Adaptation to new and changing environments: from experiments to field studies

Abstract

In today's rapidly changing world, organisms are often exposed to new or challenging environments. Following environmental change, populations may experience one or more of the following outcomes: they may disperse to a new habitat, persist through phenotypic plasticity or adaptive evolution, or go extinct. Here, I focus on adaptive evolution as a mechanism for enabling populations to respond to different types of environmental change. Adaptation may be necessary in less mobile species, or in fragmented landscapes where dispersal corridors are not available. Insects can serve as excellent models for studying the evolutionary dynamics of populations, as their life cycles are relatively short and multiple generations can occur within a few years, enabling rapid adaptation. In this dissertation, I explore the impacts of a change in phenology (Chapter 1), a challenging environment (Chapter 2), and the presence of a mountain range (Chapter 3) on the adaptation of insect populations in both the laboratory (Chapters 1-2) and in the field (Chapter 3). To begin, I studied the effects of a phenology shift using experimental evolution. Climate change can affect the length and timing of seasons, which in turn can alter the time available for insects to complete their life cycles and successfully reproduce. Intraspecific hybridization between individuals from genetically distinct populations, or admixture, can boost fitness in populations experiencing environmental challenges. Admixture can particularly benefit small and isolated populations that may have high genetic load by masking deleterious alleles, thereby immediately increasing fitness, and by increasing the genetic variation available for adaptive evolution. To evaluate the effects of admixture on populations exposed to a novel life cycle constraint, I used the red flour beetle (Tribolium castaneum) as a model system. Distinct laboratory lineages were kept isolated or mixed together to create populations containing 1 to 4 lineages. I then compared the fitness of admixed populations to 1-lineage populations while subjecting them to a shortened generation time. After an initial decline in fitness in the new environment, the admixed populations demonstrated significantly greater fitness compared to the 1-lineage populations after three generations. The timing of the increase in fitness suggests that adaptation to the novel environmental constraint occurred, as opposed to the masking of deleterious alleles. In Chapter 2, I examined the effects of consistent immigration on the probability and timing of adaptation. Theory predicts that immigration can delay extinction and provide novel genetic material that can prevent inbreeding depression and facilitate adaptation. However, when potential source populations have not experienced the new environment before (i.e., are naive), immigration can counteract selection and constrain adaptation. This study evaluated the effects of immigration of naive individuals on adaptation in experimental populations of red flour beetles. Small populations were exposed to a challenging environment, and three immigration rates (0, 1, or 5 migrants per generation) were implemented with migrants from a benign environment. Following an initial decline in population size across all treatments, populations receiving no immigration gained a higher growth rate one generation earlier than those with immigration, illustrating the constraining effects of immigration on adaptation. After seven generations, a reciprocal transplant experiment found evidence for adaptation regardless of immigration rate. Thus, while the immigration of naive individuals briefly delayed adaptation, it did not increase extinction risk or prevent adaptation following environmental change. For Chapter 3, I shifted my focus from laboratory populations to natural populations. In nature, elevation gradients provide a way to study populations across a range of environmental conditions within relatively small spatial scales. Adaptation to the local habitat might occur in response to the unique selection pressures present at different elevations, resulting in distinct populations adapted to different environments. However, if there is high habitat connectivity, gene flow can slow or prevent adaptation while also maintaining genetic variation and large population sizes. In this chapter, I used genomics to investigate the interplay between selection and gene flow in butterfly populations collected from high (>2,500m) and low (<2,000m) elevations, both east and west of the Rocky Mountains. My study focused on the Rocky Mountain subspecies of the clouded sulfur butterfly (Colias philodice eriphyle Edwards). Weak, but statistically significant, patterns of population differentiation were apparent between butterflies collected east and west of the Rockies, and eastern butterflies harbored greater genetic diversity compared to those from the west. Additionally, FST values close to zero suggest gene flow was high among the collection sites. I used a redundancy analysis to show that the observed east-west differentiation may be largely driven by greater precipitation east of the Rockies, and I identified over 16,000 putatively adaptive loci and 3,000 candidate genes associated with the environmental variables that may underly adaptive traits. In summary, my dissertation research highlights that adaptation can occur with genetic mixing or immigration in less than 10 generations in the lab (Chapters 1-2) and that adaptation to different environments can be identified among well-connected populations in the field (Chapter 3). It is well documented that gene flow can help maintain genetic variation, particularly among fragmented populations. My results emphasize that gene flow does not impede natural selection (Chapters 2-3), and that mixing between distinct populations can even promote adaptation (Chapter 1). My findings, therefore, support the use of methods such as translocation and wildlife corridors to facilitate gene flow for sexually reproducing conservation targets.