Sean M. Rogers

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Research

My main area of study is molecular evolutionary biology. The study of how organisms adapt to new environments and how this process may ultimately lead to speciation has long been considered a ‘mystery of mysteries’ in evolutionary biology. The gene is considered the most elementary unit of adaptation, yet we still do not have answers for some of the most basic questions about the molecular genetics of adaptation.

My research has therefore focused on bridging the gap between ecology and genetics towards understanding how organisms adapt to new and changing environments. I use fish species to answer these questions for primarily two reasons. First, many of the fish populations in Canada have only recently colonized the lakes and rivers they inhabit following the end of the last ice age, about 10 000 years ago. This means they have evolved and adapted to their new habitats in a very ‘rapid’ way, and in some cases comprise some of the youngest species on Earth. Second, many fish species are excellent candidates to study genetics because of their short generation time and the large number of progeny produced each generation. Both of these reasons comprise a rather unique opportunity when studying the underlying molecular mechanisms contributing to adaptation and speciation.

Lake whitefish larvae, juveniles and adults I reared at LARSA during my PhD.

Dwarf and Normal Lake whitefish species pairs (photo: Robert St-Laurent)

I worked with the lake whitefish (Coregonus clupeaformis, Mitchill) for my PhD thesis. These amazing fish are in the same family as trout and salmon and inhabit coldwater lakes all over the Northern hemisphere. In several lakes across Canada lake whitefish have evolved into two populations. This species pair is characterized by a derived form that is remarkably smaller, matures at a much earlier age and lives in the limnetic zone of lakes. This is compared to ‘normal’ form that inhabits the benthic zone of these same lakes. For these reasons, the limnetic populations are often referred to as ‘dwarf’ lake whitefish because of the difference in size from their normal counterparts. Interestingly, this dwarf form has evolved independently in several lakes, leading to the hypothesis that the ecology of the lakes has had a substantial influence on the evolution of these species pairs.

The objective of my PhD thesis was to determine the genetic basis of the differences between dwarf and normal lake whitefish. This would help us understand the genetic changes that occur during ecological divergence and adaptation to new environments.  Specifically, one of my objectives was to localize regions of the whitefish genome that were associated with adaptation and reproductive isolation between dwarf and normal populations. This would give us clues as to what evolutionary steps have led to the inability (or reduced ability) of these two populations to interbreed freely. To achieve this objective, I first made two hybrid backcrosses between dwarf and normal whitefish. Progeny from these crosses were sampled for their DNA and individually tagged (with PIT tags). This allowed me to study the inheritance of several hundred genetic markers in the progeny of both families and construct a genetic map. The genetic map provided the necessary template to localize genomic regions associated with several behavioural, physiological, and morphological traits that differentiated dwarf and normal lake whitefish.

The genetic architecture of population divergence: Linkage maps of the dwarf and Normal lake whitefish species complex and their hybrids (Rogers et al. Genetics 2007)

I measured many traits that I had identified as phenotype-environment associations and were thus associated with adaptation and reproductive isolation. This involved performing experiments on all of these fish throughout their life history, included swimming behaviour video experiments, intensive growth measurements from the juvenile stage to sexual maturity (over three years), and also measurements of size, shape, and the sex of each individual. At the end of the experiments, fish were frozen at -80 degrees Celsius to preserve their RNA (for subsequent gene expression profiling using microarrays which is currently being done in collaboration with Dr. Nicolas Derome and Dr. Andrew Whiteley).

Lake whitefish undergoing a swimming behaviour trial at LARSA and data showing that dwarf lake whitefish grow slower than their normal counterparts in the same environment (Rogers and Bernatchez 2005)

Using quantitative trait locus (QTL) mapping, I tested for associations between these traits and the genes the progeny had inherited using the genetic map. I found several regions of the genome that were linked in association with adaptive traits. More importantly, there was evidence that natural selection had influenced these regions among independently evolving species pairs inhabiting distinct lakes. The loci exhibiting a signature of selection were more likely to be associated with adaptive QTL than with other regions of the genome. This was important because it offered evidence that natural selection at these key genomic regions has been maintaining the differences between dwarf and normal lake whitefish and contributing to the rapid evolution of these species pairs. Much of this work was pioneered by Dr. Louis Bernatchez who continues to work on nearly all aspects of whitefish evolution, especially in genomics.

Genome scans of differential gene exchange for growth associated mapped QTL (yellow bars) among four natural sympatric pairs of dwarf and normal lake whitefish (a) Webster Lake (b) East Lake (c) Indian Pond, and (d) Cliff Lake. Distributions represent the categorical frequency of FST values. Growth QTL were compared to the distribution of differentiation under neutrality (green bars, see Campbell & Bernatchez 2004 for details on simulated distributions). The 95% quantile of simulated distributions delineates outlier growth QTL potentially under directional selection (i.e. FST > 95% quantile). (Rogers and Bernatchez 2005)

Genetic maps of whitefish linkage groups 1 and 4 showing the locations of adaptive QTL overlapping with outlier loci that exhibit a signature of selection among natural sympatric pairs of lake whitefish (Rogers and Bernatchez, Molecular Biology and Evolution 2007)

Current Research:

My current research has been a natural progression from my previous work. I am currently applying an experimental approach to testing conceptual issues in the genetics of adaptation to new environments using the threespine stickleback (Gasterosteus aculeatus) as my study organism. This research is being conducted in the department of Zoology at the University of British Columbia with Dr. Dolph Schluter. The threespine stickleback has emerged as a key vertebrate genomic resource leading to an excellent system whereby specific evolutionary hypotheses can be tested. (thanks in large part to the tremendous efforts of many, including Dr. Katie Peichel and Dr. David Kingsley).

Photo: Kerry Marchinko

With the collaboration of the Stanford Genome Evolution Center, I am conducting experiments that apply the theory for the genetics of adaptation to four wild populations. This experiment involves repeatedly crossing the same marine ancestor to fish from four recently colonized freshwater lakes that differ in age and degree of phenotypic divergence. Genetic and molecular tools in these crosses will be used to test predictions about the genetics of parallel adaptive trait divergence. Comparing the genetic basis of adaptations in the older, more divergent lakes with the QTL underlying younger, more recent colonizations will allow us to test specific predictions about the genetic changes that have occurred during the course of freshwater evolution.

I am also collaborating with Rowan Barrett, a PhD student in Dolph Schluter’s lab. We are experimentally testing the genetics of adaptation from standing variation by colonizing freshwater experimental ponds with natural marine fish that have been genetically confirmed to have one copy of an ancient allele at the key candidate gene (Eda) underlying freshwater armour evolution in sticklebacks. This ancient allele occurs at a very low frequency in saltwater (only 1/1000 marine sticklebacks are homozygous for the low allele), but it is fixed in most freshwater stickleback populations (Colosimo et al. 2005). Because we have colonized our ponds with marine sticklebacks that are heterozygous for Eda, we are able to predict the starting frequency of the genotypes in the next generation in the absence of selection.

Evolution ponds (photo by Rowan Barrett)

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