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A masculinizing supergene underlies an exaggerated male reproductive morph in a spider

Nature Ecology & Evolution volume 6, pages 195–206 (2022)Cite this article

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Abstract

In many species, individuals can develop into strikingly different morphs, which are determined by a simple Mendelian locus. How selection shapes loci that control complex phenotypic differences remains poorly understood. In the spider Oedothorax gibbosus, males develop either into a ‘hunched’ morph with conspicuous head structures or as a fast-developing ‘flat’ morph with a female-like appearance. We show that the hunched-determining allele contains a unique genomic fragment of approximately 3 megabases that is absent in the flat-determining allele. This fragment comprises dozens of genes that duplicated from genes found at the same as well as different chromosomes. All functional duplicates, including a duplicate of the key sexual differentiation regulatory gene doublesex, show male-specific expression, which illustrates their integrated role as a masculinizing supergene. Our findings demonstrate how extensive indel polymorphisms and duplications of regulatory genes may contribute to the evolution of co-adapted gene clusters, sex-limited reproductive morphs and the enigmatic evolution of exaggerated sexual traits in general.

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Fig. 1: Head structures of O. gibbosus and outgroup species.
Fig. 2: Genetic mapping, identification and characterization of the genomic region underlying the male reproductive morphs.
Fig. 3: Haplotype relationships and recombination at the G locus (ctg337: 640–660 kb).
Fig. 4: Identification and characterization of hunch-specific sequences spanning at least 3 Mb.
Fig. 5: Morph- and sex-specific gene expression patterns.
Fig. 6: Proposed structure and function of the morph-determining alleles at the G locus in males and females.

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Data availability

Raw DNA sequences have been deposited in the NCBI SRA (PRJNA681589). The assembled and annotated genome is available at NCBI (JAFNEN010000000). Tables with contig coverage depth and breadth, gene expression data, functional annotation, variant call format (vcf) files, linkage map results, paralogue identification and code used for the analysis and graph construction are available at Dryad70.

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Acknowledgements

We thank A. Mariscal for help in RNA extraction; K. Smistek, A. Henrard and C. Locatelli for help in taking pictures of the specimens; F. De Block, S. Cogneau, V. Vandomme and E. Veltjen for help in sampling and breeding; L. Sterck for advice on genome annotation and gene curation; N. Edelman for sharing code to depict phylogentic trees; M. Horn and T. Halter (University of Vienna) for help in the identification of contaminant bacterial contigs; and M. Berthet for help in illustrations. We thank P. Rastas for sharing scripts to integrate 10× reads in Lep-Anchor and three anonymous reviewers for their excellent suggestions and remarks on a previous version of this manuscript. The computational resources (Stevin Supercomputer Infrastructure) and services used in this work were provided by the VSC (Flemish Supercomputer Center), funded by Ghent University, FWO and the Flemish Government department EWI. This work was financially supported by Fund for Scientific Research – Flanders (1527617N) and the Joint Experimental and Molecular Unit (JEMU), funded by the Belgian Science Policy, and Austrian Science Fund Austrian Science (doc.funds programme DOC 69-B). Specimen(s) were scanned using the μCT facility in the framework of the DIGIT04 project of the Royal Belgian Institute of Natural Sciences.

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  1. Stephan Köstlbacher

    Present address: Laboratory of Microbiology, Wageningen University and Research, Wageningen, the Netherlands

Authors and Affiliations

  1. OD Taxonomy and Phylogeny, Royal Belgian Institute of Natural Sciences, Brussels, Belgium

    Frederik Hendrickx, Zoë De Corte, Gontran Sonet & Carl Vangestel

  2. Terrestrial Ecology Unity, Biology Department, Ghent University, Gent, Belgium

    Frederik Hendrickx & Carl Vangestel

  3. Department of Biology, University of Puerto Rico, Rio Piedras Campus, San Juan, Puerto Rico

    Steven M. Van Belleghem

  4. Centre for Microbiology and Environmental Systems Science, University of Vienna, Vienna, Austria

    Stephan Köstlbacher

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Contributions

F.H. conceived the project. F.H., G.S. and C.V. performed the experiments. F.H., Z.D.C., S.M.V.B., S.K. and C.V. analysed the data. F.H. drafted the manuscript with input from all authors.

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Correspondence to Frederik Hendrickx.

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Extended data

Extended Data Fig. 1 Cephalic structures of O. gibbosus and some other dwarf spider species.

(a) High-resolution micro-CT scanning of the carapaces of the hunched and flat male morphs of Oedothorax gibbosus. Legs and abdomen were removed to visualize the difference in cephalic structures. (b) Examples of male carapaces within the subfamily of dwarf spiders (Erigoninae). Depicted species are Walckenaeria furcillata, Walckenaeria mitrata, Savignya frontata, Walckenaeria acuminata, Trematocephalus cristatus, Peponocranium ludicrum, Hypomma bituberculatum and Notioscopus sarcinatus. Scale bar below each species is 500 µm.

Extended Data Fig. 2 Patterns of nucleotide diversity and divergence around the G-locus.

Nucleotide divergence (dxy, black) and diversity (π) in hunched (red) and flat (blue) males at (a) contigs identified by association analysis (20 kb windows) and (b) at ctg337 (10 kb windows).

Extended Data Fig. 3 Patterns of linkage disequilibrium around the G-locus region.

(a) Linkage disequilibrium (LD) plot (R²) for contig ctg337 based on all 16 resequenced individuals. SNP pairs in perfect LD (R² = 1) are indicated in red. Upper grey bar corresponds to region 500 kb – 800 kb displayed in Fig. 2c, with black bar corresponding to the most differentiated region between the two male morphs (640 kb – 660 kb). (b) Linkage disequilibrium (LD) plot (R²) between contig ctg337 and the 97 hunch-specific contigs based on all 8 resequenced hunched individuals. Upper black bar corresponds to region 500 kb – 800 kb displayed in Fig. 2c. Hunch-specific contigs are separated by grey-lines.

Extended Data Fig. 4 Structural variations at the G-locus region.

Details of read mappings in region 600 kb - 620 kb (upper panel) and 620 kb – 645 kb (lower panel) at ctg337. (a) Overview of region 500 kb – 800 kb on ctg337 (see Fig.2 for details) with yellow transparent rectangle highlighting the region detailed in the panels below. (b) IGV (Integrated Genomics Viewer) screenprint of mapped PacBio reads from a heterozygote hunched [Gg] and a homozygote flat [gg] offspring pool. Braces depict reads assigned to the G and g allele. Dark grey tracks show the read coverage depth at each position. Light grey tracks show mapped reads, with positions that are different from the reference sequence color coded. (c) Mapping of Illumina short reads from a homozygote hunched [GG](D1086_G) and a homozygote flat [gg](D1091_T) individual. (d) location of SNPs that segregate according to expected genotypes of the resequenced individuals at the G-locus. (e) Schematic representation of the proposed structure of the G (red) and g (blue) allele.

Extended Data Fig. 5 Identification of hunch-specific sequences.

(a) Strategy to identify contigs that are only present in the hunch-determining allele. Contigs that were considered hunch-specific have (i) significant lower coverage depths in the eight resequenced flat individuals compared to the eight resequenced hunched individuals (left panel) and (ii) positions that were only covered by Illumina short-reads in all resequenced hunched individuals and the PacBio reads of the pool of hunched offspring, but in none of the flat individuals and the pool of flat offspring (right panel, indicated in light blue). (b) Difference in coverage depth (log2 fold change) of the contigs from the PacBio reference assembly (‘Ogibo_PacBio_wtdbg2_het’) between the resequenced flat [8 homozygotes] and hunched [6 heterozygotes and 2 homozygotes] individuals (left panel) and two homozygote flat and two homozygote hunched individuals from population D only (right panel). Each dot represents a contig, with green contigs being identified as hunch specific contigs (see Supplementary text 1 for details). Y-axis displays contig length (log10 transformed).

Extended Data Fig. 6 Sex-specific expression of differentially expressed genes between the two male morphs.

Genes are color coded according to their sex-specific expression in (a) a hunched (Gg) male vs. female comparison or (b) a flat (gg) male vs. female comparison. Red genes are upregulated in males, blue genes are upregulated in females and grey genes are not differentially expressed between the sexes.

Extended Data Fig. 7 Male-specific expression of genes located on the hunch-specific sequences and their paralogs.

(a) Distribution of the log2 fold change in gene expression between Gg males (hunched males, n = 5) and Gg females (n = 4) across all predicted genes (left, grey violin), genes located within the hunch-specific sequence (central, light green violin) and the paralogs of the genes located on the hunch-specific sequence (right, dark green violin). Positive values refer to male biased expression. Genes with log2 fold change larger than 10 or smaller than −10 were truncated to 10 and −10 respectively. (b) Correlation of the sex-specific expression of genes located on the hunch-specific sequence and the sex-specific expression of their closest paralog located outside the hunch-specific sequence (rP = 0.53, P < 0.0001). Dot size is proportional to the average normalized expression of each gene. Genes depicted in green are differentially expressed between the two male morphs and genes depicted in grey are only marginally expressed in hunched and flat males and females (normalized expression < 1). Positive values refer to male biased expression.

Extended Data Fig. 8 Alignment and phylogenetic relationship of the encoded protein sequences of Dmrt of O. gibbosus and those of the spider Parasteatoda tepidariorum.

Alignment (COBALT) and maximum likelihood tree of the encoded protein sequences of all eleven Dmrt genes of O. gibbosus (Og) and those of the spider Parasteatoda tepidariorum (Pt). The tree was constructed based on the COBALT alignment (grey bars above sequences), with distances computed with RAxML v. 8.2.11 using the WAG substitution model and gamma distributed rate variation among sites. Bootstrap values are presented next to the branches. Red bar above alignments shows the location of the DM domain. Grey bar shows the alignment part that was used for tree construction. Track below the grey bar shows the distribution of conserved sites. The Dmrt gene located on the hunched fragment is indicated in green. Dmrt genes clustered on ctg151 are indicated in red.

Extended Data Fig. 9 Alignment and phylogenetic relationship of the encoded protein sequences of AChE-like genes of O. gibbosus and those of the spider Parasteatoda tepidariorum.

Alignment (COBALT) and maximum likelihood tree of the encoded protein sequences of all Acetylcholinesterase (AChE) related genes of O. gibbosus (‘Og_x’) and those of the spider Parasteatoda tepidariorum (‘XP_x’). The tree was constructed on the COBALT alignment with RAxML v. 8.2.11 using the WAG substitution model and gamma distributed rate variation among sites. Bootstrap values are presented next to the branches. Red bar above alignments shows the location of the carboxylesterase domain. Track below the red bar shows the distribution of conserved sites. The AChE genes located on the hunch-specific sequence are indicated with a green arrow, while those located outside the hunch-specific sequence are indicated in black. Sequence names of P. tepidariorum are color- coded according to their predicted function.

Extended Data Fig. 10 Evolutionary history of the supergene.

(a) Scaled coverage depths of coding sequences (CDS) located on the hunch-specific sequence (green) and the closest paralogs of these CDS (grey) for hunched males, flat males and the closely related species O. retusus and O. fuscus. Groups that are not significantly different are indicated with the same alphabetic character for CDS located on the hunch-specific sequence (upper row) and their paralogs (lower row) (Kruskall-Wallis ANOVA with Bonferroni corrected Wilcoxon pairwise rank sum test). Boxes represent median (centre line); upper and lower quartiles (box limits); 1.5x interquartile range (vertical line limits) and outliers (points). (b) Chronogram of the divergence between the Dmrt paralogs (above) and the divergence between the G and g allele (below). Both chronograms were scaled to the divergence from the outgroup species O. retusus. Triangles represent sequences within each clade. Divergence between the two alleles was based on the same genomic fragment as in Fig. 3 (ctg337: 640 kb – 660 kb). Node labels represent the posterior probability support of the clades. Blue bars represent the 95% Bayesian credible intervals of the divergence times. Midpoint rooting was used to root the trees.

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Hendrickx, F., De Corte, Z., Sonet, G. et al. A masculinizing supergene underlies an exaggerated male reproductive morph in a spider. Nat Ecol Evol 6, 195–206 (2022). https://doi.org/10.1038/s41559-021-01626-6

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