Genetic architecture and sex-specific selection govern modular, male-biased evolution of
            <i>doublesex</i>

Baral, Saurav; Gandhimathi, A.; Deshmukh, Riddhi; Kunte, Krushnamegh

doi:10.1126/sciadv.aau3753

Cited by 34 publications

(46 citation statements)

References 41 publications

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“…Within insect orders, also a strong reduction of the sequence identity in male-specific OD2 domain alignment is seen. This observed rapid evolution of male-specific dsx regions is supported by other research and is indicative of its fast evolution likely due to increased diversity of secondary sexual traits in male insects (40). In females, the sex-specific region of OD2 is relatively conserved across different insect orders.…”

Section: Resultssupporting

confidence: 82%

“…In addition, in Hymenoptera the female specific OD2 domain was found to evolve much faster than the male-specific regions. This is contrary to Diptera, Lepidoptera and Coleoptera and has been suggested to correlate with the evolution of female-dominated eusociality and female-specific caste differentiation (40). However, Nasonia is solitary as are many other hymenopteran species.…”

Section: Resultsmentioning

confidence: 90%

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Sexually dimorphic traits and male-specific differentiation are actively regulated by Doublesex during specific developmental windows inNasonia vitripennis

Wang¹,

Rensink

Fricke³

et al. 2020

Preprint

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Sexually dimorphic traits in insects are rapidly evolving due to sexual selection which can ultimately lead to speciation. However, our knowledge of the underlying sex-specific molecular mechanisms is still scarce. Here we show that the highly conserved gene, Doublesex (Dsx), regulates rapidly diverging sexually dimorphic traits in the model parasitoid wasp Nasonia vitripennis (Hymenoptera: Pteromalidae). We present here the revised full Dsx gene structure with an alternative first exon, and two additional male NvDsx isoforms, which gives important insights into the evolution of the sex-specific oligomerization domains and C-termini. We show the sex-specific NvDsx expression throughout development, and demonstrate that transient NvDsx silencing in different male developmental stages dramatically shifts the morphology of two sexually dimorphic traits from male to female, with the effect being dependent on the timing of silencing. In addition, transient silencing of NvDsx in early male larvae affects male genitalia tissue growth but not morphology. This indicates that male NvDsx is actively required to suppress female-specific traits and to promote male-specific traits during specific developmental windows. These results also strongly suggest that in N. vitripennis most sex-specific tissues fully differentiate in the embryonic stage and only need the input of NvDsx for growth afterwards. This provides a first insight into the regulatory activity of Dsx in the Hymenoptera and will help to better understand the evolutionary and molecular mechanisms involved in sex-specific development in this parasitoid wasp, which can eventually lead to the development of new synthetic genetics-based tools for biological pest control by parasitoid wasps.Significance StatementIn insects, male and female differentiation is regulated by the highly conserved transcription factor Doublesex (Dsx). The role of Dsx in regulating rapidly evolving sexually dimorphic traits has received less attention, especially in wasps and bees. Here, we mainly focused on Dsx regulation of two sexually dimorphic traits and male genitalia morphology in the parasitoid wasp, Nasonia vitripennis. We demonstrate that Dsx actively regulates male-specific tissue growth and morphology during specific developmental windows. These findings will help to better understand the molecular mechanisms underlying the rapid evolution of sexual differentiation and sexually dimorphic traits in insects, but may also be the starting point for the development of new tools for biological control of pest insects by parasitoid wasps.

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Section: Resultssupporting

confidence: 82%

Section: Resultsmentioning

confidence: 90%

Sexually dimorphic traits and male-specific differentiation are actively regulated by Doublesex during specific developmental windows inNasonia vitripennis

Wang¹,

Rensink

Fricke³

et al. 2020

Preprint

View full text Add to dashboard Cite

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“…Three female isoforms of dsx occur in P. polytes , which differ in their extent of usage of exons 3 and 4 ( figure 3 a ) [ 19 , 51 ]. We traced stage- and tissue-specific isoform activity using a combination of isoform-specific search in de-novo assembled transcriptomes and PCRs using isoform-specific primers ( figure 3 b and electronic supplementary material, table S6).…”

Section: Resultsmentioning

confidence: 99%

“…The embryonic sex differentiation may be based purely on male-specific (dsxM) and female-specific (dsxF) isoforms and their downstream targets that set in motion basic sex differences, as seen in other insects [51,55]. In P. polytes, mimetic alleles do not seem to affect larval phenotype and development [52], and allele-specific phenotypic changes only start appearing late during pupal stages [53].…”

Section: Female Isoforms Of Doublesex Co-express In Most Tissues Butmentioning

confidence: 99%

Tissue-specific developmental regulation and isoform usage underlie the role ofdoublesexin sex differentiation and mimicry inPapilioswallowtails

2020

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Adaptive phenotypes often arise by rewiring existing developmental networks. Co-option of transcription factors in novel contexts has facilitated the evolution of ecologically important adaptations. doublesex ( dsx ) governs fundamental sex differentiation during embryonic stages and has been co-opted to regulate diverse secondary sexual dimorphisms during pupal development of holometabolous insects. In Papilio polytes , dsx regulates female-limited mimetic polymorphism, resulting in mimetic and non-mimetic forms. To understand how a critical gene such as dsx regulates novel wing patterns while maintaining its basic function in sex differentiation, we traced its expression through metamorphosis in P. polytes using developmental transcriptome data. We found three key dsx expression peaks: (i) eggs in pre- and post-ovisposition stages; (ii) developing wing discs and body in final larval instar; and (iii) 3-day pupae. We identified potential dsx targets using co-expression and differential expression analysis, and found distinct, non-overlapping sets of genes—containing putative dsx- binding sites—in developing wings versus abdominal tissue and in mimetic versus non-mimetic individuals. This suggests that dsx regulates distinct downstream targets in different tissues and wing colour morphs and has perhaps acquired new, previously unknown targets, for regulating mimetic polymorphism. Additionally, we observed that the three female isoforms of dsx were differentially expressed across stages (from eggs to adults) and tissues and differed in their protein structure. This may promote differential protein–protein interactions for each isoform and facilitate sub-functionalization of dsx activity across its isoforms. Our findings suggest that dsx employs tissue-specific downstream effectors and partitions its functions across multiple isoforms to regulate primary and secondary sexual dimorphism through insect development.

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“…2004; Baral et al. 2019). Third, fitness costs of higher pleiotropy may be overcome by increasing functional modularity through the relaxation of stabilizing selection (Collet et al.…”

Section: Discussionmentioning

confidence: 99%

Copulatory function and development shape modular architecture of genitalia differently in males and females

et al. 2020

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Genitalia are multitasking structures whose development is mediated by numerous regulatory pathways. This multifactorial nature provides an avenue for multiple sources of selection. As a result, genitalia tend to evolve as modular systems comprising semi‐independent subsets of structures, yet the processes that give rise to those patterns are still poorly understood. Here, we ask what are the relative roles of development and function in shaping modular patterns of genitalia within populations and across species of stink‐bugs. We found that male genitalia are less integrated, more modular, and primarily shaped by functional demands. In contrast, females show higher integration, lower modularity, and a predominant role of developmental processes. Further, interactions among parts of each sex are more determinant to modularity than those between the sexes, and patterns of modularity are equivalent between and within species. Our results strongly indicate that genitalia have been subjected to sex‐specific selection, although male and female genitalia are homologous and functionally associated. Moreover, modular patterns are seemingly constant in the evolutionary history of stink‐bugs, suggesting a scenario of multivariate stabilizing selection within each sex. Our study demonstrates that interactions among genital parts of the same sex may be more fundamental to genital evolution than previously thought.

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Genetic architecture and sex-specific selection govern modular, male-biased evolution of doublesex

Cited by 34 publications

References 41 publications

Sexually dimorphic traits and male-specific differentiation are actively regulated by Doublesex during specific developmental windows inNasonia vitripennis

Sexually dimorphic traits and male-specific differentiation are actively regulated by Doublesex during specific developmental windows inNasonia vitripennis

Tissue-specific developmental regulation and isoform usage underlie the role ofdoublesexin sex differentiation and mimicry inPapilioswallowtails

Copulatory function and development shape modular architecture of genitalia differently in males and females

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