Adaptation to increasing elevation via metabolic rates and mitochondrial genetics in Andean birds

Abstract

Closely related species often replace each other at different elevations, a pattern that results in high biodiversity in mountains. Species range limits are set by physiological adaptation to gradients in temperature and oxygen availability as well as by competition with species above and below them on the gradient. As mountains warm due to climate change and many species move upward in elevation it is increasingly important to understand the mechanisms of climatic adaptation and competition that govern where and when species will persist, migrate, or go extinct. We investigated the genetics and physiology of tapaculos (Passeriformes: Rhinocryptidae), a group of small, weakly flying birds known for their narrow elevation ranges across the Andes, where as many as 6 species may replace each other on one transect. We first looked for selection on the mitochondrial genome, which is thought to be important in adaptation to elevation, in 85 members of this clade across South America. We found a signature of intensified positive selection on mitochondrial genes among species with mid-point elevations above 3000 m, suggesting metabolic adaptation to the harsh, high-altitude environment. We then measured metabolic rates and mitochondrial function in the field in four species of the genus Scytalopus that replace each other in a series along the Manu elevation gradient in Southeastern Peru. We found that higher elevation species have higher Basal Metabolic Rates (BMR) and more extreme Lower Critical Temperatures (LCTs), suggesting adaptation to the cold. However, these differences do not have a clear basis in mitochondrial function, which was broadly similar across species. Rather, higher-elevation species are smaller overall but have larger relative organ masses and maintain lower body temperatures, which may be adaptations to meeting the high thermogenic demands of their environment. These four species conform well to expectations of the Competitive-Exclusion Tolerance Rule (Martin & Ghalambor, 2023), with each species up the gradient being a poorer competitor (smaller body size) but having adapted to a harsher part of the gradient that more competitive species cannot occupy. We discuss these results in the context of theories about the importance of climate, competition, and ecotones in the distribution of Andean organisms, predicting that species living in the highest-elevation forests just below the treeline may be at the greatest risk of extinction due to climate change.