evolution of the cercal sensory system in a tropical cricket clade

Evolution of the cercal sensory system in a tropicalcricket clade (Orthoptera: Grylloidea: Eneopterinae):a phylogenetic approach

LAURE DESUTTER-GRANDCOLAS1*, ELODIE BLANCHET2,3, TONY ROBILLARD1,CHRISTELLE MAGAL2, FABRICE VANNIER2 and OLIVIER DANGLES2,4.5

1Muséum national d’Histoire naturelle, Département Systématique et Evolution, UMR7205 CNRS,57 rue Cuvier, CP 50, 75231 Paris, Cedex 05, France2Institut de Recherche sur la Biologie de l’Insecte, UMR CNRS 6035, Faculté des Sciences etTechniques, Avenue Monge – Parc Grandmont, 37200 Tours, France3CIRAD Acridologie, F-34398 Montpellier, France4IRD, UR 072, Laboratoire Evolution, Génomes et Spéciation, UPR 9034, CNRS, 91198Gif-sur-Yvette, Cedex, France5Université Paris-Sud 11, 91405 Orsay, Cedex, France

Received 27 May 2009; accepted for publication 25 September 2009bij_1371 614..631

The diversity of sensory systems in animals has poorly been explored on a phylogenetic basis at the species level.We addressed this issue using cricket cerci, comprising abdominal appendages covered with touch- and air-sensitive hairs. Scanning electron microscopy measurements and spatial analyses of hair positioning were used toquantify the structural diversity of cercal structures. Eighteen Eneopterinae and two Gryllidae (outgroups) werestudied from a phylogenetic perspective. Cerci were revealed to be complex, diverse, and variable between cricketspecies. Based on maximum likelihood estimations, the ancestral Eneopterinae cercus had a small size, and its hairequipment allowed the use of both air and touch mechanoreception. The evolution of Eneopterinae cerci was mainlyunconstrained by the phylogeny; it was rather a punctuated process, involving apical transformations, and wasmostly unrelated to environmental patterns. All studied species have enhanced their overall perceptive capacitiescompared to the ancestor. Most have longer cerci with more and/or longer hairs. Sensory abilities have improvedeither in the direction of touch or air movement detection, or both, without discarding the potential for any sensorycapacity that was already present ancestrally. This pattern is consistent with the hypothesis of an evolutionarytrade-off for sensory performances. © 2010 The Linnean Society of London, Biological Journal of the LinneanSociety, 2010, 99, 614–631.

ADDITIONAL KEYWORDS: escape behaviour – evolution – filiform hair – predation pressure – setae arrays.

INTRODUCTION

Both structural and functional properties of periph-eral sensory organs can affect the way in which per-ceptual systems evolve in response to selectionpressures by mates or predators (Barth & Schmid,2001). During the last 10 years, research on thediversity and evolution of sensory organs has focused

on comparisons of morphologies among species irre-spective of the phylogenetic history of animals(Chittka & Briscoe, 2001; Dangles et al., 2009).Several studies have investigated the phylogeneticposition of sensory organs among clades (mainlyabove the family level) and provided estimates of thetime of appearance of particular features inherent toeach lineage (e.g. vision and olfaction in mammals:Barton, Purvis & Harvey, 1995; hearing in verte-brates: Fay & Popper, 2000; fish electroreception:Alves-Gomes, 2001; ultrasonic hearing in mantids:*Corresponding author. E-mail: [email protected]

Biological Journal of the Linnean Society, 2010, 99, 614–631. With 3 figures

© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99, 614–631614

Yager & Svenson, 2008). However, our knowledge ofhow sensory systems have diverged in form and infunctional properties at the species level remainsfragmentary. To date, it is limited to a handful ofstudies that have investigated relationships betweenthe evolutionary development of vision and the effi-ciency of the communication of colour signals (Parker,McKenzie & Ahyong, 1998; Prum & Torres, 2003;Smith et al., 2004; Wickham et al., 2006; Cummings,2007; Briscoe, 2008). With the exception of bat echolo-cation (Jones & Rydell, 1994; Jones & Holderied,2007), mantid audition (Yager & Svenson, 2008), andvibration sounding via substrate hammering in para-sitoid wasps (Laurenne, Karatolos & Quicke, 2009),phylogenetic information on other types of sensorysystems at the species level is lacking.

Mechanoreception is one of the most widespreadmeans of sensing in the animal world. It is anancient sensory modality in Arthropod history, and isconsidered to have appeared more than 300 Myabecause it is present in all the ancient invertebratelineages, such as crustaceans, spiders, and insects(Dictyoptera, Orthoptera, Lepidoptera) (Tautz &Markl, 1978; Jacobs, 1995; Barth, 2002). In cricketsand other orthopteroids, mechanosensors include notonly touch receptors (i.e. the trichoid hairs), but alsoair particle movement receptors (i.e. the filiformhairs), which are among the highest performingsensors in the animal kingdom (Shimozawa,Murakami & Kumagai, 2003). Filiform hairs are spe-cialized to mediate responses to faint air currents,such as near-field air flows emitted by approachingpredators. Crickets possess many short filiform hairs,serving as acceleration sensors, and fewer long hairsused as velocity sensors (Shimozawa & Kanou,1984a, b). Variation in the filiform hairs array struc-ture in terrestrial systems may emerge from anadaptation of the mechanosensory system to ambienttransmission as a result of variation in air turbu-lence (e.g. in caves versus in tree canopy) or topredation pressure (abundance, type of predator)(Dangles et al., 2006a). Because any new environ-ment could induce different natural selection on asensory system (Endler & Basolo, 1998), it is likelythat the sensing of predatory signals by cricketscould be optimized in local habitats. Taken together,this implies a potential association between the airenvironment, the mechanosensory system of the prey,and predator signals (Humphrey, Barth & Voss,2003).

Cercal mechanoreceptors are outstandingly used bycrickets to detect approaching predators (Steiner,1968; Gnatzy, 1996; Dangles, Casas & Coolen, 2006b).The cercal system of crickets has long reached thestatus of a textbook example for neuro-ethologists,although virtually nothing is known about the evolu-

tion of these sensors. In the present study, we attemptto address the evolution of characters associated withthe cercal mechanoreceptors of Eneopterinae crickets(Orthoptera: Grylloidea) using structural data sets.Eneopterinae comprise a diverse assemblage of tropi-cal crickets that live in a wide array of habitats (e.g.leaf litter and tree canopy in forests; low bushes inopen areas; edge trees), are active by day or duringthe night, and are preyed upon by a huge diversity ofpredators (e.g. arachnids, parasitoid wasps, frogs,and bats). This information, together with knowledgeof phylogenetic relationships (Robillard & Desutter-Grandcolas, 2004, 2006), is used to analyse the pat-terns of cercal trait evolution and deduce a hypothesison receptor evolution.

MATERIAL AND METHODSTAXON SAMPLING

On the basis of the phylogeny by Robillard &Desutter-Grandcolas (2004, 2006), we selected 18Eneopterinae species (Table 1) and two outgroups,Gryllus bimaculatus and Acheta domesticus (Ortho-ptera: Grylloidea: Gryllinae). Aside from deliberateattempts to include taxa allowing documentation ofthe maximum number of nodes, taxa were sampledopportunistically (i.e. only adult male specimens withundamaged left cerci were included), and randomlywith respect to cercal morphologies. For all species,the length of the median femur was measured tocontrol for allometry in some morphological param-eters of the cerci (e.g. total length, base diameter).

To discuss possible relationships between the evo-lution of cercus morphology and changes in crickethabitat, data on the distribution and ecology of theselected species were gathered based on observationsof the authors and published taxonomic works(Table 1). They have been described as consisting offour biological characters, referred to as B1 to B4(Table 2; see also Appendix). Geographic distributions(B1) have been codified as: (0) Oceania, (1) Australia,(2) Indo-Malaysia, and (3) the Neotropics. Ecologicaldata include the biotope where the species live, thehabitat where the species is active, and its nycthem-eral period of activity. The biotope (B2) has beendescribed as three alternative states: (0) rainforest,(1) woodland/shrubland, and (2) grassland/bare soil.Similarly, four different habitats (B3) have been con-sidered: (0) leaf litter/ground, (1) grass, (2) shrub/thicket, and (3) tree trunk. Nycthemeral activity (B4)is described as a binary character: (0) nocturnal or (1)diurnal.

States have been defined to avoid too many auta-pomorphic states, and to take into account thevarious degrees of precision encountered in the

EVOLUTION OF CERCAL SENSORY SYSTEM 615


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descriptions of species biotope and habitat. Polymor-phism has been taken into account (see Appendix).These characters were optimized onto the tree usingaccelerated and delayed transformation optimizationprocedures, to characterize ancestral Eneopterinae,and test for their general pattern of change.

MORPHOLOGICAL ANALYSIS ON CERCI

The cercal canopy structure was examined by scan-ning electron microscopy (SEM; DSM 982 GEMINI,LEO Microscopie) of cerci that had been dissectedfrom crickets, dehydrated, and sputter coated withplatinum. To perform a complete survey of allsensory hairs inserted on the three-dimensionalconical surface of the cercus (Fig. 1), we built a rotat-ing stage that allowed us to take pictures from dif-ferent angles under the microscope. For each species,we took a set of ¥200 mm magnification SEM picturesfrom the base to the tip of the cercus at two angleviews (0° and 180°). Depending on cercus size, a totalof five to 12 SEM pictures were taken for each of the20 species. Five additional pictures at lower magni-fication (¥40) were taken to measure the length oflong filiform hairs (see below). For technical reasons,

no replication was performed for the present study.This is unlikely to represent any limitation to thestudy because weak inter-individual variability(< 5%) in the structure of the cercal hair canopy isgenerally observed within the same population (e.g.Nemobius sylvestris: Dangles et al., 2005; Gryllusbimaculatus: Magal et al., 2006). Indeed, the percent-ages of variation of all characters vary from 46%(character C28) to 708% (character C20), with amean value of 191% (Table 3), which largely exceededintraspecific variation.

Three types of hair sensilla have long beenobserved in crickets (Fig. 1): the trichoid hairs, whichare deeply inserted, and the filiform and clavatehairs, which are freely articulated (Edwards & Palka,1974). Clavate hairs are club-shaped, located only inthe inner basal area of the cerci, and are involved ingravity perception (Horn & Bischof, 1983). Trichoidand filiform hairs are located on the whole cercussurface, and are involved, respectively, in touch andair perception (Edwards & Palka, 1974). All hairsensilla vary greatly in size, although the filiformhairs are much more variable than the other two.Some hairs that statistically lied outside the overallpattern of the cercal hair length distribution (referred

Table 2. List of cercal and biological characters for 18 Eneopterinae crickets

Number Characters Number Characters

Cercus, general Filiform hairs (following)C1 Length (mm) Filiform hairs, Length distribution (following)C2 Length/femur II length C20 * Number of outliersC3 Base diameter (mm) C21 * Number of hairs > 1500 mmC4 Base diameter/femur II length C22 * Length separating short and long hairs (mm)

Club-shaped setae CS C23 * Proportion of short filiform setaeC5 Total number C24 * Mean length of short hairs (mm)C6 Mean length of pedicel (mm) C25 * Variance of short hairs length (mm)C7 Length of CS zone/cercus length (mm) C26 * Proportions of outliers

Trichoid setae Spatial distributionC8 Total number C27 * All hairs: basal/total number of filiform setaeC9 Mean density (nb/mm2) C28 * All hairs: outer/total number of filiform setaeC10 Maximal length (mm) C29 * Short hairs : basal/total number of filiform setaeC11 Mean length (mm) C30 * Short hairs : outer/total number of filiform setaeC12 Length variance (mm) C31 * Outliers : basal/total number of filiform setae

Spatial distribution C32 * Outliers : outer/total number of filiform setaeC13 * Basal/total number of trichoid setae C33 * Hairs > 1500 mm : basal/total number of filiform setaeC14 * Outer/total number of trichoid setae C34 * Hairs > 1500 mm : outer/total number of filiform setaeFiliform hairs C35 * Nearest neighbour distance (mm)C15 Total numberC16 Mean density (nb/mm2) Biological charactersC17 Exponential diameter/length coefficient B1 Geographic distribution

Length distribution B2 BiotopeC18 * Maximal length (mm) B3 HabitatC19 * Variance of all hairs length (mm) B4 Nycthemeral activity



to as outliers in the present study) could be moredirectly involved in predator detection (Magal et al.,2006).

For each cricket species, four types of morphologicalmeasurements were performed from SEM pictures:(1) measurements related to the cercus (length, basediameter, and total area); (2) measurements relatedto filiform hairs (number, spatial coordinates, andbase diameter); (3) measurements related to clavatehairs (number, length, and area of the insertion zone);and (4) measurements related to trichoid hairs(number, length). Trichoid hairs were counted andmeasured in ten zones (50 ¥ 50 mm) that were ran-domly selected on each side of the cercus. All mea-surements were performed using Scion Image forWindows (Scion Corporation; for further details, seeDangles et al., 2006b).

STATISTICAL ANALYSIS

Cercal hair length (L) can be precisely estimated fromhair base diameter (d) because there is a strongallometric relationship, L = a ¥ db, between these twovariables (Kumagai, Shimozawa & Baba, 1998; Magalet al., 2006). On the basis of simultaneous measure-ments of lengths and base diameters for a series of 40hairs perfectly located in the plane of the photograph,a and b were calculated for each cricket species. Wethen measured the base diameter of all hairs insertedover the cercus and established the hair length dis-tributions for the cerci. Frequency distributions ofhair length were decomposed into Gaussian distribu-tions using a combination of a Newton-type methodand expectation maximization algorithms. Mean (mN),variance (sN), and proportion (pN) for each N compo-nent distributions were calculated using ‘mixture dis-tribution’ in R software (R Development Core Team).

Filiform hairs coordinates allowed us to investigatepotential modifications in the spatial arrangement ofreceptors among species. We used the pair correlationfunction G(r) (Diggle, 1983) to analyse the arrange-ment of cercal filiform hairs for each cricket species.In accordance with guidelines described by Apanaso-vich et al. (2003), the conical point pattern of hairsover the cercus was cut lengthwise into two piecescorresponding to the external and the internal sidesof the cercus. The basal part of the cercus was notconsidered for spatial analyses because of the pres-ence of aggregated clavate hairs. The distributionpattern (random, aggregated or regular) of filiformhairs was evaluated by comparing the observed datawith the null model of complete spatial randomness(Diggle, 1983; Dangles et al., 2009). All spatial analy-ses were performed using ‘Spatial Stat’ in R software(R Development Core Team).

REFERENCE PHYLOGENY

The phylogeny of Eneopterinae has been previouslyinvestigated with both morphological (Robillard &Desutter-Grandcolas, 2004; Robillard, 2006) andmolecular (Robillard & Desutter-Grandcolas, 2006)data sets, using maximum parsimony and direct opti-mization, respectively. The monophyly of the subfam-ily was attested and five monophyletic tribes weredefined.

The most extended morphological analysis (Robil-lard, 2006) was used in the present study as thereference phylogeny. It comprised 41 species, belong-ing to 16 of the 18 genera presently known in thesubfamily and six species belonging to four othercricket subfamilies (Gryllinae, Itarinae, Tafaliscinae,and Landrevinae).

Parenthetic trees with branch lengths wereobtained by submitting the data matrix to PAUP

Figure 1. Cricket cerci as sensory organs. A, singing male of Agnotecous sarramea, with cerci in natural position. B, cercifeatures (L, cercus length; D, cercus basal diameter) and zones (internal/external, basal/apical); clavate hairs arerestricted to the inner surface of cerci base. C, scanning electron microscopy of the cercus, showing filiform (fi), trichoid(tr), and clavate (cl) hairs.



4.0b4a (Swofford, 1998) using basic commands, andrepresented with TREEVIEW, version 1.6.6 (Page,1996) (see Supporting Information).

PHYLOGENETIC ANALYSIS OF CERCAL CHARACTERS

We analysed the modalities of evolution of cercaltraits using a generalized least squares approachimplemented in CONTINUOUS (Pagel, 1997, 1999),which assumes a Brownian motion process forcontinuous character evolution. Two random-walkmodels were tested for each character of the datamatrix, namely a standard constant-variance model(Continuous, model A) and a directional random-walk

model (Continuous, model B), which allows the detec-tion of the presence of evolutionary trends in a dataset according to a topology (Pagel, 1997). The modelthat has a greater log-likelihood value is considered tobetter fit the data.

To study trait evolution further, we analysed thescaling parameters associated with the model bestadjusted to data. These parameters, denoted l, d, andk (Pagel, 1997, 1999), estimate the impact of phylo-geny in trait evolution (l), the tempo of trait evolution(d), and the mode (gradual versus punctational) oftrait evolution (k). l estimates the phylogenetic asso-ciation of a trait, but not the variance of the traitattributed to phylogeny (Freckleton, Harvey & Pagel,

Table 3. Minimal, maximal and mean values of each cercal character observed in Eneopterinae, and their calculatedancestral values

Characternumber

Minimumvalue

Maximumvalue Mean ± SD

Scaling parametersk/d/l

Ancestral value(±SD)

C1 4065 19 852 8525 ± 3762 0.00/2.78/0.00 6975 ± 65C2 0.80 3.85 2.01 ± 0.83 0.00/2.57/0.00 1.49 ± 0.02C3 223.0 923.1 596.3 ± 183.3 0.00/1.92/0,41 515.4 ± 5.5C4 0.08 0.17 0.14 ± 0.02 0.00/1.91/0.27 0.11 ± 0.00C5 57 154 109 ± 27 0.00/2.24/0.35 102 ± 1C6 9.3 58.7 30.4 ± 13.4 0.00/2.16/0.50 32.4 ± 0.2C7 0.05 0.30 0.17 ± 0.07 0.00/1.00/0.70 -40.00 ± 0.03C8 384 4617 1671 ± 1011 0.00/2.01/0.21 1344 ± 16C9 197 883 423 ± 138 0.00/1.71/0.53 320 ± 5C10 40.0 389.2 185.0 ± 87.3 0.00/2.47/0.00 117.5 ± 1.5C11 23.6 275.2 125.9 ± 61.9 0.00/2.13/0.00 80.2 ± 1.8C12 7.46 68.91 31.44 ± 16.16 0.00/3.00/0.00 16.7 ± 0.1C13 0.09 0.55 0.24 ± 0.11 0.00/2.03/0.26 0.17 ± 0.00C14 0.33 0.64 0.53 ± 0.07 0.00/2.79/0.00 0.48 ± 0.00C15 102 906 502 ± 189 0.00/2.05/0.00 289 ± 6C16 24 637 173 ± 144 0.00/2.40/0.00 68 ± 1C17 1.22 2.68 1.76 ± 0.38 0.00/2.13/0.11 1.37 ± 0.02C18 648.0 2453.0 1358.8 ± 491.4 0,00/1.73/0.46 887.4 ± 24.2C19 561.7 1476.6 938.4 ± 296.1 0.00/1.00/0.75 -1660.4 ± 270.6C20 0 85 12 ± 20 0.00/2.43/0.00 7 ± 0C21 0 11 2 ± 3 0.00/1.00/0.95 -4 ± 1C22 200 700 357 ± 133 0,00/1.00/0.53 171 ± 9C23 0.42 0.94 0.65 ± 0.13 0.00/2.51/0.00 0.59 ± 0.01C24 94.0 427.8 194.5 ± 74.8 0.00/1.00/0.36 97.7 ± 2.9C25 68.9 372.6 169.5 ± 87.6 0.00/2.22/0.00 108.3 ± 2.1C26 0.000 0.123 0.025 ± 0.032 0.00/1.92/0.00 0.014 ± 0.001C27 0.12 0.50 0.33 ± 0.1 0.00/2.05/0.00 0.19 ± 0.01C28 0.41 0.67 0.56 ± 0.07 0.00/1.53/0.54 0.24 ± 0.01C29 0.08 0.53 0.31 ± 0.11 0.00/2.14/0.00 0.19 ± 0.00C30 0.32 0.79 0.58 ± 0.12 0.00/2.81/0.00 0.52 ± 0.00C31 0.00 1.00 0.38 ± 0.38 0.00/1.81/0.00 0.20 ± 0.01C32 0.00 1.00 0.54 ± 0.34 0.00/1.66/0.56 0.38 ± 0.01C33 0.00 1.00 0.47 ± 0.47 0.00/2.20/0.00 0.04 ± 0.00C34 0.00 1.00 0.56 ± 0.43 0.00/1.00/0.88 -0.19 ± 0.36C35 20 65 34 ± 11 0.00/1.54/0.53 16 ± 1



2002). The significance of parameter values in termsof properties of trait evolution is summarized inTable 4.

The tests for parameters l and d compare theanalyses performed, respectively, with the defaultvalue of 1 (H0) and with the ML estimate (MLE) ofthe parameter (H1). Each analysis results in a log-likelihood value (Lh). The log-likelihood ratio test(LRT) [LRT = -2(Lh0 - Lh1)] is then compared with achi-square distribution with one degree of freedom.For parameter k, the test involves a default value of0 against MLE (Pagel, 1999).

Ancestral values of cercal traits were finally esti-mated using the most appropriate value of each

parameter and under the best-fit model of evolution(model B in the present study; Table 5). Ancestralvalues, denoted alpha values in CONTINUOUS, areby default calculated for the whole data matrix,including outroup taxa. Because we were interestedin the evolution of cercal traits in Eneopterinae, alphavalues for each tree were corrected using the pathlength between the basal node of the tree and thebasal node of Eneopterinae, according to the relation-ship given in CONTINUOUS: ancestral value = a-value + b-value ¥ path length, where b is the rateparameter of model B. Because ancestral values varyaccording to scaling parameter values, a similarthreshold of 0.05 was applied to the chi-square tests

Table 4. Meaning of the scaling parameters used by the Brownian models of evolution of the CONTINUOUS package(Pagel, 1997, 1999)

Scaling parameters 0 < 1 1 > 1

l – Contributionof phylogeny

Trait evolutionindependent ofphylogeny

Phylogeny has minimaleffects

Trait evolutionconstraint byphylogeny

Not defined

d – Tempo ofevolution

Not defined Early rapid change,then stasis(hypothesis ofadaptive radiation)

Changes regular alongbranch length(Default gradualism)

Temporally laterchange (hypothesis ofspecific adaptation)

k – Mode ofevolution

Punctationalevolution

Stasis on longerbranches

Default gradualism More change on longerbranches

Table 5. Test of Brownian models of evolution for each cercal character

Characternumber Lh: A model

Lh: B model(H0; l = 1; d = 1)

Characternumber Lh: A model

Lh: B model(H0; l = 1; d = 1)

C1 -490.834 ± 0.119 -490.799 ± 0.158 (*) C19 -387.120 ± 0.060 -387.077 ± 0.098 (*)C2 -100.343 ± 0.145 -100.222 ± 0.138 (*) C20 -209.925 ± 0.043 -209.754 ± 0.046 (*)C3 -364.800 ± 0.065 -364.705 ± 0.135 (*) C21 -116.469 ± 0.155 -116.399 ± 0.157 (*)C4 27.089 ± 0.091 27.164 ± 0.149 (*) C22 -341.439 ± 0.051 -341.288 ± 0.121 (*)C5 -276.730 ± 0.093 -276.532 ± 0.205 (*) C23 -46.421 ± 0.090 -46.368 ± 0.141 (*)C6 -216.539 ± 0.084 -216.192 ± 0.302 (*) C24 -319.399 ± 0.059 -319.372 ± 0.084 (*)C7 21.100 ± 0.054 21.297 ± 0.137 (*) C25 -311.848 ± 0.129 -311.817 ± 0.159 (*)C8 -416.707 ± 0.064 -416.657 ± 0.107 (*) C26 92.041 ± 0.036 92.279 ± 0.046 (*)C9 -354.568 ± 0.027 -354.472 ± 0.072 (*) C27 -5.484 ± 0.128 -5.395 ± 0.168 (*)C10 -312.321 ± 0.132 -312.283 ± 0.173 (*) C28 -35.376 ± 0.056 -35.263 ± 0.127 (*)C11 -293.622 ± 0.162 -293.549 ± 0.235 (*) C29 -6.350 ± 0.107 -6.283 ± 0.155 (*)C12 -229.075 ± 0.179 -229.045 ± 0.212 (*) C30 -39.384 ± 0.059 -39.361 ± 0.078 (*)C13 3.293 ± 0.054 3.401 ± 0.102 (*) C31 -43.845 ± 0.034 -43.812 ± 0.032 (*)C14 -34.817 ± 0.076 -34.765 ± 0.117 (*) C32 -40.822 ± 0.020 -40.600 ± 0.109 (*)C15 -359.616 ± 0.090 -359.590 ± 0.118 (*) C33 -39.363 ± 0.044 -39.363 ± 0.044 (*)C16 -330.308 ± 0.042 -330.307 ± 0.042 (*) C34 -26.681 ± 0.093 -26.585 ± 0.123 (*)C17 -91.601 ± 0.083 -91.533 ± 0.135 (*) C35 -230.632 ± 0.045 -230.474 ± 0.138 (*)C18 -403.032 ± 0.116 -402.922 ± 0.199 (*)

A, nondirectional model; B, directional model; Lh, log-likelihood value. (*), model of evolution better fitting the data.



of the three scaling parameters for all 35 characters(Table 3; see also Supporting Information). Model Ballows ancestral values to be outside of the interval ofvalues documented for the terminals.

Each analysis was performed using all four topolo-gies. The mean ± SD of Lh and scaling parametersare given in the Supporting Information, whereas theminimum, maximum, mean, and estimated ancestralvalues of cercal traits are summarized in Table 3.

RESULTSCERCI OBSERVATIONS AND CHARACTERS OF INTEREST

The three types of hairs, even if always present oneneopterine cerci, are not equivalent in term of vari-ability, and so the number of characters required todescribe them differs; filiform hairs are clearly themost variable sensilla on cricket cerci. In total, 35cercal characters were defined, referred to as charac-ters C1 to C35 (Table 2; see also Appendix). Theydescribe the general properties of the cerci (4), andthat of the clavate (3), trichoid (7), and filiform (21)hairs. The amount of variation of the charactersshows the variability of the cerci structures amongthe species (Table 3). No two species within thestudied clade show similar cerci, whatever theirdegree of relationship (see Appendix). We found greatdifferences among cricket species with respect tocercus length (from 4.1 mm in Nisitrus vittatus to19.8 mm in Cardiodactylus novaeguineae) and cercusbasal diameter (from 0.22 mm in Salmanites wittilikoto 0.92 mm in Eneoptera surinamensis). Although allspecies bore the three types of hairs (filiform, trichoid,and clavate) on their cerci, they showed importantvariation in terms of total number, density, length,and spatial distribution of the hairs (see Appendix).Of particular importance, the distribution of filiformhairs reveals differences in total number of hairs andnumber of hairs longer than 0.500 mm. By contrast,filiform hairs did not vary much in minimal length(0.020–0.030 mm).

PHYLOGENETIC ANALYSIS OF CERCAL CHARACTERS

Tables 3 and 5 (see also Supporting Information) reca-pitulate the analyses performed to evaluate cercaltrait evolution. All studied characters have greater Lhvalues under the directional random-walk model (B)than under the standard random-walk model (A).Model B is thus to be preferred to analyse cercalevolution and was used in all subsequent analyses.

Contribution of phylogeny to cercal evolution(scaling parameter l)For all characters, the alternative hypothesis(l differs from 1) is supported (P = 0.025 for C21;P < 0.001 for all other characters). In subsequenthypotheses of eneopterine ancestral values, l hasbeen given its MLE values for all traits. lMLE arelargely distributed between 0 and 1, although 17characters have lMLE equal to zero (i.e. these traitsevolve across the species as if they had no phyloge-netic component) and eight have lMLE < 0.5 (seeSupporting Information). The first category includesseveral traits that are likely to directly influence theperceptive performances of the cerci (Table 6), such ascercus length (C1 and C2), the length of trichoid hairs(C10, C11, and C12), the number and mean density offiliform hairs (C15 and C16), the number of longfiliform outliers (C20), the proportion of short filiformhairs and long filiform outliers (C23 and C26), andseveral distributional characters of trichoid (C14)and filiform (C27, C29, C30, C31, and C33) hairs. Bycontrast, the characters that appear to be moreconstrained by the topology relate to the number(C21) and basal distribution (C34) of filiformhairs > 1500 mm, the length variance of filiform hairs(C19), and the length of clavate hair zone (C7).

Tempo of evolution (scaling parameter d)Results for d are more contrasted than for l (seeSupporting Information). Four characters (C7, C19,C21, and C34) support the null hypothesis (d = 1,P < 0.05) (i.e. their changes are regularly distributed

Table 6. Key morphological characters for predator detection by cricket cerci, and biological significance of their evolution

Character number Described trait Biological significance of an increase in described trait

CercusC1, C2 Length Detection further away from cricket’s body

Trichoid sensilla (touch-sensing)C9 Mean density

Increased sensitivity in touch receptionC10 Maximal length

Filiform hairs (air-sensing)C16 Mean density

Increased sensitivity to air signalsC18 Maximal lengthC20 Number of outlier setae Increased sensitivity to low velocity air signals



along branch length; gradual evolution). These char-acters behaved differently also for parameter l. Forall the other characters, the alternative hypothesis iscorroborated (d > 1, P < 0.05), supporting a hypothesisof apical changes on the topology (i.e. a hypothesis ofspecific adaptation). No character had null d-value,suggesting that changes in cercal traits did not occurat basal nodes of the trees (i.e. there is no support foradaptive radiation in the evolution of eneopterinecerci).

Mode of evolution (scaling parameter k)For all cercal traits, the null hypothesis (k = 0) issupported (see Supporting Information) (i.e. changesin cercal traits are consistent with a process of punc-tational evolution, even for C7, C19, C21, and C34).

ANCESTRAL ENEOPTERINE CERCUS

As shown in Table 3, all ancestral values are com-prised within the interval of values documented herefor Eneopterinae cerci, except for C22, C28, and C35(lower values). For characters C7, C19, C21, and C34,estimated ancestral values are negative. These fourcharacters, which are otherwise the only ones thatbetter fit with d and l equal or close to 1.00 (seeSupporting Information), are perhaps less adequatelydescribed by the directional model of evolutionthrough the whole tree. They are not included in ourcharacterization of the ancestral cerci.

Compared to mean values of cercal traits, theputative eneopterine ancestor is characterized byminimal, occasionally intermediate, properties forcercus shape and size, and hair equipment (Fig. 2): allancestral values are below mean values, and oftenclose to minimal ones. Ancestral cerci are short(approximately 7 mm), with an intermediate basediameter (0.5 mm). The number and length of clavatehairs have mean values, whereas the number, meandensity and maximal length of trichoid and filiformhairs are very low. Trichoid and filiform hairs aremoreover distributed mostly on the apical and exter-nal regions of the cerci, especially outliers and filiformhairs > 1500 mm. Ancestral cerci have also few verylong filiform hairs (seven outliers, a proportion of0.014), although this value is close to the meanobserved in sampled species.

From this ancestral condition, eneopterine cercievolved through a general pattern of diversification,involving a general increase of most cercal properties,as shown by the distribution of observed values com-pared to ancestral ones (Fig. 2). Only the charactersdescribing cercus diameter (C3 and C4), the numberand length of clavate hairs (C5 and C6), and thedistribution of external trichoid and short filiformhairs (C14 and C30) have evolved toward lowervalues as well.

EVOLUTION OF KEY MORPHOLOGICAL PARAMETERS

To better understand patterns of cerci evolution fromthe ancestral form, we analysed patterns of changesfor seven characters involved in key sensory functionsof the cercal sensory system (Table 6). For each char-acter, we compared specific values with mean andancestral values (Fig. 3).

Cercus lengthA general pattern of diversification is clearly docu-mented for C1 and C2, and this diversificationinvolves values either higher (increase in cercuslength), or lower (decrease in cercus length) thanancestral values. Taking into account the phylogeny, ageneral increase in cercus length is thus documentedin Lebinthini, Xenogryllini, Eneopterini p.p., andEurepini, whereas a decrease is obvious in Nisitriniand a partial reversal in Eurepini p.p. (Eurepellamjöbergi) and Eneopterini (Ligypterus linharensis).

Trichoid hairsFor both C9 (mean density) and C10 (maximallength), most species show values comprised betweenthe ancestral value and the mean (12 and 11, respec-tively). Compared to the ancestral value, a generalincrease of the trichoid equipment thus occurred inEneopterinae.

Filiform hairsAs in other features, a general increase of filiformhairs properties occurred; only one (Ponca venosa)and three (Salmanites wittiliko, Lebinthus lifouensis,E. mjöbergi) species have values lower than ancestralvalues for C16 and C18, respectively. The number ofoutliers (C20) shows a less clear pattern of change,increasing in some species (Agnotecous sarramea, thetwo Eneoptera, Nisitrus vittatus and Swezwilderiabryani in the Nisitrini, and Xenogryllus marmoratus),but being very low in most Eurepini and the otherEneopterini, and nul in the neotropical P. venosa andAustralian S. wittiliko.

Is there a trade-off between key morphological fea-tures? The Nisitrini (Paranisitra longipes, S. bryani,N. vittatus), Ligypterus species (Ligypterus fuscus,L. linharensis, Eneopterini), S. wittiliko (Eurepini)and Lebinthus lifouensis (Lebinthini) are character-ized by a decrease or a slight increase in cercuslength. These taxa seem to ‘compensate’ for this by anincrease in hair features: the density and length ofboth hair types (P. longipes), with a higher increase inthe filiform hairs (L. fuscus, L. linharensis), or densityand length of filiform hairs only, including outliers (S.bryani, N. vittatus), or only the density of both hairs(S. wittiliko). Taxa with longer cerci (Cardiodactylusnovaeguineae, X. marmoratus, Eurepa wirkutta,



Myara unicolor, Arilpa wirrilla) show an increase ofthe maximal length of trichoid hairs. On the reverse,a decrease in one hair type is compensated by anincrease in the other (Eneoptera surinamensis, P.venosa). In the same way, for each hair type, oneproperty always appears to compensate the other (L.lifouensis, S. bryani, N. vittatus, E. surinamensis, P.venosa, E. mjöbergi, M. unicolor). No taxa show aconcomitant decrease in both hair types.

CERCI, ECOLOGY, AND DISTRIBUTION

Most diurnal species have short cerci, often shorterthan ancestral one (N. vittatus, L. fuscus, L. linha-rensis, S. wittiliko), whereas species active at night

or during all day have long to very long cerci.Nycthemeral rhythm is not related, however, tothe number of outliers: diurnal species have many(N. vittatus, E. surinamensis, Eneoptera guyanensis)or very few (L. fuscus, L. linharensis, S. wittiliko)outliers, wherever they live, and the same is truefor nocturnal species. Diurnal species, however,show increased filiform properties, rather than tri-choid ones (Fig. 3).

Apart from this, no clear relationship appears toexist between the biotope or the habitat, and cercifeatures. For example, leaf litter species have moreand longer trichoid hairs than ancestral condition,but they have also longer filiform hairs. The twospecies living in very open areas (X. marmoratus, A.

Figure 2. Diversity of cercal character values in Eneopterinae crickets. For each character, the interval of documentedvalues is shown, together with the mean and estimated ancestral values. Morphological characters are shown in light redwhen lower than ancestral values, in light green when lower than mean values but always greater than ancestral values,and in dark green when larger than mean values and hence larger than ancestral values. Characters for which ancestralvalues could not be estimated are represented by dotted lines. Characters are detailed in Table 2. Character values aredetailed in the Appendix.



wirrilla) have both long cerci, but their hair equip-ment is very different (Fig. 3).

Finally, distribution, which is coherent with phy-logeny and could be indicative of communities ofpredators, may partly explain cerci similarity, at leastfor some clades. Nisitrini, for example, are character-ized by very short cerci with many filiform hairs;trichoid properties and outlier number differ greatly,however, in P. longipes on the one hand, and N.vittatus and S. bryani on the other. The impact ofecology in this pattern is hard to assume because thenatural history of P. longipes and S. bryani isunknown.

In the same line of idea, closely-related speciesshow very similar key morphological features: the twoEneoptera species (Neotropics), the two Ligypterusspecies (Neotropics), and the two Agnotecous species(Oceania). Their ecology is, however, either similar(Ligypterus), very close (Eneoptera; Robillard &Desutter-Grandcolas, 2005) or partly different (Agno-

tecous species, which both live in the leaf litter, butsing either in the leaf litter, such as Agnotecousyahoue, or on shrubs and tree trunks, such as A.sarramea; these taxa may belong to different speciesgroups; Desutter-Grandcolas & Robillard, 2006).

Optimization of biological characters show that,ancestrally, Eneopterinae were living in open areas(woodland, shrubland), being either diurnal or noc-turnal on either grass or shrub, whereas its cerci hadminimal values for all key characters (Figs 2, 3). Noneof the present day species whose ecology resemblesthat of this putative ancestor (C. novaeguineae, N.vittatus, Eneoptera species, E. mjöbergi, S. wittilikoand E. wirkutta) has cerci of this kind.

DISCUSSION

Cricket cerci are remarkable organs with exquisitesensory capacities (Shimozawa et al., 2003). However,because very few model species have been studied to

Figure 3. Evolution of distributional, biological, and key morphological characters in Eneopterinae. Only the speciesdocumented for cercal characters are shown on the phylogeny. Eur, Eurepini (Oceania); Ene, Eneopterini (Neotropics);Leb, Lebinthini, Indo-Malaysia and Oceania; Nis, Nisitrini, Indo-Malaysia and Oceania; Xen, Xenogryllini, Paleotropics.Ecological characters: Biotope (B2): fine dots, shrubland/woodland; large dots, grassy areas; strippes, forest. Nyctemeralactivity (B4): strippes, nocturnal; squares, diurnal. Habitat (B3): LL, leaf litter/ground; Gs, grass; Sh, shrub/thicket; TT,tree trunk. Key morphological characters: C1, cercus length; C2, cercus length related to body size; C9, trichoid density;C10, trichoid maximal length; C16, filiform density; C18, filiform maximal length; C20, number of filiform outliers.Morphological characters are shown in light red when lower than ancestral values, in light green when lower than meanvalues but always greater than ancestral values, and in dark green when larger than mean values and hence larger thanancestral values.



date, little is known about their structural and func-tional diversity. They have also never been used in aphylogenetic approach, which precludes hypothesesabout their possibly adaptive condition (Chittka &Briscoe, 2001) and other specific evolutionary path-ways (Brooks & McLennan, 1991, 2002; Harvey &Pagel, 1991). For example, phylogenetic methodscan infer the ancestral sensory conditions of extantspecies, thus testing whether evolution has occurredin a predicted direction; for example, as a result of thecolonization of new habitats (Cummings, 2007). Also,because of their specific methodological require-ments, phylogenetic analyses lead to refined defini-tions of studied characters (Desutter-Grandcolas,1997c; Desutter-Grandcolas, D’Haese & Robillard,2003) and a better sampling of studied taxa, with thepotential discovery of new, outstanding model species(Edwards, Still & Donoghue, 2007; Christin et al.,2009). Below, we first discuss the diversity of cercaltraits in a phylogenetic context and confront our datawith the ecology of cricket species. We then emphasizethe evolution of key cercal traits from their ancestralstate and discuss predation as the major evolutionarypressure for cercal sensory evolution.

OVERALL DIVERSITY AND PHYLOGENETIC ANALYSIS

OF ENEOPTERINE CERCI

We analysed the diversity of cercal structures in asmall cricket group, the Eneopterinae, which com-prises less than 200 species worldwide. Comparisonwith the data available on other cricket species(Gnatzy & Schmidt, 1971; Edwards & Palka, 1974;Bischof, 1975; Dumpert & Gnatzy, 1977; Kämper,1992; Desutter-Grandcolas, 1998; Dangles et al.,2006b) shows that crickets in general, and Eneopteri-nae in particular, have globally homogenous cercifrom a qualitative point of view and always bear threetypes of hairs (i.e. the trichoid, filiform, and clavatehairs), with the latter being an apomorphy of thewhole cricket clade (Desutter-Grandcolas, 2003).Cerci are, however, extremely variable quantitatively,even though not to the same extent for all characters:in the studied clade, no two species showed identicalcerci, whatever their degree of relationship (Table 3;see also Appendix), even though key morphologicalfeatures may be very close in sister species (Fig. 3).

From a phylogenetic point of view, our data provedto be better adjusted to the directional random-walkmodel implemented in CONTINUOUS (Table 5),attesting to the presence of evolutionary trends incercal transformations. For key morphological char-acters, this trend is clearly toward an increase incercus length and hair equipment (Fig. 3).

Analysis of scaling parameter l also revealed thatthe evolution of most cercal characters is not, or only

slightly, constrained by the phylogeny, and the powerof the test is substantiated by the size of our data set(Freckleton et al., 2002). According to other scalingparameters, cercal characters evolved punctually andmostly apically on the tree. This pattern does notsupport a hypothesis of adaptive radiation. Instead, itis congruent with hypotheses of specific adaptations,which in turn could result from selective pressure.

Four characters behaved differently, being moreconstrained by the phylogeny and evolving gradually.They describe traits involved in gravity perception(C7, length of clavate hair zone) or air-sensing (C19,variance of filiform hair length; C21, C34 number andbasal distribution of filiform hairs > 1500 mm). Thispattern of evolution may be related to lower selectionpressure, especially for apomorphic characters suchas clavate hairs (Desutter-Grandcolas, 2003), or char-acters involved in basic air-sensing performance.

CERCAL TRAITS AND EVOLUTIONARY PRESSURES

One of the main limitations in our understanding ofcercal evolution is that our knowledge of the selectionpressures that comes into play remains fragmentary.For example, there is evidence that the cercal–giantinterneurone system also provides sensory feedbackduring song production (Kämper & Dambach, 1985),plays a role in flight initiation and maintenance (Liber-sat & Camhi, 1988), and is involved in mating behavior(Sakai & Ootsubo, 1988; Snell & Killian, 2000; Ritz &Sakaluk, 2002), a situation consistent with the conceptof the cercal system being a generalist perceptivesystem (Jacobs, Miller & Aldworth, 2008). Otherparameters disregarded in the present study may alsoinfluence cercal evolution. For example, the shortercerci observed in the clade Lebinthus–Agnotecouscould be related to the very short size of the wings,which no longer cover the basis of the cerci (Robillard& Desutter-Grandcolas, 2004).

Because cerci are fundamentally used for environ-mental sensing, environmental variables such as thehabitat and predation pressures could be seminalfactors in cercal evolution. It can then be hypoth-esized that species that have come to occupy the samekind of habitat independently, and hence possibly facethe same type of predator, may present similar cercalfeatures. This should be particularly true for keymorphological characters, which are directly involvedin stimuli perception. Conversely, cercal charactersspecialized in the perception of different kinds ofstimuli should present different patterns of evolution.

Evidence indicating that sensory traits may be evo-lutionarily correlated with the environmental charac-teristics in which species live has been reported byseveral groups for sensors such as bat echolocation(Jones & Rydell, 1994), butterfly vision (Douglas



et al., 2007), and surfperch vision (Cummings, 2007).For example, Cummings (2007) showed that thedivergence of estimated performance relative to thesurfperch ancestor was predicted by species-specifichabitat characteristics: the deeper dwelling surfperchin the California kelp forest habitat have divergedtoward luminance biased visual systems, whereasspecies occupying habitats with higher intensitiesand higher luminance variability have diverged tofavour chromatic detection. In a similar vein, Jones& Holderied (2007) reported that echolocation calldesign in bats is often influenced more by perceptualchallenges imposed by the environment than by phy-logeny. Eneopterinae are ecologically diverse, inhab-iting open or forested biotope with several habitats(grass, leaf litter, shrubs, tree trunks) and beingactive either by day or at night (Fig. 3, Table 1).Recurring associations between these features maydefine ecological categories among studied species:(1) most diurnal species live in woodland–shrublandareas (S. wittiliko, Eneoptera species, N. vittatus, andalso C. novaeguineae and M. unicolor); (2) many noc-turnal species live in rainforests and are active eitheron shrubs (P. venosa, A. sarramea) or in leaf litter(L. lifouensis, A. yahoue); (3) Ligypterus species arediurnal and live in forest leaf litter; and (4) nocturnalEurepini living in open areas are active in leaf litterand shrubs (E. mjöbergi, M. unicolor). The resultsobtained in the present study indicate that none ofthese species groups are characterized by specificcercal features: species with similar habitats andactivity periods have very different cerci, as shown forexample by A. sarramea and P. venosa: no ecomorphsensu Harmon et al. (2005) can be defined on the basisof cercal characters. Therefore, the confrontation ofcercal structures with species ecology does not provideclear support for the influence of habitat in shapingthe cercal traits of eneopterine cricket species. Onereason for this lack of correlation could be the scale atwhich species habitat is documented today, and thismight be out of proportion with cercal sensing.Another reason may be our limited knowledge onselection pressures that comes into play in the differ-ent habitats. Although the role of cerci for predatordetection is well established (see below), we knowvirtually nothing about communities of predators inthe different categories of habitats where crickets live.This conclusion echoes the recent finding that spidersare a main predatory group of the European woodcrickets (Grylloidea, Nemobiinae, Nemobius sylvestris;Dangles et al., 2006a). Spiders produce transient flowof a type that has very little resemblance to the flowproduced by flying wasps (Casas, Steinmann &Dangles, 2008). Yet all the neuroethological work con-ducted previously with crickets assumed that flyingwasps and toads were predators of crickets. In the

same line, ontogenetic changes may occur in the cercalsystem during cricket growth, together with changesin predation pressures. In the European wood cricket,adults thus were found to be less predated thanjuveniles as a mere consequence of their larger size(Dangles et al., 2006c). The lack of correlation betweenadult cercal traits and species ecology could then bethe result of a decrease in predation pressure inadults, coupled with the onset of new cercal functions,especially those related to reproduction.

PREDATION AND CERCAL EVOLUTION FROM

THE ANCESTOR

Despite the caveats expressed above regarding themultiple roles that cerci play in the life of a cricket,predator detection is still the best documented func-tion for the cricket cercal sensory system (Gnatzy,1996; Dangles et al., 2006b, c) as well as the mostrobust argument for explaining cercal evolution todate. The present phylogenetic study provides indi-rect support to the hypothesis that predatory pres-sures may indeed be of central importance for theevolution of cricket cerci. We found that cercal lengthexperiences a significant increase from its ancestralstate. This trend suggests that expanding perceptionto a further distance has been globally maximizedthroughout Eneopterinae evolution: all things beingkept equal, longer cerci can perceive stimuli at alarger distance from the cricket body. Because theintensity of air signals emitted by approaching preda-tors rapidly decreases with the distance from preda-tors (Casas et al., 2008), even the short distancesgained by crickets enabling them to perceive thefaintest air signals further from their body can besignificant for survival because they keep predatorsat a distance (Dangles et al., 2006b). For example, a5-mm increase in cercus length would correspond to a100-ms gain in escape time with respect to a predatorapproaching at 5 cm s-1 (e.g. wolf spider; Dangleset al., 2006c). This gain corresponds to approximately50% of the minimal reaction time that crickets needto escape. Moreover, longer cerci can also maximizetouch-sensing by trichoid or filiform hairs furtherfrom cricket’s body. Indeed, we found a generalincrease in air and touch-sensing through growthand/or multiplication of the involved hairs, withoutfavouring one modality of sensing at the completeexpense of the other. Reduction events always concernonly one type of hair (either touch- or air-sensitive)and are always counter-balanced by an increase of theother hair type properties. This balance betweentouch- and air-sensing agrees with the definition of anevolutionary trade-off proposed by Stephens & Wiens(2008: 78), namely ‘an evolutionary increase in oneaspect of performance or fitness (relative to the ances-



tral state) associated with an evolutionary decrease ina related aspect of performance or fitness, on the samebranch of the phylogeny’. Because both air- and touch-receptors are involved in cricket escape (Gnatzy &Kämper, 1990; Dangles et al., 2007) this trade-offbetween the two types of hairs is likely to be a responseto variable predatory pressures. To our knowledge, thepresent study of the cercal sensory system of crickets isone of the first quantitative examples providing phy-logenetic arguments for the role of predatory pressuresin the evolution of sensory prey systems and quanti-fying the observed sensory trade-offs.

The results obtained demonstrate that cricket cercihave evolved according to a pattern that is not con-strained by phylogenetic topology. Cerci experienceda general increase of sensory equipment, involvingmostly apical transformations, and a trade-off betweentouch- and air-sensing receptors. This pattern cannotbe explained by the available data on species habitatand nycthemeral activity, but support a hypothesis ofpredatory selective pressure. In another context, pre-dation is also the main selective pressure put forwardto explain the evolution of singing crickets, in terms ofsignal detection by hearing a predator, and signalmodification or loss (Robinson & Hall, 2002). Eneop-terinae are unique among crickets for their modulatedand ultrasonic calling songs (up to 26 kHz, Robillard,2009), which may result from predatory pressure(Robillard, Grandcolas & Desutter-Grandcolas, 2007).The evolution of their cerci may further demonstratethe underlying strength of predation, as well as itscomplex influence.

ACKNOWLEDGEMENTS

This work is part of the research conducted within theCricket Inspired perCeption and Autonomous DecisionAutomata (CICADA) project (IST-2001-34718) andwithin the Customized Intelligent Life Inspired Arrays(CILIA) project (FP6-IST-016039). These projects areboth funded by the European Community under the‘Information Society Technologies-IST’ Program,Future and Emergent Technologies (FET), LifelikePerception Systems action. We are grateful to JérômeCasas, coordinator of the CICADA project and WorkPackage leader in the CILIA project at the IRBI(University of Tours), for insightful comments on pre-vious versions of the manuscript. We thank G. Kergoat(INRA, France) and F. Legendre (MNHN, France) fortheir help regarding the use of comparative methods.

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SUPPORTING INFORMATION

Additional Supporting Information may be found in the online version of this article:

Doc S1. Topologies and branch lengths of the four phylogenetic trees documented for Eneopterinae phylogeny(Robillard, 2006).Table S1. Test for scaling parameter l.Table S2. Test for scaling parameter d.Table S3. Test for scaling parameter k.

Please note: Wiley-Blackwell are not responsible for the content or functionality of any supporting materialssupplied by the authors. Any queries (other than missing material) should be directed to the correspondingauthor for the article.



evolution of the cercal sensory system in a tropical cricket clade

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