Natural selection on plasticity of thermal traits in a highly seasonal environment.

Leonardo D Bacigalupe,Juan D Gaitán‐Espitia,Mark Trinder,Barry Sinervo,Manuel Ruiz‐Aravena,Aura M Barria,Avia Gonzalez‐Mendez

doi:10.1111/eva.12702

Abstract

For ectothermic species with broad geographical distributions, latitudinal/altitudinal variation in environmental temperatures (averages and extremes) is expected to shape the evolution of physiological tolerances and the acclimation capacity (i.e., degree of phenotypic plasticity) of natural populations. This can create geographical gradients of selection in which environments with greater thermal variability (e.g., seasonality) tend to favor individuals that maximize performance across a broader range of temperatures compared to more stable environments. Although thermal acclimation capacity plays a fundamental role in this context, it is unknown whether natural selection targets this trait in natural populations. Additionally, understanding whether and how selection acts on thermal physiological plasticity is also highly relevant to climate change and biological conservation. Here, we addressed such an important gap in our knowledge in the northernmost population of the four‐eyed frog, Pleurodema thaul. We measured plastic responses of critical thermal limits for activity, behavioral thermal preference, and thermal sensitivity of metabolism to acclimation at 10 and 20°C. We monitored survival during three separate recapture efforts and used mark‐recapture integrated into an information‐theoretic approach to evaluate the relationship between survivals as a function of the plasticity of thermal traits. Overall, we found no evidence that thermal acclimation in this population is being targeted by directional selection, although there might be signals of selection on individual traits. According to the most supported models, survival increased in individuals with higher tolerance to cold when cold‐acclimated, probably because daily low extremes are frequent during the cooler periods of the year. Furthermore, survival increased with body size. However, in both cases, the directional selection estimates were nonsignificant, and the constraints of our experimental design prevented us from evaluating more complex models (i.e., nonlinear selection).

Highlights

It is well known that environmental temperature (Ta) is the abiotic factor with major influence in the evolution, ecology, and physi‐ ology of most of the biodiversity in the planet (Angilletta, 2009 and references therein)
This relation‐ ship between performance and body temperature has been de‐ scribed by a thermal performance curve (TPC) (Angilletta, 2009; Huey & Berrigan, 2001) which has often been used to describe the thermal ecology and evolution of ectotherms (Gilchrist, 1995; Huey & Kingsolver, 1989), their phenotypic plasticity (Schulte, Healy, & Fangue, 2011), and to predict their responses to climate change (Clusella‐Trullas, Blackburn, & Chown, 2011; Sinclair et al, 2016)
Populations inhabiting highly sea‐ sonal environments characterized by daily extreme tempera‐ tures provide a natural laboratory to evaluate the role of natural selection on the plasticity of critical thermal limits and preferences. We addressed such important gaps in our knowledge by measuring for the first time survival as a function of the plasticity of thermal critical temperatures (CTMax and CTMin), preferred temperature (TPref), and thermal sensitivity of metabolism (Q10; the magnitude of change in metabolic rate for a 10oC change in body temperature) after acclimating individuals to 10 and 20°C in the northernmost population of the four‐eyed frog Pleurodema thaul

Summary

| INTRODUCTION

It is well known that environmental temperature (Ta) is the abiotic factor with major influence in the evolution, ecology, and physi‐ ology of most of the biodiversity in the planet (Angilletta, 2009 and references therein). The mechanistic understanding of these conceptual frameworks has improved with recent studies showing how in thermally variable environments directional se‐ lection acts on TPC parameters favoring organisms that maximize performance across a broader range of temperatures (Logan, Cox, & Calsbeek, 2014) despite the ability of ectotherms to thermo‐ regulate behaviorally (Buckley, Ehrenberger, & Angilletta, 2015) Notwithstanding this progress, whether natural selection targets thermal acclimation capacity (i.e., physiological plasticity) itself in natural populations remains unknown. The understanding of whether and how selection acts on thermal physiological plasticity of natural populations is not just an import‐ ant fundamental research topic in evolutionary ecology, but it is relevant to other fields such as climate change and biological con‐ servation (Chown et al.., 2010; Gaitán‐Espitia, Marshall, et al, 2017; Gaitán‐Espitia, Villanueva, et al, 2017; Merilä & Hendry, 2014) This is true for populations in unpredictable, extreme, or het‐ erogeneous habitats at the edge of the species distribution, because climate change is predicted to increase their risk of local extinction (Hoffmann & Sgrò, 2011). Integrating this understanding into managing programs will improve planning conservation efforts aiming for the long‐term persistence of populations at the edges of species’ ranges

| METHODS

| DISCUSSION

Findings

CONFLICT OF INTERESTS