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Lack of Female Preference for Nuptial Gifts May Have Led to Loss of the Male Sexual Trait

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Abstract

Evolutionary loss of sexual traits may occur if the forces that maintain those traits weaken or disappear. Females may evolve resistance or a change in preference if the male sexual trait decreases their fitness (e.g., coercive or deceptive traits). In nuptial gift-giving spiders, males offer a food gift wrapped in silk during courtship, taking advantage of female foraging motivation. Males may also produce worthless gifts, which could select for female emancipation from deception and subsequent loss of gift function. This might be the case in the two known species of the spider genus Trechaleoides (Trechaleidae). Here, we examined the females’ preference for nuptial gifts, and gift function as male mating effort and/or male protection in both species. Trechaleoides keyserlingi males offering gifts acquired significantly fewer matings than males without gifts and thus, we verified no female preference for the gift. In T. biocellata males never produced a gift, although they experienced a high risk of pre-copulatory cannibalism. To assess whether T. biocellata females possess a pre-existing sensory bias for nuptial gifts, they were presented with heterospecific T. keyserlingi males with and without gifts. No female preference was detected, and the gift did not protect males from sexual cannibalism. If silk-wrapped nuptial gifts are ancestral in the spider family Trechaleidae, a basal loss of female preference for the gift in the genus Trechaleoides could be hypothesized. This may subsequently have changed the gift’s sexual function in T. keyserlingi and led to the complete loss of the gift-giving behaviour in T. biocellata.

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Acknowledgements

We thank Laura Montes de Oca for her help in spider and prey maintenance; Manuel Vitola, Juan Llopart, Alexander Lemos and Silvina Cortés for their help in the field and laboratory experiments. We thank Sebastián Horta, Sistema Nacional de Áreas Protegidas (SNAP, Uruguay) and Intendencia de Treinta y tres for supporting us during the spider samplings. We are especially indebted to Daniel Hernan, Cesar García and Federico Calavia for their invaluable help in spider collection, in providing us shelter and for all of the great talks and moments during our stages at Quebrada de los Cuervos, Treinta y tres, Uruguay.

Funding

MMV, CPP and MG were supported by Comisión Sectorial de Investigación Científica (CSIC). MMV and CPP were supported by Agencia Nacional de Investigación e Innovación (ANII), Comisión Académica de Posgrado (CAP) postgraduate scholarships, and Programa de Desarrollo de las Ciencias Básicas (PEDECIBA), Montevideo, Uruguay. MJA and IHT were supported by Sistema Nacional de Investigadores (SNI) ANII, and PEDECIBA Montevideo, Uruguay. MJA was supported by Caldeyro-Barcia National Science Award (PEDECIBA).

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  1. Programa de Desarrollo de las Ciencias Básicas (PEDECIBA), Facultad de Ciencias, Universidad de la República, Montevideo, Uruguay

    M. Martínez Villar & C. Pavón-Peláez

  2. Departamento de Ecología y Evolución, Facultad de Ciencias, Universidad de la República, Montevideo, Uruguay

    M. Martínez Villar, M. Germil, C. Pavón-Peláez & I. H. Tomasco

  3. Sección Entomología, Facultad de Ciencias, Universidad de la República, Montevideo, Uruguay

    M. Martínez Villar, C. Pavón-Peláez & M. J. Albo

  4. Departament of Biology, Aarhus University, Aarhus, Denmark

    T. Bilde & S. Toft

  5. Departamento de Ecología y Biología Evolutiva, Instituto de Investigaciones Biológicas Clemente Estable, Montevideo, Uruguay

    M. J. Albo

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  1. M. Martínez Villar
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Contributions

MJA conceived the idea and designed the laboratory work. MMV, MG, CPP and ST performed the behavioural experiments. MMV and MJA carried out the statistical analyses and wrote the paper with the input from CPP, IHT, ST and TB. All authors critically revised all versions. All authors gave final approval for publication and agree to be held accountable for the work performed therein.

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11692_2023_9606_MOESM1_ESM.mp4

Supplementary Material 1: Video S1. Occurrence of sexual cannibalism of T. biocellata female on T. keyserlingi male. This video was recorded during the experiments: “Heterospecific test of female preference and cannibalism”. In this trial the male (below) carrying a nuptial gift (wrapped housefly) approached courting the female (above). Once the male contacted the female, both sexes remained motionless (T = 0 in video). After seconds, the female jumped over the male (attack), the male exposed and offered the gift displaying the hyperflexion posture. The female grabbed the gift and both sexes remained in a face-to-face position holding the gift. Afterwards, the female seized the male with her legs, the male attempted to escape, but she succeed in cannibalize him

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Martínez Villar, M., Germil, M., Pavón-Peláez, C. et al. Lack of Female Preference for Nuptial Gifts May Have Led to Loss of the Male Sexual Trait. Evol Biol 50, 318–331 (2023). https://doi.org/10.1007/s11692-023-09606-3

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