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Research article - Peer-reviewed, 2021

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

Vinterstare, Jerker; Ugge, Gustaf M. O. Ekelund; Hulthen, Kaj; Hegg, Alexander; Bronmark, Christer; Nilsson, Per Anders; Zellmer, Ursula Ronja; Lee, Marcus; Parssinen, Varpu; Sha, Yongcui; Bjorneras, Caroline; Zhang, Huan; Gollnisch, Raphael; Herzog, Simon D.; Hansson, Lars-Anders; Skerlep, Martin; Hu, Nan; Johansson, Emma; Langerhans, Randall Brian;

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.

Keywords

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

Published in

Journal of Evolutionary Biology

2021, volume: 34, number: 10, pages: 1554-1567
Publisher: WILEY

Authors' information

Lund University
Ugge, Gustaf M. O. Ekelund
University of Skovde
Ugge, Gustaf M. O. Ekelund
Lund University
Hulthen, Kaj
Lund University
Hegg, Alexander
Lund University
Bronmark, Christer
Lund University
Nilsson, Per Anders
Lund University
Zellmer, Ursula Ronja
Uppsala University
Lee, Marcus
Lund University
Parssinen, Varpu
Lund University
Sha, Yongcui
Lund University
Bjorneras, Caroline
Lund University
Zhang, Huan
Institute of Hydrobiology, CAS
Gollnisch, Raphael
Lund University
Herzog, Simon D.
Lund University
Hansson, Lars-Anders
Lund University
Skerlep, Martin
Lund University
Hu, Nan
Lund University
Johansson, Emma
Lund University
Langerhans, Randall Brian
University of North Carolina

UKÄ Subject classification

Evolutionary Biology

Publication Identifiers

DOI: https://doi.org/10.1111/jeb.13918

URI (permanent link to this page)

https://res.slu.se/id/publ/115562