Cargando…

Physiological Stress Integrates Resistance to Rattlesnake Venom and the Onset of Risky Foraging in California Ground Squirrels

Using venom for predation often leads to the evolution of resistance in prey. Understanding individual variation in venom resistance is key to unlocking basic mechanisms by which antagonistic coevolution can sustain variation in traits under selection. For prey, the opposing challenges of predator a...

Descripción completa

Detalles Bibliográficos
Autores principales: Holding, Matthew L., Putman, Breanna J., Kong, Lauren M., Smith, Jennifer E., Clark, Rulon W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7601495/
https://www.ncbi.nlm.nih.gov/pubmed/32992585
http://dx.doi.org/10.3390/toxins12100617
_version_ 1783603435103322112
author Holding, Matthew L.
Putman, Breanna J.
Kong, Lauren M.
Smith, Jennifer E.
Clark, Rulon W.
author_facet Holding, Matthew L.
Putman, Breanna J.
Kong, Lauren M.
Smith, Jennifer E.
Clark, Rulon W.
author_sort Holding, Matthew L.
collection PubMed
description Using venom for predation often leads to the evolution of resistance in prey. Understanding individual variation in venom resistance is key to unlocking basic mechanisms by which antagonistic coevolution can sustain variation in traits under selection. For prey, the opposing challenges of predator avoidance and resource acquisition often lead to correlated levels of risk and reward, which in turn can favor suites of integrated morphological, physiological and behavioral traits. We investigate the relationship between risk-sensitive behaviors, physiological resistance to rattlesnake venom, and stress in a population of California ground squirrels. For the same individuals, we quantified foraging decisions in the presence of snake predators, fecal corticosterone metabolites (a measure of “stress”), and blood serum inhibition of venom enzymatic activity (a measure of venom resistance). Individual responses to snakes were repeatable for three measures of risk-sensitive behavior, indicating that some individuals were consistently risk-averse whereas others were risk tolerant. Venom resistance was lower in squirrels with higher glucocorticoid levels and poorer body condition. Whereas resistance failed to predict proximity to and interactions with snake predators, individuals with higher glucocorticoid levels and in lower body condition waited the longest to feed when near a snake. We compared alternative structural equation models to evaluate alternative hypotheses for the relationships among stress, venom resistance, and behavior. We found support for stress as a shared physiological correlate that independently lowers venom resistance and leads to squirrels that wait longer to feed in the presence of a snake, whereas we did not find evidence that resistance directly facilitates latency to forage. Our findings suggest that stress may help less-resistant squirrels avoid a deadly snakebite, but also reduces feeding opportunities. The combined lethal and non-lethal effects of stressors in predator–prey interactions simultaneously impact multiple key traits in this system, making environmental stress a potential contributor to geographic variation in trait expression of toxic predators and resistant prey.
format Online
Article
Text
id pubmed-7601495
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher MDPI
record_format MEDLINE/PubMed
spelling pubmed-76014952020-11-01 Physiological Stress Integrates Resistance to Rattlesnake Venom and the Onset of Risky Foraging in California Ground Squirrels Holding, Matthew L. Putman, Breanna J. Kong, Lauren M. Smith, Jennifer E. Clark, Rulon W. Toxins (Basel) Article Using venom for predation often leads to the evolution of resistance in prey. Understanding individual variation in venom resistance is key to unlocking basic mechanisms by which antagonistic coevolution can sustain variation in traits under selection. For prey, the opposing challenges of predator avoidance and resource acquisition often lead to correlated levels of risk and reward, which in turn can favor suites of integrated morphological, physiological and behavioral traits. We investigate the relationship between risk-sensitive behaviors, physiological resistance to rattlesnake venom, and stress in a population of California ground squirrels. For the same individuals, we quantified foraging decisions in the presence of snake predators, fecal corticosterone metabolites (a measure of “stress”), and blood serum inhibition of venom enzymatic activity (a measure of venom resistance). Individual responses to snakes were repeatable for three measures of risk-sensitive behavior, indicating that some individuals were consistently risk-averse whereas others were risk tolerant. Venom resistance was lower in squirrels with higher glucocorticoid levels and poorer body condition. Whereas resistance failed to predict proximity to and interactions with snake predators, individuals with higher glucocorticoid levels and in lower body condition waited the longest to feed when near a snake. We compared alternative structural equation models to evaluate alternative hypotheses for the relationships among stress, venom resistance, and behavior. We found support for stress as a shared physiological correlate that independently lowers venom resistance and leads to squirrels that wait longer to feed in the presence of a snake, whereas we did not find evidence that resistance directly facilitates latency to forage. Our findings suggest that stress may help less-resistant squirrels avoid a deadly snakebite, but also reduces feeding opportunities. The combined lethal and non-lethal effects of stressors in predator–prey interactions simultaneously impact multiple key traits in this system, making environmental stress a potential contributor to geographic variation in trait expression of toxic predators and resistant prey. MDPI 2020-09-27 /pmc/articles/PMC7601495/ /pubmed/32992585 http://dx.doi.org/10.3390/toxins12100617 Text en © 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Holding, Matthew L.
Putman, Breanna J.
Kong, Lauren M.
Smith, Jennifer E.
Clark, Rulon W.
Physiological Stress Integrates Resistance to Rattlesnake Venom and the Onset of Risky Foraging in California Ground Squirrels
title Physiological Stress Integrates Resistance to Rattlesnake Venom and the Onset of Risky Foraging in California Ground Squirrels
title_full Physiological Stress Integrates Resistance to Rattlesnake Venom and the Onset of Risky Foraging in California Ground Squirrels
title_fullStr Physiological Stress Integrates Resistance to Rattlesnake Venom and the Onset of Risky Foraging in California Ground Squirrels
title_full_unstemmed Physiological Stress Integrates Resistance to Rattlesnake Venom and the Onset of Risky Foraging in California Ground Squirrels
title_short Physiological Stress Integrates Resistance to Rattlesnake Venom and the Onset of Risky Foraging in California Ground Squirrels
title_sort physiological stress integrates resistance to rattlesnake venom and the onset of risky foraging in california ground squirrels
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7601495/
https://www.ncbi.nlm.nih.gov/pubmed/32992585
http://dx.doi.org/10.3390/toxins12100617
work_keys_str_mv AT holdingmatthewl physiologicalstressintegratesresistancetorattlesnakevenomandtheonsetofriskyforagingincaliforniagroundsquirrels
AT putmanbreannaj physiologicalstressintegratesresistancetorattlesnakevenomandtheonsetofriskyforagingincaliforniagroundsquirrels
AT konglaurenm physiologicalstressintegratesresistancetorattlesnakevenomandtheonsetofriskyforagingincaliforniagroundsquirrels
AT smithjennifere physiologicalstressintegratesresistancetorattlesnakevenomandtheonsetofriskyforagingincaliforniagroundsquirrels
AT clarkrulonw physiologicalstressintegratesresistancetorattlesnakevenomandtheonsetofriskyforagingincaliforniagroundsquirrels