Year of Award

2019

Document Type

Dissertation - Campus Access Only

Degree Type

Doctor of Philosophy (PhD)

Degree Name

Organismal Biology, Ecology, and Evolution

Department or School/College

Division of Biological Sciences

Committee Chair

Jeffrey M. Good

Commitee Members

Creagh W. Breuner, Douglas J. Emlen, Lila Fishman, L. Scott Mills

Keywords

Evolution, Genomics, Population genetics

Publisher

University of Montana

Abstract

Adaptation is central to the origin and persistence of biodiversity in changing environments. A thorough understanding of adaptation requires knowledge of the genetic basis of adaptive traits. Does adaptation proceed through many mutations of small effect or a few mutations of large effect? Does selection act primarily on new mutations or standing genetic variation? To what extent does introgressive hybridization contribute to adaptive standing variation? And what processes shape the maintenance of adaptive variation across space and time? Historically, we have been mostly restricted to theoretical answers to these questions due to the extraordinary challenge of measuring genetic variation in populations. However, technological advances in DNA sequencing in the 21st century opened the door for genomic studies of adaptation in natural populations at previously unimaginable scales. Nonetheless, we still lack a clear understanding of how specific adaptive changes arise in populations and contribute to fitness variation in the wild.

Across boreal and temperate forests in the northern hemisphere, at least 21 mammal and bird species shed their brown summer coats and grow fresh white coats in anticipation of winter snowfall. Snowshoe hares (Lepus americanus) represent perhaps the most iconic example of this seasonal camouflage strategy, which provides a substantial advantage in remaining hidden from predators in snow-covered landscapes. However, in a striking case of local adaptation, snowshoe hares in mild environments along portions of their range edge remain brown during winter. My dissertation seeks to advance our understanding of local adaptation by combining population genomic and phylogenomic datasets with population genetic modeling to dissect the genetic basis and evolutionary history of seasonal camouflage variation in snowshoe hares.

In Chapter 1, I present a review of targeted sequence capture, a powerful genomic tool to help resolve the genetic basis of adaptation in wild populations. I discuss practical considerations for designing and carrying out a targeted capture study and research areas where targeted capture approaches are poised to make important contributions. In Chapter 2, I use targeted capture, whole genome sequencing, and allele-specific expression assays to investigate the genetic underpinnings of locally adaptive seasonal camouflage in snowshoe hares. First, I show that variation in winter coat color in snowshoe hares from the Pacific Northwest is determined by simple genetic changes that influence seasonal expression of the Agouti pigmentation gene. By sequencing the genomes of additional species of hares and jackrabbits (genus Lepus), I demonstrate that the recessive Agouti variant carried by winter-brown snowshoe hares derives from introgressive hybridization with black-tailed jackrabbits (Lepus californicus), a closely related species that also remains brown in the winter. This study provides one of the first examples of introgression underlying the evolution of a trait of known ecological relevance in mammals. In Chapter 3, I generate additional targeted capture and whole genome data to explore the evolutionary history of brown winter camouflage in greater depth. My analyses suggest that populations of brown winter hares in the Pacific Northwest have recently expanded their range into coastal environments and, as a consequence, have accumulated high levels of deleterious variation. This range expansion was likely enabled by ancient introgression of the Agouti gene, which recently spread through coastal environments. However, in the far northwestern edge of the snowshoe hare range, brown winter camouflage has evolved independently, highlighting an important role of convergent evolution in local adaptation to range edge environments. Finally, in Chapter 4, I use population genetic simulations to advance our understanding of adaptive introgression. Preliminary data suggest that differences between hybridizing populations in the relative efficacy of genetic purging and local adaptation are crucial factors influencing the fixation probability of an introgressed beneficial mutation.

Snow cover duration is predicted to dramatically decrease over the next century due to climate change, which may intensify directional selection for winter-brown camouflage. Collectively, my dissertation makes important contributions towards our understanding of how snowshoe hares and other species may respond to past and ongoing change to the environment.

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© Copyright 2019 Matthew R. Jones