How does evolution shape genomes?

How do genomes structure evolutionary change?

 

Evolution has produced a system for transmitting information between generations and across time and space. It is intricate, robust, messy — and I want to understand it.

A genome is the unit of inheritance: you got one copy in full from each of your biological parents. Each of those genomes has been shaped by a rich evolutionary history and can tell us about events that happened thousands or millions of years ago. And the architecture of a genome — its size, its division into chromosomes, its gene content, and so on — influences how the information it carries is inherited. In doing so, the genome architecture affects the future paths available to evolution, potentially shutting some down while clearing the way for others.


The genomics of adaptation

 
Genetic diversity (π) and divergence (DXY) at RAD loci associated with stickleback habitat type (blue: freshwater, Red: marine). See our preprint on  bioRxiv  for more details!

Genetic diversity (π) and divergence (DXY) at RAD loci associated with stickleback habitat type (blue: freshwater, Red: marine). See our preprint on bioRxiv for more details!

Adaptive evolution shapes genetic variation throughout the genome. Directional selection removes variation locally, both genomically and geographically, while balancing and spatially variable selection have the potential to maintain variation over long spans of evolutionary time. What forms of selection are the predominant drivers of genomic diversity? How do globally and locally adaptive alleles contribute to observed patterns of genomic diversity? When did they evolve? And what kinds of variation -- from single nucleotide polymorphism to chromosomal rearrangements -- are important during adaptation?

I studied these questions extensively as a graduate student and continue to do so as a postdoc. Working in stickleback, I modified restriction site-associated DNA sequencing (RAD-seq) to identify patterns of sequence diversity and divergence between locally adapted populations. This work, published in Evolution Letters, demonstrated that much of the genetic variation involved in local adaptation is organized into haplotypes that are millions of years old, even when the populations themselves were founded a mere 10,000 years ago.

Genetic and Genomic Architecture

An genome scan of genetic differentiation (FST) shows different architectures depending on the map used. Top is the physical map (measured in base pairs). The Y axis and coloration depict FST. The next three rows are genetic maps (measured in genetic distance) from individuals homozygous or heterozygous for a chromosomal inversion.

An genome scan of genetic differentiation (FST) shows different architectures depending on the map used. Top is the physical map (measured in base pairs). The Y axis and coloration depict FST. The next three rows are genetic maps (measured in genetic distance) from individuals homozygous or heterozygous for a chromosomal inversion.

How many genetic loci contribute to adaptation? How many genomic regions? These questions are related but distinct. Genomes vary widely in size, gene content, and structure. These factors among many others affect how the genetic material is shuffled by recombination during meiosis. A single genetic locus may represent a single nucleotide position when (scaled) recombination rates are very high, or it may include many millions of basepairs locked together in a chromosomal inversion.

I find the integration of genetic maps and physical genomes fascinating and, ultimately, critical for our understanding of evolution. In stickleback fish, I study how recombination rate variation alters patterns of inheritance and how rate variation itself has likely been subject to adaptive evolution.

I am looking ahead to new opportunities to tackle these questions using sequencing and molecular technologies that will make high-resolution maps available for almost any system.

 

The spatial and temporal scale of adaptation

populations of Mimulus guttatus have adapted to extreme environments in Yellowstone National Park. The main photo is of an annual plant living on thermally heated soil. Inset: a perennial plant avoids both drought and hard freezes in a creek near Old Faithful.

populations of Mimulus guttatus have adapted to extreme environments in Yellowstone National Park. The main photo is of an annual plant living on thermally heated soil. Inset: a perennial plant avoids both drought and hard freezes in a creek near Old Faithful.

As a postdoc in Lila Fishman's lab at the University of Montana, I study populations of the yellow monkeyflower, Mimulus guttatus, to understand how organisms adapt to drastic changes in habitat, either across geography or through time. In Yellowstone National Park, populations of M. guttatus have adapted to live next to thermal springs. These habitats are devoid of nearly all plant species, but M. guttatus has managed to eke out a living this extreme environment. Moreover, many thermal populations exist throughout the park, interspersed among the more 'typical' M. guttatus populations that represent the ancestral form.

What are the genetic and genomic bases of thermal adaptation? Have geographically distinct populations adapted independently multiple times or is adaptive genetic variation shared among populations? Did these alleles originate within the park or has gene flow brought alleles to these populations from elsewhere in the species' range? Results are forthcoming...