A conserved somatic sex determination cascade instructs trait-specific sexual dimorphism in horned dung beetles.

London C Mitchell, Armin P Moczek, Erica M Nadolski
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Abstract

Sex-specific trait expression represents a striking dimension of morphological variation within and across species. The mechanisms instructing sex-specific organ development have been well studied in a small number of insect model systems, suggesting striking conservation in some parts of the somatic sex determination pathway while hinting at possible evolutionary lability in others. However, further resolution of this phenomenon necessitates additional taxon sampling, particularly in groups in which sexual dimorphisms have undergone significant elaboration and diversification. Here, we functionally investigate the somatic sex determination pathway in the gazelle dung beetle Digitonthophagus gazella , an emerging model system in the study of the development and evolution of sexual dimorphisms. We find that RNA interference (RNAi) targeting transformer (tra) caused chromosomal females to develop morphological traits largely indistinguishable from those normally only observed in males, and that tra RNAi is sufficient to induce splicing of the normally male-specific isoform of doublesex in chromosomal females, while leaving males unaffected. Further, intersex RNAi was found to phenocopy previously described RNAi phenotypes of doublesex in female but not male beetles. These findings match predictions derived from models of the sex determination cascade as developed largely through studies in Drosophila melanogaster . In contrast, transformer2 RNAi resulted in larval mortality and was not sufficient to affect doublesex splicing, whereas RNAi targeting Sex-lethal and two putative orthologs of hermaphrodite yielded no obvious phenotypic modifications in either males or females, raising the possibility that the function of a subset of sex determination genes may be derived in select Diptera and thus non-representative of their roles in other holometabolous orders. Our results help illuminate how the differential evolutionary lability of the somatic sex determination pathway has contributed to the extraordinary morphological diversification of sex-specific trait expression found in nature.

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雄性是默认性别:角蜣螂性别决定级联的功能意义。
性别特异性状的表达是物种内和物种间形态变异的一个显著方面。在少数昆虫模式系统中,对指导性别特异性器官发育的机制进行了深入研究,结果表明体细胞性别决定途径的某些部分具有显著的保守性,而另一些部分则暗示可能存在进化上的不稳定性。然而,要进一步研究这一现象,还需要对更多的类群进行取样,尤其是在那些性二型经历了重大发展和多样化的类群中。在这里,我们对瞪羚蜣螂(Digitonthophagus gazella)的体细胞性别决定途径进行了功能性研究,瞪羚蜣螂是研究性二形发育和进化的一个新兴模式系统。我们发现,以转化子1(tra1)为靶标的RNA干扰(RNAi)会导致染色体上的雌性出现与通常只在雄性身上观察到的形态特征基本无异的性状,而且tra1 RNAi足以诱导染色体上的雌性出现通常为雄性特异的双性同工酶剪接,而雄性则不受影响。此外,在雌性甲虫而非雄性甲虫中,发现双性 RNAi 表型与之前描述的双性 RNAi 表型相同。这些发现符合主要通过对黑腹果蝇的研究而建立的性别决定级联模型的预测。与此相反,transformer2 RNAi导致幼虫死亡,但不足以影响双性基因的剪接,而针对Sex-lethal和雌雄同体的两个假定直向同源物的RNAi则没有在雄性或雌性甲虫中产生明显的表型改变。我们的研究结果有助于阐明体细胞性别决定途径在进化过程中的不同易变性是如何导致自然界中性别特异性状表达的异常形态多样化的。
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