Jumping gene gave fish a freshwater start

 

 

 

 

When organisms evolve to occupy new environments, what adaptations are necessary for the transitions, and how predictable are these solutions when the transitions occur repeatedly? On page 886 of this issue, Ishikawa et al. (1) describe a refreshingly precise and thorough example of how a single adaptive genetic innovation has repeatedly allowed marine fish to colonize and diversify in freshwater. Whereas previous studies on evolutionary transitions and subsequent radiations to new ecological niches have largely focused on morphology (2, 3), the new study neatly links ecology, physiology, and genetics through a dietary adaptation.

A gene insertion technology (4) allowed Ishikawa et al. to demonstrate that increasing the number of copies of a single gene, fatty acid desaturase 2 (Fads2), in a marine-adapted lineage of threespine stickleback enables the fish to survive on a freshwater diet. Fads2 encodes an enzyme crucial for fatty acid synthesis, so increasing the number of Fads2 genes in a fish genome compensates for the dietary dearth of fatty acids such as docosahexaenoic acid (DHA) in freshwater.

Stickleback harboring only one copy of Fads2 need a DHA-enriched diet to survive. By contrast, some lineages have evolved to have two copies of Fads2, produce more fatty acid themselves, and survive better under DHA-restricted diets. Ishikawa et al. found that engineering extra copies of Fads2 into single-copy stickleback fish was sufficient to fulfill nutritional requirements for freshwater survival. Genetic mapping revealed that other genetic regions also influence survival on freshwater diets; these would be worthwhile avenues to explore.

The findings of Ishikawa et al. also offer a broad view on connections between Fads2 and freshwater colonization. All freshwater stickleback populations surveyed across three continents appear to have been seeded by an ancestor with at least one duplicated copy of Fads2. Furthermore, some of these Fads2 copies 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, the authors examined 48 other fish species with full genome sequences available. Even after controlling for evolutionary history, the authors found that across ray-finned fish, species with freshwater populations have substantially more Fads2 copies than species without freshwater populations. This suggests that Fads2 duplications have played a crucial role in evolutionary transitions to freshwater diets, not just for multiple stickleback lineages but for ray-finned fish more generally.

The ubiquity of this repeated evolutionary past raises questions about when and how often major ecological transitions occur in any given fish lineage. Ishikawa et al. dated the timing of the original Fads2 duplication in extant freshwater stickleback to 800,000 years ago. However, fossil evidence clearly shows that stickleback had evolved to live in freshwater well before this time (5). It appears that Fads2 may be only the most recent chapter in a long history of transitions both to and from freshwater.

So how is it that one gene became two? An advantage of taking a thorough molecular approach is that Ishikawa et al. have identified a mechanism underlying the adaptive copying of a pivotal genetic innovation such as Fads2. Key genetic variation can be acquired through hybridization (6) or gene duplication (7). Ishikawa et al. show a very specific mechanism by which duplications occur. Transposons (or “jumping genes”) are repetitive sequences that can insert themselves, and any DNA in between them, into other parts of the genome. Ishikawa et al. show that transposons are responsible for the multiple independent duplications of Fads2 in different freshwater stickleback populations.

Transposons are a classic example of a selfish genetic element because of their ability to replicate, often at a fitness cost to the rest of the genome (or the individual organism) (8). Genome-wide surveys often correlate transposon abundance with particular lineages (9, 10) or evolutionary innovations to adapt to rapidly changing environments, such as the appearance of parasites that become locked into a constantly coevolving arms race with hosts. For example, a pathogen can evolve the best virulent variations of a gene to infect the host while the host evolves the best resistant allele to survive parasitism (11). The study of Ishikawa et al. is unusual in pinpointing an adaptive role for transposons that directly increase the number of copies of a key metabolic gene in a vertebrate. The threshold at which additional Fads2 copies will lower rather than increase freshwater fish fitness remains an open question. No fish surveyed by the authors had more than three copies of the Fads2 gene.

Most people are familiar with the major evolutionary transition of vertebrates from water to land. Less appreciated, and more repeatable, are those transitions between marine habitats and freshwater. In both cases, colonizing a new habitat has resulted in rapid diversification for some lineages. Although all fish originated in saltwater, there are currently more species of ray-finned fish in freshwater than in marine environments, and the vast majority of marine ray-finned fish species have freshwater ancestors that migrated back to saltwater (12). More studies like that of Ishikawa et al. will help to pinpoint the genetic variation necessary for repeated evolutionary transitions to different environments.

 

 

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