My research focuses on understanding genomic mechanisms underlying adaptation and speciation. How do populations adapt to different selective landscapes, what genetic variation experiences selection and where does this variation come from (de novo mutation, standing variation or introgression)? And when does adaptation lead to the evolution of reproductive isolation between populations and ultimately to their coexistence as new species? With next-generation sequencing data, it is now possible to identify the genetic targets of selection in unprecedented resolution and to reconstruct the sequence of events ultimately leading to new species, by studying different stages of the speciation process with population genetic methods. The models I am using for different stages of speciation have been adaptive radiations in threespine stickleback (Gasterosteus aculeatus s.l.) in Europe and North America and among East African cichlids from the Lake Victoria region.
Genomics of rapid ecological speciation
Threespine stickleback have been released into the large Lake Constance catchment around 150 years ago and have since then colonized both lake and stream habitats successfully, making roughly 50% of today’s fish biomass in the lake. Adaptation to the two habitats led to divergence between lake and stream ecotypes in body size, body armor, feeding morphology, nuptial color and life history: lake fish get much bigger, have larger bony plates, eat more planctonic than benthic prey, have redder throats, start breeding one year later and get older than stream fish. In a study in PLoS Genetics, we showed that they even started to breed in sympatry while maintaining ecotypic divergence, making them an unusual case of ecological speciation with very early sympatry. Genomic divergence associated with these two ecotypes persists on multiple chromosomes despite ongoing gene flow, in particular in low recombination regions where the genetic basis of many divergent traits is also found.
Speciation driven by selection on nuptial color
A very young (<90 years) old pond near Bern harbors a small, peculiar population of threespine stickleback with two male morphs: larger red-throated males breed on the steep and shady shore and make tiny, concealed nests, while smaller orange-throated males breed on the open, sunny and deeper pond bottom and make large crater nests. In a paper in Molecular Ecology, we showed that divergence is limited to nuptial coloration and extended phenotype (nest), but absent in predator defense, feeding and swimming performance traits, and that this divergence is reflected in moderate genomic divergence on multiple chromosomes containing potential candidate genes involved in color vision. We also found that females prefer either the orange males or show a tendency to prefering the red male in an experimental setup, published in a recent paper in Evolutionary Ecology Research. Therefore, sexual selection, interacting with the environment, has likely led to divergence and stabilization of these two morphs in full sympatry – a situation that could be the earliest stage of ecological speciation.
Origin of and adaptation in an emerging adaptive radiation
Stickleback from very different origin have adapted to lake and stream environments in several catchments across Switzerland: a Rhone lineage from South-Western Europe was introduced into Lake Geneva, an Eastern European lineage into Lake Constance and a mixture of these two and a Northern European Rhine lineage have colonized Lake Biel. We found that ecotype differentiation in the genome persist only in Lake Constance against high amounts of gene flow. Furthermore, we used demographic modelling to date the split between the different lineages colonizing these lakes and to find out whether gene flow between the lineages has occurred and potentially contributed to the repeated divergence of lake and stream ecotypes.
The three previous projects have been part of my PhD research supervised by Ole Seehausen, Laurent Excoffier and Katie Wagner and conducted at the University of Bern and Eawag, Switzerland, in close collaboration with my colleagues Kay Lucek, Joana Meier and my BSc student Anna Feller.
Adaptation genomics in an “older” adaptive radiation
The adaptive radiation of threespine stickleback on the Haida Gwaii archipelago in Western Canada started after the retreat of the ice sheets roughly 12,000 years ago, where stickleback invaded many different ecological theaters, varying in predator composition, water chemistry and system size from large to small lakes and streams, oligotrophic to dystrophic to eutorphic lakes. Adaptation in stickelback to these environments led to the largest phenotypic diversity observed in any stickleback radiation, with light spectrum, system size and predator composition being the main predictors of phenotypic variation. In my first postdoc with Tom Reimchen at the University of Victoria, Canada, and in collaboration with David Kingsley, Felicity Jones and Federica di Palma, I am exploring the genomic targets of repeated selection across the radiation using 58 whole genomes. We discovered that convergent evolution in a color vision gene between threespine stickleback alleles and 200 million years old duplicates of the same genes has allowed the stickleback to colonize and adapt to blackwater systems in a repeated fashion.
Unraveling the largest known recent vertebrate radiation
The East African Lake Victoria contains more than 500 species of cichlid fish that evolved since the lake re-filled 15,000 years ago, making this the largest young adaptive radiation among vertebrates. Starting in 2017, in my second postdoc with Ole Seehausen and Laurent Excoffier, and in collaboration with Joana Meier and Matt McGee at University of Bern and Eawag, Switzerland, I will use the power of whole genome data to reconstruct the evolutionary history behind this largest recent adaptive radiation in vertebrates, to identify targets of natural and sexual selection and to test different hypotheses on the origin of adaptive radiation, such as the role of a hybrid swarm or a syngameon origin in triggering radiations.