Predation risk and the evolution of a vertebrate stress response: Parallel evolution of stress reactivity and sexual dimorphism

Jerker Vinterstare*, Gustaf Magnus Oskar Ekelund Ugge, Kaj Hulthén, Alexander Hegg, Christer Brönmark, Anders Nilsson, Marcus Lee, Varpu Pärssinen, Simon David Herzog, Yongcui Sha, Caroline Björnerås, Huan Zhang, Raphael Gollnisch, Lars-Anders Hansson, Martin Škerlep, Nan Hu, Emma Johansson, Brian Langerhans

*Corresponding author for this work

Research output: Contribution to journalJournal articleResearchpeer-review

Abstract

Predation risk is often invoked to explain variation in stress responses. Yet, the answers to several key questions remain elusive, including the following: (1) how predation risk influences the evolution of stress phenotypes, (2) the relative importance of environmental versus genetic factors in stress reactivity and (3) sexual dimorphism in stress physiology. To address these questions, we explored variation in stress reactivity (ventilation frequency) in a post-Pleistocene radiation of live-bearing fish, where Bahamas mosquitofish (Gambusia hubbsi) inhabit isolated blue holes that differ in predation risk. Individuals of populations coexisting with predators exhibited similar, relatively low stress reactivity as compared to low-predation populations. We suggest that this dampened stress reactivity has evolved to reduce energy expenditure in environments with frequent and intense stressors, such as piscivorous fish. Importantly, the magnitude of stress responses exhibited by fish from high-predation sites in the wild changed very little after two generations of laboratory rearing in the absence of predators. By comparison, low-predation populations exhibited greater among-population variation and larger changes subsequent to laboratory rearing. These low-predation populations appear to have evolved more dampened stress responses in blue holes with lower food availability. Moreover, females showed a lower ventilation frequency, and this sexual dimorphism was stronger in high-predation populations. This may reflect a greater premium placed on energy efficiency in live-bearing females, especially under high-predation risk where females show higher fecundities. Altogether, by demonstrating parallel adaptive divergence in stress reactivity, we highlight how energetic trade-offs may mould the evolution of the vertebrate stress response under varying predation risk and resource availability.

Original languageEnglish
JournalJournal of Evolutionary Biology
Volume34
Issue number10
Pages (from-to)1554-1567
Number of pages14
ISSN1010-061X
DOIs
Publication statusPublished - Oct 2021
Externally publishedYes

Keywords

  • bahamas mosquitofish
  • poeciliidae
  • predation risk
  • predator-prey interactions
  • resource availability
  • sexual dimorphism
  • stress physiology
  • stress response
  • trade-offs
  • ventilation frequency

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