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

Summary 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- β 2 ( TSH β 2 ) gene exhibited significantly lower mRNA expression in pituitary glands of stream-resident sticklebacks relative to marine sticklebacks. Some of the difference in TSH β 2 transcript levels can be explained by cis -regulatory differences at the TSH β 2 gene locus. Consistent with these expression differences, a strong signature of divergent natural selection was found at the TSH β 2 genomic locus. By contrast, there were no differences between the marine and stream-resident ecotypes in mRNA levels or genomic sequence in the paralogous TSH β 1 gene. Our data indicate that evolutionary changes in hormonal signaling have played an important role in the postglacial adaptive radiation of sticklebacks.