Genetic and Morphological Evidence for Local Climate Adaptation in the Americas

Abstract

This dissertation investigates environmental drivers of genetic and morphological variation in the American tropics. Using SNP data and spatially-dense 3D craniofacial landmarks, this project will test the hypotheses that: (1) Mesoamerican populations will show evidence of selection on genes that protect against heat stroke; (2) highland Andeans will show signals of selection on genes that protect against hypothermia, and (3) highland Andeans will exhibit craniofacial changes associated with enhanced conditioning of cold, dry air. Over the past two million years, humans dispersed across the planet and managed to thrive in a variety of distinct ecological niches -- a process often facilitated by local adaptive evolution. Classic examples of this include high altitude (e.g., Andes) and circumpolar zones (e.g., Siberia), where humans have adapted to low oxygen availability and low ambient temperatures. Despite the extreme temperatures of high altitude (cold/arid) and lowland rainforest (hot/humid), there have been very few studies (if any at all) to examine the genetic substrate of local adaptation to these specific ecological niches. To fill this void, this dissertation applies a population genetics framework to identify targets of selection in two Indigenous communities from Central and South America. To investigate putative adaptations to high heat and humidity, Chapter 1 interrogates SNP data from 65 Mexican Mayans from the Yucatán Peninsula. To identify putative adaptations to the tundra- like environment of high altitude, Chapter 2 reports selection scans on SNP data derived from 514 Peruvian Quechua. Chapter 3 reports a geometric morphometrics analysis on facial reconstructions from these two populations: using spatially-dense 3D point clouds, this project xv investigates whether the Andean sample follows craniofacial patterns associated with cold climate that are exhibited in populations from high-latitude or circumpolar environments. The results indicate that both populations underwent strong selective sweeps surrounding genes that might offset niche-specific thermal stress, supporting the first two hypotheses. In Mexican Mayans, there is evidence of selection in genes related to water/salt homeostasis (AKAP11), mitochondrial protein uncoupling (ETFB), vasodilation (BDKRB2), and cellular responses to heat stress (BAG6). In Peruvian Quechua, there was significant evidence of selection in genes related to adaptive thermogenesis (DYNC1H1), brown fat cell differentiation (ZNF52), cellular responses to thermal stress (FAF1), and thyroid-mediated body temperature regulation (DUOX family). Geometric morphometrics analysis showed that midfacial protrusion and lengthened nasal aperture -- which are seen in cold-adapted populations from Tierra del Fuego, Siberia, and the Aleutian Islands -- are exhibited in the putatively cold-adapted Peruvian Quechua population. These results are consistent with the third hypothesis that Andean populations would exhibit craniofacial changes that facilitate the conditioning of cold, harsh mountain air. This dissertation provides some of the first evidence of cold climate adaptation unique to high altitude as well as in the context of the global South. Additionally, this is likely some of the first explicit evidence of heat adaptation derived from a population genetics framework. These results cast light on how niche-specific adaptation may have contributed to broad evolutionary changes in human ancestors and their relatives. To this end, this research provides a case study of genetic adaptations to a novel ecological stress that can unfold over a relatively short interval (<13,000 years): broadly, local climate adaptation likely played a role in shaping variation for a myriad of critical biological processes ranging from metabolism to thyroid function.