Discrete genetic modules underlie divergent reproductive strategies in three-spined stickleback

A central challenge in biology is to understand how complex behaviors evolve. Reproductive behaviors are frequently subject to strong selection and complex behavioral traits often evolve as an integrated package. However, it is unclear whether suites of traits evolve through a few pleiotropic genetic changes, each affecting many behaviors, or by accumulating several changes that, when combined, give rise to an entire package of correlated traits. Typically, three-spined stickleback exhibit paternal care, a behavior that characterizes the entire Gasterosteidae family. However, an unusual "white" three-spined stickleback ecotype exhibits a suite of traits associated with the evolutionary loss of paternal care. In the white ecotype, males disperse embryos from their nests rather than care for them, build loose nests, exhibit high rates of courtship, and are relatively small in body size. These differences are apparent in stickleback reared in a common garden environment, suggesting the differences have a heritable basis. In an F2 intercross (n = 76 to 133), we show that these traits are genetically uncorrelated and map to different genomic regions, suggesting that components of the white reproductive strategy segregate independently and evolved through the addition of multiple genetic changes. Moreover, distinct sets of genes may be involved in regulating the same motor pattern across contexts. These results contribute to the growing body of evidence that behavioral diversity observed in nature may evolve by accumulating and combining alleles, each with modular effects, and show that this principle applies to a suite of behavioral traits that form an integrated strategy.