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The transcriptomic basis of tissue- and nutrition-dependent sexual dimorphism in the beetle Onthophagus taurus.

ABSTRACT: Sexual dimorphism accounts for a large fraction of intraspecific diversity. However, not all traits are equally sexually dimorphic; instead, individuals are mosaics of tissues that vary in their ability to exhibit dimorphism. Furthermore, the degree of a trait's sexual dimorphism is frequently environment-dependent, with elaborate sexual dimorphism commonly being restricted to high nutritional conditions. Understanding the developmental basis and evolution of condition-dependent sexual dimorphism can be critically informed by determining - across tissues and nutritional conditions - what sex-biased genes are deployed and how they interact and translate into functional processes. Indeed, key theories concerning the evolution of condition-dependent sexually dimorphic traits rest on assumptions regarding their developmental genetic underpinnings, yet, have largely gone unexamined by empirical studies. Here, we provide such evidence by investigating the transcriptomic basis of tissue- and nutrition-dependent sexual dimorphism in the bull-headed dung beetle Onthophagus taurus. Our findings suggest (1) that generating morphological sexual dimorphism requires sex-biased gene expression in and developmental remodeling of both sexes, regardless of which sex exhibits externally visible trait exaggeration, (2) that although sexually dimorphic phenotypes are comprised of traits underlain by independent repertoires of sex-biased gene expression, they act similarly at a functional level, and (3) that sexual dimorphism and condition-dependence share common genetic underpinnings specifically in sexually-selected traits.

SUBMITTER: Ledon-Rettig CC

PROVIDER: S-EPMC4752365 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundHorned beetles, in particular in the genus Onthophagus, are important models for studies on sexual selection, biological radiations, the origin of novel traits, developmental plasticity, biocontrol, conservation, and forensic biology. Despite their growing prominence as models for studying both basic and applied questions in biology, little genomic or transcriptomic data are available for this genus. We used massively parallel pyrosequencing (Roche 454-FLX platform) to produce a comprehensive EST dataset for the horned beetle Onthophagus taurus. To maximize sequence diversity, we pooled RNA extracted from a normalized library encompassing diverse developmental stages and both sexes.ResultsWe used 454 pyrosequencing to sequence ESTs from all post-embryonic stages of O. taurus. Approximately 1.36 million reads assembled into 50,080 non-redundant sequences encompassing a total of 26.5 Mbp. The non-redundant sequences match over half of the genes in Tribolium castaneum, the most closely related species with a sequenced genome. Analyses of Gene Ontology annotations and biochemical pathways indicate that the O. taurus sequences reflect a wide and representative sampling of biological functions and biochemical processes. An analysis of sequence polymorphisms revealed that SNP frequency was negatively related to overall expression level and the number of tissue types in which a given gene is expressed. The most variable genes were enriched for a limited number of GO annotations whereas the least variable genes were enriched for a wide range of GO terms directly related to fitness.ConclusionsThis study provides the first large-scale EST database for horned beetles, a much-needed resource for advancing the study of these organisms. Furthermore, we identified instances of gene duplications and alternative splicing, useful for future study of gene regulation, and a large number of SNP markers that could be used in population-genetic studies of O. taurus and possibly other horned beetles.

Project description:Insects feeding on plant sap, blood, and other nutritionally incomplete diets are typically associated with mutualistic bacteria that supplement missing nutrients. Herbivorous mammal dung contains more than 86% cellulose and lacks amino acids essential for insect development and reproduction. Yet one of the most ecologically necessary and evolutionarily successful groups of beetles, the dung beetles (Scarabaeinae) feeds primarily, or exclusively, on dung. These associations suggest that dung beetles may benefit from mutualistic bacteria that provide nutrients missing from dung. The nesting behaviors of the female parent and the feeding behaviors of the larvae suggest that a microbiome could be vertically transmitted from the parental female to her offspring through the brood ball. Using sterile rearing and a combination of molecular and culture-based techniques, we examine transmission of the microbiome in the bull-headed dung beetle, Onthophagus taurus. Beetles were reared on autoclaved dung and the microbiome was characterized across development. A ~1425 bp region of the 16S rRNA identified Pseudomonadaceae, Enterobacteriaceae, and Comamonadaceae as the most common bacterial families across all life stages and populations, including cultured isolates from the 3(rd) instar digestive system. Finer level phylotyping analyses based on lepA and gyrB amplicons of cultured isolates placed the isolates closest to Enterobacter cloacae, Providencia stuartii, Pusillimonas sp., Pedobacter heparinus, and Lysinibacillus sphaericus. Scanning electron micrographs of brood balls constructed from sterile dung reveals secretions and microbes only in the chamber the female prepares for the egg. The use of autoclaved dung for rearing, the presence of microbes in the brood ball and offspring, and identical 16S rRNA sequences in both parent and offspring suggests that the O. taurus female parent transmits specific microbiome members to her offspring through the brood chamber. The transmission of the dung beetle microbiome highlights the maintenance and likely importance of this newly-characterized bacterial community.

Project description:Despite sharing nearly the same genome, individuals within the same species can vary drastically in both morphology and behaviour as a function of developmental stage, sex or developmental plasticity. Thus, regulatory processes must exist that enable the stage-, sex- or environment-specific expression of traits and their integration during ontogeny, yet exactly how trait complexes are co-regulated and integrated is poorly understood. In this study, we explore the developmental genetic basis of the regulation and integration of environment-dependent sexual dimorphism in behaviour and morphology in the horn-polyphenic dung beetle Onthophagus taurus through the experimental manipulation of the transcription factor doublesex (dsx). The gene dsx plays a profound role in the developmental regulation of morphological differences between sexes as well as alternative male morphs by inhibiting horn formation in females but enabling nutrition-responsive horn growth in males. Specifically, we investigated whether experimental downregulation of dsx expression affects male and female aggressive and courtship behaviours in two social contexts: interactions between individuals of the same sex and interactions between males and females. We find that dsx downregulation significantly alters aggressiveness in both males and females, yet does so differently for both sexes as a function of social context: dsxRNAi males exhibited elevated aggression towards males but showed reduced aggression towards females, whereas dsxRNAi females became more aggressive towards males, while their aggressiveness towards other females was unaffected. Moreover, we document unexpectedly high levels of female aggression independent of dsx treatment in both wild-type and control-injected individuals. Lastly, we found no effects of dsxRNAi on courtship and mating behaviours. We discuss the role of dsx in the regulation of sex-specific and plastic behaviours, the unexpectedly high levels of aggression of hornless dsxRNAi males in relation to the well-established description of the hornless sneaker phenotype and the potential ecological function of high female aggression.

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The transcriptomic basis of tissue- and nutrition-dependent sexual dimorphism in the beetle Onthophagus taurus.

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