Key metabolic gene for recurrent freshwater colonization and radiation in fish

This story is a great example of gene-environment interactions. When organisms evolve — so that they might occupy a new environment — what adaptations in the genome are required for this transition? Authors [see attached article & editorial] have determined the precise mechanism for explaining how a single adaptive genetic innovation has repeatedly been used to allow saltwater fish to colonize and diversify into an ability to live in fresh water. This study is a creative study (of ecology, physiology, and genetics, combined) to understand a dietary adaptation. Authors used a gene insertion technology to demonstrate that, by increasing the number of copies of a single gene [fatty-acid desaturase-2 gene (Fads2)] in a marine-adapted lineage of threespine stickleback enables the fish to survive on a fresh-water diet.

Fads2 encodes an enzyme that is crucial for fatty-acid synthesis; therefore, increasing the number of Fads2 genes in the fish genome compensates for the dietary lack of fatty acids — such as docosahexaenoic acid (DHA) — in fresh water. Fatty acids are apparently more abundant in salt water. Stickleback fish harboring only one copy of Fads2 require a DHA-enriched diet to survive in fresh water. In contrast, the genomes of some lineages have evolved to have two copies of Fads2, thereby producing more fatty acid endogenously (i.e. no need for dietary supplementation), and they survived better under DHA-restricted diets. Authors engineered extra copies of Fads2 into single-copy stickleback fish, and they showed that this was sufficient to fulfill nutritional requirement for freshwater survival.

All fresh-water stickleback populations — surveyed across three continents — appear to have been derived from an ancestor having at least one duplicated Fads2 gene. Moreover, some of these duplicated Fads2 genes encode different protein sequences (which could alter the adaptive function of the enzyme — in addition to increasing the number of copies produced). In addition to the stickleback, authors examined 48 other fish species having full genome sequences available. Even after controlling for evolutionary history, authors found that across all ray-finned fish, species with fresh-water populations have substantially more copies of the Fads2 gene than species having no fresh-water populations. This finding suggests that Fads2 gene duplications have played an important role in evolutionary transitions to freshwater diets — not just for multiple stickleback lineages but, more generally, for ray-finned fish.

Authors dated the timing of the original Fads2 duplication in present-day freshwater stickleback to 800,000 years ago; however, fossil

evidence shows that stickleback had evolved to live in freshwater well before this time. Thus, it appears that the Fads2 story may be only the most recent chapter in a long history of fish transitions — both to, and from, fresh water. Authors also identified a mechanism underlying the adaptive copying of a pivotal genetic innovation such as Fads2.

Key genetic variation can be acquired through hybridization, or by gene duplication. Intriguingly, this article shows a very specific mechanism by which gene duplications can occur. Transposons (or “jumping genes”) are repetitive sequences that can insert themselves (and any DNA in between them) into other parts of the genome. Authors discovered that transposons are responsible for the multiple independent duplications of Fads2 in different fresh-water stickleback populations. This article is unusual in pinpointing an adaptive role for transposons — that directly increase the number of copies of a key metabolic gene in a vertebrate (animal with a spine). No fish surveyed by the authors had more than three copies of the Fads2 gene. Although all fish had originated in salt water, there are currently more species of ray-finned fish in fresh-water than in marine environments, and the vast majority of marine ray-finned fish species have freshwater ancestors that migrated back to saltwater. 😊


Science 31 May 2o19; 364: 886-889 & editorial pp 831-832

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