Gene-Environment Interactions for Growth and Gene Expression within Panmixia: Relevance for the Conservation and Management of American Eel

Elucidating strategies adopted by species to cope with heterogeneous environments is a central tenet of evolutionary biology. At one extreme of a continuum, species characterized by restricted gene flow and strong phylopatry develop local adaptations to the environment that each population occupies. At the other end, for species characterized by weak genetic structuring, random dispersal and limited phylopatry, gene flow may preclude the development of stable local adaptation. Instead, theory predicts that phenotypic plasticity may provide a better adaptive response to environmental heterogeneity by enhancing fitness through differential growth, survival, and reproduction. Phenotypic plasticity is typically described by reaction norms suspected to result from differential gene regulation underlying phenotypic expression in different environments. Yet, very few studies have tested for the simultaneous occurrence of plasticity in phenotypic and gene expression. Because it possibly represents the fish species occupying the broadest range of environmental conditions and yet appears totally panmictic, the American eel is one of the most likely candidates to exhibit adaptive phenotypic plasticity. In this study, we tested for the occurrence of gene-environment interactions underlying both phenotypic and gene expression in this species. Thus, freshly landed glass eels were collected from two locations with contrasted adult phenotypes in nature: one site (Mira River, Nova Scotia) characterised by relatively fast growth, occurrence of both sexes and early sexual maturation and a second site (Grande-Rivière-Blanche, Québec), where only females occurs and are characterised by slower growth, larger size at maturity and late sexual maturation. Common garden experiments in two salinity conditions showed a plastic response to growth, whereby eels of both origins grew faster in brackish water. Unexpectedly for a panmictic species, however, we also observed a nearly significant trend for origin*salinity interactions. Differential growth between eels from both origins was maintained throughout the 27 months experiment. Microarray experiments that simultaneously compared the expression of >2000 genes also revealed a pronounced plastic response to gene regulation between salinities for both origins. Again, we observed significant origin*salinity interactions for numerous genes involved in a wide array of biological functions. Altogether, these results show that eel’s growth and gene expression are highly plastic to environmental conditions. Moreover, differences in reactions norms observed between origins suggest that these plastic responses may have a genetic basis and therefore could be adaptive. The potential relevance of those findings for management and conservation of eel will be discussed.