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Temporal stability of sex ratio distorter prevalence in natural populations of the isopod Armadillidium vulgare

Heredity volume 133, pages 287–297 (2024)Cite this article

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Abstract

In the terrestrial isopod Armadillidium vulgare, many females produce progenies with female-biased sex ratios due to two feminizing sex ratio distorters (SRD): Wolbachia endosymbionts and a nuclear non-mendelian locus called the f element. To investigate the potential impact of these SRD on the evolution of host sex determination, we analyzed their temporal distribution in six A. vulgare populations sampled between 2003 and 2017, for a total of 29 time points. SRD distribution was heterogeneous among populations despite their close geographic locations, so that when one SRD was frequent in a population, the other SRD was rare. In contrast with spatial heterogeneity, our results overall did not reveal substantial temporal variability in SRD prevalence within populations, suggesting equilibria in SRD evolutionary dynamics may have been reached or nearly so. Temporal stability was also generally reflected in mitochondrial and nuclear variation. Nevertheless, in a population, a Wolbachia strain replacement coincided with changes in mitochondrial composition but no change in nuclear composition, thus constituting a typical example of mitochondrial sweep caused by endosymbiont rise in frequency. Rare incongruence between Wolbachia strains and mitochondrial haplotypes suggested the occurrence of intraspecific horizontal transmission, making it a biologically relevant parameter for Wolbachia evolutionary dynamics in A. vulgare. Overall, our results provide an empirical basis for future studies on SRD evolutionary dynamics in the context of multiple sex determination factors co-existing within a single species, to ultimately evaluate the impact of SRD on the evolution of host sex determination mechanisms and sex chromosomes.

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Fig. 1: Geographic location of the six Armadillidium vulgare populations analyzed in this study.
Fig. 2: Prevalence of Wolbachia and the f element in six Armadillidium vulgare populations sampled at different time points.
Fig. 3: Mitochondrial haplotype network of six Armadillidium vulgare populations sampled at different time points.
Fig. 4: Mitochondrial haplotype counts across years for three Armadillidium vulgare populations.
Fig. 5: Structure analysis of six Armadillidiium vulgare populations sampled at different time points.
Fig. 6: Discriminant Analysis of Principal Components scatterplot.

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Data availability

Mitotypes are available in GenBank under accession numbers OR074129 to OR074131. All other data are provided in the supplementary information.

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Acknowledgements

We thank Sébastien Verne and Victorien Valette for assistance with sample collection. This work was funded by Agence Nationale de la Recherche Grants ANR-15-CE32-0006 (CytoSexDet) to RC and TR, and ANR-20-CE02-0004 (SymChroSex) to JP, and intramural funds from the CNRS and the University of Poitiers.

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Authors and Affiliations

  1. Laboratoire Ecologie et Biologie des Interactions, Equipe Ecologie Evolution Symbiose, Université de Poitiers, UMR CNRS 7267, Bât. B31, 3 rue Jacques Fort, TSA 51106, Poitiers, Cedex 9, France

    Sylvine Durand, Romain Pigeault, Isabelle Giraud, Anaïs Loisier, Nicolas Bech, Frédéric Grandjean, Jean Peccoud & Richard Cordaux

  2. Laboratoire Biogéosciences, Université Bourgogne Franche-Comté, UMR CNRS 6282, Dijon, France

    Thierry Rigaud

  3. Université Paris-Saclay, CNRS, IRD, UMR Évolution Génomes Comportement Écologie, Gif-sur-Yvette, France

    Richard Cordaux

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  1. Sylvine Durand
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Contributions

RC, JP and TR designed the experiments. FG, NB and JP sampled populations. SD, IG and AL performed laboratory work. SD, RP and NB performed data analyses. RC and SD wrote the first draft of the manuscript. TR, JP, NB, RP and FG amended the manuscript.

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Correspondence to Richard Cordaux.

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No specific permission was required for sampling the populations from Beauvoir, Chizé, Gript and La Crèche because they were located in public areas. Populations from Coulombiers and Poitiers were sampled on private lands after the land owners gave permission to conduct sampling on the sites.

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Durand, S., Pigeault, R., Giraud, I. et al. Temporal stability of sex ratio distorter prevalence in natural populations of the isopod Armadillidium vulgare. Heredity 133, 287–297 (2024). https://doi.org/10.1038/s41437-024-00713-1

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