Ornament Evolution in Dragon Lizards: Multiple Gains and Widespread Losses Reveal a Complex History of Evolutionary Change
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UC Davis UC Davis Previously Published Works Title Ornament evolution in dragon lizards: multiple gains and widespread losses reveal a complex history of evolutionary change Permalink https://escholarship.org/uc/item/38r8200z Journal Journal of Evolutionary Biology, 19(3) ISSN 1010-061X Authors Ord, T J Stuart-Fox, D Publication Date 2006-05-01 Peer reviewed eScholarship.org Powered by the California Digital Library University of California doi:10.1111/j.1420-9101.2005.01050.x Ornament evolution in dragon lizards: multiple gains and widespread losses reveal a complex history of evolutionary change T. J. ORD*&D.STUART-FOX *Section of Evolution and Ecology, University of California, Davis, USA School of Animal, Plant and Environmental Science, University of the Witwatersrand, Wits, South Africa Keywords: Abstract Agamidae; The expression in females of ornaments thought to be the target of sexual comparative methods; selection in males is a long-standing puzzle. Two main hypotheses are ecological constraint; proposed to account for the existence of conspicuous ornaments in both sexes genetic correlation; (mutual ornamentation): genetic correlation between the sexes and sexual lizard; selection on females as well as males. We examined the pattern of ornament ornaments; gains and losses in 240 species of dragon lizards (Agamidae) in order to phylogenetic reconstruction; elucidate the relative contribution of these two factors in the evolution of sexual dimorphism; mutual ornamentation. In addition, we tested whether the type of shelter used sexually selected traits. by lizards to avoid predators predicts the evolutionary loss or constraint of ornament expression. We found evidence that the origin of female ornaments is broadly consistent with the predictions of the genetic correlation hypothesis. Ornaments appear congruently in both sexes with some lineages subsequently evolving male biased sexual dimorphism, apparently through the process of natural selection for reduced ornamentation in females. Nevertheless, orna- ments have also frequently evolved in both sexes independently. This suggests that genetic correlations are potentially weak for several lineages and sexual selection on females is responsible for at least some evolutionary change in this group. Unexpectedly, we found that the evolutionary loss of some ornaments is concentrated more in males than females and this trend cannot be fully explained by our measures of natural selection. 2000b). The prevailing view is that sexual selection acts Introduction on males to produce male biased sexual dimorphism. The Males of many animals use exaggerated physical fea- widespread occurrence of ornamentation in both sexes is tures, or ornaments, as sexual advertisements or signals therefore puzzling, but surprisingly few studies have during aggressive encounters. Such ornaments include examined this phenomenon. Furthermore, traditional the spectacular plumage of many birds (e.g. Andersson emphasis has been on explaining the evolutionary gain et al., 2002) and the elongated tail filaments and dark of ornamental traits targeted by sexual selection in males. vertical bars exhibited by many fishes (e.g. Basolo, However, a growing number of studies are showing that 1990,1991; Moretz & Morris, 2003). The origin of such many sexually selected traits are often lost more times elaborate ornamentation is a topic of long-standing than they have evolved (reviewed in Wiens, 2001). This interest to biologists. Sexual selection (Darwin, 1874) is trend is taxonomically widespread (e.g. insects – Emlen widely believed to be the driving force behind the et al., 2005; fish – Basolo, 1996; amphibians – Emerson, evolution of most extravagant male traits. Yet, structures 1996; lizards – Wiens, 1999; Quinn & Hews, 2000; birds – assumed to be exclusively selected for in males are also O¨ deen & Bjo¨ rklund, 2003; de Kort & Ten Cate, 2004) but frequently observed in females (reviewed in Amundsen, remains largely unexplained (Wiens, 2001). Two main hypotheses are proposed to account for the Correspondence: T.J. Ord, Section of Evolution and Ecology, University of California, Davis, One Shields Avenue, Davis, CA 95616-8755, USA. existence of conspicuous ornaments in both sexes: Tel.: +1 530 752 3075; fax: +1 530 752 1449; genetic correlation between the sexes (e.g. Lande, e-mail: [email protected] 1980) and/or sexual selection on females as well as ª 2005 THE AUTHORS 19 (2006) 797–808 JOURNAL COMPILATION ª 2005 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 797 798 T. J. ORD AND D. STUART-FOX males (e.g. Amundsen, 2000a,b). Darwin realized that gular sacs, nape/dorsal crests, fleshy spines/horns and many of the structures he postulated to have evolved as a rostral appendages (Fig. 1) that are extended or exag- consequence of sexual selection on males were also gerated through posturing during territorial disputes expressed in females. He explained this phenomenon and may also provide cues during mate choice through a process of ‘inheritance’ in which traits selected (Darwin, 1874; Carpenter & Ferguson, 1977; Greer, for in males become ‘transferred’ to females (Darwin, 1989; Shine, 1990; Manthey & Schuster, 1996; Wat- 1874, pp. 236). Lande (1980; Lande & Arnold, 1985) kins, 1998; Schulte et al., 2002; Townsend & Larson, formalized this idea with a mathematical model that 2002; Osborne, 2005). In a previous study (Stuart-Fox explained how a genetic correlation between the sexes & Ord, 2004), we found dragon species that possessed might lead to traits selected for only in males to also many ornaments are also highly sexually dimorphic in appear in females. Depending on the strength of this head size, the latter characteristic typically reflecting correlation, a trait initially expressed in both sexes could the intensity of sexual selection experienced by species eventually become restricted to one sex through natural (e.g. male-male competition often selects for males selection. Natural selection will favour reduced orna- with larger body or head size – Andersson, 1994). mentation if the production or maintenance of conspic- However, dragons living in open habitats, where there uous ornaments is energetically costly (e.g. Basolo & is an expected increase in predation pressure, are Alcaraz, 2003) and/or increases the risk of predation significantly less likely to evolve ornaments, and this (e.g. Wallace, 1889; Stuart-Fox et al., 2003; see also trend seems to be more pronounced in females than Langerhans et al., 2005). While the strength of sexual males (Stuart-Fox & Ord, 2004). Natural selection selection is enough to override the influence of natural appears to have constrained the evolution of ornamen- selection on males, this cost will select against the tation in dragon lizards although the precise mechan- expression of ornaments in females and ultimately result ism is unknown. We hypothesized that the types of in the evolution of sexual dimorphism. The genetic shelters used by species occupying open vs. closed correlation hypothesis predicts an evolutionary gain in habitats may exert selection on dragon ornamentation ornamentation in both sexes simultaneously, followed by (Stuart-Fox & Ord, 2004). Specifically, species occupy- an eventual loss of ornamentation in females. ing open habitats tend to flee into dense ground Alternatively, female ornamentation may itself be vegetation, rock crevices or burrows as their primary the product of sexual selection (West-Eberhard, 1983; escape mechanism whereas closed forest species tend to Amundsen, 2000a,b). Frequent intrasexual disputes hide behind tree trunks or branches. Species occupying over territories and other resources among members open habitats should therefore be less likely to evolve of both sexes have been documented in a variety of protruding ornaments. We test this hypothesis by taxa (e.g. fish – Forsgren et al., 2004; lizards – Martins, examining the influence of shelter type on the 1993; birds – Langmore, 1998; Heinsohn et al., 2005; evolution of ornamentation. Our goal was to determine Siefferman & Hill, 2005). Because the sexes share the whether natural selection (via shelter type) explains vast majority of their genome, intrasexual selection will ornament loss, especially in females as predicted by the presumably favour the evolution of similar ornamental genetic correlation hypothesis. traits in both males and females, particularly in the Few attempts have been made to examine the presence of genetic correlations (Amundsen, 2000a). macroevolutionary origins of sexual dimorphism in Male mate choice is another mechanism by which sexually selected traits (Dunn et al., 2001; Wiens, 2001; ornamentation might evolve in females and may even O¨ deen & Bjo¨ rklund, 2003; Emlen et al., 2005), especially promote female biased sexual dimorphism (Amundsen, with respect to the relative contribution of genetic 2000a; Griggio et al., 2005). The mutual sexual selec- correlation and mutual sexual selection on the presence tion hypothesis predicts an evolutionary gain and of ornaments in both sexes (Amundsen, 2000b; Wiens, subsequent retention of ornamentation in both sexes. 2001). In addition, the influence of natural selection on Most importantly, the historical appearance of orna- the pattern of gains and losses of sexually selected traits ments in males and females does not necessarily have remains largely unexplored within a comparative frame- to occur in concert. For example, sexual selection work. In this study, we use data on ornamentation in might initially produce