On the origins of sexual dimorphism in butterflies

Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06511, USA.
Proceedings of the Royal Society B: Biological Sciences (Impact Factor: 5.05). 12/2010; 278(1714):1981-8. DOI: 10.1098/rspb.2010.2220
Source: PubMed


The processes governing the evolution of sexual dimorphism provided a foundation for sexual selection theory. Two alternative processes, originally proposed by Darwin and Wallace, differ primarily in the timing of events creating the dimorphism. In the process advocated by Darwin, a novel ornament arises in a single sex, with no temporal separation in the origin and sex-limitation of the novel trait. By contrast, Wallace proposed a process where novel ornaments appear simultaneously in both sexes, but are then converted into sex-limited expression by natural selection acting against showy coloration in one sex. Here, we investigate these alternative modes of sexual dimorphism evolution in a phylogenetic framework and demonstrate that both processes contribute to dimorphic wing patterns in the butterfly genera Bicyclus and Junonia. In some lineages, eyespots and bands arise in a single sex, whereas in other lineages they appear in both sexes but are then lost in one of the sexes. In addition, lineages displaying sexual dimorphism were more likely to become sexually monomorphic than they were to remain dimorphic. This derived monomorphism was either owing to a loss of the ornament ('drab monomorphism') or owing to a gain of the same ornament by the opposite sex ('mutual ornamentation'). Our results demonstrate the necessity of a plurality in theories explaining the evolution of sexual dimorphism within and across taxa. The origins and evolutionary fate of sexual dimorphism are probably influenced by underlying genetic architecture responsible for sex-limited expression and the degree of intralocus sexual conflict. Future comparative and developmental work on sexual dimorphism within and among taxa will provide a better understanding of the biases and constraints governing the evolution of animal sexual dimorphism.

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    • "A majority of nymphalid species has females with more eyespots than males, supporting data previously obtained for the genus Bicyclus [10]. However, a significant proportion of species display the opposite pattern, and many species are monomorphic in total eyespot number. "
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    ABSTRACT: Differences between sexes of the same species are widespread and are variable in nature. While it is often assumed that males are more ornamented than females, in the nymphalid butterfly genus Bicyclus, females have, on average, more eyespot wing color patterns than males. Here we extend these studies by surveying eyespot pattern sexual dimorphism across the Nymphalidae family of butterflies. Eyespot presence or absence was scored from a total of 38 wing compartments for two males and two females of each of 450 nymphalid species belonging to 399 different genera. Differences in eyespot number between sexes of each species were tallied for each wing surface (e.g., dorsal and ventral) of forewings and hindwings. In roughly 44% of the species with eyespots, females had more eyespots than males, in 34%, males had more eyespots than females, and, in the remaining 22% of the species, there was monomorphism in eyespot number. Dorsal and forewing surfaces were less patterned, but proportionally more dimorphic, than ventral and hindwing surfaces, respectively. In addition, wing compartments that frequently displayed eyespots were among the least sexually dimorphic. This survey suggests that dimorphism arises predominantly in "hidden" or "private" surfaces of a butterfly's wing, as previously demonstrated for the genus Bicyclus.
    Full-text · Article · Dec 2013
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    • "Nevertheless, there are a handful of studies addressing this question, where the authors have been able to identify genes involved in regulating sexual dimorphism, and predict an ancestral state of monomorphic expression for some traits (Emlen et al. 2007; Williams et al. 2008; Moczek and Rose 2009; Williams and Carroll 2009; Khila et al. 2012). A phylogenetic analysis of wing pattern evolution in butterflies also found evidence that for some traits, sex-limited gene expression occurred simultaneously as the trait arose in a lineage; whereas, for other traits there was an ancestral state of dimorphic expression, followed by the subsequent loss of expression in one sex (Oliver and Monteiro 2011). An additional mechanism for controlling sex-specific gene expression is through alternative splicing (McIntyre et al. 2006). "
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    ABSTRACT: As the evolutionary interests of males and females are frequently divergent, a trait value that is optimal for the fitness of one sex is often not optimal for the other. A shared genome also means that the same genes may underlie the same trait in both sexes. This can give rise to a form of sexual antagonism, known as intralocus sexual conflict (IASC). Here, a tug-of-war over allelic expression can occur, preventing the sexes from reaching optimal trait values, thereby causing sex-specific reductions in fitness. For some traits, it appears that IASC can be resolved via sex-specific regulation of genes that subsequently permits sexual dimorphism; however, it seems that whole-genome resolution may be impossible, due to the genetic architecture of certain traits, and possibly due to the changing dynamics of selection. In this review, we explore the evolutionary mechanisms of, and barriers to, IASC resolution. We also address the broader consequences of this evolutionary feud, the possible interactions between intra- and interlocus sexual conflict (IRSC: a form of sexual antagonism involving different loci in each sex), and draw attention to issues that arise from using proxies as measurements of conflict. In particular, it is clear that the sex-specific fitness consequences of sexual dimorphism require characterization before making assumptions concerning how this relates to IASC. Although empirical data have shown consistent evidence of the fitness effects of IASC, it is essential that we identify the alleles mediating these effects in order to show IASC in its true sense, which is a "conflict over shared genes."
    Full-text · Article · Jun 2013 · Ecology and Evolution
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    • "has been demonstrated in butterflies (Oliver & Monteiro, 2011), then it is not indicative of the past IASC. Similarly, sexual dimorphism can evolve via pleiotropy if a trait under selection in one sex is correlated with a different selectively neutral trait in the other sex (Bonduriansky & Chenoweth, 2009). "
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    ABSTRACT: Alternative reproductive tactics (ARTs) are characterized by consistent and discrete variations in the reproductive behaviors (e.g. mating, fighting, and nesting) of members of the same sex. Selection against intermediate expression of reproductive traits (disruptive selection) can lead to the evolution of ARTs, and can generate intralocus tactical conflict (IATC) when traits that are homologous across ARTs are not at their adaptive optimum. As the sexes and ARTs are both examples of discrete alternative phenotypes, much of what we have learned about intralocus sexual conflict can be applied to ARTs. We outline three criteria necessary to demonstrate IATC and discuss methods for testing these criteria. By determining the extent to which traits involved in ARTs are experiencing IATC, we will gain a better understanding of the benefits of behavioral plasticity, the extent to which both morphological and behavioral traits involved in ARTs are not at their phenotypic optimum, and the extent to which release from IATC can explain the relationship between ARTs and speciation. In addition, IATC may improve our understanding of the relationship between sexual and tactical dimorphism.
    Full-text · Article · Jan 2013 · Advances in the Study of Behavior
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