Ecological genomics of high altitude adaptation in Rufous-collared sparrows (Zonotrichia capensis)

Abstract

Adaptation is among the most prominent subjects in evolutionary biology. Despite its ubiquity in nature, many details of how adaptation occurs in natural populations remain poorly understood. Of particular interest are the genes and biochemical pathways that underlie adaptive phenotypes and how plasticity in these systems contributes to adaptive evolution. In this dissertation, I address these questions by investigating the molecular genetic basis of high-altitude adaptation in the Rufous-collared Sparrow (Zonotrichia capensis), a species with a broad altitudinal distribution in the Andes. First, I examined the role that variable selection pressures along elevational gradients play in the population genetic structure of Z. capensis. I found that mitochondrial gene flow was severely reduced along elevational transects relative to latitudinal control transects. Nuclear gene flow, however, was not affected by the elevational gradient. These results suggest that natural selection constrains mitochondrial gene flow along elevational gradients. The mitonuclear discrepancy was consistent with local adaptation of mitochondrial haplotypes, highlighting the importance of metabolic pathways in high-altitude adaptation in Z. capensis. Second, I used a newly developed genomic tool, a zebra finch (Taeniopygia guttata) cDNA microarray, to measure variation in genome-wide patterns of gene expression between high- and low-elevation populations of Z. capensis. I found that nearly 200 genes, many of which were involved in metabolic processes, were differentially expressed when individuals were sampled at their native altitudes. A common garden experiment demonstrated substantial plasticity in gene expression, and these results suggest that plasticity in the biochemical pathways that underpin cold and hypoxia compensation in Z. capensis may mechanistically contribute to enabling its broad altitudinal distribution. Finally, I examined geographic variation in metabolic gene expression along an elevational gradient. Although metabolic adjustments are often involved in thermal stress response and temperature decreases linearly with elevation in the Andes, expression of metabolic genes was non-linearly related to elevation. These results suggest a decoupling of metabolic gene expression and local temperature regimes. This decoupling may have several explanations, but the most plausible seem to be related to either physiological tradeoffs between thermal stress and hypoxia compensation, or genetically encoded expression differences.