steps until a
reduced model was obtained. The model that best represented the data was considered to be the
model with the lowest AIC value. For competition trials, the relationship between fight initiation
and status was analyzed using a chi-square test of independence. All statistical analyses were
two-tailed and performed in R (R Core Team, 2014).
50
Courtship Outcome and Signal Characteristics Related to Status
To assess whether male status (roaming versus guarding) affected courtship success, a
generalized linear mixed model with a binary logistic regression link was used with courtship
success as the outcome variable. The model included random effects of female ID and female
experience (1st, 2nd or 3rd trial for a given female) to account for repeated use of females in trials.
Female experience was included as a random effect since models using female experience as a
fixed effect were unresolved, suggesting that experience does not affect courtship outcome.
Initial models included status, male size, condition, pulse duration, vibration rate, season, and
female mass. I also included interaction factors: status x vibration rate and status x season, where
‘season’ is a factor representing the time of the mating season (early, middle, late) when males
were collected. I also performed several simple linear regressions to explore relationships
between body size and courtship vibration rate, courtship duration, and female mass.
Contest Outcome and Male Characteristics Related to Status
To examine which attributes of male opponents predicted overall contest outcome
(whether the winning male was a guarder or a roamer), I tested several models using either
independent or composite (difference) measures of the traits of competing roaming and guarding
males (mass and vibration rate). Since preliminary analysis revealed that mass and size were
highly correlated (F1,164= 403.9, p=2..2e-16) and previous research has emphasized male mass as
a primary determinant of contest outcomes (Elias et al., 2008; Elias, Sivalinghem, et al., 2010),
size and condition were not included in these models to avoid collinearity. Testing both
independent and composite measures of male traits is consistent with game theory models
suggesting that contest outcomes may depend on self-assessment or relative assessment of RHP,
and other studies suggesting correlates of fight outcomes may include the difference between the
traits of competing males (Hammerstein & Parker, 1982; Maynard Smith & Parker, 1976;
51
Mesterton-Gibbons, Marden, Dugatkin, Biology, & Labs, 1996; G. A. Parker, 1974; Taylor &
Elwood, 2003). In addition to male traits, contest duration, occurrence of escalation, status of
initiating male (guarding versus roaming), and female mass were all included as predictor
variables in the models. Preliminary linear regressions showed that male mass and size were
highly correlated.
To determine whether male status predicts success in male-male contests independent of
other measured traits, one focal male within each contest was randomly chosen for analysis. This
was done to be able to use status as an independent variable while avoiding pseudoreplication
from use of males who fought against one another. The full model initially included contest
outcome (winning versus losing) as the dependent variable and the predictors were: male status,
vibration rate, mass, size and initiation of interactions (yes versus no) by focal individuals. Two-
way interaction terms between status x vibration rate and status x season were also included.
Scalar predictor variables were tested both as absolute values and as the difference between the
focal individual and his opponent. To establish the degree to which body size was correlated with
aggressive vibration rate, I performed a simple linear regression with size as the predictor
variable of vibration rate. I then investigated whether guarding or roaming males were more
likely to initiate a fight, regardless of contest outcome, through a Pearson’s χ2 test of
independence.
Results
Courtship Trials and Signal Characteristics Related to Male Status
The final generalized linear mixed model predicting courtship success included female
mass, courtship duration, vibration rate, season, and an interaction between male status and
vibration rate (Table 3.1). Courtship outcome depended strongly on vibratory signal rate and
52
courtship duration, but there was no significant effect of female mass, nor of the time of season
when males were collected (final model, Table 3.1). Males with higher vibration rates and longer
courtships were more likely to mate regardless of status (Figure 3.1). There was a significant
negative correlation between courtship duration and vibration rate (β=-28.3, p <0.001),
suggesting that males with higher vibration rates mated relatively quickly and that males with
low vibration rates could mate successfully if they persisted sufficiently long in courtship.
Female mass and an interaction between male status and vibration rate were marginally
significant (Table 3.1) so I explored these variables further. Heavier females were more likely to
mate, however this was not because such females are courted more intensely by males. A simple
linear regression revealed no association between male courtship effort (vibration rate or
courtship duration) and female weight (β=0.00448, p=0.917 and β=-1.32, p=0.389, respectively).
The interaction between male status and vibration rate arises because courtship success increases
with vibration rate more steeply for guarding males compared to roaming males (Fig. 3.1).
Overall, except at extremely low vibration rates (<5.0 pulses/min), guarding males tended to be
more successful at courtship than roaming males (Fig. 3.1).
In other studies, male size predicts success in fighting (e.g. Bridge et al., 2000;
Lindstrom, 1988) so we also examined this variable further. Simple linear regression revealed
that body size and courtship vibration rate were significantly positively correlated (F1,59= 4.945,
p=0.03; Fig. 3.2), however body size was not included in the final model as an independent
factor (Table 3.1).
53
Table 3. 1. Predictors of courtship success in laboratory trials of Phidippus clarus males
collected in the field as successful guards or as roamers.
Fixed Effects in Full model Final Model
Male status (roamer-guarder) --
Male size --
Male condition --
Mean pulse duration --
Mean vibration rate F1,54=9.647, p=0.00300*
Female courtship experience --
Courtship duration F1,54=9.679, p=0.00300*
Female mass F1,54=3.545, p=0.0650
Time of season F2,54=2.262, p=0.114
Collection field --
Male status x vibration rate F1,54=3.378, p=0.0720
Male status x time of season -- 1 determined as the model with the lowest AIC following backwards stepwise logistic regression
*Significant at α=0.05
-- denotes factor was dropped in final model
54
Fig. 3. 1. Relationship between courtship success in laboratory trials and the courtship vibration
rate of Phidippus clarus males collected in the field as guarders (dashed line, open circles) or
roamers (solid line, filled circles). Curves are independent logistic regressions to visualize
differences between roamers and guarders in the effect of vibration rate on courtship, using
vibration rate of either roamers or guarders as predictors of courtship success (guarders: β=0.110,
p=0.0615; roamers: β=0.0363, p=0.432).
55
Fig. 3. 2. Relationship between male body size index and courtship vibration rate for Phidippus
clarus males collected in the field as guarders (open circles) or roamers (filled circles). Body size
index is the first principle component of a PCA that includes cephalothorax and first leg
measurements, see Table 2.1, Chapter two).
56
Contest Outcome and Signal Characteristics Related to Male Status
Both Males in Model:
Males competing in male-male contest trials were, on average, similar in size (5%
different in mass). In the final logistic regression model for contests between males, the
aggressive vibration rates of both male opponents significantly predicted the contest outcome
(Table 3.2). A Hosmer-Lemeshow goodness of fit test for the final model showed no evidence of
poor fit (χ2 = 7.76, df = 8, p-value = 0.458). The odds of a male winning were positively
correlated with his own aggressive vibration rate (β=0.195, p=0.0294; Table 3.2) and negatively
correlated to the aggressive vibration rates of his opponent (β=-0.197, p=0.0287). The collection
season of both males, along with presence of escalation remained in the final model, however
none significantly predicted contest outcome (Table 3.2). Replacing individual male phenotypic
and signalling traits in the model with composite (difference) measures of mass and vibration
rates resulted in a similar importance of the relative vibration rate of competitors (Table 3.3,
Figure 3.3). However, when relative values of these variables were used, escalation was a
significant predictor of contest outcome. Contests in which roamers were successful were more
likely to involve escalation than contests won by guarders (β=-2.415, p=0.0462). A Hosmer-
Lemeshow goodness of fit test for this final relative model showed no evidence of poor fit (χ2 =
8.5996, df = 8, p-value = 0.3772).
57
Table 3.2. Predictors of success in laboratory staged male-male competition trials between males
collected as guarders (G) or roamers (R) in nature across the mating season from multiple fields.
Backwards step-wise logistic regression analysis of contest outcomes incorporating absolute
measurements of phenotypic traits for both contestants.
Variables in Full model Final Model 1
Competition duration ---
Female mass ---
Roamer season Early – Mid: β=1.38, p=0.486
Early – Late: β=-1.49, p=0.498
Guarder season Early – Mid: β=1.40, p=0.473
Early – Late: β=3.34, p=0.175
Roamer vibration rate β=-0.197, p=0.0287*
Guarder vibration rate β=0.195, p=0.0294
Roamer mass ---
Guarder mass ---
Escalation β=-2.34, p=0.0703
Initiator ---
Guarder collection field ---
Roamer collection field --- 1 determined as the model with the lowest AIC following backwards stepwise logistic regression
*Significant at α=0.05
58
Table 3. 2. Logistic regression analysis of contest outcomes incorporating relative measurements
of contestants’ phenotypic traits.
Variables in Full model Final Model 1
Competition duration ---
Female weight ----
Roamer season Early – Mid: β=1.36, p=0.488
Early – Late: β=-1.44, p=0.508
Guarder season Early – Mid: β=1.39, p=0.475
Early – Late: β=3.25, p=0.175
Relative vibration rate β=0.195, p=0.0284*
Relative mass ---
Escalation β=-2.41, p=0.0462*
Initiator ---
Guarder collection field ---
Roamer collection field --- 1 determined as the model with the lowest AIC following backwards stepwise logistic regression
*Significant at α=0.05
59
Fig. 3. 3. The relationship between the competitive success of Phidippus clarus males collected
in the field as guarders and roamers, and the relative rate of aggressive vibrations produced
during laboratory competition trials.
60
Focal-Male Model:
Analysis of factors predicting the success of one randomly chosen focal male from each
trial allowed direct tests of the effect of male status on contest outcome. The final model
revealed that focal males were more likely to win if their aggressive vibration rate was high, not
independently of, but relative to, their opponents (Table 3.4, β=0.0032, p=0.764 and Table 3.5,
β=0.134, p=0.0187, respectively). A Hosmer-Lemeshow goodness of fit test for the final model
using absolute values showed no evidence of poor fit (χ2 = 1.4328, df = 8, p-value = 0.9938).
Guarding males were significantly more likely to win contests than roaming males overall (Table
3.4, β=-1.75, p=0.0334) but were only marginally more likely to win if the model included
vibration rate and mass values relative to those of their opponent (Table 3.5; β=-1.44, p=0.0568).
A Hosmer-Lemeshow goodness of fit test for the final relative model using relative values
showed no evidence of poor fit (χ2 = 5.744, df = 7, p-value = 0.5699). There were no significant
interactions between male status and vibration rate (Table 3.4). There was no significant effect of
season on the likelihood of a male winning (Table 3.5).
Unlike courtship vibration rates, there was no significant relationship between male size
and aggressive vibration rates (F1,48=1.848, p=0.181; Fig. 3.4).
61
Table 3. 3. Focal-male analysis of contest outcomes in staged competitive trials between field
collected males using absolute measurements of male phenotypic traits.
Variables in Full model Final Model 1
Male status (R relative to G) β=-1.75, p=0.0334
Male mass ---
Mean pulse duration ---
Mean vibration rate β=0.0032, p=0.764
Escalation Present ---
Initiator ---
Collection field ---
Season (mid relative to early) ---
Season (late relative to early) ---
Male status x vibration rate β=0.0580, p=0.137
Male status x season --- 1 determined as the model with the lowest AIC following backwards stepwise logistic regression
*Significant at α=0.05
Table 3. 4. Focal-male analysis of contest outcomes in staged competitive trials between field
collected males using relative measurements of male phenotypic traits.
Variables in Full model Final Model 1
Male status (R relative to G) β=-1.44, p=0.0568
Relative mass ---
Relative pulse duration ---
Relative vibration rate (G - R) β=0.134, p=0.0187
Escalation Present ---
Initiator ---
Collection field ---
Season (mid relative to early) β=-1.09, p=0.278
Season (late relative to early) β=0.421, p=0.686
Status x vibration rate ---
Status x season --- 1 determined as the model with the lowest AIC following backwards stepwise logistic regression
*Significant at α=0.05
62
Fig. 3. 4. Relationship between aggressive vibration rate and body size of randomly chosen focal
males in competitive contests between Phidippus clarus males collected in the field.
63
Along with guarding males being more successful at winning contests than roaming
males when the model included their absolute values of vibration rate and mass, a chi-squared
test revealed that guarding males were significantly more likely to initiate contests than were
roaming males (guarders: 73.3 % of contests; roamers: 26.7 % of contests; χ2= 9.0909, df = 1, p
= 0.00257).
Discussion
Guarding Male Courtship Success
I hypothesized that successfully guarding males experience greater mating success
through competitive exclusion and by being higher genetic quality males and thus possessing
traits favoured by female choice. I predicted that guarding males would experience higher
courtship success than roaming males, but results from courtship trials revealed that guarding
success did not significantly predict courtship success. However, along with the expected
positive effect of courtship vibration rate on mating success, there was a marginally significant
interaction between status and courtship vibration rate. Guarding males tended to experience a
greater increase in courtship success with increasing vibration rate than roaming males and
tended to have a higher courtship success except at the extremely low vibration rates. This
suggests that guarding success, as determined by the outcome of male-male contests, may also be
associated with signalling traits and potentially the efficacy of their transmission within the
context of courtship. Female use of multiple signals or cues in assessing male quality has been
demonstrated in numerous studies (Bro-Jørgensen, 2010; Johnstone, 1996), and while there are
several theories as to why and how multiple signals have evolved, it is widely believed that they
may facilitate detection and/or improve reception of viability indicators (Candolin, 2003; Iwasa
& Pomiankowski, 1994). Given the complex multimodal nature of P. clarus communication
64
(including visual, vibratory and chemosensory), it is feasible that P. clarus females assess males
through multiple modalities simultaneously and respond differentially to signals depending on
the specific cues presented by a given male. Successfully guarding males with superior fighting
ability may give off specific cues that facilitate better detection of the honest information
contained within vibratory signals, and the presence of these cues may therefore explain the
interaction between vibration rate and status found in this study. One such characteristic of
signals that may influence the transmitting of information contained within male vibration rates
(unmeasured here due to limitations of the experimental setup) is signal intensity. Higher
intensities (measured as amplitude) improve signal reception (Ritschard, Riebel, & Brumm,
2010), and it has been shown in birds, insects, and anurans that females base mating decisions on
song or signal amplitudes in addition to frequencies (Arak, 1988; Castellano, Rosso, Laoretti,
Doglio, & Giacoma, 2000; Latimer & Sippel, 1987). Thus it may be that guarders are able to
produce more intense vibrations relative to their body size and can therefore elicit stronger
female preference for any given vibration rate in comparison to roamers. As vibration rate was
the most significant predictor of mating success, this marginal interactive effect may be non-
trivial to male fitness within the context of a highly competitive and restricted breeding season.
The correlation between, and female preference for, high vibration rates and large body
size found in this and other studies, may mean that guarding males are preferred as mates over
roaming males by virtue of being larger. While guarding success did not directly predict a higher
mating success, it is possible that the larger average size and the better signal reception of
guarding male courtship signals mean that males able to successfully defend immature females
may also be favoured by female choice and thus experience higher likelihoods of courtship
success once females moult. This effect has been observed in the broad-headed skink (Eumeces
65
laticeps), where large males who were shown to exclude smaller males from gaining access to
females were likewise favoured by female choice (Cooper & Vitt, 1993). Moreover, the “good
genes” hypothesis (Hamilton & Zuk, 1982) was implicated as the associative mechanism
between female choice and guarding success in this species, with females using the area of head
colouration as an honest signal of male size (Cooper & Vitt, 1993). As it has been proposed that
courtship-related signals are honest indicators of male quality in P. clarus (Sivalinghem et al.,
2010), the association between these signals and traits important in mate guarding success is
likewise consistent with the “good genes” hypothesis. In addition to possessing superior
competitive abilities, guarding males may be of overall superior quality to their roaming
counterparts. Furthermore, since courtship success is ultimately necessary for the evolution of
male mating strategies, differences in female preference between successful and unsuccessful
guarding males in terms of courtship signal efficacy and body size may be significant in terms of
the selection on male traits related to mate guarding in nature.
Guarding Male Contest Success
Results of male-male contests between roaming and guarding opponents found no
significant effect of weight or size differences between opponents. Given that previous research
has found male mass as an important determinant of contest success (Elias et al., 2011, 2008), it
is possible that the average 5% mass difference between opponents in the present study was not
biologically relevant and therefore undetectable through statistical analysis. Supporting a
minimum threshold for an effect of mass/size differences on contest outcomes, Hack et al. (1997)
demonstrated that size-advantages disappeared when size asymmetries dropped below 10%
between opponents of the mate guarding orb-weaver spider M. segmentata.
66
Despite not finding results consistent with previous research on the effect of male size in
staged contests, the significantly larger average size of guarding males found in the field
suggests that this may be an important determinant of mate-guarding success in this species
when size differences are above a specific threshold. Body size has been shown to be an
indicator of RHP, in the context of mate guarding, in various taxa (Austad, 1983; Briffa, 2008;
Clutton-Brock et al., 1979; Wells, 1988). In a study on the scorpion Euscorpius flavicaudis,
Benton (1992) found that larger and stronger males tended to initiate and win more fights, thus
allowing them to hold on to guarding positions for longer. Consequences for mate-guarding of
size asymmetries have likewise been predicted by game theory models, where opponents may
use assessment of resource value and relative or self-assessment of RHP to inform strategic
decisions (Enquist & Leimar, 1983, 1987; Hammerstein & Parker, 1982; G. A. Parker, 1974).
Differences in body size or weight can often be the source of asymmetries in RHP, and this has
been shown empirically within the context of agonistic contests over resources such as territories
and retreat sites (Englund & Olsson, 1990; Lindström & Pampoulie, 2005; Polak, 1994; Reichert
& Gerhardt, 2011; Wells, 1988) and in P. clarus specifically, over mates (Elias et al., 2008;
Kasumovic et al., 2009). Given evidence based on both theoretical and empirical studies, larger,
heavier P. clarus males are predicted to have greater fighting abilities and thus a better ability to
over-come ownership and experience effects of resident males to obtain and defend guarding
positions.
After controlling for the previously established size and weight advantage in male-male
contests, results from this study suggest that aggressive male vibration rate is the most important
predictor of fight success (Table 3.2, 3.3, 3.5). This is consistent with results from previous
studies assessing male competition in P. clarus, where likelihood of winning increased with
67
increasing vibration rate, and likewise with increasing asymmetries in favour of the higher
vibrating male (Elias et al., 2008). Interestingly however, guarding males were still more likely
to win contests even after controlling for vibration rate (Table 3.4). Contrasted with the effect of
vibration rate within a courtship context, the effect of aggressive vibration rate on contest
outcome was not influenced by status (Table 3.4), and aggressive vibration rate was not
significantly correlated with male size. This suggests that the competitive advantage guarding
males possess is not exclusively related to vibratory aspects of a male’s aggressive display,
despite the importance of these signals in the outcomes of staged contests. A greater size
asymmetry between males may have allowed for statistical analysis to detect the correlation
between male size and vibration rate and its influence on contest outcomes. Given the high
density of males during the breeding season and of male size variation, it is likely that in nature
males encounter competitors of all sizes, and thus that size-related vibrational advantages in male
interactions may play a significant role in guarding success. This is even more likely given the
size disparity found between guarding and roaming males (Chapter two).
While results from Chapter two, indicate that male body size and signals containing
information on size (vibration rate) are key factors in determining guarding success, a significant
guarder advantage in male-male fights (Table 3.4) suggests that guarders possess additional traits
contributing to their success. Consistent with the observed fighting advantage after controlling
for size, inherent size-independent components of RHP have been proposed in previous studies
in the absence of a predicted size-advantage in male-male contests (e.g. Reichert & Gerhardt,
2011; Sigurjónsdóttir & Parker, 1981). The absence of a significant interaction between status
and aggressive vibration rate suggests the presence of other guarder traits providing additional
advantages in contests beyond those conveyed by size. There is no clear evidence that guarders
68
are able to produce better, or more effective, aggressive signals as has been suggested in the case
of courtship. Non-vibratory characteristics of guarders may include a higher fight motivation,
which would explain the significantly higher likelihood of guarders initiating fights compared
with roamers. As threat displays may function to transmit information on aggressive motivation
and intentions in addition to direct fighting ability (Hofmann & Schildberger, 2001), a higher
propensity to initiate aggressive displays may play a role in the success of guarding P. clarus
males in nature.
Along with other components of RHP (i.e. size), males may use assessment of
motivational states during encounters in decisions of whether to escalate or retreat (Hofmann &
Schildberger, 2001) and studies have demonstrated that high motivation may enable males to win
against larger opponents (Kotiaho, Alatalo, Mappes, & Parri, 1999; Wagner, 1989). While the
propensity to initiate did not directly translate into contest success here, this trait may give
guarding males an additional advantage where pre-determined males are not forced to interact
within staged contests. The increased likelihood of a roaming male winning once a fight
escalated to true physical fighting between opponents of similar RHP seems to support this idea,
whereby only roaming males possessing comparable RHP would choose to escalate in the face of
an initiating guarding male. When RHP-matched intruding and resident males interact in natural
settings, initial aggressive visual displays conveying information both on willingness to fight and
on body size (via presentation of leg span and tibial brushes) may play a larger role in
determining the outcome of male-male contests than in enclosed arena-based experiments. As it
has been suggested that the importance of body size could be over-estimated in staged
encounters between males (Lindström & Pampoulie, 2005), more research is required to address
this possibility.
69
Overall, the results indicate that guarding and courtship success are correlated, where
males who are successful at guarding in the field also experience heightened courtship success
with females encountered within staged experiments. The observed association between traits
favoured in both contexts suggest that females may also benefit from this mating strategy,
whereby competition facilitates mating opportunities with preferred mates for females. Guarders
do better in both contexts mainly because they are larger and have higher vibration rates.
However, a disproportionate gain from vibratory signal increases within a courtship context and
a size-independent advantage in male-male contests suggests that other inherent traits of guarders
not captured by these analyses may be related to their success in natural field conditions. Given
the capacity for resource value, ownership advantages, experience effects, and readiness to fight
to significantly influence the outcome of male-male contest (Dodson & Schwaab, 2001; Elias et
al., 2008; Enquist & Leimar, 1987; Hack et al., 1997; Hofmann & Schildberger, 2001; Hsu &
Wolf, 2001; Kasumovic et al., 2011), the higher likelihood of guarders to initiate contests may be
associated with size-independent traits that enhance the mate-guarding advantages of larger,
more actively vibrating males in nature.
70
CHAPTER 4: GENERAL CONCLUSION
Results from Chapter two found evidence consistent with selection through precopulatory
mate-guarding favouring large body size in P. clarus males. In conjunction with a large-male
advantage in staged contests (Elias et al., 2008; Hoefler, 2007; Kasumovic et al., 2009, 2010,
2011; Sivalinghem et al., 2010), these findings implicate the role of size-determined outcomes
of direct male-male competition in mate-guarding success in the field. Guarders were
significantly larger than roamers exclusively around the period of female moult. This is expected
if there is heightened competition for guarding positions with females who are close to moulting.
The observed variation in size disparity between guarders and roamers across the season is
consistent with predictions of both the takeover and fight effort hypotheses. Evidence in support
of mutual predictions from these hypotheses suggest that the importance of takeovers between
males and thus direct male-male contests on mate-guarding success in P. clarus is directly tied to
the heightened reproductive value for males of females surrounding their final moult. Given the
protandry in this species and the opportunities for additional matings through courtship instead
of guarding, relaxed selection on male size in mate guarding success early and late in the season
emphasizes the importance of different and potentially opposing selective forces that can interact
to drive the evolution of male mating strategies.
I examined the consequences of such shifting opportunities for male-male competition
and female choice by assessing the association between mate guarding success and male
performance in courtship and competitive contexts. These studies revealed that male signalling
traits determined courtship and contest success. Vibration rates of males predicted courtship and
male-male contest success, the outcomes of which favour more actively vibrating males. As
vibration rates are significantly correlated with male size in both contexts, these results provide
further evidence for the role of male size in mate guarding success in the field and suggest that
71
selection via female choice may reinforce the filtering effect of male competition. In some cases,
mate guarding represents a form of sexual conflict, through for example, disproportionate costs
of guarding to one sex or the exclusion of preferred mates (Arnqvist, 1988; Hirotani, 1994).
However, my results indicate that mate-guarding in P. clarus may offer mutual benefits to males
and females, whereby small, presumably poor-quality males disfavoured by female preference
are denied mating opportunities through competitive exclusion.
While evidence suggests that larger males experience higher guarding success surrounding
the period of female moult and that this selection may be the consequence of direct size-related
male-male contests, guarding males seem to possess traits independent of size that result in some
degree of additional advantages in both courtship and competitive contexts. As guarders
produced marginally more effective courtship signals and were more likely to initiate and win
male-male contests independent of size, processes determining mate guarding success in the field
are likely complex and influenced by the interaction of multiple phenotypic and behavioural
traits. Together, the strong influence of seasonal timing on size-related sexual selection through
mate-guarding with the added presence of size-independent traits conferring guarding advantages
stress the importance of variable environmental conditions and non-static traits on the processes
of sexual selection and their impact on the evolution of reproductive tactics.
72
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