Gene expression during genital morphogenesis in the ground beetle <i>Carabus maiyasanus</i>

Nomura, Shota; Fujisawa, Tomochika; Sota, Teiji

doi:10.1111/1744-7917.12712

Cited by 5 publications

(14 citation statements)

References 55 publications

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“…Previously, we clarified the expression timing profiles of genes related to metamorphosis and genital morphogenesis of C . maiyasanus at different stages, which provided basic information for studying interspecific differences in gene expression related to species-specific genital morphology ( Nomura et al 2020 ).…”

Section: Introductionmentioning

confidence: 99%

Role of Sex-Concordant Gene Expression in the Coevolution of Exaggerated Male and Female Genitalia in a Beetle Group

Nomura

Fujisawa

Sota

2021

Molecular Biology and Evolution

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Some sexual traits, including genitalia, have undergone coevolutionary diversification toward exaggerated states in both sexes among closely related species, but the underlying genetic mechanisms that allow correlated character evolution between the sexes are poorly understood. Here, we studied interspecific differences in gene expression timing profiles involved in the correlated evolution of corresponding male and female genital parts in three species of ground beetle in Carabus (Ohomopterus). The male and female genital parts maintain morphological matching, whereas large interspecific variation in genital part size has occurred in the genital coevolution between the sexes toward exaggeration. We analyzed differences in gene expression involved in the interspecific differences in genital morphology using whole transcriptome data from genital tissues during genital morphogenesis. We found that the gene expression variance attributed to sex was negligible for the majority of differentially expressed genes, thus exhibiting sex-concordant expression, although large variances were attributed to stage and species differences. For each sex, we obtained co-expression gene networks and hub genes from differentially expressed genes between species that might be involved in interspecific differences in genital morphology. These gene networks were common to both sexes, and both sex-discordant and sex-concordant gene expression were likely involved in species-specific genital morphology. In particular, the gene expression related to exaggerated genital size showed no significant intersexual differences, implying that the genital sizes in both sexes are controlled by the same gene network with sex-concordant expression patterns, thereby facilitating the coevolution of exaggerated genitalia between the sexes while maintaining intersexual matching.

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Section: Introductionmentioning

confidence: 99%

Role of Sex-Concordant Gene Expression in the Coevolution of Exaggerated Male and Female Genitalia in a Beetle Group

Nomura

Fujisawa

Sota

2021

Molecular Biology and Evolution

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“…Our results revealed the spatio–temporal dynamics of the development of divergent genital parts. These findings are expected to facilitate future gene expression and knockdown analyses using Ohomopterus ground beetles, which are currently based on broad tissue types and rough developmental stages, introducing uncertainties in the identification of candidate genes associated with divergence in genital morphologies (Fujimaki et al, 2014; Fujisawa et al, 2019; Nomura et al, 2019; Sota et al, 2018). Our results improve our understanding of the precise developmental stages and tissues contributing to species‐specific genital differentiation and will contribute to the construction a novel platform for evo–devo studies of the diversification of genital morphologies.…”

Section: Discussionmentioning

confidence: 99%

“…The CP and VA in Ohomopterus ground beetles have been studied in behavioral and evolutionary contexts, including the identification of candidate genes or genomic regions associated with genital diversification (Fujimaki et al, 2014; Fujisawa et al, 2019; Nomura et al, 2019; Sasabe et al, 2007, 2010; Sota et al, 2018). An understanding of the morphogenesis of genitalia, including spatio–temporal differences between species, can provide a precise framework for analyses of the differential expression and functions of candidate genes.…”

Section: Introductionmentioning

confidence: 99%

Heterochrony and growth rate variation mediate the development of divergent genital morphologies in closely related Ohomopterus ground beetles

Terada

Nishimura

Hirayama

et al. 2020

Evolution and Development

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The rapid divergence of genital morphology is well studied in the context of sexual selection and speciation; however, little is known about the developmental mechanisms underlying divergence in genitalia. Ground beetles in the subgenus Ohomopterus genus Carabus have species‐specific genitalia that show coevolutionary divergence between the sexes. In this study, using X‐ray microcomputed tomography, we examined the morphogenesis of male and female genitalia in two closely related Ohomopterus species with divergent genital morphologies. The morphogenetic processes generating the male and female genitalia at the pupal stage were qualitatively similar in the two species. The male aedeagus and internal sac and female bursa copulatrix were partially formed at pupation and developed gradually thereafter. The species‐specific genital parts, male copulatory piece, and female vaginal appendix differed in the timing and rate of development. The relatively long copulatory piece of Carabus maiyasanus began to develop earlier, but subsequent rates of growth were similar in the two species. The timing of the formation of the vaginal appendix and initial growth rates were similar, but subsequent rapid growth led to a longer vaginal appendix in C. maiyasanus. Thus, substantial interspecific differences in the size of genital parts were mediated by different underlying developmental mechanisms between the sexes (i.e., a shift in the developmental schedule in males and a change in growth rate in females). These results revealed the spatio–temporal dynamics of species‐specific genital structure development, providing a novel platform for evo–devo studies of the diversification of genital morphologies.

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“…2017; Nomura et al. 2019), what is the role played by development in biasing (co)evolution? Despite often coevolving, male and female genitalia may still exhibit strikingly divergent degrees of elaboration, rates of differentiation and diversity of associated developmental genes (Genevcius et al.…”

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confidence: 99%

“…2018; Nomura et al. 2019; Simmons and Fitzpatrick 2019). May these differences be explained by contrasting roles of development and function acting differentially on males and females?…”

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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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Gene expression during genital morphogenesis in the ground beetle Carabus maiyasanus

Cited by 5 publications

References 55 publications

Role of Sex-Concordant Gene Expression in the Coevolution of Exaggerated Male and Female Genitalia in a Beetle Group

Role of Sex-Concordant Gene Expression in the Coevolution of Exaggerated Male and Female Genitalia in a Beetle Group

Heterochrony and growth rate variation mediate the development of divergent genital morphologies in closely related Ohomopterus ground beetles

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

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