Is thermal plasticity itself shaped by natural selection? An assessment with desert frogs
Natural selection on plasticity of thermal traits in a highly seasonal environment
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 . 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.
 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
 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
 Scheiner SM. 1993. Plasticity as a selectable trait: Reply to Via. The American Naturalist. 142: 371–373. doi: 10.1086/285544
 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
 Via S. 1993. Regulatory genes and reaction norms. The American Naturalist. 142: 374–378. doi: 10.1086/285542
Wolf Blanckenhorn (2018) Is thermal plasticity itself shaped by natural selection? An assessment with desert frogs. Peer Community in Evolutionary Biology, 100048. 10.24072/pci.evolbiol.100048
Evaluation round #2
DOI or URL of the preprint: 10.1101/191825
Version of the preprint: 2
Author's Reply, None
Decision by Wolf Blanckenhorn, 27 Feb 2018
The second version of this manuscript is much improved. In particular, the context has been changed completely, and the selection analysis now conforms more to standard analyses in the field. Nevertheless, I still believe that the AIC analysis does not add much to the study, but in fact rather obscures the fact that no selection on physiological plasticity has been found. This is an important (negative) result, which of course can always be argued away due to sample size limitations (cf. P11, L379ff), but I would not go as far here. I think these negative results should be recommended after another revision!
Reviewed by Dries Bonte, 05 Feb 2018
Reviewed by Nadia Aubin-Horth, 05 Feb 2018
Reviewed by Wolf Blanckenhorn, 05 Feb 2018
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/191825
Version of the preprint: 1
Author's Reply, None
Decision by Wolf Blanckenhorn, 28 Dec 2017
We obtained 3 external reviews for the paper "Natural selection on plasticity of thermal traits in a highly seasonal environment" by Leonardo Bacigalupe et al. All reviewers saw merit in this study and think that it can eventually be recommended by PCI EvolBio after extensive revisions, which however are necessary and strongly recommended before. The reviews were consistent in the sense that the reviewers identified two aspects that need extensive revision. First, the context of climate change needs to be revised, as only a single population of this frog was studied in its natural habitat, thus experiencing no climate change but natural seasonal fluctuations. Second, the statistical analysis needs extensive revision according to the comments of the reviewers.