Evolution of Sex-Specific Traits through Changes in HOX-Dependent doublesex Expression

Tanaka, Kohtaro; Barmina, Olga; Sanders, Laura E.; Arbeitman, Michelle N.; Kopp, Artyom

doi:10.1371/journal.pbio.1001131

Cited by 125 publications

(203 citation statements)

References 63 publications

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“…melanogaster shows noticeable sexual dimorphism in their SCR expression pattern as reported by the earlier studies (Barmina and Kopp, 2007;Tanaka et al, 2011) and the same pattern is observed in D. rajasekari in the present study. The prothoracic SCR expression domain in males extends upto the distal border of the ts1 whereas in case of female foreleg pupal disc, the expression will not extend to the distal margin.…”

Section: Marked Enhancement In Expression Of Scr Features the Speciessupporting

confidence: 92%

“…double sex, the somatic sex regulator gene is responsible for providing the sex specific information for the development of sex comb in D. melanogaster and other species of the cluster (Barmina and Kopp, 2007;Randsholt and Santamaria 2008;Tanaka et al, 2011). It is interesting that, dsx expression is also seen in the leg discs of species like D. willistoni and D. hydei, which do not have sexually dimorphic bristles on their tarsal segments, and in various other species like D. immigrans and Zaprionus tuberculatus, which do not have a sex comb but have certain other sexually dimorphic tarsal structures (Tanaka et al, 2011). In this context, it is possible that, changes in DAC protein, and gain in the expression level of SCR in the tarsal segments are earlier steps in the evolutionary switching over of the developmental program, and this might have been followed by establishing a link with the dsx pathway at a subsequent stage, culminating in the evolution of the sexually dimorphic new trait sex comb.…”

Section: Bric-a-brac Expression Is Not Altered During Sex Comb Evolutionmentioning

confidence: 99%

“…Studies in the species of Sophophora group (Barmina and Kopp, 2007;Kopp, 2011;Randsholt and Santamaria, 2008) have shown that within the sub-genus, variations in the sex comb morphology, are strongly correlated with a modulation in spatial and quantitative expression of homeotic gene Sex combs reduced (Scr) in the 1st and 2nd tarsal segments of the prothoracic leg discs of male Drosophila. Loss and gain of this morphological structure in different species among Sophophora has been strictly correlated to the loss or gain and alterations in expression of SCR in the tarsal segments.…”

Section: Introductionmentioning

confidence: 99%

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Evolution of sex comb from the primitive bristle pattern in drosophila is associated with modification in the developmental regulatory protein dachshund

Devi

Amruthavalli

Shyamala

2013

Genesis

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Summary: Sex comb is a recently evolved male specific character confined to the Sophophoran group of Drosophila. Such innovations in phenotypes as Waddington proposed, are, outcome of ''canalization'' in developmental pathways that occur due to mutations creating ''choice points'' in genetic regulatory pathways. Our interest in the present study is to understand the shifts in genetic network, which has lead to the origin of sex comb from the basic bristle pattern that is seen in rest of the members of Drosophilidae. Here we have made a comparative analysis of expression of some of the key regulators of sex comb morphogenesis, between D. melanogaster and a group of selected species, which primitively lack sex comb. Sex combs reduced (Scr), dachshund (dac), and bric-a-brac (bab) gene expression were studied. We show that, primitive bristle pattern is marked by a strikingly down regulated expression of Sex combs reduced in the first tarsal segment of the prothoracic leg discs of male flies. Further a remarkable change with respect to Dachshund, an activator of sex combs reduced gene in the sex comb regulatory pathway, is seen. This is attributed to changes in DAC protein that might have taken place between the two groups of species. bric-a-brac does not reveal any significant expression modulation between the sex comb bearing and the primitive patterned species. Earlier works had shown that within the Sophophoran group, dynamic changes in SCR expression is responsible for the diversity seen in sex comb morphology, where as no such variation is witnessed with respect to DAC expression. Our findings have demonstrated that the scenario is different between the group primitively lacking sex comb and D. melanogaster wherein an obvious change in the protein has taken place. genesis 51:97-109, 2013. V V C 2012 Wiley Periodicals, Inc.

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Section: Marked Enhancement In Expression Of Scr Features the Speciessupporting

confidence: 92%

Section: Bric-a-brac Expression Is Not Altered During Sex Comb Evolutionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Evolution of sex comb from the primitive bristle pattern in drosophila is associated with modification in the developmental regulatory protein dachshund

Devi

Amruthavalli

Shyamala

2013

Genesis

View full text Add to dashboard Cite

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“…Third, recent studies have also revealed that dsx is a nexus for the evolution of sexually dimorphic traits; all cases understood at the molecular level involve either changes in cis-regulatory sequences of dsx target genes (11,12) or changes in the expression of dsx itself (13,14). In addition, the recent finding that developing Drosophila are mosaic for dsx expression-and thus are mosaic for the potential for sexual differentiation-has led to increased appreciation for the potential of evolution through tissuespecific changes in dsx activity (15).…”

mentioning

confidence: 99%

“…In addition, the recent finding that developing Drosophila are mosaic for dsx expression-and thus are mosaic for the potential for sexual differentiation-has led to increased appreciation for the potential of evolution through tissuespecific changes in dsx activity (15). Indeed, it was recently found that the diversification of sex combs in Drosophila species is correlated with changes in dsx expression patterns (14).…”

mentioning

confidence: 99%

Diversification of doublesex function underlies morph-, sex-, and species-specific development of beetle horns

Kijimoto

Moczek

Andrews

2012

Proc. Natl. Acad. Sci. U.S.A.

156

188

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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 RNAimediated 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.cooption | polyphenism | evolutionary novelty | interchangeability | weak linkage

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Both cell‐autonomous mechanisms and hormones contribute to sexual development in vertebrates and insects

Bear

Monteiro

2013

BioEssays

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The differentiation of male and female characteristics in vertebrates and insects has long been thought to proceed via different mechanisms. Traditionally, vertebrate sexual development was thought to occur in two phases: a primary and a secondary phase, the primary phase involving the differentiation of the gonads, and the secondary phase involving the differentiation of other sexual traits via the influence of sex hormones secreted by the gonads. In contrast, insect sexual development was thought to depend exclusively on cell-autonomous expression of sexspecific genes. Recently, however, new evidence indicates that both vertebrates and insects rely on sex hormones as well as cell-autonomous mechanisms to develop sexual traits. Collectively, these new data challenge the traditional vertebrate definitions of primary and secondary sexual development, call for a redefinition of these terms, and indicate the need for research aimed at explaining the relative dependence on cell-autonomous versus hormonally guided sexual development in animals.

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Evolution of Sex-Specific Traits through Changes in HOX-Dependent doublesex Expression

Abstract: Analysis in Drosophila suggests that evolutionary changes in the spatial regulation of the transcription factor doublesex play a key role in the origin, diversification, and loss of sex-specific structures.

Cited by 125 publications

References 63 publications

Evolution of sex comb from the primitive bristle pattern in drosophila is associated with modification in the developmental regulatory protein dachshund

Evolution of sex comb from the primitive bristle pattern in drosophila is associated with modification in the developmental regulatory protein dachshund

Diversification of doublesex function underlies morph-, sex-, and species-specific development of beetle horns

Both cell‐autonomous mechanisms and hormones contribute to sexual development in vertebrates and insects

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