The evolution of social behaviour in Blaberid cockroaches with diverse habitats and social systems: phylogenetic analysis of behavioural sequences

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  • The evolution of social behaviour in Blaberidcockroaches with diverse habitats and social systems:phylogenetic analysis of behavioural sequences

    FRDRIC LEGENDRE1*, CYRILLE A. DHAESE1, PIERRE DELEPORTE2,ROSELI PELLENS1, MICHAEL F. WHITING3, KLAUS SCHLIEP4 andPHILIPPE GRANDCOLAS1

    1Origine, Structure et Evolution de la Biodiversit, Dpartement Systmatique et Evolution, Musumnational dHistoire naturelle, UMR 7205 CNRS, CP 50, 45, rue Buffon, 75005 Paris, France2Station Biologique, Universit de Rennes 1, UMR 6552 CNRS, F-35380 Paimpont, France3Department of Biology, Brigham Young University, 693 Widtsoe Building, Provo, UT 84602, USA4Dpartement Systmatique et Evolution, Musum national dHistoire naturelle, Systmatique,Adaptation, Evolution, Universit Paris VI, UMR 7138 CNRS, 9 quai St Bernard, 75005 Paris,France

    Received 2 July 2013; revised 10 September 2013; accepted for publication 10 September 2013

    The adequacy and utility of behavioural characters in phylogenetics is widely acknowledged, especially forstereotyped behaviours. However, the most common behaviours are not stereotyped, and these are usually seen asinappropriate or more difficult to analyze in a phylogenetic context. A few methods have been proposed to deal withsuch data, although they have never been tested on samples larger than six species, which limits their evolutionaryinterest. In the present study, we perform behavioural observations on 13 cockroach species and derive behaviouralphylogenetic characters with the successive event-pairing method. We combine these characters with morphologicaland molecular data (approximately 6800 bp) in a phylogenetic study of 41 species. We then reconstruct ancestralstates of the behavioural data to study evolution of social behaviour in these insects with regard to their socialsystems (i.e. solitary, gregarious, and subsocial) and diversity of habitat choice. We report for the first time thatnonstereotyped behavioural data are adequate for phylogenetic analyses: they are no more homoplastic thantraditional data, and support several phylogenetic relationships that we discuss. From an evolutionary perspective,we show that the solitary species Thanatophyllum akinetum does not display original behavioural interactions,suggesting phylogenetic inertia of interactive behaviours despite a radical change in social structure. Conversely,the subsocial species Parasphaeria boleiriana shows original behavioural interactions, which could result from itspeculiar social system or habitat. We conclude that phylogenetic approaches in studies of behaviour are useful fordeciphering evolution of behaviour and discriminating between its different modalities, even for nonstereotypedcharacters. 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 5877.

    ADDITIONAL KEYWORDS: phylogenetic inertia sociality successive event-pairing method Zetoborinae.

    INTRODUCTIONStudies of behaviour and phylogenetics have a longand common history (Darwin, 1859; Whitman, 1898;Heinroth, 1909; Lorenz, 1941). After a period of doubtconcerning the concept of behavioural homology in theearly 1970s (Atz, 1970), the adequacy and utility of

    behavioural characters in phylogenetics is now widelyacknowledged (Prum, 1990; de Queiroz & Wimberger,1993; Proctor, 1996; Noll, 2002; Price & Lanyon, 2002;Desutter-Grandcolas & Robillard, 2003; Cap et al.,2008; Pickett, 2010), as long as behavioural charactersare clearly defined (Wenzel, 1992). As for morphologi-cal and molecular data, behavioural homology hypoth-eses must be formulated using classical homologycriteria (Remane, 1952), and especially the criterion of*Corresponding author. E-mail: legendre@mnhn.fr

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    Biological Journal of the Linnean Society, 2014, 111, 5877. With 3 figures

    2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 587758

    mailto:legendre@mnhn.fr

  • position in behavioural sequences (Baerends, 1958;Robillard et al., 2006; Legendre et al., 2008b), as is thecase for DNA or developmental sequences (Edgar,2004; Schulmeister & Wheeler, 2004; Wheeler et al.,2006; Legendre, Whiting & Grandcolas, 2013).

    Ever since the first ethological studies, comparativeanalyses have focused mainly on highly stereotypedbehaviours, such as courtship and ritualized behav-iours, which have the advantage of being fixed (oralmost fixed) and easy to compare (Hinde & Tinbergen,1958; Wenzel, 1992). Other behaviours, apparentlymore variable and difficult to analyze, have, untilrecently, been neglected in phylogenetic analyses ofbehaviour (Japyass et al., 2006; Legendre et al.,2008b; Japyass & Machado, 2010). Unsurprisingly,all of these recent studies suggest the need for amore accurate coding of behaviour, considering itssequential dimension and focusing on behaviouraltransitions as phylogenetic characters. However, dif-ferent methodological coding options and supportingrationales have been proposed. In the present study,we consider the successive event-pairing method(Legendre et al., 2008b), which emphasizes the impor-tance of the too often neglected criterion of position intemporal sequences for assessing behavioural homol-ogy. The successive event-pairing method uses transi-tions among acts in nonstereotyped behaviouralsequences as phylogenetic characters. These charac-ters are derived from matrices of transition where eachcell is filled with the frequency of a transition betweentwo acts (Legendre et al., 2008b).

    In the phylogenetic literature, behavioural acts areoften considered in isolation (e.g. the presence/absenceof behavioural acts), whereas they are alwaysexpressed in a peculiar behavioural context, which is ofprime importance as it is well-known among etholo-gists (cf. displacement and ritualized behaviours;McFarland, 1993). For example, the behavioural actleg kick in mammals could be expressed either inplaying, affiliative or agonistic interactions. It is thesame behavioural act (the criterion of special quality isfulfilled) but expressed in different contexts (the crite-rion of position is not satisfied). Similarly, in socialinsects, leg kick after receiving an antennal solicita-tion would be a different phylogenetic character thanleg kick after having been bitten. The criterion ofspecial quality is again fulfilled but not the positioncriterion given that leg kick is expressed after twodifferent stimulations and then stands in two differentpositions. Behavioural studies have shown that theseshort sequential behavioural patterns within long andnonstereotyped sequences are stable and largely her-itable (Gautier, 1974; Grandcolas, 1991; van Baarenet al., 2002, 2003a), which are two qualities requiredfor phylogenetic characters. Therefore, the observationof two different contexts coupled with inheritance

    information legitimizes the definition of two differentbehavioural characters for phylogenetic analysis.Thus, the successive event-pairing method is consist-ent with two classical homology criteria: the specialquality and position criteria (Remane, 1952). Quali-tative and quantitative characters can be definedaccording to the presenceabsence of a behaviouralcharacter and its frequency of occurrence, respec-tively. Indeed, frequency information is also stableand largely heritable and can thus be studied in aphylogenetic context, with the main problem beingcharacter state delineation (a problem for every kind ofcontinuous phylogenetic data and hence not specific tobehavioural data). Consequently, the successive event-pairing method appears to be useful and legitimatefor the study of the evolution of behaviour in aphylogenetic context. To date, it has only been testedon a small illustrative data set.

    By employing an extended taxonomic sampling, thepresent study aimed at showing that successive event-pairing not only (1) brings new informative datathat are not more homoplastic than traditional (i.e.molecular and morphological) characters, but also(and more evolutionarily relevant) (2) allows detailedhypotheses to be inferred about the evolution of socialbehaviour. The evolution of social behaviour is a vividand fertile field encompassing several pivotal evolu-tionary questions (Hamilton, 1964; Michener, 1969;Trivers, 1971; Lin & Michener, 1972; Wilson, 1975;Emlen, 1982; Thorne, 1997; Lehmann & Keller, 2006;Okasha, 2006; Clutton-Brock et al., 2009; Foley &Gamble, 2009; Garcia & De Monte, 2013). All of theseissues would benefit from being considered more oftenin a comparative framework (Price, Clapp & Omland,2011).

    To achieve our aim, we focus on the evolution ofsocial behaviour in cockroaches. By sampling gregari-ous, solitary, and subsocial species, we can trackbehavioural changes possibly associated with changesin social systems. Moreover, given that it is oftenclaimed that environmental conditions strongly influ-ence the evolution of social systems (Jarman, 1974;Slobodchikoff, 1984; Gautier, Deleporte & Rivault,1988; Slobodchikoff & Shields, 1988; Velicer, Kroos &Lenski, 1998; Foley & Gamble, 2009; Hatchwell,2009; Kaplan, Hooper & Gurven, 2009), we also trackbehavioural changes with regard to habitats.

    MATERIAL AND METHODSBEHAVIOURAL OBSERVATIONS AND

    BEHAVIOURAL CHARACTERS

    Thirteen species were selected, of which five were pre-viously studied (Grandcolas, 1991; Legendre, Pellens& Grandcolas, 2008a), and behavioural data were

    COCKROACH SOCIAL BEHAVIOUR 59

    2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 5877

  • gathered. We focused on the Zetoborinae subfamily,our target group for social evolution that has alreadybeen well studied in the field and laboratory (Schal,Gautier & Bell, 1984; Grandcolas, 1998; van Baarenet al., 2002, 2003a; Pellens, Grandcolas & da Silva-Neto, 2002; Pellens, Legendre & Grandcolas, 2007b;Legendre et al., 2008a), and on the Blaberinae sub-family, a closely-related group (Inward, Beccaloni &Eggleton, 2007; Pellens et al., 2007a; Djernaes et al.,2012). Within Zetoborinae, Thanatophyllum akinetumGrandcolas, 1991 is solitary (Grandcolas, 1993a) andParasphaeria boleiriana Grandcolas & Pellens, 2002 issubsocial (Pellens et al., 2002). The other Zetoborinaespecies studied are gregarious (Grandcolas, 1993a; vanBaaren et al., 2003b). Within these two subfamilies,only one other genus comprises solitary species (i.e.Hyporhicnoda, showing an independent origin ofsolitariness; Grandcolas, 1998), whereas no other sub-social genus is known. For comparison purposes, wealso studied the behaviour of four additional gregari-ous species from four different subfamilies: theDiplopterinae Diploptera punctata Eschscholtz, 1822,the Oxyhaloinae Nauphoeta cinerea Olivier, 1789, theGyninae Gyna capucina Gerstaecker, 1883, and thePycnoscelinae Pycnoscelus surinamensis Linnaeus,1758. We followed the protocol described in Legendreet al. (2008a) to record behavioural interactions andthen applied the successive event-pairing method(Legendre et al., 2008b), using both qualitative andquantitative data, to derive behavioural charactersanalyzable in a phylogenetic context.

    PHYLOGENETIC ANALYSIS

    Even though we focus on social evolution in theZetoborinae and Blaberinae subfamilies, we performeda phylogenetic analysis at the larger scale of theBlaberidae family, as a result of instability in inter-subfamilial phylogenetic relationships in the litera-ture (Maekawa et al., 2003; Inward et al., 2007; Pellenset al., 2007a). The ingroup included 33 species, and 32identified genera, sampling the 11 known subfamiliesin Blaberidae: six Zetoborinae, six Blaberinae, sixPanesthiinae, three Oxyhaloinae, three Perisphaer-iinae, two Epilamprinae, two Geoscapheinae, twoDiplopterinae, one Gyninae, one Pycnoscelinae, andone Panchlorinae. Outgroups comprised three Pseudo-phyllodromiidae and five Blattellidae, two familiespreviously inferred as being sister-groups to Blabe-ridae (Grandcolas, 1996; Inward et al., 2007), withEctobius sylvestris Poda, 1761 used as rootingoutgroup.

    Six molecular markers, for a total amount ofapproximately 6800 bp, were used to reconstructBlaberidae relationships: 12S rRNA (approximately350 bp), 16S rRNA (approximately 510 bp), 18S rRNA

    (approximately 1880 bp), 28S rRNA (approximately2200 bp), cytochrome oxidase subunit I (COI, 1210 bp),and cytochrome oxidase subunit II (COII, 683 bp). Wegenerated 183 molecular sequences, 117 of which arenew and specific to the present study, and completedour sampling with 30 sequences downloaded fromGenBank (Table 1). Primers and molecular techniqueswere described in Legendre et al. (2008c). In addition,morphological and behavioural data sets were com-piled (Table 1). Morphological characters came fromGrandcolas (1993b) and include 39 phylogeneticallyinformative characters. Behavioural characters camefrom dyadic social interactions (Legendre et al., 2008b)and include 213 phylogenetically informative charac-ters. Separate and combined phylogenetic analyseswere performed using parsimony and probabilisticmethods, which are two approaches with their ownstrengths and weaknesses (Felsenstein, 1978; Siddall,1998). The combined phylogenetic matrix is providedin the Supporting information (File S1).

    In parsimony, analyses were computed under directoptimization (Wheeler, 1996) with POY, version 4.1.1(Varn, Vinh & Wheeler, 2010). As in Legendre et al.(2008c), ribosomal sequences were preliminary alignedwith MUSCLE, version 3.6 (Edgar, 2004) and parti-tioned according to highly conserved regions (Wheeleret al., 2006), whereas protein coding genes werealigned based on the conservation of codon readingframe in SEQUENCHER, version 4.0 (Genecodes,1999), and treated as pre-aligned data in POY. Ini-tially, a combined analysis of all molecular data wasconducted with 100 replicates and tree bisectionreconection (TBR) branch swapping, followed by 400rounds of treefusing (Goloboff, 1999). A long-branchattraction (LBA) artefact was, however, suspected inthe resulting topology (see Supporting information,Fig. S1; L = 13401 steps). This artefact hypothesiswas tested and corroborated by both a Bayesiananalysis (see Supporting information, Fig. S2; lnL = 58999.58; Bergsten, 2005) and a parsimonyanalysis performed without the long-branched taxon,namely T. akinetum (see Supporting information,Fig. S3; L = 13107 steps; Siddall & Whiting, 1999).Indeed, in both cases, the phylogenetic position ofD. punctata was very different from the one shown inthe Supporting information (Fig. S1) (see alsoDiscussion). Consequently, T. akinetum molecularsequences were removed before we conducted asensitivity analysis (gap: transversions: transitions)testing four parameter sets (1:1:1, 2:1:1, 2:2:1, and4:2:1). Finally, this molecular partition was concat-enated with behavioural and morphological data torun a total evidence analysis with 100 replicates andTBR branch swapping followed by 400 treefusingrounds. Nodal support was assessed through parti-tioned Bremer values (PBV) and Jackknife supports

    60 F. LEGENDRE ET AL.

    2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 5877

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    COCKROACH SOCIAL BEHAVIOUR 61

    2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 5877

  • (JS). PBV were calculated with TREEROT, version 3(Sorenson & Franzosa, 2007), using POY impliedalignment and 100 replicates, whereas JS were calcu-lated in POY with 50% of characters removed for 1000replicates.

    In Bayesian analyses, molecular data were alignedprior to tree reconstruction with MUSCLE, version 3.6(Edgar, 2004) and analyzed, with and without morpho-logical and behavioural data. For molecular data, themost appropriate model of evolution was estimatedwith MRMODELTEST, version 2.3 (Nylander, 2004),using Akaike information criterion (Akaike, 1973;Posada & Buckley, 2004). Phenotypic (i.e. morphologyand behaviour) characters were treated as standardin MRBAYES, version 3.1.2 (Ronquist & Huelsenbeck,2003), with the Mkv model of character evolution(Lewis, 2001). Mixed-model analyses allowing differ-ent parameter variations between partitions wereperformed using MRBAYES (Ronquist & Huelsenbeck,2003; Nylander et al., 2004) and we selected the best-fitting partitioning strategy according to Bayes factorscores (Kass & Raftery, 1995; Nylander et al., 2004). Ascore above 10 was considered as a strong evidence forthe best of two models (Kass & Raftery, 1995). Wetested whether we should allow: (1) the nucleotidepartition to be subdivided according to the differentmarkers; (2) the phenotypic partition to be subdividedin morphology and behaviour partitions; (3) a gammadistribution of among rate variation for phenotypicpartitions; and (4) different parameters according tonucleotide codon positions for COI and COII.

    For Bayesian analyses, which all includedT. akinetum sequences because probabilistic phylo-genetic methods are less sensitive to LBA bias, fourchains and two runs were performed for 10 to 60millions of generations, with trees sampled every10006000 generations. We checked for convergence ofour results ensuring that the potential scale reductionfactor approached 1.0 for all parameters and that themean SD of split frequencies converged towards zero.Finally, we used TRACER, version 1.5 (Rambaut &Drummond, 2009), to check that our effective samplesize was sufficiently large for a meaningful estimationof parameters and also to assess the burn-in.

    ANCESTRAL STATE RECONSTRUCTIONS

    In parsimony, ancestral states of behavioural datawere reconstructed with WINCLADA, version 1.00.08(Nixon, 1999; command Optimizations), and we spe-cifically focused on ancestral states tied to socialcategories and habitats shifts. In other words, westudied nodes where a change in social system orhabitat occurs and checked whether these changestake place concomitantly with behavioural transfor-mations. We did not formally reconstruct ancestral

    states for social systems because, as a too broadlydefined character, it could be potentially misleading(Desutter-Grandcolas & Robillard, 2003; Grandcolas& DHaese, 2004; Robillard et al., 2006; Grandcolaset al., 2011; Avils & Harwood, 2012; Doody,Burghardt & Dinets, 2013). However, it might be usedin an exploratory approach and would suggest herethat a gregarious way of life was the ancestral con-dition for Zetoborinae. Given that T. akinetum andP. boleiriana are the only solitary and subsocialZetoborinae, respectively, changes in social system inZetoborinae would therefore occur along the terminalbranches leading to these two taxa. We thus focusedon their autapomorphies. For habitats, data origi-nated from several studies (Grandcolas, 1993a, c;Pellens et al., 2002; Pellens et al., 2007b). Finally, toevaluate whether the behavioural transformationsconcomitant with social system changes were morenumerous than expected by chance alone, we per-formed a randomization test. For this test, we gener-ated 10 000 randomized behavioural matrices, bypermuting each column independently, and parsimo-niously reconstructed ancestral states on our optimaltopology. We then computed the ratios number ofminimal and maximal autapomorphies/tree lengthfor both the solitary and subsocial species. Weobtained a random distribution for each species andcompared the values observed in our case study withthese random distributions. This randomization testwas designed with the R package phangorn 1.3.0(Schliep, 2011) and the script is provided in theSupporting information (Doc. S1).

    In a probabilistic framework, ancestral state recon-structions were performed under a Bayesian approachwith multistate as implemented in BayesTraits (Pagel,Meade & Barker, 2004; Pagel & Meade, 2007). We usedthe optimal topology and branch lengths from theBayesian analysis with the best-fitting partitioningstrategy (see above). Default parameters were usedexcept for the rate deviation parameter (ratedev = 100)to ensure reaching an adequate acceptance rate (i.e.between 20% and 40%). Ancestral states of behaviouraldata were reconstructed with a special focus on themost recent common ancestor (MRCA) of the solitaryT. akinetum and its sister-group on one hand, and ofthe MRCA of the subsocial P. boleiriana and its sister-group on the other hand. Comparing these ancestralstates with the character states found in T. akinetumand P. boleiriana, respectively, allowed us to assesstheir behavioural autapomorphies. Ancestral statereconstructions were run five times independentlywith five millions iterations each, and significantreconstructions were assumed when Bayes factorscores exceeded 2 (command fossil). Similarly, ances-tral state reconstructions were performed for habitats,using a hyperprior with an exponential distribution

    62 F. LEGENDRE ET AL.

    2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 5877

  • (command rjhp exp 0 10). The parameters of theexponential distribution were previously estimatedwith maximum likelihood analyses (Pagel & Meade,2007).

    RESULTSBEHAVIOURAL OBSERVATIONS

    Twenty-four behavioural acts were identified from thedyadic sequences of the different species (Tables 2, 3).Repertoire size ranged from 13 (D. punctata andParadicta rotunda Grandcolas, 1992) to 20 acts(P. boleiriana), with the solitary species T. akinetumhaving a medium-sized repertoire (17 acts) (Table 3).For the present study, 100 experiments were con-ducted, which correspond to the recording of 692behavioural sequences, and 56 experiments origi-nated from Grandcolas work (1991). On average,behavioural sequences were five to seven acts longbut ranged from two to 25 acts. Details about behav-ioural observations and their analysis out of aphylogenetic context will be provided elsewhere(F. Legendre, A. Gasc, M. Depraetere, P. Deleporte,R. Pellens & P. Grandcolas, unpubl. data).

    PHYLOGENETIC ANALYSIS

    The most parsimonious molecular tree in equalweighting is provided in the Supporting information

    (Fig. S3; L = 13107 steps). Blaberidae, Oxyhaloinae,and Geoscapheinae were monophyletic, whereasPanesthiinae and Zetoborinae were paraphyletic. Mostrelationships were stable to parameter changes asrevealed by Navajo rugs, apart from three successivedeep nodes and a subset within Panesthiinae.

    The total evidence analysis resulted in a singlemost parsimonious topology (L = 13968 steps; Fig. 1)quite similar to the molecular one. Blaberidaewere monophyletic with high PBV and JS values(BV = 35; JS = 100). Oxyhaloinae (BV = 35; JS = 100)and Geoscapheinae (BV = 19; JS = 100) were alsomonophyletic. Panesthiinae were paraphyletic withrespect to Geoscapheinae, Perisphaeriinae were para-phyletic as a result of the position of P. surinamensis(the single Pycnoscelinae of the study), and Zeto-borinae were paraphyletic as a result of the positionof the Blaberinae Phoetalia pallida Brunner deWattenwyl, 1865. The nested position of P. pallidawithin Zetoborinae was an unexpected but stableand highly supported result (BV = 30; JS = 100; seealso Supporting information, Fig. S3). If P. pallidais considered as effectively belonging to Zetoborinae,four out of the eight tested subfamilies were foundto be monophyletic (Blaberinae, Geoscapheinae,Oxyhaloinae, and Zetoborinae), two were paraphyle-tic (Panesthiinae and Perisphaeriinae), and twowere polyphyletic (Epilamprinae and Diplopterinae).

    Table 2. List of behaviours, with their abbreviations, displayed by the cockroaches

    Behaviours promotinginteractions (positive)

    MT Moving towards the other individualAC Antennal contact with the body of the other individualMA Mutual antennationCB Climbing onto the body of the other individual with one to six legs

    Behaviours favouring departureor a break in the interactions(negative)

    PS An individual puts its pronotum under the other and stands up suddenlyKL An individual kicks the other with one legPP An individual pushes the other with its pronotumSP Stilt posture. An individual rises on its legsSA Stilt posture combined with antennal movementSD Rapidly after a stilt posture, an individual goes downBI An individual bites the otherSJ An individual jumps suddenly towards the otherGD An individual goes downGA An individual goes down and hides its antennaeRO Rotation: turning away from the other individual (without significant

    displacement of the centre of gravity of the body)WD Withdrawal. An individual moves away from the otherWP An individual moves away from the other but stops in proximityES Escape. An individual moves quickly away from the otherWA Sudden withdrawal of the antenna(e)TP Tilt posture. An individual gives way of legs on its stimulated sideFP Freezing posture. An individual does not move at all

    Behaviours without particularsignificance

    GrA Grooming behaviour of the antennaGL Grooming behaviour of the legSQ Stands quiet. The individual stands quiet after a stimulation

    COCKROACH SOCIAL BEHAVIOUR 63

    2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 5877

  • Tab

    le3.

    Beh

    avio

    ura

    lre

    pert

    oire

    sof

    the

    13sp

    ecie

    sst

    udi

    ed

    Spe

    cies

    /beh

    avio

    ura

    lac

    tsM

    TA

    CM

    AC

    BP

    SP

    PK

    LS

    PS

    AS

    DS

    JB

    IG

    DG

    AT

    PF

    PR

    OW

    DE

    SW

    PG

    rAG

    LW

    AS

    Q

    Bla

    beru

    sd

    isco

    idal

    isX

    XX

    XX

    XX

    XX

    XX

    XX

    XX

    XD

    iplo

    pter

    apu

    nct

    ata

    XX

    XX

    XX

    XX

    XX

    XX

    XE

    ubl

    aber

    us

    dis

    tan

    tiX

    XX

    XX

    XX

    XX

    XX

    XX

    XX

    XX

    XX

    Gyn

    aca

    puci

    na

    XX

    XX

    XX

    XX

    XX

    XX

    XX

    XL

    anxo

    blat

    taem

    argi

    nat

    aX

    XX

    XX

    XX

    XX

    XX

    XX

    XX

    Nau

    phoe

    taci

    ner

    eaX

    XX

    XX

    XX

    XX

    XX

    XX

    XX

    XP

    arad

    icta

    rotu

    nd

    aX

    XX

    XX

    XX

    XX

    XX

    XP

    aras

    phae

    ria

    bole

    iria

    na

    XX

    XX

    XX

    XX

    XX

    XX

    XX

    XX

    XX

    XX

    Ph

    oeta

    lia

    pall

    ida

    XX

    XX

    XX

    XX

    XX

    XX

    XX

    XX

    XP

    hor

    tioe

    can

    imba

    taX

    XX

    XX

    XX

    XX

    XX

    XX

    XX

    Pyc

    nos

    celu

    ssu

    rin

    amen

    sis

    XX

    XX

    XX

    XX

    XX

    XX

    X

    Sch

    ult

    esia

    lam

    pyri

    dif

    orm

    isX

    XX

    XX

    XX

    XX

    XX

    XX

    XX

    XX

    XX

    Th

    anat

    oph

    yllu

    mak

    inet

    um

    XX

    XX

    XX

    XX

    XX

    XX

    XX

    XX

    X

    Abb

    revi

    atio

    ns

    ofbe

    hav

    iou

    ral

    acts

    are

    asde

    fin

    edin

    Tabl

    e2.

    64 F. LEGENDRE ET AL.

    2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 5877

  • 100

    100

    100

    100

    100

    100

    94

    96

    68

    83

    87

    91

    100

    92

    81

    92

    100

    96

    100

    90

    92

    98

    100

    100

    100

    77

    100

    87

    88

    100

    100

    100

    100

    100

    100

    100

    100

    100

    45

    35

    32

    16

    23

    25

    6

    11

    2

    4

    7

    8

    19

    10

    6

    10

    37

    9

    20

    7

    8

    10

    21

    30

    39

    10

    17

    3

    9

    23

    17

    35

    57

    39

    17

    73

    38

    41

    Panchlorinae

    Diplopterinae

    Oxyhaloinae

    Epilamprinae

    Diplopterinae

    Zetoborinae

    Blaberinae

    Gyninae

    Epilamprinae

    Pycnoscelinae

    Perisphaeriinae

    Panesthiinae

    Geoscapheinae

    Blaberinae

    Blaberidae

    Macropanesthia rhinoceros

    Geoscapheus woodwardi

    Ancaudellia shawi

    Miopanesthia deplanata

    Panesthiinae

    Panesthia cribrata

    Caeparia crenulata

    Salganea esakii

    Pseudoglomeris sp.

    Trichoblatta pygmaea

    Pycnoscelus surinamensis

    Laxta sp.

    Archimandrita tessellata

    Blaberus discoidalis

    Eublaberus distanti

    Monastria sp.

    Paradicta rotunda

    Epilampra sp.

    Gyna capucina

    Phortioeca nimbata

    Lanxoblatta emarginata

    Zetobora sp.

    Thanatophyllum akinetum

    Schultesia lampyridiformis

    Phoetalia pallida

    Parasphaeria boleiriana

    Calolampra sp.

    Rhabdoblatta formosana

    Henschoutedenia sp.

    Nauphoeta cinerea

    Gromphadorhina portentosa

    Diploptera punctata

    Panchlora nivea

    Loboptera decipiens

    Blattella germanica

    Xestoblatta cavicola

    Paratemnopteryx collonianie

    Isoldaia sp.

    Dendroblatta sp.

    Supella longipalpa

    Ectobius sylvestris

    Figure 1. Most parsimonious tree found in the analysis combining molecules (without Thanatophyllum akinetumsequences), morphology and behaviour (L = 13968; CI = 0.40; RI = 0.38). All characters and transformations were equallyweighted. Numbers above and below branches are Bremer and Jackknife support values, respectively.

    COCKROACH SOCIAL BEHAVIOUR 65

    2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 5877

  • Overall, the optimal topology was well supported, withapproximately 80% of the nodes having JS and PBVsupport above or equal to 90 and 10, respectively.

    Consistency and retention indices of the behav-ioural partition were similar to those of the molecularpartition and its normalizd PBV showed that, withmorphology, behaviour brought a strong phylogeneticsignal (Table 4).

    In a Bayesian framework, a general time reversiblemodel with a proportion of invariant sites and agamma distributed rate variation among sites wasselected for molecular data as the best fit of themodels investigated (model GTR + I + ). As for thebest-fitting partitioning strategy, the results are sum-marized in Tables 5, 6. It shows that allowing eachmarker to have its own model, taking into accountnucleotide positions in protein-coding genes, andadding a gamma-distributed rates across charactersfor phenotypic data was the best-fitting strategy (i.e.model with 12 partitions). We found the monophylyof the Blaberidae family and of Oxyhaloinae andGeoscapheinae subfamilies with maximal posteriorprobabilities (see Supporting information, Fig. S4;ln L = 62138.00). Similar to the parsimony analyses,Zetoborinae, including P. pallida, and Blaberinae sub-families were monophyletic as well. The main disa-greement between both approaches concerned deeperrelationships, most of which are poorly supported.Indeed, the Bayesian topology showed several shortinternal branches within Blaberidae. Similarly, sen-sitivity analysis revealed that the less stable nodescorresponded to inter-subfamilial relationships (seeSupporting information, Fig. S3). This disagreementbetween both methods, however, had no consequenceon our hypotheses on the evolution of social behaviourgiven that, in both cases, Zetoborinae and Blaberinaewere closely related.

    ANCESTRAL STATE RECONSTRUCTIONS:BEHAVIOUR AND SOCIALITY

    In parsimony, unambiguous ancestral state recon-structions (Fig. 2) revealed that behavioural auta-

    pomorphies range from 0 to 66. The solitary speciesT. akinetum had 19 autapomorphies, whereas thesubsocial species P. boleiriana had 66 autapomorphies.

    Thanatophyllum akinetum autapomorphies(Table 7) comprised the presence of eight and theabsence of three qualitative behavioural characters.The eight other autapomorphies were quantitativecharacters (frequences of behavioural transitions;Legendre et al., 2008b). Seven out of the eight auta-pomorphies exhibited by this solitary species werebehaviours that tend to limit interactions betweenindividuals (e.g. bite, leg kick, escape) (Table 7).

    Some P. boleiriana autapomorphies are listed inTable 7. Out of the 59 qualitative behavioural charac-ters coded present for this species, 27 were behavioursinvolving avoidance reactions, 11 were behavioursinvolving aggressive reactions, and only nine werebehaviours involving positive reactions to solicita-tions, with the 12 remaining characters being withoutobvious signification. Parasphaeria boleiriana hadthe highest number of autapomorphies, although itwas also the species with the largest repertoire,such that this result could be expected if we suspecteda correlation between repertoire richness and numberof autapomorphies. This correlation was tested andrejected (r = 0.439, P > 0.10; data not shown).

    Ancestral state reconstructions in a Bayesian frame-work gave similar behavioural autapomorphies forboth species as the parsimony reconstructions, despitetopological differences. Indeed, 75% of T. akinetum andP. boleiriana autapomorphies were shared in bothparadigms. Within the remaining 25%, only threecharacter states were significantly supported as auta-pomorphies (i.e. 4%; Bayes factor > 2). Note that, out ofthe 85 (13 + 72) qualitative behavioural charactersinferred as autapomorphies for these two species,29 were only exhibited either by T. akinetum orP. boleiriana (i.e. consistency index of 1).

    Finally, the solitary species T. akinetum did not ex-hibit more behavioural autapomorphies than expectedby chance alone (randomization tests: P = 0.962 andP = 0.986 for minimal and maximal changes, respec-tively), whereas the subsocial species P. boleiriana

    Table 4. Phylogeny-related statistics for molecular, morphological and behavioural partitions in the parsimony totalevidence analysis

    Partitions CI RI Bremer % Bremer (%) NI nPBV

    Molecules 0.37 0.31 658 82.1 1848 4.4Behaviour 0.52 0.36 123 15.4 213 7.2Morphology 0.64 0.62 20 2.5 39 6.4Total 0.38 0.32 801 100.0 2100

    CI, consistency index; RI, retention index; NI, number of informative characters; for each partition i: % Bremeri = Bremeri/ BremerTOTAL and nPBV Bremer NIi i i= (% ) .100 nPBV is a normalized PBV.

    66 F. LEGENDRE ET AL.

    2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 5877

  • did (randomization tests: P < 0.001 in both cases)(Fig. 3).

    ANCESTRAL STATE RECONSTRUCTION:BEHAVIOUR AND HABITATS

    Unambiguous behavioural character optimization wasinvestigated with regard to habitats. Even thoughhabitat is not a very precisely defined character, it canbe optimized a posteriori to tree reconstruction, andbehavioural changes occurring concomitantly withsome habitat change can be inferred. Some internalnodes had an unknown habitat state as a result of ahigh diversity in habitats and a few missing data,although two of them were studied within Zetoborinaeand Blaberinae: the nodes related to treeholes andloose bark habitats (Fig. 2). No unambiguous behav-ioural change was associated with either habitat shift.Note that, in both cases, the plesiomorphic habitat wasambiguous. Two other habitat shifts were inferred forPanesthiinae and Geoscapheinae (Fig. 2) but, becauseno species from these subfamilies was ethologicallystudied, we do not discuss these habitat shifts anyfurther.

    Behavioural comparisons between species living insimilar habitats were also performed. The sisterspecies Lanxoblatta emarginata Burmeister, 1838and Phortioeca nimbata Burmeister, 1838 both liveunder loose bark, are very similar morphologicallyand share similar repertoires (Table 3). However,each had peculiar behavioural autapomorphies(Table 8) involving proportionally more positive reac-tions for P. nimbata (approximately 43%) than forL. emarginata (approximately 33%). Species living intreeholes were even more behaviourally diverse.Eublaberus distanti Kirby, 1903 had 43 behaviouralautapomorphies, among which several involve veryTa

    ble

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    663

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    633

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    Table 6. Summary of the Bayesian analyses showingBayes factor scores used to assess the best fitting partitionstrategy

    AnalysesBayesfactor Interpretation

    A versus B 80.32 Significant = allow thesubdivision of phenotypic data

    B versus C 5839.50 Significant = allow thesubdivision of molecular data

    C versus D 35.20 Significant = add a gamma lawto the Markov k model

    D versus E 2462.10 Significant = allow subdivisionof coding gene according tonucleotide positions

    Scores above 10 are significant.

    COCKROACH SOCIAL BEHAVIOUR 67

    2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 5877

  • Nauphoeta cinerea

    Lanxoblatta emarginata

    Phortioeca nimbata

    Thanatophyllum akinetum

    Schultesia lampyridiformis

    Parasphaeria boleiriana

    Diploptera punctata

    Phoetalia pallida

    Rhabdoblatta formosana

    Zetobora sp.

    Calolampra sp.

    Ectobius sylvestris

    Blattella germanica

    Dendroblatta sp.

    Gromphadorhina portentosa

    Henschoutedenia sp.

    Isoldaia sp.

    Loboptera decipiens

    Panchlora nivea

    Paratemnopteryx collonianie

    Supella longipalpa

    Xestoblatta cavicola

    Pycnoscelus surinamensis

    Eublaberus distanti

    Blaberus discoidalis

    Gyna capucina

    Paradicta rotunda

    Panesthia cribrata

    Epilampra sp.

    Monastria sp.

    Ancaudellia shawi

    Archimandrita tessellata

    Caeparia crenulata

    Geoscapheus woodwardi

    Laxta sp.

    Macropanesthia rhinoceros

    Miopanesthia deplanata

    Panesthiinae

    Pseudoglomeris sp.

    Salganea esakii

    Trichoblatta pygmaea

    45

    2

    0

    6620

    54

    0

    0

    00

    0

    0

    2219

    1943

    00

    24

    430

    0

    15

    00

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    0

    11

    19

    00

    0

    0

    solitary

    Social systems:

    solitary

    gregarious

    solitary?

    solitary/gregarious

    solitary

    gregarious

    solitary

    gregarious

    gregarious

    gregarious

    gregarious

    gregarious

    gregarious

    gregarious?

    gregarious

    ?

    subsocial

    ?

    ?

    ?

    ?

    ?

    gregarious

    gregarious

    gregarious

    gregarious

    solitary

    solitary

    ?

    gregarious

    gregarious

    gregarious

    subsocial

    subsocial

    gregarious

    gregarious

    ?

    gregarious?

    ?

    subsocial

    ?

    ?

    ?

    ?

    ?

    ?

    ?

    litter

    Habitats:

    litter

    litter

    litter

    litter

    litter

    bird nests

    litter

    treeholes

    treeholes

    treeholes

    treeholes

    treeholes

    mould

    loose bark

    loose bark

    dead wood, loose bark

    dead wood

    epiphytes

    dead wood

    dead wood

    dead wood

    dead wood

    loose bark

    loose bark

    under dead branches

    treeholes

    cortical

    cortical

    treeholes

    dead wood

    dead wood

    inside soil

    inside soilParsimony analyses

    Bayesian analyses

    Habitat Ancestral State Reconstructions:

    Figure 2. Unambiguous ancestral state reconstructions of behavioural data on the most parsimonious tree withinformation about habitats and social systems. The species whose behaviour was studied are shown in black. Numberson branches represent the number of unambiguous behavioural changes. Large arrows point at nodes with habitatchanges in parsimony. Pie diagrams illustrate the probability associated with these habitat changes in Bayesianreconstructions.

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  • aggressive behaviours (jump SJ; pronotal attack PS; push with pronotum PP) (Table 8), whereasBlaberus discoidalis Serville, 1838 showed no unam-biguous behavioural autapomorphy. As for P. rotunda,it had few autapomorphies (N = 15), most of whichwere the absence of some behavioural transitions.

    DISCUSSIONBEHAVIOURAL DATA IN PHYLOGENETICS AND THE

    SUCCESSIVE EVENT-PAIRING METHOD

    When the successive event-pairing method was pro-posed, it was conceptually defined and applied to anillustrative case study involving five species (Legendreet al., 2008b). In the present study, we extend thisdataset and show that the method remains operationaland efficient with this larger sampling. First, behav-ioural characters defined with the successive event-pairing method are no more homoplastic thantraditional characters as revealed by their consistencyand retention indices. Second, these behavioural data

    bring a substantial signal for tree reconstruction witha high normalized Bremer support. Thus, the presentstudy shows once again that behavioural characterscan be valuable phylogenetic characters (Wenzel, 1992;de Queiroz & Wimberger, 1993; Proctor, 1996; Brooks& McLennan, 2002; Cap, Aulagnier & Deleporte,2002). This property has already been mentioned forstereotyped behaviours (de Queiroz & Wimberger,1993; Robillard et al., 2006) but never for charactersderived from nonstereotyped behavioural sequencessuch as those used here.

    Most interestingly, the successive event-pairingmethod allows testing and proposing detailed hypo-theses in the evolution of behaviour as exemplifiedhere with the social behaviour of Zetoborinae andBlaberinae cockroaches. We focused on a few species toassess their behavioural peculiarities in a phylogeneticcontext. These species were selected either given theirsocial systems (the solitary species T. akinetum andthe subsocial species P. boleiriana) or their habitats(species living in treeholes and under loose bark).

    Table 7. List of behavioural autapomorphies of the solitary and subsocial species

    Autapomorphic behavioural transitions coded for Thanatophyllum akinetum: a solitary species

    Present MT (moving toward)/BI (bite)AC (antennal contact)/KL (leg kick)KL (leg kick)/AC (antennal contact)SA (stilt + antennation)/WP (light withdrawal)BI (bite)/ES (escape)RO (rotation)/KL (leg kick)WP (light withdrawal)/GA (go down and hide antennae)SQ (stands quiet)/GA (go down and hide antennae)

    Absent AC (antennal contact)/SP (stilt posture)SP (stilt posture)/WD (withdrawal)WP (light withdrawal)/WD (withdrawal)

    The most relevant autapomorphic behavioural transitions coded for Parasphaeria boleiriana: a subsocial species

    Present MT (moving toward)/TP (tilt posture)MT (moving toward)/GA (go down and hide antennae)PP (push with pronotum)/PP (push with pronotum)PP (push with pronotum)/KL (leg kick)PP (push with pronotum)/TP (tilt posture)KL (leg kick)/PP (push with pronotum)KL (leg kick)/TP (tilt posture)SP (stilt posture)/GD (go down)SP (stilt posture)/WP (light withdrawal)SP (stilt posture)/ES (escape)TP (tilt posture)/PP (push with pronotum)GD (go down)/KL (leg kick)ES (escape)/ES (escape)

    Autapomorphies found only in parsimony analysis are shown in normal type. Autapomorphies found only in Bayesiananalysis are shown in italics Autapomorphies found in both parsimony and Bayesian analyses are shown in bold.

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  • SOLITARINESS, SUBSOCIALITY, ADAPTATION, ANDPHYLOGENETIC INERTIA

    The shifts from gregariousness to solitariness orsubsociality imply the loss or gain of key features(tolerance to conspecifics and parental care, respec-tively) and related behaviours (Wilson, 1971). In thiscontext, we would expect either numerous behav-ioural changes concomitant to these shifts in socialsystems or at least a few but highly significant behav-ioural changes in species interactions.

    Because aggregation behaviour can be explained interms of interactions between individuals (Jeansonet al., 2005), solitariness could thus be explained byspecific behaviours, including aggressions, whichwould favour spacing among conspecifics (King, 1973).Previous studies (Grandcolas, 1991; Legendre et al.,2008a) showed that the solitary species T. akinetumhas a lower tolerance to conspecifics compared to

    closely-related gregarious species, with individualspassively spacing themselves out instead of remainingaggregated. However, ancestral state reconstructionsof behavioural data show that T. akinetum has only 19behavioural autapomorphies, which is similar to themean number observed for all the species studied, andthat its repertoire does not include additional aggres-sive behavioural acts. Therefore, T. akinetum has notevolved solitary habits by deeply changing its behav-iour, and aggressive behaviours by themselves cannotexplain its solitary way of life. Previous studies alreadyfailed to demonstrate a causal link between aggres-siveness and solitariness in cockroaches in broad butnonphylogenetic species comparisons (Breed, Hinkle &Bell, 1975; Bell et al., 1979; Gorton & Gerhardt, 1979).Given the lack of significant behavioural differentia-tion, evolution toward solitariness in T. akinetumwould have involved a common ancestral repertoireused in a slightly different way, and not have resultedfrom dramatic changes in behavioural interactions.A close look at behavioural transitions shows that mostof T. akinetum autapomorphies are related to actslimiting interactions and that dyadic interactions wereless often initiated with the act moving toward aconspecific than for other species, but instead resultedgenerally from fortuitous encounters. In this species,individuals do not refuse interactions (Legendre et al.,2008a) but they do not look for them either. Thus,solitariness would be explained by a simple lack ofintraspecific attraction, except for reproduction pur-poses. In the field, individuals disperse away immedi-ately after hatching so that conspecific interactions arerare, as already suggested by a 2-month field study(Grandcolas, 1993a). Given such dispersal habits,behavioural acts favouring social interactions areprobably not expressed in the field and hence wouldnot be submitted to strong selection. In other words,they cannot be counter-selected, if we consider that thecost of their cognitive maintenance is insignificant.Such evolution of solitariness would fit the notion ofphylogenetic inertia (phylogenetic constraint sensuMcKitrick, 1993, or stasis sensu Schwenk, 1995)because solitariness did not come with numerous oroutstanding behavioural changes. Even though soli-tariness in Amazonian forest litter can be seen asadvantageous to face predation pressures for instance(e.g. from army ants; Grandcolas & Deleporte, 1994;Grandcolas, 1998), the potential of T. akinetum forsocial activity is mainly characterized by nonfunc-tional plesiomorphic character states and thus cannotbe considered as an adaptation (Coddington, 1988;Deleporte, 2002; Grandcolas & DHaese, 2003).

    For subsociality, P. boleiriana is behaviourally themost autapomorphic of all species studied. The occur-rence of such a high number of autapomorphies fits amodel of evolution where a change in social system

    Distribution of minimal changes

    normalised number of changes

    0.00 0.02 0.04 0.06 0.08 0.10

    020

    4060

    Distribution of minimal changes

    normalised number of changes

    0.00 0.02 0.04 0.06 0.08 0.10

    010

    3050

    P = 0.962

    P < 0.001

    Thanatophyllum akinetum

    Parasphaeria boleiriana

    Freq

    uenc

    yFreq

    uenc

    y

    Figure 3. Result of the randomization test showing thatthe solitary species Thanatophyllum akinetum (top) hasfew behavioural autapomorphies. The random distribu-tion (histogram) reveals that a higher number of auta-pomorphies than the one observed for T. akinetum (greydash line) might be reached by chance (P = 0.962). Bycontrast, the probability that the subsocial speciesParasphaeria boleiriana (bottom) shows so many behav-ioural autapomorphies by chance is extremely low(P < 0.001). For both species, the results are similar whenmaximal number of changes are considered (P = 0.986 andP < 0.001, respectively; data not shown).

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  • comes with numerous changes in social interactions.These behavioural changes could also result fromusing a very peculiar habitat (galleries in dead wood)because it is the only xylophagous and wood-livingspecies behaviourally studied so far in this group.In this habitat hypothesis, the numerous auta-pomorphies observed in this species could be secondaryadaptations (sensu Gould & Vrba, 1982), such as tiltand stilt postures (Legendre et al., 2008b). Thesepostures probably reduce the possibility of beingpassed by a conspecific in a gallery, which could beadvantageous for food or shelter access. Behaviouralstudies on other xylophagous species or on speciesliving in dead wood (e.g. Panchlora spp., Cryptocercusspp., Panesthiinae) could help to assess the relativeimpact of this habitat on sociality and behaviourevolution (Park, Grandcolas & Choe, 2002; Bell, Roth& Nalepa, 2007). Eventually, they would allow refine-ment of the role of the different evolutionary forcesacting on the evolution of cockroach sociality, as wasthe case in other organisms (Clutton-Brock, 2009;Foley & Gamble, 2009; Hatchwell, 2009; Keller,2009).

    For both T. akinetum and P. boleiriana, our resultswould obviously gain from supplementary replicates(closely-related species with the same habitat andsocial system) to allow any generalization, althoughsuch species are unknown. This lack of replication isa recurrent limitation of any homology approach(sensu Winkler, 2000), which nonetheless offers strongopportunities in evolutionary biology (Weber &Agrawal, 2012).

    ECOLOGICAL PRESSURES AND SOCIAL EVOLUTION

    Blaberidae, and cockroaches in general, use a diver-sity of habitats (Bell et al., 2007). Seven differenthabitats are used by the 13 species investigated in thepresent study, which limits both intrahabitat com-parisons and the establishment of detailed evolution-ary scenarios. Indeed, the most ancestral habitats areambiguous as a result of this high diversity. Nonethe-less, two habitat changes can be inferred: towardloose bark and toward treeholes. Our study suggeststhat these changes do not necessarily imply manybehavioural modifications because these habitat

    Table 8. Behavioural differences despite similar habitats

    The most relevant autapomorphic behavioural transitions coded for Lanxoblatta emarginata and Phortioeca nimbata:two species living under loose bark

    Present (L. emarginata) MT (moving toward)/SP (stilt posture)SP (stilt posture)/AC (antennal contact)SA (stilt + antennation)/CB (climbing)SA (stilt + antennation)/GA (go down and hide antennae)SD (stilt then go down)/RO (rotation)RO (rotation)/SP (stilt posture)WP (light withdrawal)/MA (mutual antennation)WP (light withdrawal)/SA (stilt + antennation)WP (light withdrawal)/GD (go down)

    Present (P. nimbata) SP (stilt posture)/CB (climbing)SA (stilt + antennation)/MT (moving toward)GD (go down)/MT (moving toward)GA (go down and hide antennae)/SP (stilt posture)WD (withdrawal)/GD (go down)GL (leg grooming)/RO (rotation)

    The most relevant autapomorphic behavioural transitions coded for Eublaberus distanti: a species living in treeholes

    Present AC (antennal contact)/PS (pronotal attack)AC (antennal contact)/SJ (jump)MA (mutual antennation)/PS (pronotal attack)MA (mutual antennation)/SJ (jump)CB (climbing)/PP (push with pronotum)SJ (jump)/GD (go down)PP (push with pronotum)/PP (push with pronotum)PS (pronotal attack)/WP (light withdrawal)

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  • transitions involve no unambiguous and concomitantchange in behavioural characters. This result sup-ports the idea that habitat does not play a strong rolein Zetoborinae behavioural and social evolution, asalready suggested (Grandcolas, 1998).

    Intrahabitat comparisons reveal that, even thoughL. emarginata and P. nimbata share similar reper-toires and behavioural activities (Legendre et al.,2008a), they also have their own behavioural auta-pomorphies. These results are consistent with theconclusions of van Baaren et al. (2002), who qualifiedP. nimbata as a species more gregarious thanL. emarginata. Indeed, we find that P. nimbataautapomorphies include proportionally more behav-ioural transitions favouring social interactions (i.e.behavioural answers that do not lead to stopping orlimiting interactions) than those of L. emarginata.Behavioural differences between species sharingsimilar habitats are even more pronounced betweenE. distanti and B. discoidalis, a result that has alsobeen shown in adult interactions (Gautier & Forast,1982). These outcomes call for moving toward theuse of detailed behavioural studies in social evolu-tion rather than the early broadly defined socialcategories (e.g. gregarious), as already advocatedelsewhere (Desutter-Grandcolas & Robillard, 2003;Grandcolas & DHaese, 2004; Robillard et al., 2006;Grandcolas et al., 2011; Avils & Harwood, 2012;Doody et al., 2013).

    BLABERIDAE PHYLOGENETICS

    Zetoborinae is a monophyletic Neotropical group ofcockroaches belonging to the Blaberidae family,although its phylogenetic position within the family isnot clearly established, with some incongruencebetween several morphological and molecular studies(Grandcolas, 1993b, 1998; Grandcolas & DHaese,2001; Maekawa et al., 2003; Inward et al., 2007;Pellens et al., 2007a; Roth et al., 2009; Djernaes et al.,2012). On the basis of various morphological andbehavioural characters, McKittrick (1964) defined theBlaberidae for the first time. At that time, the rela-tionships between subfamilies were not yet establishedcladistically, and she did not use any formal method-ology, so that several groups were para- or polyphyletic(Grandcolas, 1996). Particularly, in her Blaberodcomplex comprising Panesthiinae, Zetoborinae, andBlaberinae, the latter subfamily was paraphyletic. In acladistic analysis based on morphology, Grandcolas(1993b) defined Zetoborinae and Blaberinae subfami-lies as two monophyletic sister-taxa. Later, fourmolecular studies dealt with Blaberidae phylogeneticsusing very diverse taxon samples of Zetoborinaeand Blaberinae (Grandcolas & DHaese, 2001;Maekawa et al., 2003; Inward et al., 2007; Pellens

    et al., 2007a). Although both subfamilies were oftenclosely related, the comparison of the three mostrecent topologies reveals that they share only tworesults: monophyly of the Blaberidae family and ofthe clade (Geoscapheinae + Panesthiinae). This com-parison highlights the instability in Blaberidaephylogenetics, especially in inter-subfamilial rela-tions, as well as the need for further phylogeneticanalyses of this group.

    Thus, Blaberidae relationships were reconstructedin the present study from molecular, morphological,and behavioural characters to obtain a phylogeneticassumption as robust as possible for investigatingsocial evolution in Zetoborinae (Grandcolas et al.,2001). To our knowledge, this is the first molecularstudy of this cockroach family testing the monophylyof eight out of the eleven subfamilies.

    The phylogenetic analysis with all molecular dataresulted in a single most parsimonious tree (see Sup-porting infromation, Fig. S1), wherein D. punctata(Diplopterinae) was nested within (Blaberinae +Zetoborinae) as sister-taxon to the ZetoborinaeT. akinetum. This result is surprising and makes littlesense from both morphological and biogeographicalperspectives. Indeed, Blaberinae and Zetoborinae areexclusively Neotropical, whereas D. punctata lives inthe Indo-Pacific region. Similarly, Blaberinae andZetoborinae are each characterized by very peculiargenitalia characters (Roth, 1970a, b; Grandcolas, 1991,1993b) that they do not share with D. punctata. A LBAartefact was thus suspected and corroborated, on theone hand, by the topology obtained when T. akinetumwas removed, with D. punctata then found as sister-taxon to the Malagasy Oxyhaloinae (see Supportinginformation, Fig. S3), and, on the other hand, by thetopology obtained in Bayesian inference (see Support-ing information, Fig. S2).

    The phylogenetic position of P. pallida is anothersurprising result. Phoetalia pallida exhibits appar-ently typical Blaberinae genitalia with a complexseries of spine rings (Roth, 1970b) and other sub-familial morphological synapomorphies (Grandcolas,1993b). Yet, it is constantly associated with Zeto-borinae species in our phylogenetic analyses, whichwould support an outstanding case of convergence ingenitalia morphological evolution between P. pallidaand Blaberinae species.

    Despite these two surprising results, our combinedanalysis supports the monophyly of Blaberidae and offour subfamilies as previously considered in phylo-genetic systematics, if Phoetalia is considered as aZetoborinae. In addition, the clade (Geoscapheinae +Panesthiinae) is also well-supported as monophyletic.By contrast, our results disagree with current tax-onomy about Epilamprinae and Diplopterinae, withthe former subfamily being under-sampled here and

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  • already known to be phylogenetically and taxonomi-cally heterogeneous (Roth, 1971). Inter-subfamilialrelationships are less stable and supported by shortbranches. These short internal branches could eitherresult from a fast diversification or from a lack ofappropriate data to document this period of Blaberidaediversification. Similar to previous analyses, our sam-pling does not allow this question to be answered, thusprompting the need for further investigations.

    Nevertheless, our combined approach with molecu-lar, morphological, and behavioural data derived fromthe successive event-pairing method (Legendre et al.,2008b) allows a thorough investigation of the evolutionof social behaviour within Zetoborinae and Blaberinae,and provides the most documented phylogenetichypothesis for the lineage under study. This calls forintegrative approaches in phylogenetics, in the sensethat as many relevant characters as possible should beintegrated into the phylogenetic matrix (Grandcolaset al., 2001) to obtain a robust topology for testingevolutionary hypotheses. Diversifying sources ofphylogenetic characters will presumably increase thechance of obtaining strong phylogenetic support acrossthe whole topology. In this context, the successiveevent-pairing method represents a suitable way ofintegrating behavioural data in phylogenetic analyses.

    CONCLUSIONS

    In the present study, we demonstrate the usefulnessof the successive event-paring method in phylogeneticanalyses. With this method, behavioural data fromnonstereotyped behavioural sequences bring substan-tial information to the reconstruction of phylogenetictrees and the investigation of the evolution of behav-iour. In our case study, shifting from gregariousnessto solitariness does not imply numerous or outstand-ing changes in behavioural repertoires and dyadicbehavioural interactions. Conversely, shifting fromgregariousness to subsociality comes with numerousbehavioural changes. These results are achieved as aresult of a homology approach (sensu Winkler, 2000)and show that, as recently suggested (Price et al.,2011), phylogenetic approaches in behaviour investi-gation are useful for deciphering behaviour evolutionand discriminating between its different evolutionarymodalities. Also, numerous behavioural studies oncockroaches have focused on aggressiveness (Gautier& Forast, 1982; van Baaren et al., 2007), notablywith the aim of studying the dominance hierarchy indiverse social systems. Here, the 13 species observedshow a high level of aggressiveness, which suggeststhat aggressiveness is a plesiomorphic and wide-spread condition in this clade. Consequently, aggres-sion would not be that decisive in Blaberidae socialevolution and future studies might focus on solicita-

    tion and tolerance behaviours to investigate the evo-lution of sociality in this group.

    ACKNOWLEDGEMENTS

    This study was developed during the course of a PhDgranted by French Ministre de la Recherche to FL.Molecular work was carried out partly in MichaelWhitings laboratory (Brigham Young University,Provo) and partly in Ward Wheelers laboratory(American Museum of Natural History, New York). Itwas supported by the Programme Pluri-Formation(PPF) Etat et structure phylogntique de labiodiversit actuelle et fossile directed by PhilippeJanvier (FL), by NSF DEB-0120718 (MFW) and by aNASA postdoctoral fellowship through the AMNH(CAD). The foregoing PPF also supported a field tripto French Guiana where FL and PG collected livingspecimens. Most of the phylogenetic analyses werecarried out using the resources of the ComputationalBiology Service Unit from the Museum nationaldHistoire naturelle (MNHN, Paris), which was par-tially funded by Saint Gobain. We thank three anony-mous reviewers for their helpful comments. We alsothank Herv Amat and Station Biologique dePaimpont for providing help and facilities for behav-ioural observations, as well as Odette Morvan andJean Cerda for their assistance in French Guiana. KSwas supported by the Musum national dHistoirenaturelle.

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    SUPPORTING INFORMATION

    Additional Supporting Information may be found in the online version of this article at the publishers web-site:

    Figure S1. Most parsimonious tree (L = 13401) obtained from the complete molecular data set in equalweighting. Note the dubious position of Diploptera punctata within (Zetoborinae + Blaberinae).Figure S2. Result of the Bayesian analysis including all molecular data (ln L = 58999.58). Model GTR + I + ,with subdivision of protein coding gene according to nucleotide positions. Note that Diploptera punctata does notbelong anymore to (Blaberinae + Zetoborinae).Figure S3. Most parsimonious tree obtained from the molecular data (without Thanatophyllum akinetum)in equal weighting (L = 13107). Sensitivity analyses are displayed as Navajo rugs (black = monophyly;grey = paraphyly; white = polyphyly). Note that Diploptera punctata is not nested anymore within Zetoborinae.Figure S4. Result of the Bayesian analysis combining molecular, morphological and behavioural data (analysisE; for models used, see Table 5). Note the short internal branches within Blaberidae.Doc S1. Phangorn_script.doc. Script used in Phangorn 1.3.0 for the randomization test.File S1. Phylogenetic_matrix.nex. Phylogenetic matrix including behavioural, morphological, and moleculardata.

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