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

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 ofPitx1. In three populations of brook stickleback in Alberta, Canada, pelvic reduction did not involvePitx1. Instead, pelvic reduction in one population involved a mutation in an exon ofTbx4, and it involved a mutation in an intron ofLmbr1in 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 is redundancy in the genetic basis of this adaptive polymorphism, but it is not clear whether this 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, I 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 calledPitx1is 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. It’s remarkable thatPitx1is always the gene underlying this adaptive loss of spines in freshwater threespine stickleback populations. I was interested in whether this “genetic parallelism” extended to other species of stickleback that have also evolved the loss of pelvic spines. I looked at three populations of brook stickleback (which are never found in the ocean), each of which contains individuals with and without pelvic spines. I found that thePitx1genetic 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 theLmbr1gene, and in Shunda Lake, pelvic spine loss results from a mutation in theTbx4gene.