Sexual shape dimorphism accelerated by male-male competition, but not prevented by sex-indiscriminate parental care in dung beetles (Scarabaeidae).
ABSTRACT: Dimorphic sexual differences in shape and body size are called sexual dimorphism and sexual size dimorphism, respectively. The degrees of both dimorphisms are considered to increase with sexual selection, represented by male-male competition. However, the degrees of the two dimorphisms often differ within a species. In some dung beetles, typical sexual shape dimorphisms are seen in male horns and other exaggerated traits, although sexual size dimorphism looks rare. We hypothesized that the evolution of this sexual shape dimorphism without sexual size dimorphism is caused by male-male competition and their crucial and sex-indiscriminate provisioning behaviors, in which parents provide the equivalent size of brood ball with each of both sons and daughters indiscriminately. As a result of individual-based model simulations, we show that parents evolve to provide each of sons and daughters with the optimal amount of resource for a son when parents do not distinguish the sex of offspring and males compete for mates. This result explains why crucial and sex-indiscriminate parental provisioning does not prevent the evolution of sexual shape dimorphism. The model result was supported by empirical data of Scarabaeidae beetles. In some dung beetles, sexual size dimorphism is absent, compared with significant sexual size dimorphism in other horned beetles, although both groups exhibit similar degrees of sexual shape dimorphism in male horns and other exaggerated traits.
Project description:Male horn dimorphism is a rather common phenomenon in dung beetles, where some adult individuals have well-developed head horns (i.e., major males), while others exhibit diminished horn length (i.e., minor males). We focused on horn dimorphism and associated head and pronotum shape variations in Copris lunaris. We examined the allometric relationship between horn length (i.e., cephalic and pronotal horns) and maximum pronotum width (as index of body size) by fitting linear and sigmoidal models for both sexes. We then asked whether head and pronotum shape variations, quantified using the geometric morphometric approach, contributed to this allometric pattern. We found that female cephalic and pronotal horn growth showed a typical isometric scaling with body size. Horn length in males, however, exhibited sigmoidal allometry, where a certain threshold in body size separated males into two distinct morphs as majors and minors. Interestingly, we highlighted the same allometric patterns (i.e., isometric vs. sigmoidal models) by scaling horn lengths with pronotum shape, making evident that male horn dimorphism is not only a matter of body size. Furthermore, the analysis of shape showed that the three morphs had similar heads, but different pronota, major males showing a more expanded, rounded pronotum than minor males and females. These morphological differences in C. lunaris can ultimately have important functional consequences in the ecology of this species, which should be explored in future work.
Project description:Sex-specific trait expression is frequently associated with highly variable, condition-dependent expression within sexes and rapid divergence among closely related species. Horned beetles are an excellent example for studying the molecular basis of these phenomena because horn morphology varies markedly among species, between sexes, and among alternative, nutritionally-cued morphs within sexes. In addition, horns lack obvious homology to other insect traits and provide a good opportunity to explore the molecular basis of the rapid diversification of a novel trait within and between species. Here we show that the sex-determination gene doublesex (dsx) underlies important aspects of horn development, including differences between sexes, morphs, and species. In male Onthophagus taurus, dsx transcripts were preferentially expressed in the horns of the large, horned morph, and RNAi-mediated knockdown of dsx dramatically altered male horn allometry by massively reducing horn development in large males, but not in smaller males. Conversely, dsx RNAi induced ectopic, nutrition-sensitive horn development in otherwise hornless females. Finally, in a closely related species (Onthophagus sagittarius) that has recently evolved a rare reversed sexual dimorphism, dsx RNAi revealed reversed as well as novel dsx functions despite an overall conservation of dsx expression. This suggests that rapid evolution of dsx functions has facilitated the transition from a regular sexual dimorphism to a reversed sexual dimorphism in this species. Our findings add beetle horns to existing examples of a close relationship between dsx and sexual trait development, and suggest that dsx function has been coopted to facilitate both the evolution of environmentally-cued intrasexual dimorphisms and rapid species divergences in a novel trait.
Project description:Here we reconstruct the evolutionary shift towards floral simulation in orchid mantises and suggest female predatory selection as the likely driving force behind the development of extreme sexual size dimorphism. Through analysis of body size data and phylogenetic modelling of trait evolution, we recovered an ancestral shift towards sexual dimorphisms in both size and appearance in a lineage of flower-associated praying mantises. Sedentary female flower mantises dramatically increased in size prior to a transition from camouflaged, ambush predation to a floral simulation strategy, gaining access to, and visually attracting, a novel resource: large pollinating insects. Male flower mantises, however, remained small and mobile to facilitate mate-finding and reproductive success, consistent with ancestral male life strategy. Although moderate sexual size dimorphisms are common in many arthropod lineages, the predominant explanation is female size increase for increased fecundity. However, sex-dependent selective pressures acting outside of female fecundity have been suggested as mechanisms behind niche dimorphisms. Our hypothesised role of predatory selection acting on females to generate both extreme sexual size dimorphism coupled with niche dimorphism is novel among arthropods.
Project description:The general morphology of the insect head has remained relatively unchanged through more than 400 million years of evolution. Yet throughout this period this same region has also become a hotspot for evolutionary novelty, yielding structures such as the eyestalks of stalk-eyed flies or the cephalic horns of dung beetles. How novelty can be integrated within ancient complex traits without disrupting the function and formation of that trait is a foundational, yet largely unresolved question in developmental and evolutionary biology. Here, we approached this question by performing unique, head compartment specific RNAseq using the heads of Onthophagus taurus beetles, which bear impressive posterior horns in males. We sequenced the transcriptomes in horned males and hornless females from six distinct head compartments covering two major axes of patterning: anterior to posterior (AP) and medial to lateral (ML). Our results provide evidence of differential compartmentalization of the head along both AP and ML axes, and reveal striking parallels between morphological and transcriptomic complexity – that is, head regions with more complex morphologies, such as the posterior region, are more transcriptionally intricate compared to morphologically homogenous regions, such as the anterior of the head. Our findings support the hypothesis that the integration of novel traits within ancestral trait complexes may require the recruitment of additional genes and pathways into the networks instructing within and among compartment development. However, sexual dimorphism in posterior horn development was not paralleled by a corresponding sexual dimorphism in transcriptional complexity, instead hornless females exhibited approximately the same diversity of differentially expressed genes across posterior head compartments than did horn-bearing males. Overall design: Dorsal head regions of male and female pre-pupae larvae were dissected into six distinct compartments: left and right posterior, medial posterior, left and right anterior, and medial anterior.
Project description:Male genitalia exhibit patterns of divergent evolution driven by sexual selection. In contrast, for many taxonomic groups, female genitalia are relatively uniform and their patterns of evolution remain largely unexplored. Here we quantify variation in the shape of female genitalia across onthophagine dung beetles, and use new comparative methods to contrast their rates of divergence with those of male genitalia. As expected, male genital shape has diverged more rapidly than a naturally selected trait, the foretibia. Remarkably, female genital shape has diverged nearly three times as fast as male genital shape. Our results dispel the notion that female genitalia do not show the same patterns of divergent evolution as male genitalia, and suggest that female genitalia are under sexual selection through their role in female choice.
Project description:In many songbirds the larger vocal repertoire of males is associated with sexual dimorphism of the vocal control centers and muscles of the vocal organ, the syrinx. However, it is largely unknown how these differences are translated into different acoustic behavior.Here we show that the sound generating structures of the syrinx, the labia and the associated cartilaginous framework, also display sexual dimorphism. One of the bronchial half rings that position and tense the labia is larger in males, and the size and shape of the labia differ between males and females. The functional consequences of these differences were explored by denervating syringeal muscles. After denervation, both sexes produced equally low fundamental frequencies, but the driving pressure generally increased and was higher in males. Denervation strongly affected the relationship between driving pressure and fundamental frequency.The syringeal modifications in the male syrinx, in concert with dimorphisms in neural control and muscle mass, are most likely the foundation for the potential to generate an enhanced frequency range. Sexually dimorphic vocal behavior therefore arises from finely tuned modifications at every level of the motor cascade. This sexual dimorphism in frequency control illustrates a significant evolutionary step towards increased vocal complexity in birds.
Project description:Beetle horns are attractive models for studying the evolution of novel traits, as they display diverse shapes, sizes, and numbers among closely related species within the family Scarabaeidae. Horns radiated prolifically and independently in two distant subfamilies of scarabs, the dung beetles (Scarabaeinae), and the rhinoceros beetles (Dynastinae). However, current knowledge of the mechanisms underlying horn diversification remains limited to a single genus of dung beetles, Onthophagus. Here we unveil 11 horn formation genes in a rhinoceros beetle, Trypoxylus dichotomus. These 11 genes are mostly categorized as larval head- and appendage-patterning genes that also are involved in Onthophagus horn formation, suggesting the same suite of genes was recruited in each lineage during horn evolution. Although our RNAi analyses reveal interesting differences in the functions of a few of these genes, the overwhelming conclusion is that both head and thoracic horns develop similarly in Trypoxylus and Onthophagus, originating in the same developmental regions and deploying similar portions of appendage patterning networks during their growth. Our findings highlight deep parallels in the development of rhinoceros and dung beetle horns, suggesting either that both horn types arose in the common ancestor of all scarabs, a surprising reconstruction of horn evolution that would mean the majority of scarab species (~35,000) actively repress horn growth, or that parallel origins of these extravagant structures resulted from repeated co-option of the same underlying developmental processes.
Project description:The origins of novel complex phenotypes represent one of the most fundamental, yet largely unresolved, issues in evolutionary biology. Here we explore the developmental genetic regulation of beetle horns, a class of traits that lacks obvious homology to traits in other insects. Furthermore, beetle horns are remarkably diverse in their expression, including sexual dimorphisms, male dimorphisms, and interspecific differences in location of horn expression. At the same time, beetle horns share aspects of their development with that of more traditional appendages. We used larval RNA interference-mediated gene function analysis of 3 cardinal insect appendage patterning genes, dachshund, homothorax, and Distal-less, to investigate their role in development and diversification of beetle horns within and between species. Transcript depletion of all 3 patterning genes generated phenotypic effects very similar to those documented in previous studies that focused on general insect development. In addition, we found that Distal-less and homothorax, but not dachshund, regulate horn expression in a species-, sex-, body region-, and body size-dependent manner. Our results demonstrate differential co-option of appendage patterning genes during the evolution and radiation of beetle horns. Furthermore, our results illustrate that regulatory genes whose functions are otherwise highly conserved nevertheless retain the capacity to acquire additional functions, and that little phylogenetic distance appears necessary for the evolution of sex- and species-specific differences in these functions.
Project description:Common scientific wisdom assumes that spider sexual dimorphism (SD) mostly results from sexual selection operating on males. However, testing predictions from this hypothesis, particularly male size hyperallometry, has been restricted by methodological constraints. Here, using geometric morphometrics (GMM) we studied for the first time sex-differential shape allometry in a spider (<i>Donacosa merlini</i>, Araneae: Lycosidae) known to exhibit the reverse pattern (i.e., male-biased) of spider sexual size dimorphism. GMM reveals previously undetected sex-differential shape allometry and sex-related shape differences that are size independent (i.e., associated to the y-intercept, and not to size scaling). Sexual shape dimorphism affects both the relative carapace-to-opisthosoma size and the carapace geometry, arguably resulting from sex differences in both reproductive roles (female egg load and male competition) and life styles (wandering males and burrowing females). Our results demonstrate that body portions may vary modularly in response to different selection pressures, giving rise to sex differences in shape, which reconciles previously considered mutually exclusive interpretations about the origins of spider SD.
Project description:Conclusive evidence for sexual dimorphism in non-avian dinosaurs has been elusive. Here it is shown that dimorphism in the shape of the dermal plates of Stegosaurus mjosi (Upper Jurassic, western USA) does not result from non-sex-related individual, interspecific, or ontogenetic variation and is most likely a sexually dimorphic feature. One morph possessed wide, oval plates 45% larger in surface area than the tall, narrow plates of the other morph. Intermediate morphologies are lacking as principal component analysis supports marked size- and shape-based dimorphism. In contrast, many non-sex-related individual variations are expected to show intermediate morphologies. Taphonomy of a new quarry in Montana (JRDI 5ES Quarry) shows that at least five individuals were buried in a single horizon and were not brought together by water or scavenger transportation. This new site demonstrates co-existence, and possibly suggests sociality, between two morphs that only show dimorphism in their plates. Without evidence for niche partitioning, it is unlikely that the two morphs represent different species. Histology of the new specimens in combination with studies on previous specimens indicates that both morphs occur in fully-grown individuals. Therefore, the dimorphism is not a result of ontogenetic change. Furthermore, the two morphs of plates do not simply come from different positions on the back of a single individual. Plates from all positions on the body can be classified as one of the two morphs, and previously discovered, isolated specimens possess only one morph of plates. Based on the seemingly display-oriented morphology of plates, female mate choice was likely the driving evolutionary mechanism rather than male-male competition. Dinosaur ornamentation possibly served similar functions to the ornamentation of modern species. Comparisons to ornamentation involved in sexual selection of extant species, such as the horns of bovids, may be appropriate in predicting the function of some dinosaur ornamentation.