Adaptive Divergence in the Thyroid Hormone Signaling Pathway in the Stickleback Radiation

During adaptive radiations, animals colonize diverse environments, which requires adaptation in multiple phenotypic traits [1]. Because hormones mediate the dynamic regulation of suites of phenotypic traits [2-4], evolutionary changes in hormonal signaling pathways might contribute to adaptation to new environments. Here we report changes in the thyroid hormone signaling pathway in stream-resident ecotypes of threespine stickleback fish (Gasterosteus aculeatus), which have repeatedly evolved from ancestral marine ecotypes [5-8]. Stream-resident fish exhibit a lower plasma concentration of thyroid hormone and a lower metabolic rate, which is likely adaptive for permanent residency in small streams. The thyroid-stimulating hormone-beta 2 (TSH beta 2) gene exhibited significantly lower mRNA expression in pituitary glands of stream-resident sticklebacks relative to marine sticklebacks. Some of the difference in TSH beta 2 transcript levels can be explained by cis-regulatory differences at the TSP beta 2 gene locus. Consistent with these expression differences, a strong signature of divergent natural selection was found at the TSH beta 2genomic locus. By contrast, there were no differences between the marine and stream-resident ecotypes in mRNA levels or genomic sequence in the paralogous TSH beta 1 gene. Our data indicate that evolutionary changes in hormonal signaling have played an important role in the postglacial adaptive radiation of sticklebacks.