Research ArticleEVOLUTIONARY BIOLOGY

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

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Science Advances  08 May 2019:
Vol. 5, no. 5, eaau3753
DOI: 10.1126/sciadv.aau3753
  • Fig. 1 Functional roles of dsx during development of holometabolous insects.

    (A) The activity of dsx in sex-determination pathways illustrated in a representative genus of each insect order. (B) Examples of sexual weapons (large mandibles and horns in male beetles), sexual ornaments (sex combs in male Drosophila), large wings associated with dispersal in female Nasonia, and female-limited mimetic polymorphism in swallowtail butterflies that are developmentally regulated by dsx (12, 13, 15). (C) Developmental outcomes regulated by dsx fall into three broad functional categories apart from early embryonic sexual differentiation. masc, masculinizer; fem, feminizer. [Photo credit: N. Gompel (Drosophila melanogaster), A. P. Moczek (Onthophagus taurus), R. R. Choudhury (Nasonia vitripennis), and M. Yago (Cyclommatus metallifer and Trypoxylus dichotomous), used with permission, and K. Kunte (P. polytes)].

  • Fig. 2 Phylogenetic relationships and exon usage among insect orders in relation to dsx evolution.

    (A) A mito-nuclear phylogeny of the four orders sampled. (B) dsx gene tree based on its coding sequence. In (A) and (B), adjacent clades are colored pink and purple, and the outgroups are colored gray and black, for contrast. (C) Exon usage of dsx across insect orders. Exons are numbered arbitrarily on the basis of mRNA initiation as per scientific convention and indicate a generalized exonic organization of dsx in holometabolous insects. Order-wise exon organization of the translated product of dsx is depicted in the center with domains and sex-specific regions colored based on sequence homology. Only those exons that are translated are shown, but 5′ and 3′ untranslated exons (not shown) may have poorly understood regulatory functions. OD1 is a DM DNA-binding domain, and OD2 is a DSX dimerization domain. Exon 5a, unique to Coleoptera, is homologous to OD2.

  • Fig. 3 Exon-level molecular evolution and functional partitioning of dsx across insect orders.

    Rates of molecular evolution (average substitutions; top panels) and signatures of selection with reference to nonsynonymous and synonymous substitutions (dN/dS ratios; bottom panels) per codon for each dsx exon are shown separately for each insect group. The exons are arranged according to sequence homology, and the two domain regions are highlighted. Arrows point toward sites under episodic (green arrows) and/or pervasive (magenta arrows) positive selection.

  • Fig. 4 Molecular evolution across genic regions.

    Rate of molecular evolution across different genic regions (A) and proportion of sites under purifying selection (B), in each insect group.

  • Fig. 5 Protein structural conservation in various domain and sex-specific regions of dsx in insects.

    Drosophila melanogaster crystal structures for OD1 and OD2 were used as a reference for protein modeling from the dsx sequences. (A) Superimposition of protein structures in each exonic region. RMSD as a measure of structural deviation between protein backbones and the number of species used for protein modeling are also shown. (B) Comparison of protein structural differences across exonic regions and insect orders, which highlights male-biased evolution of the Dsx protein. Since protein structures are relatively similar in sister species, only representatives of each genus were chosen for this comparison (see table S1 for the list of species used for modeling and fig. S1 for structures of domains and sex-specific regions of each insect order).

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/5/5/eaau3753/DC1

    Fig. S1. Protein structural conservation in various domain and sex-specific regions of Dsx across insect orders.

    Table S1. Species, GenBank accession numbers, and exons of dsx sequences used in this study.

    Table S2. Regression log file.

    Table S3. Sites under episodic and pervasive positive selection in different insect groups and specific lineages.

  • Supplementary Materials

    The PDF file includes:

    • Fig. S1. Protein structural conservation in various domain and sex-specific regions of Dsx across insect orders.
    • Legends for tables S1 to S3

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    Other Supplementary Material for this manuscript includes the following:

    • Table S1 (Microsoft Excel format). Species, GenBank accession numbers, and exons of dsx sequences used in this study.
    • Table S2 (.txt format). Regression log file.
    • Table S3 (Microsoft Excel format). Sites under episodic and pervasive positive selection in different insect groups and specific lineages.

    Files in this Data Supplement:

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