Plasticity and evolutionary divergence in gene expression associated with alternative habitat use in larvae of the European Fire Salamander

Abstract

Transcriptomes of organisms reveal differentiation associated with the use of different habitats. However, this leaves open how much of the observed differentiation can be attributed to genetic differences or to transcriptional plasticity. In this study, we disentangle causes of differential gene expression in larvae of the European fire salamander from the Kottenforst forest in Germany. Larvae inhabit permanent streams and ephemeral ponds and represent an example of a young evolutionary split associated with contrasting ecological conditions. We hypothesized that adaptation towards differences in water temperature plays a role because the thermal regime between stream and pond habitats differs notably. Tissue samples from tail fins of larvae were collected to study gene expression using microarrays. We found ample evidence for differentiation among larvae occupying different habitats in nature with 2,800 of 11,797 genes being differentially expressed. We then quantified transcriptional plasticity towards temperature and genetic differentiation based on controlled temperature laboratory experiments. Gene-by-environment interactions modelling revealed that 28% of the gene expression divergence observed among samples in nature could be attributed to plasticity related to water temperature. Expression patterns of only a small number of 101 genes were affected by the genotype. Our analysis demonstrates that effects of environmental factors must be taken into account to explain variation of gene expression in salamanders in nature. Notwithstanding, it provides first evidence that genetic factors determined gene expression divergence between pond and stream ecotypes and could be involved in adaptive evolution.

Adaptation to climate change through genetic accommodation and assimilation of plastic phenotypes

“…The higher baseline expression of environmentally responsive genes noted in these studies might represent an evolved response to a frequently encountered stress, allowing these populations to maintain tolerance in the absence of an acclimatization response. Overlaps between the genetic basis of plasticity and population divergence have also been observed in European fire salamanders, Salamandra salamandra [106], grayling Thymallus thymallus [107] and wall lizards P. muralis [85].…”

Latitudinal divergence in a widespread amphibian: Contrasting patterns of neutral and adaptive genomic variation

“…Genomic studies along environmental gradients in amphibians are slowly starting to accumulate (Bonin et al, ; Czypionka et al, ; Guo et al, ; Pastenes et al, ; Yang et al, ). Guo et al () used pooled RAD‐seq and showed genomic adaptive divergence among Bufo andrewsi populations along an altitudinal gradient on the Tibetan plateau, identifying candidate SNPs located in genes that may be involved in high‐altitude adaptation.…”

“…In amphibians, several studies have found phenotypic evidence for adaptive divergence and counter‐gradient variation along wide environmental gradients, highlighting the importance of growing season length as a selective factor (e.g., Berven, ; Berven, Gill, & Smith‐Gill, ; Laugen, Laurila, Räsänen, & Merilä, ; Luquet, Léna, Miaud, & Plénet, ; Muir, Biek, Thomas, & Mable, ; Palo et al, ). However, until recently, population genomic studies investigating adaptive variation along environmental gradients in amphibians have been relatively scarce (but see Bonin, Taberlet, Miaud, & Pompanon, ; Czypionka, Goedbloed, Steinfartz, & Nolte, ; Guo, Lu, Liao, & Merilä, ; Pastenes et al, ; Yang, Qi, & Fu, ), and no studies, to our knowledge, have focused on genomic divergence along latitudinal gradients, probably reflecting the general scarcity of genomic resources for amphibians (but see Hammond et al, ; Hellsten et al, ; Session et al, ; Shu, Laurila, Suter, & Räsänen, ; Sun et al, ).…”

Plasticity‐led evolution: A survey of developmental mechanisms and empirical tests

“…In such a time series, samples during the early stages of an evolutionary sequence may be useful in distinguishing between PLE and mutation-driven evolution (Levis & Pfennig, 2019b). For example, one could demonstrate greater environmental sensitivity of ancestral alleles compared to derived ones (e.g., Corl et al, 2018;Parsons et al, 2016) and/or use comparisons among outgroups or ancestors and descendants to evaluate divergence in environmental sensitivity in gene regulation or expression (e.g., Czypionka, Goedbloed, Steinfartz, & Nolte, 2018;Koch et al, 2017). These genetic tests would also require additional evidence that there was ancestral plasticity before fixation of a particular phenotype, and this evidence of ancestral plasticity might take many forms.…”

“…These genetic tests would also require additional evidence that there was ancestral plasticity before fixation of a particular phenotype, and this evidence of ancestral plasticity might take many forms. For example, one could demonstrate greater environmental sensitivity of ancestral alleles compared to derived ones (e.g., Corl et al, 2018;Parsons et al, 2016) and/or use comparisons among outgroups or ancestors and descendants to evaluate divergence in environmental sensitivity in gene regulation or expression (e.g., Czypionka, Goedbloed, Steinfartz, & Nolte, 2018;Koch et al, 2017).…”