Why are some species so much more successful in colonizing new ecosystems than others? Are they serendipitously in the right place at the right time? Are some habitats friendlier to newcomers than others? The three-spined stickleback (Gasterosteus aculeatus) exemplifies a successful colonizer with freshwater and marine populations on three different continents. However, its close relative, the Japan Sea stickleback (G. nipponicus) does not – they live only in marine environments, except for occasional forays inland to spawn. Why have some sticklebacks moved permanently inland while others have remained out at sea?
Work led by Asano Ishikawa, from the National Institute of Genetics and the Graduate University for Advanced Studies in Japan, argues that it depends on what animals can (or cannot) eat. Food is surprisingly different between freshwater and marine environments: freshwater ecosystems typically lack nutrients, especially long-chain polyunsaturated fatty acids such as DHA (docosahexaenoic acid). Hypothesizing that the scarcity of fatty acids limited the colonization of freshwater habitats, Ishikawa and colleagues integrated rearing experiments, genomics and genetically modified fish to compare how globetrotting three-spined sticklebacks and homebody Japan Sea sticklebacks cope with fat-free diets.
Regardless of salinity, three-spined sticklebacks survived better than Japan Sea sticklebacks on a DHA-free diet. Interestingly, survival only really started to drop off for the latter about 40 days after fertilization, the same age at which young Japan Sea sticklebacks migrate seaward in the wild. The poor survival matched lower brain and eye DHA levels, suggesting that Japan Sea sticklebacks cannot make and/or store DHA as effectively as their cosmopolitan cousins. Feeding Japan Sea sticklebacks fat-enriched meals solved the problems brought on by freshwater, linking freshwater morality and lack of DHA.
Why did diet matter for Japan Sea stickleback survival in freshwater? Perusing the sticklebacks’ genomes, the team found extra copies and higher activity of the fatty acid desaturases 2 (Fads2) gene in three-spined sticklebacks compared with their homebody relatives. Fads2 encodes an enzyme that metabolizes fatty acids such as DHA.
Encouraged by their findings, the team delved deeper into how Fads2 related to freshwater survival. They produced Japan Sea sticklebacks with a more active Fads2 gene to examine how this gene played into freshwater tolerance. Japan Sea sticklebacks with boosted Fads2 survived better in freshwater and had more DHA, mimicking the three-spined sticklebacks. Survival in freshwater depends on getting enough fats, and the Fads2 enzyme made all the difference for sticklebacks. It also turned out that three-spined sticklebacks naturally have an extra copy of the Fads2 gene. How did they manage to turn one copy of the Fads2 gene into two?
Looking closely at the structure of the three-spined stickleback genome around the extra Fads2 gene, the team found that it is messy and cluttered with short, repetitive sequences called transposons. These elements copy and paste themselves – and anything in their vicinity – randomly throughout the genome. Nearly a million years ago, some transposons copied Fads2 and took it on an adventure to a new location in another chromosome, opening a world of possibilities for the three-spined but not the Japan Sea stickleback.
A messy copy-and-paste job changed the course of three-spined stickleback history. Unlike their close relatives, these fish managed to eke out a living in a new, but nutrient-thin, environment. Understanding why only some species seize the opportunities of new habitats is a complicated question, but for fishes, more Fads2 makes freshwater colonization a piece of cake.