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Diversification of Doublesex Function Underlies Morph-, Sex-, and Species

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Diversification of Doublesex Function Underlies Morph-, Sex-, and Species Diversification of doublesex function underlies morph-, sex-, and species-specific development of beetle horns Teiya Kijimoto, Armin P. Moczek1, and Justen Andrews Department of Biology, Indiana University, Bloomington, IN 47405 Edited by Gene E. Robinson, University of Illinois at Urbana–Champaign, Urbana, IL, and approved October 19, 2012 (received for review November 11, 2011) Sex-specific trait expression is frequently associated with highly Onthophagus suggested that differential dsx expression is associ- variable, condition-dependent expression within sexes and rapid ated with morph-specific development of horns. Specifically, rel- divergence among closely related species. Horned beetles are an ative to the abdominal epidermis of the same individual, dsx excellent example for studying the molecular basis of these phe- expression was consistently elevated in the horn tissue, but not the nomena because horn morphology varies markedly among species, legs, of horned males (5, 6). between sexes, and among alternative, nutritionally-cued morphs Second, previous studies have shown that dsx has a highly within sexes. In addition, horns lack obvious homology to other conserved function as the terminal gene in the sex determination insect traits and provide a good opportunity to explore the mo- pathway that regulates the sex-limited expression of downstream lecular basis of the rapid diversification of a novel trait within and genes, leading to sexually dimorphic development and behavior between species. Here we show that the sex-determination gene across diverse insects (7–9). The structure and function of dsx are doublesex (dsx) underlies important aspects of horn develop- best understood from studies in Drosophila.InDrosophila mel- ment, including differences between sexes, morphs, and species. anogaster, a hierarchy of sex-determination genes acts to regulate In male Onthophagus taurus, dsx transcripts were preferentially the expression of sex-specific isoforms of the Dsx transcription expressed in the horns of the large, horned morph, and RNAi- factor, which in turn regulates the sex-limited expression of down- mediated knockdown of dsx dramatically altered male horn al- stream cytodifferentiation genes responsible for the elaboration lometry by massively reducing horn development in large males, of sexually dimorphic traits (10). Comparative analyses have re- but not in smaller males. Conversely, dsx RNAi induced ectopic, vealed that even though the sex-determination pathway upstream nutrition-sensitive horn development in otherwise hornless of dsx is divergent across insect orders, dsx itself is highly con- females. Finally, in a closely related species (Onthophagus sagit- served. In particular, in all insects examined thus far, the key tarius) that has recently evolved a rare reversed sexual dimor- features of dsx structure and function appear to be conserved— phism, dsx RNAi revealed reversed as well as novel dsx functions specifically, the expression of male- and female-specific Dsx tran- despite an overall conservation of dsx expression. This suggests scription factors generated through alternative splicing of an exon that rapid evolution of dsx functions has facilitated the transition included in dsx transcripts in males and excluded in females (8). from a regular sexual dimorphism to a reversed sexual dimorphism Third, recent studies have also revealed that dsx is a nexus for in this species. Our findings add beetle horns to existing examples the evolution of sexually dimorphic traits; all cases understood at of a close relationship between dsx and sexual trait development, the molecular level involve either changes in cis-regulatory se- and suggest that dsx function has been coopted to facilitate both quences of dsx target genes (11, 12) or changes in the expression the evolution of environmentally-cued intrasexual dimorphisms of dsx itself (13, 14). In addition, the recent finding that devel- and rapid species divergences in a novel trait. oping Drosophila are mosaic for dsx expression—and thus are mosaic for the potential for sexual differentiation—has led to in- cooption | polyphenism | evolutionary novelty | interchangeability | creased appreciation for the potential of evolution through tissue- weak linkage specific changes in dsx activity (15). Indeed, it was recently found that the diversification of sex combs in Drosophila species is xaggerated secondary sexual traits are common products of correlated with changes in dsx expression patterns (14). Esexual selection, often diverge rapidly between closely related Here we investigated the gene structure, expression, and func- species, and frequently exhibit condition-dependent expression tion of dsx in two congeneric species of horned beetles, Ontho- (1). In extreme cases, conditional expression of secondary sexual phagus taurus and Onthophagus sagittarius, which exhibit highly traits is discrete and results in the production of alternative, divergent patterns of phenotype expression. O. taurus has a dra- intrasexual morphs (2). For instance, the exaggerated horns of matic intrasexual and intersexual dimorphism in horn develop- horned beetles are typically present only in males; have diversified ment typical for the genus and thought to reflect the ancestral dramatically in size, shape, and location across thousands of character state of horn development in Onthophagus. O. sagit- species; and—among conspecific males—frequently develop in a tarius shared a common ancestor with O. taurus ∼5 Mya, but has conditional, nutrition-dependent manner. In such cases, only since evolved a pattern of horn development radically divergent males with access to optimal feeding conditions during the larval from the ancestral pattern still seen in O. taurus, including the stage grow into large, major males with fully developed horns, which are then used as weapons in aggressive encounters with conspecific males. In contrast, poor larval feeding conditions re- Author contributions: T.K., A.P.M., and J.A. designed research; T.K. performed re- sult in males developing into smaller, nonaggressive sneaker or search; T.K., A.P.M., and J.A. analyzed data; and T.K., A.P.M., and J.A. wrote the paper. minor morphs with disproportionately smaller horns (3, 4). The authors declare no conflict of interest. In this study, we investigated whether morph-, sex-, and species- This article is a PNAS Direct Submission. fi speci c development of secondary sexual traits, as seen in horned Data deposition: The sequences reported in this paper have been deposited in the Gen- beetles, may arise through the use of a shared developmental Bank database (accession nos. JN165757–JN165768). genetic machinery. In particular, we focused on the somatic 1To whom correspondence should be addressed. E-mail: [email protected]. sex-determination gene doublesex (dsx), for three reasons. First, This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. recent array-based studies on horned beetles of the genus 1073/pnas.1118589109/-/DCSupplemental 20526–20531 | PNAS | December 11, 2012 | vol. 109 | no. 50 www.pnas.org/cgi/doi/10.1073/pnas.1118589109 Downloaded by guest on September 30, 2021 rare expression of a reversed sexual dimorphism as well as horn asingledsx isoform that was expressed in both sexes (Otdsxb;Fig.1 development in a novel location not used by O. taurus or more B and C). basal branches in the Onthophagus phylogeny (16). We sought to Each of the Otdsxf transcripts has female-specific sequences, investigate the degree to which dsx might mediate the differential including translation termination codons, that are absent from development of horns across different developmental and evo- the Otdsxm and Otdsxb transcripts (Fig. S1 A and B). Thus, the lutionary contexts. Our results suggest that dsx functions to reg- organization of female-specific transcripts is most similar to that ulate sex-specific development of horns, that this function has of the silkmoth Bombyx mori, which also expresses multiple dsxf been coopted to enable the nutritionally-cued development of al- transcripts that encode DsxF protein isoforms with different ternative male morphs, and that dsx function has further diversified C-terminal sequences (8, 17) (Fig. S1C). Unlike in Drosophila,the to facilitate rapid and extreme species divergences in the expression male dsx isoform shares all of its putative coding exons with the of a novel trait. female isoforms (Fig. 1B and Fig. S1A). We found that when translated, all sex-specific isoforms have all of the functional Results and Discussion domains commonly present in other insects, including the olig- dsx Gene Structure and Expression Are Conserved in O. taurus Relative omerization domains (ODs) 1 and 2 (Fig. S1 B–D). Specifically, to Other Insects. We first investigated the gene structure and func- overall identity of translated sequences is 46% for the male- tion of dsx in O. taurus, a species with a typical intrasexual and specificisoform,45–47% for DsxF1, and 46–47% for DsxF2 intersexual dimorphism in horn development (Figs. 1 and 2). The compared with B. mori. The predicted OD1 (also known as DM O. taurus dsx gene architecture and inferred protein sequence are domain) and OD2 share 93% and 55% sequence identity, respec- similar to those in other insects (Fig. 1 A and B). Specifically, O. tively, with the corresponding regions in D. melanogaster.Incon- taurus expresses sex-specific dsx mRNA isoforms (Fig. 1 B and C), trast, the dsx transcript shared by both sexes (Otdsxb) includes
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