Same trait, different genes: pelvic spine loss in three brook stickleback populations in Alberta

Abstract

The genetic basis of phenotypic or adaptive parallelism can reveal much about constraints on evolution. This study investigated the genetic basis of a canonically parallel trait: pelvic spine reduction in sticklebacks. Pelvic reduction has a highly parallel genetic basis in threespine stickleback in populations around the world, always involving a deletion of the pel1 enhancer of Pitx1. We conducted a genome-wide association study to investigate the genetic basis of pelvic spine reduction in three populations of brook stickleback in Alberta, Canada. Pelvic reduction did not involve Pitx1 in any of the three populations. Instead, pelvic reduction in one population involved a mutation in an exon of Tbx4, and it involved a mutation in an intron of Lmbr1 in the other two populations. Hence, the parallel phenotypic evolution of pelvic spine reduction across stickleback genera, and among brook stickleback populations, has a non-parallel genetic basis. This suggests that there may be redundancy in the genetic basis of this adaptive polymorphism, but it is not clear whether a lack of parallelism indicates a lack of constraint on the evolution of this adaptive trait. Whether the different pleiotropic effects of different mutations have different fitness consequences, or whether certain pelvic reduction mutations confer specific benefits in certain environments, remains to be determined. Lay SummaryIn this study, we looked for the genetic basis of a well-studied trait in stickleback fish: the pelvic spines. This structure (i.e. the pelvic girdle and attached spines) has a shared developmental basis (and is homologous to) the pelvic bones and hind limbs of all tetrapods (including humans). We know from studying mice, fish, humans, and even manatees that there are several genes that could affect the development of pelvic spines and hind limbs. In one species of stickleback, the threespine stickleback, however, a single gene called Pitx1 is always involved in the loss of pelvic spines in populations that have adapted to freshwater lakes. This replicated evolution of the same trait in the same environmental conditions is called parallel evolution. Its remarkable that Pitx1 is always the gene underlying this adaptive loss of spines in freshwater threespine stickleback populations. We were interested in whether this "genetic parallelism" extended to other species of stickleback that have also evolved the loss of pelvic spines. We looked at three populations of brook stickleback (which are never found in the ocean), each of which contains individuals with and without pelvic spines. We found that the Pitx1 genetic parallelism does not extend to brook stickleback, and, in fact, the genetic basis of pelvic spine loss differs between populations. In Muir Lake and Astotoin Lake, pelvic spine loss results from a mutation in the Lmbr1 gene, and in Shunda Lake, pelvic spine loss results from a mutation in the Tbx4 gene.