Biosciences Research Seminar - Key physiological genes important for freshwater adaptation and life history evolution

Organisms exhibit diverse life histories that adapt to complex environments. How has such diversity evolved in nature? In contrast to morphological divergence, the genetic molecular mechanisms underlying life history evolution in wild organisms are largely unknown. Recently, we discovered key genes responsible for life history diversification using the three-spined stickleback (Gasterosteus aculeatus species complex) as a model system. Stickleback are primarily marine, but colonized postglacial freshwater habitats and radiated into diverse ecotypes. First, we found that multiple freshwater populations had an increased ability to synthesize omega-3 fatty acids as a dietary adaptation and exhibited an extended breeding season, possibly to increase their reproductive fitness in new habitats. Our genomic and transcriptome analyses revealed gene duplication of Fads2 (fatty acid desaturase) is important for adaptation to a freshwater diet and reduced expression of TSHß2 (thyroid stimulating hormone ß2) likely contributes to elongated breeding periods. Overexpression of Fads2 by transgenesis increased the omega-3 biosynthesis and survival rate among fish fed a freshwater-derived diet. Knockout of TSHß2 by genome editing demonstrated that fish showed signs of maturation even under a short photoperiod, which suppresses reproduction in ancestral marine populations. Importantly, both Fads2 and TSHb2 have been repeatedly involved in the evolution of similar life history traits in different lineages. Multiple freshwater ray-finned fishes showed convergent increases in Fads2s copies, indicating its key role in freshwater colonization across a wide range of taxa. Convergent reduced expression of TSHß2 occurred via different genetic mechanisms in the North American and Japanese populations of the three-spined sticklebacks and has also been observed in the nine-spined stickleback and medaka fish, indicating its crucial role in extending breeding periods. These results implied that Fads2 and TSHß2 might be a hotspot of life history evolution. Further analysis revealed that the gene duplication of Fads2 might be mediated by transposons and TSHß2 played a pleiotropic role in the regulation of gonad development, body size, behaviour, and brain transcriptome. Our results suggest potential mechanisms, mutational bias, and optimal pleiotropy that make a gene a hotspot of life history evolution.