Background

Methods

Results

Conclusions

The development of sequencing techniques and increased availability of genome assemblies have enabled comparative studies on genome evolution in the non-model organisms to better understand genomic diversity and adaptation. Using genomic data, we investigated evolutionary questions in the kangaroo rats (genus Dipodomys), a group of New World rodents adapted to arid and semi-arid habitats, and we revealed examples of genomic signatures of their speciation and adaptive evolution. We first resolved the taxonomic issue of whether the formerly conspecific species with different karyotypes, the agile kangaroo rat (AKR, D, agilis, 2N=62) and the Dulzura kangaroo rat (DKR, D. simulans, 2N=60) are distinct species. The results supported their species level status with no evidence of sympatry or interspecific gene flow. We estimated their divergence time as ~0.7 Mya in middle Pleistocene, followed by a ~5-fold decline in the DKR’s effective population size (Ne) to ~20,000 at ~0.1 Mya, recently recovering to ~50,000, converging with that of AKR. AKR is generally distributed to higher elevations than DKR, and we investigated the inter- and intra-specific effects of elevation. The mean length of runs of homozygosity (ROHs) was negatively correlated with the elevation, suggested more structured populations at higher elevations in the two species, yet the levels of nucleotide diversity (π) were constant. AKR showed more selective sweeps than DKR, apparently associated with adaptation to high elevation, e.g., thermoregulation and response to hypoxic stress, and intraspecific comparisons among populations also revealed selective sweeps associated with local adaptation linked to elevation. The changes identified appeared to be regulatory. Finally, we employed data-driven and hypothesis-driven approaches to identify genes under positive selection in arid adapted heteromyids (kangaroo rats and mice and pocket mice) and convergently in unrelated arid adapted rodents including jerboa, gerbil, and cactus mouse. Notable among the candidate genes were those involved in energy production and hemostasis, and in response to osmotic stress.

Exposure to environmental stress is a common feature of the life of most organisms, making the ability to cope with such stress imperative to survival and persistence. In particular, small populations that experience inbreeding and inbreeding depression may be particularly vulnerable to the effects of environmental stress. However, we lack and understanding of the factors that contribute to the considerable variation in effects of stress on the expression of inbreeding depression. In this dissertation I examined the role of four factors in determining the outcome of inbreeding-stress interactions.

First I investigated the relationship between stress level, measured as the reduction in fitness a stress causes relative to benign conditions, and the magnitude of inbreeding depression. I found a strong positive linear relationship both in laboratory populations and populations exposed to field conditions, whereby inbreeding depression increases as the level of stress increases. Contrary to initial predictions, in a three year field study I found winter conditions were more stressful and induced greater inbreeding depression relative to summer conditions.

Second, I examined how different types of abiotic and biotic stresses affect the expression of inbreeding depression both during exposure (larval survival) and after exposure (male mating). I found that during exposure, only heat and competitive stress amplified inbreeding depression relative to benign conditions, while ethanol and bacterial stress did not. In addition, I found that exposure to stress during development significantly reduced inbreeding depression for competitive male mating success, but only for the two biotic stresses.

Finally, I investigated how stress and sexual selection affect the expression of inbreeding depression in males versus females. I found a striking difference in the magnitude of inbreeding depression expressed in the sexes, with males suffering a two-fold higher cost to being inbred that females. This is presumably due sexual selection, via female choice and/or male competitive interactions, increasing selection against inbred males expressing deleterious alleles.