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Evolution and development of male-specific leg brushes in Drosophilidae

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Abstract

The origin, diversification, and secondary loss of sexually dimorphic characters are common in animal evolution. In some cases, structurally and functionally similar traits have evolved independently in multiple lineages. Prominent examples of such traits include the male-specific grasping structures that develop on the front legs of many dipteran insects. In this report, we describe the evolution and development of one of these structures, the male-specific “sex brush.” The sex brush is composed of densely packed, irregularly arranged modified bristles and is found in several distantly related lineages in the family Drosophilidae. Phylogenetic analysis using 250 genes from over 200 species provides modest support for a single origin of the sex brush followed by many secondary losses; however, independent origins of the sex brush cannot be ruled out completely. We show that sex brushes develop in very similar ways in all brush-bearing lineages. The dense packing of brush hairs is explained by the specification of bristle precursor cells at a near-maximum density permitted by the lateral inhibition mechanism, as well as by the reduced size of the surrounding epithelial cells. In contrast to the female and the ancestral male condition, where bristles are arranged in stereotypical, precisely spaced rows, cell migration does not contribute appreciably to the formation of the sex brush. The complex phylogenetic history of the sex brush can make it a valuable model for investigating coevolution of sex-specific morphology and mating behavior.

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The datasets used in this study are included in the manuscript or will be made available in GenBank upon publication.

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Acknowledgements

We thank the US Drosophila species stock center, Ehime University Drosophila stock center, J.-R. David, S. Prigent, and M. Watada for Drosophila strains and specimens; Developmental Studies Hybridoma Bank for antibodies; A. Comeault, A. Gloss, M. Lang, D. Matute, D. Miller, V. Orgogozo, and N. Whiteman for genome assemblies; M. Toda for advice on Zaprionus phylogeny; G. Rice for D. immigrans images; and A. Yassin for comments on the manuscript. We also thank the MCB Light Microscopy Imaging Facility, Department of Cell Biology and Human Anatomy EM Lab, and Materials Science and Engineering AMCaT Lab at UC Davis for equipment and imaging assistance, and Gwyneth Card and W. Ryan Williamson for use of the Photron camera. AK and OB are grateful to N. Gompel for allowing some of this work to be conducted in his lab while on a sabbatical visit, and to members of the Gompel lab for treating them as their labmates.

Funding

This work was supported by NIH grant 5R35GM122592 to AK, NIH grant F32 GM135998 to BYK, and by funds from Ludwig-Maximilians-Universität München to Nicolas Gompel, in whose lab some of the work was conducted. The Olympus FV1000 confocal used in this study was purchased using NIH Shared Instrumentation Grant 1S10RR019266-01.

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Authors and Affiliations

  1. Department of Evolution and Ecology, University of California–Davis, Davis, CA, USA

    Kohtaro Tanaka, Olga Barmina, Ammon Thompson & Artyom Kopp

  2. Basic Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA

    Kohtaro Tanaka

  3. Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, USA

    Jonathan H. Massey

  4. Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, VA, USA

    Jonathan H. Massey

  5. Department of Biology, Stanford University, Stanford, CA, 94305, USA

    Bernard Y. Kim

  6. Department of Genetics, University of North Carolina, Chapel Hill, NC, 27599, USA

    Anton Suvorov

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  1. Kohtaro Tanaka
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  7. Artyom Kopp
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AK conceived the study. KT, OB, BYK, AK and JHM performed experiments and collected data. KT, BYK, AS, AT, and AK analyzed the data. KT and AK wrote the manuscript with contributions from AT, BYK, and AS.

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Correspondence to Kohtaro Tanaka.

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Tanaka, K., Barmina, O., Thompson, A. et al. Evolution and development of male-specific leg brushes in Drosophilidae. Dev Genes Evol 232, 89–102 (2022). https://doi.org/10.1007/s00427-022-00694-3

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