Natural selection on plasticity of thermal traits in a highly seasonal environment
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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).
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It is well known that climatic factors – most notably temperature, season length, insolation and humidity – shape the thermal niche of organisms on earth through the action of natural selection. But how is this achieved precisely? Much of thermal tolerance is actually mediated by phenotypic plasticity (as opposed to genetic adaptation). A prominent expectation is that environments with greater (daily and/or annual) thermal variability select for greater plasticity, i.e. better acclimation capacity. Thus, plasticity might be selected per se.
A Chilean group around Leonardo Bacigalupe assessed natural selection in the wild in one marginal (and extreme) population of the four-eyed frog Pleurodema thaul (Anura: Leptodactylidae) in an isolated oasis in the Atacama Desert, permitting estimation of mortality without much potential of …
It is well known that climatic factors – most notably temperature, season length, insolation and humidity – shape the thermal niche of organisms on earth through the action of natural selection. But how is this achieved precisely? Much of thermal tolerance is actually mediated by phenotypic plasticity (as opposed to genetic adaptation). A prominent expectation is that environments with greater (daily and/or annual) thermal variability select for greater plasticity, i.e. better acclimation capacity. Thus, plasticity might be selected per se.
A Chilean group around Leonardo Bacigalupe assessed natural selection in the wild in one marginal (and extreme) population of the four-eyed frog Pleurodema thaul (Anura: Leptodactylidae) in an isolated oasis in the Atacama Desert, permitting estimation of mortality without much potential of confounding it with migration [1]. Several thermal traits were considered: CTmax – the critical maximal temperature; CTmin – the critical minimum temperature; Tpref – preferred temperature; Q10 – thermal sensitivity of metabolism; and body mass. Animals were captured in the wild and subsequently assessed for thermal traits in the laboratory at two acclimation temperatures (10° & 20°C), defining the plasticity in all traits as the difference between the traits at the two acclimation temperatures. Thereafter the animals were released again in their natural habitat and their survival was monitored over the subsequent 1.5 years, covering two breeding seasons, to estimate viability selection in the wild. The authors found and conclude that, aside from larger body size increasing survival (an unsurprising result), plasticity does not seem to be systematically selected directly, while some of the individual traits show weak signs of selection.
Despite limited sample size (ca. 80 frogs) investigated in only one marginal but very seasonal population, this study is interesting because selection on plasticity in physiological thermal traits, as opposed to selection on the thermal traits themselves, is rarely investigated. The study thus also addressed the old but important question of whether plasticity (i.e. CTmax-CTmin) is a trait by itself or an epiphenomenon defined by the actual traits (CTmax and CTmin) [2-5]. Given negative results, the main question could not be ultimately solved here, so more similar studies should be performed.
References
[1] Bacigalupe LD, Gaitan-Espitia, JD, Barria AM, Gonzalez-Mendez A, Ruiz-Aravena M, Trinder M & Sinervo B. 2018. Natural selection on plasticity of thermal traits in a highly seasonal environment. bioRxiv 191825, ver. 5 peer-reviewed by Peer Community In Evolutionary Biology. doi: 10.1101/191825
[2] Scheiner SM. 1993. Genetics and evolution of phenotypic plasticity. Annual Review in Ecology and Systematics 24: 35–68. doi: 10.1146/annurev.es.24.110193.000343
[3] Scheiner SM. 1993. Plasticity as a selectable trait: Reply to Via. The American Naturalist. 142: 371–373. doi: 10.1086/285544
[4] Via S. 1993. Adaptive phenotypic plasticity - Target or by-product of selection in a variable environment? The American Naturalist. 142: 352–365. doi: 10.1086/285542
[5] Via S. 1993. Regulatory genes and reaction norms. The American Naturalist. 142: 374–378. doi: 10.1086/285542 -
