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Sexual selection on a female copulatory device in an insect with nuptial gifts

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Abstract

Male genitalia are rapidly evolving structures, often driven by sexual selection to increase fertilisation success. Although sexual selection on females can be strong in systems where males provide offspring care or feed their mates, sometimes resulting in the evolution of female ornamentation, there are no actual estimates of direct sexual selection on female genitalia. In a New Zealand ground weta, Hemiandrus pallitarsis (Orthoptera: Ensifera, Anostostomatidae), females possess a genitalic device (the accessory organ) that is necessary for successful copulation and the acquisition of glandular food-gifts from males. These nutritious gifts are known to result in sexual competition among females in other ensiferan species. In ground weta, the gifts are probably important in avoiding starvation during a months-long period when caring for (their lifetime production of) eggs and offspring. Here, we test the hypothesis that the accessory organ is a sexually selected device in H. pallitarsis by measuring the female Bateman gradient, Jones index, and directional sexual selection on the accessory organ. Using newly developed and characterised microsatellite loci, we analyse offspring and/or stored sperm to estimate female mating frequency for the first time in ground weta. As predicted, we found both a positive Bateman gradient and Jones index for females, and evidence of directional sexual selection on accessory organ length. Although organ length does not correlate well with female fecundity, it may increase mating success by indicating her condition and thus quality of her offspring care.

Significance statement

Female genitalia have largely been studied in the context of exerting selection on males, while the potential for selection on females via mate acquisition or manipulation of males is virtually unstudied. Such selection may be relevant in systems where males make investments in reproduction (offspring-care; mate-feeding), and females are subject to strong sexual selection, occasionally possessing sexual ornaments. Using microsatellite analysis of offspring and stored sperm to estimate mating frequency, we provide the first evidence of directional sexual selection on a female genital device (accessory organ) found in species of maternal care-providing ground weta. In our focal species, Hemiandrus pallitarsis, we found that females with more mates produced more offspring and females with longer accessory organs obtained more mates. These findings suggest that the female genital device is a secondary sexual trait, although may have additional mechanical functions.

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Data availability

All data generated or analysed during this study are available in the Dryad repository: https://doi.org/10.5061/dryad.s1rn8pkbh.

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Acknowledgements

We thank Mary Morgan Richards and Lindsay Coome for their help collecting data; Doug Currie, Marc Johnson, Rosalind Murray, and Clint Kelly for comments on the research and manuscript; and the New Zealand Department of Conservation (for permits) and anonymous referees for valuable comments on the manuscript.

Funding

This research was supported by a Natural Sciences and Engineering Research Council of Canada Discovery Grant to DTG.

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Correspondence to Jessica H. Browne.

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The authors declare no competing interests.

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Communicated by N. Wedell

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Browne, J.H., Gwynne, D.T. Sexual selection on a female copulatory device in an insect with nuptial gifts. Behav Ecol Sociobiol 77, 138 (2023). https://doi.org/10.1007/s00265-023-03415-6

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  • DOI: https://doi.org/10.1007/s00265-023-03415-6

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