doi 10.1098/rspb.2000.1417 Intrasexual selection predicts the evolution of signal complexity in lizards Terry J. Ord1*,DanielT.Blumstein1,2,3 and Christopher S. Evans2 1Department of Biological Sciences, and 2Department of Psychology, Macquarie University, Sydney, NSW 2109, Australia 3Department of Organismic Biology, Ecology and Evolution, University of California, Los Angeles, CA 90095-1606, USA Sexual selection has often been invoked in explaining extravagant morphological and behavioural adap- tations that function to increase mating success. Much is known about the e¡ects of intersexual selection, which operates through female mate choice, in shaping animal signals. The role of intrasexual selection has been less clear. We report on the ¢rst evidence for the coevolution of signal complexity and sexual size dimorphism (SSD), which is characteristically produced by high levels of male^male competition. We used two complementary comparative methods in order to reveal that the use of complex signals is asso- ciated with SSD in extant species and that historical increases in complexity have occurred in regions of a phylogenetic tree characterized by high levels of pre-existing size dimorphism. We suggest that signal complexity has evolved in order to improve opponent assessment under conditions of high male^male competition. Our ¢ndings suggest that intrasexual selection may play an important and previously under- estimated role in the evolution of communicative systems. Keywords: sexual selection; sexual size dimorphism; visual communication; signal complexity; evolution; the comparative method In many taxa, competition between males over 1. INTRODUCTION resources characteristically produces an asymmetry in The extraordinary diversity of animal signals has body size between the sexes. Thus, the advantages of fascinated biologists since Darwin (1872; Hauser 1996; larger size for males typically results in sexual size Bradbury & Vehrencamp 1998). Complex signals are dimorphism (SSD). In iguanian lizards, the success of known to have evolved in response to sexual selection males competing for territories and other resources is (Andersson 1994), properties of the signalling environ- positively correlated with body size (Greenberg & Noble ment (Endler 1992), predation risk (Stoddard 1999) and 1944; Rand 1967; Jenssen 1970b; Trivers 1972, 1976; social organization (Blumstein & Armitage 1997). Recent Stamps 1977, 1983; Ruby 1978, 1984; Schoener & Schoener studies have particularly focused on the role of intersexual 1980, 1982; Tokarz 1985; Cooper & Vitt 1987; Anderson selection. The cumulative e¡ects of female mate choice & Vitt 1990; Baird et al. 1997; Johnston 1997; Jenssen & decisions have caused profound changes in signal struc- Nunez 1998). Male^male competition is thus the predo- ture, producing elaborate ornaments (Basolo 1990; minant factor in£uencing the evolution of larger-male Andersson 1994; Endler & Basolo 1998) and complex SSD (Trivers 1976; Schoener & Schoener 1980; Stamps vocalizations (Ryan 1998; Collins 1999). Much less is 1983; Vitt 1983; Carothers 1984; Vitt & Cooper 1985; known about the role of intrasexual selection. Anderson & Vitt 1990; Hews 1990; Perry 1996; Baird Agamid and iguanid lizards primarily communicate et al. 1997; Johnston 1997; Stamps et al. 1997; Wikelski & using visual displays. These are composed of discrete Trillmich 1997) and this measure provides an estimate of movements, often delivered in a predictable sequence, the historical level of competitive intensity. together with characteristic postures and changes in body Jenssen (1978) speculated that large display repertoires coloration. Exchanges of such signals between males are should reduce the risk of injury for lizards when male^ an important component of territory defence (Carpenter male agonistic interactions are frequent. If the outcome of 1978). Signal complexity varies across species and is such contests is also in£uenced by signal complexity, as quanti¢ed by the number of modi¢ers added to a basic has been demonstrated in birds (Krebs et al. 1978), then head-nod or push-up display (Jenssen 1977, 1978). Modi- we should expect complex signals to evolve with ¢ers include dewlap extensions, tail wagging, arm increasing SSD. In the present study, we tested this waving, crest raising, body compression/in£ation, back prediction by exploring whether the degree of intrasexual arching, body raising/tilting and changes in colour. selection in lizards, as estimated by SSD, predicts the Variation in modi¢er use determines function and in£u- evolution of signal complexity, as measured by repertoire ences the outcome of social interactions (Jenssen 1977; size. Martins 1991). Signalling behaviour is known to a¡ect the ¢tness of the sender because it is important in both male^ male contests (Trivers 1976) and female mate choice 2. METHODS (Jenssen 1970a). However, the considerable variation We ¢rst examined all available published accounts of SSD between species in repertoire size remains unexplained. and signal behaviour for iguanian lizards (205 sources covering 133 species). The subset of accounts providing complete informa- tion on both signal complexity and SSD (see electronic *Author for correspondence ([email protected]). Appendix A available on The Royal Society's Web site) was Proc. R. Soc. Lond. B(2001)268,737^744 737 & 2001 The Royal Society Received 11 September 2000 Accepted 22 November 2000 738 T. J. Ord and others The evolution ofsignal complexity in lizards identi¢ed (117 sources covering 63 species) from this larger data Table 1. The correlation of SSD and repertoire size in set (T. J. Ord, unpublished data). Visual displays of iguanian iguanian lizards lizards are principally performed by males and invariably consist of stereotyped head and body movements commonly one-tailed termed `head-nod' and/or `push-up' displays. These `core' displays species data d.f. r p-value are elaborated by the addition of modi¢ers (Jenssen 1977, 1978), which vary across species and account for a considerable propor- raw 62 0.36 0.002 tion of display diversity.We therefore used the number of display corrected for body size 62 0.37 0.001 modi¢ers reported for each species in order to quantify signal independent contrasts 52 0.29 0.018 complexity. While our hypothesis explicitly focuses upon male^ (polytomies unresolved) male signal exchanges, some modi¢ers are also reported to be corrected for body size 52 0.27 0.026 independent contrasts 62 0.29 0.011 employed during courtship. SSD was determined from compari- (polytomies randomly resolved) sons of male:female snout^vent length. Values of 1 thus indicate corrected for body size 62 0.27 0.016 sexes of equal size, those greater than 1 larger-male SSD and those less than 1 larger-female SSD. (1996). Species within Sceloporus were positioned by Wiens (a) Calculation of standardized independent & Reeder (1997). We could ¢nd no published hypothesis contrasts for Microlophus. In order to account for possible phylogenetic non-independence of species data, we gathered additional published data on phylo- geny and calculated standardized independent contrasts (Purvis While independent contrasts can be calculated from trees & Rambaut 1995). possessing polytomies (i.e. where the precise relationship No single, published, phylogenetic hypothesis included all between species is unknown), we also wished to compare species of interest, so a composite tree was compiled from contrast-based results with those from the concentrated changes several sources (see electronic Appendix A). In some cases, test (CCT) (see below). For this purpose, we conducted addi- several phylogenetic hypotheses were available. We `ranked' tional analyses by randomly resolving polytomies using hypotheses with those based on combined morphological and MacClade software v. 3.08a (Maddison & Maddison 1992, molecular data favoured over purely molecular hypotheses, 1999). which were in turn preferred over purely morphological hypo- Standardized independent contrasts are a common way of theses. While trees constructed from molecular data are not controlling for phylogenetic non-independence. We used the pro- necessarily superior to those based solely on morphology and, gram CAIC, v. 2.6.2 (http://evolve.bio.ic.ac.uk/evolve/software/ indeed, may su¡er from their own uncertainty problems (see caic/index.html) (see also Purvis & Rambaut 1995) to calculate Wiens & Hollingsworth 2000), those based on molecular data contrasts, which were then used in regression analyses. Data on tended to be the more recently proposed hypotheses and were branch lengths (which represent time since speciation) were only thus favoured. If hypotheses were still equally ranked, those available for a small subset of species. In order to include the based on parsimony methods of tree construction were given maximum number of species in our analyses, we set all branch preference. Species synonyms were checked using the `EMBL lengths to be equal.We selected the `Crunch'algorithm for contrast Reptile Database' (http://www.embl-heidelberg.de/uetz/living analyses. Regressions were forced through the origin following reptiles.html). Purvis &Rambaut(1995) (seealsoGarland etal.1992). Using these criteria, the following sources were used to SSD in lizards is associated with overall body size (Stamps construct a composite phylogenetic hypothesis. 1983).Usingadditionalpublisheddata (seeelectronic Appendix A), contrasts for body size (male snout^vent length) were regressed