One of the most fundamental questions in evolutionary biology is “how do new species arise?”. Since the time of Darwin, much progress has been made in understanding the ecological and evolutionary forces that lead to the formation of new species. However, understanding the genetic basis of speciation has been impeded by the fact that species are, by definition, reproductively isolated from each other. Sticklebacks are a particularly compelling model system for genetic studies of the early stages of speciation, as pairs of stickleback populations have adapted to divergent, but overlapping habitats. These “species pairs” are morphologically and behaviorally distinct from each other and exhibit reproductive isolation in the wild. Most of the barriers between them are behavioral, and most of these species pairs can be crossed in the lab to generate viable and fertile hybrids, enabling genetic studies of the phenotypic traits that contribute to reproductive isolation and speciation.
We have pioneered genetic studies of the traits that contribute to reproductive isolation between several different stickleback species pairs, including a unique species pair in Japan. Through extensive behavioral analyses and crosses in the lab, as well as intensive studies in the field, we demonstrated that divergence in male mating displays, female preferences, and hybrid male sterility contribute to nearly complete reproductive isolation between the species in the wild. Our genetic mapping of these traits revealed that hybrid male sterility mapped to the X chromosome, providing empirical evidence for the theoretical prediction that the X chromosome should play an important role in hybrid male sterility. Further, we demonstrated that a difference in male mating behavior maps to a neo-sex chromosome system found in the Japan Sea species. Our work therefore uncovered a new role for sex chromosome evolution in the process of speciation.
More recently, I have collaborated with Dolph Schluter (University of British Columbia) to investigate the genetic basis of traits that contribute to adaptation and reproductive isolation between the benthic-limnetic species pairs, which have evolved in the last 15,000 years as a result of adaptation to distinct foraging habitats within several lakes. Our genetic mapping studies have been performed by growing the crosses in semi-natural ponds that approximate the habitats in the wild, allowing us to map phenotypes that are difficult or simply impossible to measure in the lab. We uncovered a mostly additive and genome-wide genetic architecture for tradeoffs in feeding performance between distinct trophic niches; these results were surprising given the recent divergence and ongoing gene flow in the benthic-limnetic species pair. These studies have allowed us to address long-standing theory about the genetic basis of speciation with gene flow.
Population genomic studies to identify regions of the genome that appear to be under divergent selection between species have become increasingly popular in the field of speciation research. Although these studies can identify genotypes that contribute to fitness or reproductive isolation, a major challenge is to connect these genotypes to the phenotypes that are actually under selection. To overcome this challenge and better identify connections between genotypes, phenotypes and selection in the wild, we plan to integrate whole genome sequencing data with the results of our genetic linkage mapping studies in multiple stickleback species pairs (i.e. Japanese species pair, benthic-limnetic, lake-stream).
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