Thermal phenotypic plasticity of pre- and post-copulatory male harm buffers sexual conflict in wild Drosophila melanogaster

Abstract

Strong sexual selection frequently leads to sexual conflict and ensuing male harm, whereby males increase their reproductive success at the expense of harming females. Male harm is a widespread evolutionary phenomenon with a strong bearing on population viability. Thus, understanding how it unfolds in the wild is a current priority. Here, we sampled a wild Drosophila melanogaster population and studied male harm across the normal range of temperatures under which it reproduces optimally in nature by comparing female lifetime reproductive success and underlying male harm mechanisms under monogamy (i.e., low male competition/harm) vs. polyandry (i.e., high male competition/harm). While females had equal lifetime reproductive success across temperatures under monogamy, polyandry resulted in a maximum decrease of female fitness at 24°C (35%), reducing its impact at both 20°C (22%), and 28°C (10%). Furthermore, female fitness components and pre- (i.e., harassment) and post-copulatory (i.e., ejaculate toxicity) mechanisms of male harm were asymmetrically affected by temperature. At 20ºC, male harassment of females was reduced, and polyandry accelerated female actuarial ageing. In contrast, the effect of mating on female receptivity (a component of ejaculate toxicity) was affected at 28ºC, where the mating costs for females decreased and polyandry mostly resulted in accelerated reproductive ageing. We thus show that, across a natural thermal range, sexual conflict processes and their effects on female fitness components are plastic and complex. As a result, the net effect of male harm on overall population viability is likely to be lower than previously surmised. We discuss how such plasticity may affect selection, adaptation and, ultimately, evolutionary rescue under a warming climate.

Data availability

All data generated or analysed during this study are included in the manuscript. Source data files are uploaded to Dryad repository(https://doi.org/10.5061/dryad.pzgmsbcqz), along with R script https://doi.org/10.5281/zenodo.7350587

The following data sets were generated

Article and author information

Author details

  1. Claudia Londoño-Nieto

    Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, Valencia, Spain
    For correspondence
    claudia.londonon@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7408-7327
  2. Roberto García-Roa

    Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, Valencia, Spain
    Competing interests
    The authors declare that no competing interests exist.
  3. Clara Garcia-Co

    Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, Valencia, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4126-5940
  4. Paula González

    Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, Valencia, Spain
    Competing interests
    The authors declare that no competing interests exist.
  5. Pau Carazo

    Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, Paterna, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1525-6522

Funding

Ministerio de Ciencia e Innovación (PID2020-118027GB-I00)

  • Pau Carazo

Generalitat Valenciana (AICO/2021/113)

  • Pau Carazo

Ministerio de Educación y Formación Profesional (FJC2018-037058-I)

  • Roberto García-Roa

Marie Sklodowska Curie (HORIZON-MSCA-2021-PF-01 101061275)

  • Roberto García-Roa

Ministerio de Asuntos Económicos y Transformación Digital, Gobierno de España (PRE2018-084009)

  • Claudia Londoño-Nieto

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2023, Londoño-Nieto et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 737
    views
  • 126
    downloads
  • 4
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Claudia Londoño-Nieto
  2. Roberto García-Roa
  3. Clara Garcia-Co
  4. Paula González
  5. Pau Carazo
(2023)
Thermal phenotypic plasticity of pre- and post-copulatory male harm buffers sexual conflict in wild Drosophila melanogaster
eLife 12:e84759.
https://doi.org/10.7554/eLife.84759

Share this article

https://doi.org/10.7554/eLife.84759

Further reading

    1. Ecology
    Mercury Shitindo
    Insight

    Tracking wild pigs with GPS devices reveals how their social interactions could influence the spread of disease, offering new strategies for protecting agriculture, wildlife, and human health.

    1. Ecology
    2. Neuroscience
    Ralph E Peterson, Aman Choudhri ... Dan H Sanes
    Research Article

    In nature, animal vocalizations can provide crucial information about identity, including kinship and hierarchy. However, lab-based vocal behavior is typically studied during brief interactions between animals with no prior social relationship, and under environmental conditions with limited ethological relevance. Here, we address this gap by establishing long-term acoustic recordings from Mongolian gerbil families, a core social group that uses an array of sonic and ultrasonic vocalizations. Three separate gerbil families were transferred to an enlarged environment and continuous 20-day audio recordings were obtained. Using a variational autoencoder (VAE) to quantify 583,237 vocalizations, we show that gerbils exhibit a more elaborate vocal repertoire than has been previously reported and that vocal repertoire usage differs significantly by family. By performing gaussian mixture model clustering on the VAE latent space, we show that families preferentially use characteristic sets of vocal clusters and that these usage preferences remain stable over weeks. Furthermore, gerbils displayed family-specific transitions between vocal clusters. Since gerbils live naturally as extended families in complex underground burrows that are adjacent to other families, these results suggest the presence of a vocal dialect which could be exploited by animals to represent kinship. These findings position the Mongolian gerbil as a compelling animal model to study the neural basis of vocal communication and demonstrates the potential for using unsupervised machine learning with uninterrupted acoustic recordings to gain insights into naturalistic animal behavior.