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.

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  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

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