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Mate Choice by Both Sexes Maintains Reproductive Isolation in aSpecies Flock of Pupfish (Cyprinodon spp) in the BahamasRhiannon J. D. West & Astrid Kodric-Brown

Department of Biology, University of New Mexico, Albuquerque, NM, USA

Correspondence

Rhiannon J. D. West, Department of Biology,

University of New Mexico, Albuquerque, NM,

USA.

E-mail: [email protected]

Received: December 2, 2014

Initial acceptance: February 2, 2015

Final acceptance: April 10, 2015

(S. Foster)

doi: 10.1111/eth.12394

Keywords: female mate choice, frequency-

dependent selection, male mate choice,

olfactory cues, reproductive isolation,

sympatric speciation, visual cues

Abstract

Female and male mate choices can reinforce reproductive isolation after

sympatric speciation. Using a binary choice design, we examine the

importance of visual cues in female mate choice in all three sympatric spe-

cies of pupfish on San Salvador Island. We also examine the importance

of olfactory cues in female choice of the hard-shelled invertebrate special-

ist (Cyprinodon brontotheroides). We examine male mate choice in two of

the three species, the scale eater (C. desquamator) and the detritivore

(C. variegatus). Females of all three species use visual cues and prefer con-

specific males. C. brontotheroides females do not use olfactory cues to dis-

criminate between conspecific and heterospecific males. Males of

C. desquamator and C. variegatus also preferentially court conspecific

females. Thus, mutual mate choice, where both females and males exhibit

mate choice, acts as a strong behavioral pre-mating isolation mechanism

in these sympatrically speciated pupfish.

Introduction

To date, studies of behavioral pre-mating isolating

mechanisms in sympatric species flocks have focused

mostly on female choice (Strecker & Kodric-Brown

1999; Kodric-Brown & Strecker 2001; Elmer et al.

2009; Kahn et al. 2010; Kek€al€ainen et al. 2010;

Kodric-Brown & West 2014). However, mutual mate

choice, where both sexes preferentially mate with

phenotypically similar individuals, would facilitate

sympatric speciation and reinforce species barriers

afterward. Mate choice by females is the classic

paradigm of sexual selection, and thus, the most

investigated mechanism for maintaining behavioral

pre-zygotic reproductive isolation. However, selection

imposed by male preferences for mates also shapes

the evolution of female traits (Andersson 1994). Male

mate choice is common in breeding systems with

paternal care of offspring (Gwynne 1991; Chen et al.

2012; Myhre et al. 2012), but a growing literature has

shown that it can occur in the absence of paternal

care (Edward & Chapman 2011). Examples include

insects (as reviewed in Bonduriansky 2001), gazelles

(Gazella marica; Wronski et al. 2012), guppies (Poecilia

reticulata), haplochromine cichlids (Astatotilapia flavii-

josephi) and swordtails (Xiphophorus malinche) in all of

which males preferentially court larger, gravid

females (Sargent et al. 1986; Dosen & Montgomerie

2004; Werner & Lotem 2006; Tudor & Morris 2009).

Sexual selection can facilitate sympatric speciation

(Ritchie 2007), particularly when the divergence is

based upon invasion of a new ecological niche (Maan

& Seehausen 2011) and is a signal of localized adapta-

tion (van Doorn et al. 2009). Generally, sexual selec-

tion in conjunction with ecological niche expansion

results in behavioral pre-zygotic isolation that main-

tains species boundaries (Strecker & Kodric-Brown

2000; Coyne & Orr 2004; Savolainen et al. 2006;

Elmer et al. 2011).

Here, we examine male mate choice in Cyprinodon

variegatus and C. desquamator two members of a three

species flock of pupfish in the Bahamas. Male mate

choice would reinforce behavioral pre-mating isola-

tion in this species flock as has been seen in some sys-

tems (Espinedo et al. 2010; Swenton 2011; Gregorio

et al. 2012), but not others (Kozak et al. 2009).

Ethology 121 (2015) 793–800 © 2015 Blackwell Verlag GmbH 793

Ethology

ethologyinternational journal of behavioural biology

We also examine the role of both visual and olfac-

tory cues in female mate choice in C. desquamator and

C. brontotheroides. Both kinds of cues function in mate

choice in other pupfish (Kodric-Brown 1983, 1996;

Strecker & Kodric-Brown 1999, 2000; Kodric-Brown

& Stecker 2001; Ludlow et al. 2001; Draud & Itzko-

witz 2004) and play a role in promoting or maintain-

ing reproductive isolation in a variety of other kinds

of organisms (Elmer et al. 2009; Smadja & Butlin

2009; Hohenlohe & Arnold 2010). We focused on

female preferences in the scale eater C. desquamator

and the hard-shelled specialist C. brontotheroides. To

date, little is known about female preferences in the

scale eater in either the field or the laboratory (Barton

& Barton 2008; Kodric-Brown & West 2014), and

nothing about female preferences in the hard-shelled

invertebrate specialist. We focused on mate choice

because it will not only provide information on the

proximal mechanisms, such as the sensory cues used

in courtship and mating in each species, but it also

will provide insights into the evolution of pre-mating

isolation in a very young species flock.

The System

Three sympatric species of pupfish occupy three saline

lakes on San Salvador Island, The Bahamas (Holtme-

ier 2001; Turner et al. 2008; Martin & Wainwright

2011). The species evolved in the last 6000 yrs, when

the lakes formed on the island (Pacheco & Foradas

1986; Hagey & Mylroie 1995; Milliken et al. 2008).

The species flock consists of a relatively rare scale

eater, C. desquamator which preys upon the other two

species, a very abundant detritivore, C. variegatus, and

a very rare hard-shelled prey specialist, C. brontothero-

ides (Holtmeier 2001; Turner et al. 2008; Martin &

Wainwright 2013a). The species differ in morphology,

ecology and behavior related to trophic specialization

(Holtmeier 2001; Barton & Barton 2008; Turner et al.

2008; Martin & Wainwright 2011, 2013a; Kodric-

Brown & West 2014; West and Reade in prep). Species

isolation is likely maintained by behavioral pre-zygotic

isolation as the three species coexist in sympatry with

overlapping habitats but readily hybridize in the labo-

ratory (Holtmeier 2001). In the field, there are large

fitness costs to hybrids (Martin & Wainwright 2013b).

C. variegatus and C. desquamator have a polygynous

mating system with males defending contiguous terri-

tories. Females mate with multiple males and deposit

several eggs on a male’s territory during a spawning

sequence. Males defending territories develop breed-

ing coloration that varies from black on the body and

fins in C. desquamator to blue iridescent on the nape

and reddish orange fins and belly in C. variegatus, and

a pale blue body with clear pectoral fins outlined with

black in C. brontotheroides (Martin & Wainwright

2013a; personal observation). However, as in most

pupfish studied to date, male breeding coloration is

facultative and can be turned on or off almost instan-

taneously (Kodric-Brown 1998; Barton & Barton

2008). Territories provide incidental protection of eggs

from predation, as males chase away females who are

attempting to forage on the territory. Territories of

C. desquamator are smaller than those of C. variegatus,

are usually located in shallower water, and are con-

fined to small, rocky outcrops near the shoreline.

Male C. variegatus courtship consists of circling below

a female and guiding her toward the substrate, while

C. desquamator males approach the female in a series

of rapid zigzag or darting movements and lead her to

the territory. In sequential trails, male detritivores

court female conspecifics and scale eaters equally,

whereas male scale eaters preferentially court conspe-

cifics (Kodric-Brown & West 2014). Territorial males

rarely shoal with conspecific females and juveniles.

Generally, territorial male detritivores and scale eaters

only shoal when they are disturbed, for example, by a

predator or an ungainly biologist, and quickly return

to their territories (personal observation). C. brontot-

heroides are very scarce in all three lakes and much of

their behavior is unknown.

M&M

Female Mate Choice

We examined the strength of female preferences for

conspecific males in F1 populations of C. variegatus,

C. desquamator, and C. brontotheroides from Crescent

Lake. It is one of the smallest lakes on San Salvador

Island with populations of all three species of pupfish

and has the highest densities of C. desquamator. Labo-

ratory raised offspring from wild-caught parents were

used to lessen potential trapping impacts on all three

species, but especially on the rare C. brontotheroides.

The parental populations consisted of 15 C. brontother-

oides and 20–30 individuals each of C. variegatus and

C. desquamator. The parental fish were housed by spe-

cies and bred in large (1.89 kl) stock tanks with a

14:10 light:dark schedule and salinity at 35 ppt., con-

sistent with salinities in Crescent Lake. Under natural

conditions in the lake, fish are exposed to heterospe-

cifics and therefore avoidance may be learned. We

raised the fish in separate tanks for several reasons: (i)

all three species readily hybridize in captivity; (ii) our

design removes the role of learning and experience of

Ethology 121 (2015) 793–800 © 2015 Blackwell Verlag GmbH794

Mate Choice Maintains Reproductive Isolation R. J. D. West & A. Kodric-Brown

heterospecifics from potentially influencing mate

choice, and (iii) prevents harassment and excessive

fin damage of C. variegatus and C. brontotheroides by

C. desquamator. The stock tanks were enriched with

plants and rocks to provide a natural environment.

Fish were fed freeze dried brine shrimp (San Francisco

Bay�) and tropical fish flakes (TetraMin�) twice daily.

Handling was minimized as much as possible. No

mortalities resulted from the behavioral trials per-

formed in this study. Offspring were raised to matu-

rity and used in all trials. For the visual trials, we used

20 females of each species, for the olfactory trials, we

used 20 female C. brontotheroides. In both visual and

olfactory trials, we used 20 males of each species in

novel combinations. No male pairs were used more

than once. The female and male choice experiments

were conducted from April 14 to June 4, 2012, and

the olfactory trials were conducted from June 4 to

September 1, 2012, during the peak of the breeding

season of these populations in the Bahamas. Fish

were raised in environmentally enriched 20-g tanks

with no more than 10 conspecific juveniles to a tank.

All adults were housed with two territorial males and

3–5 females to a tank. All females were gravid and

males were in breeding coloration and were courting

females in the holding tanks. Thus, all fish used in the

study were socially experienced. Conspecifics used in

the same trials were taken from different tanks to

avoid familiarity effects.

Visual Cues

A small pool (91 cm in diameter) was filled to a depth

of 10 cm with water at 35 ppt. salinity. Three clear

Lee’s Kritter Keeper� (30.23 9 19.81 9 20.57 cm)

tanks were placed in the pool and spaced roughly

equidistant from each other and from the pool wall.

Two males of each species were size matched within

5 mm of each other, and each pair was placed in one

of the three tanks. A limited sample size prevented us

from matching pairs for size and shape. However, size

differences within this range do not appear to affect

female or male mate choice (unpublished data from

Kodric-Brown & West 2014). A female of one of the

three species was then introduced into the center of

the pool. Ten-min tests began once she had started to

explore the pool and visited each set of males. The

time the female spent within 5 cm of each tank, either

facing or swimming parallel to the tank was recorded.

The female was removed and replaced with a female

of one of the other species, until females from all three

species had been used. One trial consisted of one set

of males and three sequential females of each species.

The males were then replaced with a novel combina-

tion of males and the tests were repeated.

Olfactory Cues

The olfactory experiments were performed to test

whether C. brontotheroides females discriminated

between the odors of conspecific and heterospecific

males. We additionally tested whether females of each

species responded differently to heterospecific males.

Thus, we tested whether C. brontotheroides and C. var-

iegatus females differed in their response to C. desqua-

mator males and similarly, whether C. brontotheroides

and C. desquamator females differed in their response

to C. variegatus males. Due to a small sample size of

C. brontotheroides males, we were unable to test the

responses of C. variegatus and C. desquamator females

to the olfactory cues from C. brontotheroides males.

We used a binary choice design to measure female

responses to olfactory cues. To obtain olfactory cues

from each species, two conspecific males were housed

in a 4-l-holding tank for 24 h. They were separated by

a clear divider with small perforations that allow for

water to flow through. They were removed for feed-

ing twice a day but otherwise were undisturbed. The

water from these males was then used in the subse-

quent female choice experiments. Following Kodric-

Brown & West (2014), female C. brontotheroides were

placed in a 22-l aquarium (PETCO Bookshelf aquar-

ium, 60 cm long 9 20.65 cm wide) filled with 20 l of

water at 35 ppt. Two lines were drawn on the front of

the aquarium to delineate three ‘compartments’. The

two outside compartments were 17 cm wide and the

middle one was 26 cm wide. Intravenous bags of 1-l

capacity (Tyco Healthcare ‘Kendall Kangaroo’ IV)

were suspended from the ceiling over each end of the

aquarium. One intravenous bag was filled with water

from conspecific males, and the other was filled with

one of the two heterospecific species’ male water. The

water was dripped into each end of the aquarium at

1 drip/s. The amount of time the female spent in each

of the end compartments was recorded for 10 min.

The female was then moved into a new aquarium,

and the procedure was repeated with male water from

the other species. We randomized both the side the

male conspecific water was dripped into and the order

the heterospecific male water was presented.

Male Mate Choice

To determine whether C. variegatus and C. desquamator

males from Crescent Lake discriminated between

conspecific and heterospecific females, we used a


R. J. D. West & A. Kodric-Brown Mate Choice Maintains Reproductive Isolation

binary-choice design. Because of insufficient numbers

of C. brontotheroides males, their preference could not

be determined. A 75.7-l aquarium was equally

divided into three 20 9 30 cm compartments with

two clear plastic dividers. Two female C. variegatus

were placed into one outside compartment of the

tank, and two female C. desquamator were placed into

the other outside compartment of the tank. To mini-

mize potential effects of size, females were matched in

size within 5 mm of standard length, although small

sample sizes limited a better size matching. A male of

one species was placed in the center compartment.

Ten-min tests began once all five fish were active. We

recorded the time the male spent swimming parallel

to or directly facing a compartment while performing

male courtship behaviors. Under the constraints of

the experimental design, male courtship behavior

consisted of sinusoidal lateral movements with

extended pectoral fins, or movement up and down

the partition next to the female, following her move-

ments on the other side of the partition. After 10 min,

the male was replaced with a male of the other spe-

cies. These experiments only tested male preference,

and as the compartments were not sealed, did not

exclude olfactory cues. A total of 24 males and 24

females of each species were used in novel combina-

tions. No female pairs were used more than once.

Statistical Analyses

Female Mate Choice

A normality test on the residuals of the visual prefer-

ence times indicated they were not normally distrib-

uted. Normality assumptions on an Anderson–Darlingtest were met with a transformation raising female

preference times to the 0.2 power (p = 0.08 AD =0.667). A general linear model with female and male

species, female by male interaction terms, and trial

number as a blocking factor was performed on the

transformed time data. A post hoc Tukey’s HSD

examined significant differences between groups.

Olfactory preference residuals were not normally

distributed and did not match any particular distribu-

tion; thus, we used Bonferroni adjusted Kruskal–Wallis tests. We examined differences in female

preferences between conspecific and heterospecific

males and between females of different species for

males of the same heterospecific species.

Male Mate Choice

Residuals of male preference times were not nor-

mally distributed. A distribution test indicated a

Johnson transformation would be appropriate

(AD = 0.261, p = 0.703). Transformed data were

then analyzed with a general linear model with

male and female species, male by female species

interaction terms, and trial number as a blocking

factor. All analyses were performed with Minitab 16

software.

Results

Female Mate Choice

The species of female (F2,104 = 9.43, p < 0.000), male

(F2,104 = 4.38 p = 0.015), and their interaction

(F4,104 = 41.07 p < 0.000) were all significant predic-

tors of the time females spent investigating visual cues

of males. The blocking factor, trial number, had no

effect on the model (F13,104 = 0.94 p = 0.518).

Females of all three species responded to visual cues

of males and spent significantly more time with males

of their own species (Fig. 1). The time females spent

with heterospecific males did not differ between spe-

cies (Fig. 1).

Females of all three species failed to discriminate

between conspecific and heterospecific males based

on olfactory cues (Table 1; and see Kodric-Brown

& West 2014). Female C. brontotheroides and female

C. variegatus did not differ in the time spent

associating with the chemical cues of male C. de-

squamator (H = 0.01, p = 0.918); nor did female

C. brontotheroides and female C. desquamator differ in

their responses to male C. variegatus (H = 0.00,

p = 1.000).

Fig. 1: Mean (�SE) association time of C. variegatus, C. brontothero-

ides, and C. desquamator females. Females prefer visual cues from

males of their own species. Means that share letters are not significantly

different from each other at a = 0.05 level.



Male Mate Choice

The blocking term, trial number, had no effect on the

model (F23,69 = 0.44, p = 0.985). Neither the species

of male (F1,69 = 0.31, p = 0.577) nor the species of

female (F1,69 = 0.11, p = 0.737) were significant pre-

dictors of time males spent with females. However,

the interaction between male and female species was

significant (F1,69 = 10.55, p = 0.002). Post hoc analyses

show that males of both species preferentially courted

conspecific females (Fig. 2: one-way ANOVAs: C. var-

iegatus males: F1,46 = 7.37, p = 0.009; Cohen’s d =0.784; r = 0.365; C. desquamator males: F1,46 = 4.99

p = 0.030, Cohen’s d = 0.644; r = 0.307).

Discussion

Our results suggest that pre-zygotic isolation is, at

least partially, maintained by female choice in

C. brontotheroides, and mutual mate choice in

C. desquamator and C. variegatus from Crescent Lake,

one of the localities of the sympatric species flock of

Bahamian pupfish on San Salvador Island. The

results of this study are consistent with those by

Kodric-Brown & West (2014) on female preferences

for conspecific males in wild-caught C. variegatus and

C. desquamator females, but differ in male responses

to females. In the current study, males were simulta-

neously presented with a conspecific and heterospeci-

fic female in a binary choice design, and both

C. desquamator and C. variegatus males preferentially

courted conspecific females. However, in trials with

field-caught fish, where males encountered females

sequentially rather than simultaneously, C. variegatus

males indiscriminately courted females of both

species, while C. desquamator males preferentially

courted conspecific females (Kodric-Brown & West

2014). These results suggest that male choice in

C. variegatus is stronger when females are encoun-

tered simultaneously. Another explanation for this

discrepancy in the results is that the current study

used laboratory-bred, na€ıve fish that were main-

tained in single species tanks. Thus, familiarity with

conspecific females may have affected preferences of

laboratory-reared C. variegatus males. Multiple studies

suggest that early experience with predators or het-

erospecifics as well as familiarity with conspecifics,

can influence female mate choice (as reviewed in

Brown & Laland 2003; Verzijden et al. 2012). To

determine the extent of sexual selection in this

system, studies examining shoaling preferences (sensu

Gabor 1999) and mate choice (sensu Strecker &

Kodric-Brown 2000) need to be conducted.

Unlike the only other sympatric species flock of

pupfish in Lago Chichancanab, Mexico (Kodric-

Brown & Stecker 2001), the Bahamian female pupfish

used visual but not olfactory cues in their mate

choice. Although the specific visually perceived traits

have yet to be identified, the females exhibit strong

conspecific association in our experimental aquaria.

Differences in coloration (e.g., Seehousen et al.

2008), body size (Nagel and Schluter 1998), and body

shape (Langerhans et al. 2007; Langerhans & Mak-

owicz 2013) are visually based cues that function in

female mate choice which, in turn, creates behavioral

pre-mating isolation barriers to reproduction. The

three species differ in jaw structure (Martin & Wain-

wright 2011), lateral barring pattern (Martin & Wain-

wright 2013a), and body shape. C. desquamator are

much more fusiform than C. variegatus and C. brontot-

heroides (West and Reade, in prep). Males differ in the

Table 1: Association times (s) of C. brontother-

oides females with conspecific and heterospeci-

fic males in olfactory trials

Female Male n Mean SD Median Statistic p

C. brontotheroides C. brontotheroides 20 321.4 282.8 258.0 H = 0.39 0.543

C. desquamator 265.5 284.7 213.5

C. brontotheroides C. brontotheroides 20 302.0 296.4 259.5 H = 0.40 0.539

C. variegatus 249.9 265.2 192.0

Females showed no preference for conspecific males (p > 0.5).

Fig. 2: Mean (�SE) courtship time for C. variegatus and C. desquama-

tor males with C. variegatus and C. desquamator females. Males of

each species prefer to associate with conspecific females (C. variegatus

males: F1,46 = 7.37, p = 0.009; C. desquamator males: F1,46 = 4.99

0.030).



height of the nuchal hump (West and Reade, in prep),

breeding coloration (Martin & Wainwright 2013a),

and courtship behavior (Kodric-Brown & West 2014).

Some combination of coloration, morphology, and

courtship likely function as visual cues in female pref-

erence as they do in other pupfish (Kodric-Brown

1983). Males may also use differences in jaw mor-

phology body shape and barring pattern to discrimi-

nate among females. Further studies of intraspecific

variation in preferences based on some combination

of shape and color may provide insight into what

visual cues are important in species discrimination

and mate choice in these pupfishes.

We focused on the two sensory modalities that

operate in mate recognition and species discrimina-

tion in the only other known sympatric species flock

of pupfishes (Strecker & Kodric-Brown 1999),

although there may be others. As territorial male

C. variegatus produce sounds (Nicoletto & Linscomb

2008), auditory cues could also contribute to species

recognition and female choice. So far, little is known

about the function of these sounds in female choice or

species recognition in pupfish. In other taxa, females

use multiple sensory modalities in mate choice (Can-

dolin 2003; Kek€al€ainen et al. 2011; van Staaden &

Smith 2011). In East African cichlids, visual cues,

such as male colors and patterns, as well as chemical

and auditory cues are used by females to identify and

mate with conspecific males (Verzijden et al. 2010;

Maruska et al. 2012).

Finally, pre-mating isolating mechanisms in C. var-

iegatus males from Crescent Lake are likely reinforced

by competition for limited breeding ground, which

causes substantial overlapping with male C. desquama-

tor territories. Territorial C. variegatus males in Cres-

cent Lake continuously encounter females of both

species (pers. observ.), and may be forced to choose

between courting conspecific versus heterospecific

females although C. variegatus females are more com-

mon. This has likely directly selected for choosey

males in Crescent Lake. Comparisons with male mate

preferences in the other lakes will reveal the general-

ity of choosiness documented here in Crescent Lake.

An unusual aspect of the Bahamian pupfish flock is

that one of the sympatric species is a scale-eating

predator (C. desquamator). Consequently, there are

two types of selective pressures (i) predation by

C. desquamator on C. variegatus and C. brontotheroides,

which reinforces assortative mating in these species

(Kodric-Brown & West 2014) and (ii) the cost of ran-

dom mating, which produces less fit hybrid offspring

(Martin & Wainwright 2013b). The cost of random

mating would be frequency dependent, thus greater

for the less abundant species, C. brontotheroides and

C. desquamator, than for the more abundant C. variega-

tus (Kodric-Brown & West 2014). Both of these selec-

tive pressures would reinforce mutual assortative

mating and, as a result, strengthen pre-mating isola-

tion. Mutual sexual selection (Almeida & deAbreu

2003; Pierotti et al. 2008; Puebla et al. 2011),

together with ecological niche invasion (Nosil 2012)

and predation (Albert & Schluter 2004) by a closely

related sister species (C. desquamator), is powerful

selective pressures that have led to pre-mating isola-

tion and effective barriers to interspecific mating in

this system.

Conclusion

Selection has likely maintained species barriers in this

system through both divergent selection and rein-

forcement selection (sensu Langerhans & Riesch

2013). Specifically, pre-mating isolation in this system

has probably been maintained by two selective pres-

sures: (i) divergent selection on ecological niche inva-

sion in the specialists and predation avoidance in the

ancestral generalists and by (ii) frequency-dependent

reinforcement selection to choose mates that mini-

mize hybridization.

Acknowledgements

Thanks to S. Levya and A. Reade for assistance in the

laboratory. D. Bolnick, R. Thornhill, P Watson, J.H.

Brown and two anonymous reviewers provided help-

ful comments on the manuscript. M. Barton provided

some specimens and invaluable discussions. Research

was performed under the University of New Mexico’s

IACUC permit no. 10-100586-MCC. RJDW was

funded through a Doctoral Dissertation Improvement

Grant from Gerace Research Centre. We thank the

Bahamian government for permission to collect and

export specimens, and Thomas Rothfus and the Ge-

race Research Centre for logistic support. We have no

conflict of interest to declare.

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