Genetic and genomic basis of adaptation and speciation

Pairs of fish species

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.

Previous research

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.

Ongoing research directions

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).

Selected publications

Stuart YE, Veen T, Weber JN, Hanson D, Ravinet M, Lohman BK, Thompson CJ, Tasneem T, Doggett A, Izen R, Ahmed N, Barrett RDH, Hendry AP, Peichel CL, Bolnick DI (2017) Contrasting effects of environment and genetics generate a continuum of parallel evolution. Nature Ecology & Evolution 1: 0158. 10.1038/s41559-017-0158

Conte GL, Arnegard ME, Best J, Chan YF, Jones FC, Kingsley DM, Schluter D, Peichel CL (2015) Extent of QTL reuse during repeated phenotypic divergence of sympatric threespine stickleback. Genetics 201: 1189-1200. 10.1534/genetics.115.182550

Arnegard ME, McGee MD, Matthews BW, Marchinko KB, Conte GL, Kabir S, Bedford N, Bergek S, Chan YF, Jones FC, Kingsley DM, Peichel CL*, Schluter D* (2014) Genetics of ecological divergence during speciation. Nature 511: 307-311. 10.1038/nature13301

Miller CT, Glazer AM, Summers BR, Blackman BK, Norman AR, Shapiro MD, Cole BL, Peichel CL, Schluter D, Kingsley D (2014) Modular skeletal evolution in sticklebacks is controlled by additive and clustered quantitative trait loci. Genetics 197: 405-420. 10.1534/genetics.114.162420

Conte GL, Arnegard ME, Peichel CL, Schluter D (2012) The probability of genetic parallelism and convergence in natural populations. Proceedings of the Royal Society B: Biological Sciences 279: 5039-5047. 10.1098/rspb.2012.2146

Malek TB, Boughman JW, Dworkin I, Peichel CL (2012) Admixture mapping of male nuptial color and body shape in a recently formed hybrid population of threespine stickleback. Molecular Ecology 21: 5265-5279. 10.1111/j.1365-294X.2012.05660.x

Kitano J, Lema SC, Luckenbach JA, Mori S, Kawagishi Y, Kusakabe M, Swanson P, Peichel CL (2010) Adaptive divergence in the thyroid hormone pathway in the stickleback radiation. Current Biology 20: 2124-2130. 10.1016/j.cub.2010.10.050

Kitano J, Ross JA, Mori S, Kume M, Jones FC, Chan YF, Absher DM, Grimwood J, Schmutz J, Myers RM, Kingsley DM, Peichel CL (2009) A role for a neo-sex chromosome in stickleback speciation. Nature 461: 1079-1083. 10.1038/nature08441

Kitano J, Bolnick DI, Beauchamp DA, Mazur MM, Mori S, Nakano T, Peichel CL (2008) Reverse evolution of armor plates in the threespine stickleback. Current Biology 18: 769-774. 10.1016/j.cub.2008.04.027

Shapiro MD*, Marks ME*, Peichel CL*, Blackman BK, Nereng K, Jonsson B, Schluter D, Kingsley DM (2004) Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 428: 717-723. 10.1038/nature02415

Peichel CL, Nereng KS, Ohgi KA, Cole BLE, Colosimo PF, Buerkle CA, Schluter D, Kingsley DM (2001) The genetic architecture of divergence between threespine stickleback species. Nature 414: 901-905. 10.1038/414901a