Iodine is an essential trace element for vertebrates. Iodine is a component of thyroid hormones, which regulate diverse physiological functions and development in animals. However, iodine is not evenly distributed throughout the earth. The ocean is rich in iodine, but iodine concentrations decrease with increasing distance from the sea. How does spatial variation in iodine availability influence the ecology and evolution of natural animal populations?
In humans, due to iodine deficiency, inland people sometimes show low thyroid function, i.e., hypothyroidism. In addition to symptoms associated with hypothyroidism, iodine deficiency leads to the enlargement of the thyroid glands, called endemic goiter, which is caused by the overactivation of the thyroid glands by thyroid-stimulating hormone (TSH) secreted by the pituitary glands. Dietary iodine supplementation suppresses both hypothyroidism and endemic goiter. Although much is known about iodine deficiency in humans, we do not know how natural animal populations respond or adapt to iodine deficiency.
The threespine stickleback (Gasterosteus aculeatus) has colonized and adapted to diverse environments, both marine and freshwater, while the closely related Japan Sea stickleback (G. nipponicus) is exclusively marine with no freshwater-resident populations identified. Thus, these two species provide an excellent model system for investigating how animals adapt to environments varying in iodine availability.
We made pure crosses and reared them in freshwater and seawater aquarium tanks as well as in outdoor freshwater mesocosms with or without iodine. We found that G. nipponicus showed goiter in freshwater mesocosm lacking iodine. These fish also had low plasma thyroid hormone levels and high expression levels of TSHβ1 in the pituitary gland, which could be suppressed by iodine supplementation. Thus, these phenotypes were similar to endemic goiter in humans. In contrast, G. aculeatus, whether they are marine or freshwater ecotypes, showed no apparent abnormalities in freshwater mesocosm lacking iodine. Furthermore, these fish had higher plasma thyroid hormone levels and lower pituitary TSHβ1 expression levels compared to G. nipponicus. These results suggest that G. aculeatus can overcome iodine deficiency possibly by efficiently obtaining or recycling iodine and/or thyroid hormones under iodine-deficient freshwater conditions.
Thus, we found that G. aculeatus and G. nipponicus genetically differ in their ability to cope with iodine deficiency. This physiological difference may contribute to the different ability to colonize freshwater environments between these two species.