Adaptive phenotypic response to climate enabled by epigenetics in a K-strategy species, the fish Leucoraja ocellata (Rajidae)

Abstract

The relative importance of genetic versus epigenetic changes in adaptive evolution is a hotly debated topic, with studies showing that some species appear to be able to adapt rapidly without significant genetic change. Epigenetic mechanisms may be particularly important for the evolutionary potential of species with long maturation times and low reproductive potential (‘K-strategists’), particularly when faced with rapidly changing environmental conditions. Here we study the transcriptome of two populations of the winter skate (Leucoraja ocellata), a typical ‘K-strategist’, in Atlantic Canada; an endemic population in the southern Gulf of St Lawrence and a large population on the Scotian Shelf. The endemic population has been able to adapt to a 10°C higher water temperature over short evolutionary time (7000 years), dramatically reducing its body size (by 45%) significantly below the minimum maturation size of Scotian Shelf and other populations of winter skate, as well as exhibiting other adaptations in life history and physiology. We demonstrate that the adaptive response to selection has an epigenetic basis, cataloguing 3653 changes in gene expression that may have enabled this species to rapidly respond to the novel environment. We argue that the epigenetic augmentation of species evolutionary potential (its regulation though gene expression) can enable K-strategists to survive and adapt to different environments, and this mechanism may be particularly important for the persistence of sharks, skates and rays in the light of future climate change.

Synthesizing the role of epigenetics in the response and adaptation of species to climate change in freshwater ecosystems

“…In agreement to these results, the potential importance of epigenetic mechanisms in constraining the evolution of K‐strategist species was stressed by Lighten et al. (), who compared the transcriptome of two recently diverged populations of the winter skate ( Leucoraja ocellata ) and found that epigenetic mechanisms determined the different profiles of gene expression observed in the populations; in addition, a relevant portion of the differentially expressed transcripts was correlated to genes whose function is involved in the different life‐history traits of the populations.…”

“…For example, Kumar and Wigge (2010) showed that the short- Varriale (2014) The levels of methylation of warm-blooded species were consistently lower than those of the cold-blooded vertebrates Garg, Chevala, Shankar, and Jain (2015) Reported that the role of DNA methylation patterns are typically associated with genes important for abiotic stress responses in three rice (Oryza sativa) cultivars (IR64, stresssensitive; Nagina 22, drought-tolerant; Pokkali, salinity-tolerant) Artemov et al (2017) Genes encoding ion channels (KCND3, CACNA1FB and ATP4A) were differentially methylated between a marine and the freshwater populations of the winter skate (Leucoraja ocellata) Sun et al (2016) Both females and males from the Nile tilapia (Oreochromis niloticus) showed an increase in methylation levels on various chromosomes after high-temperature exposure Lighten et al (2016) Epigenetic mechanisms determined the different profiles of gene expression and life-history traits of two recently diverged populations of the winter skate (Leucoraja ocellata)…”

Risk of extinction of a unique skate population due to predation by a recovering marine mammal

“…Winter skate in the sGSL also differ from winter skate elsewhere in habitat associations and a number of morphological characters (Kelly and Hanson ), and epigenetic differences have been recently identified between the two groups (Lighten et al. ). Given these striking differences, Kelly and Hanson () proposed that winter skate from the shallow waters of the sGSL may represent an undescribed endemic species distinct from L. ocellata elsewhere.…”

Genetic background and embryonic temperature affect DNA methylation and expression of myogenin and muscle development in Atlantic salmon (Salmo salar)

“…Intriguingly, differences in adaptive phenotypic responses, including body size, to climate changes enabled by epigenetics were recently reported in two populations of winter skate ( Leucoraja ocellata ) [41]. Migratory salmonids have a tendency to spawn in their homing rivers differing in seasonal and regional thermal conditions, and evidence of local genetic adaptation in muscle cellularity and body growth have been reported in wild populations [11,42,43].…”