Adaptive population divergence and directional gene flow across steep elevational gradients in a climate‐sensitive mammal

Abstract

The ecological effects of climate change have been shown in most major taxonomic groups; however, the evolutionary consequences are less well-documented. Adaptation to new climatic conditions offers a potential long-term mechanism for species to maintain viability in rapidly changing environments, but mammalian examples remain scarce. The American pika (Ochotona princeps) has been impacted by recent climate-associated extirpations and range-wide reductions in population sizes, establishing it as a sentinel mammalian species for climate change. To investigate evidence for local adaptation and reconstruct patterns of genomic diversity and gene flow across rapidly changing environments, we used a space-for-time design and restriction site-associated DNA sequencing to genotype American pikas along two steep elevational gradients at 30,966 SNPs and employed independent outlier detection methods that scanned for genotype-environment associations. We identified 338 outlier SNPs detected by two separate analyses and/or replicated in both transects, several of which were annotated to genes involved in metabolic function and oxygen transport. Additionally, we found evidence of directional gene flow primarily downslope from high-elevation populations, along with reduced gene flow at outlier loci. If this trend continues, elevational range contractions in American pikas will likely be from local extirpation rather than upward movement of low-elevation individuals; this, in turn, could limit the potential for adaptation within this landscape. These findings are of particular relevance for future conservation and management of American pikas and other elevationally restricted, thermally sensitive species.

Contrasting signatures of introgression in North American box turtle (Terrapenespp.) contact zones

“…Diminishing sequencing costs coupled with an upsurge in genomic annotations have facilitated extensive application of this reverse-ecology approach within a variety of ecological contexts. Examples include inference of adaptive divergence in seasonal growth and variability in immune responses (Rödin-Mörch et al 2019), biodiversity response to environmental gradients (temperature, Keller & Seehausen 2012; altitudinal, Guo et al 2016; elevational, Waterhouse et al 2018; Teske et al 2019), and an increased capacity to examine contemporary effects, such as that of anthropogenic modulation of reproductive boundaries (Garroway et al 2010; Taylor et al 2014; Grabenstein & Taylor 2018). A result is an increased resolution with which to gauge how environmental and climatic shifts over both geologic and contemporary timescales shift species distributions and alter pre-existing adaptive gradients (Rosenzweig et al 2008; Taylor et al 2015; Ryan et al 2018).…”

Divergent selection along elevational gradients promotes genetic and phenotypic disparities among small mammal populations

“…Such mixed effects of contrasting climatic variables on a short scale reflect marked heterogeneous vegetation zonation along mountain slopes, in some cases mirroring tropical-temperate forest transitions. In contrast, elevational gradients over a small geographic scale may facilitate migration, especially in species with a high dispersal capacity, thereby constraining morphological and genetic divergence (Branch et al, 2017;Kawecki & Ebert, 2004;Keller et al, 2013;Nosil et al, 2008;Ohsawa & Ide, 2008;Sexton, Hangartner, & Hoffmann, 2014;Waterhouse, Erb, Beever, & Russello, 2018). Individuals living in distinct elevation zones are thus expected to show phenotypic and genetic disparities owing to strong divergent ecological selection (Branch, Jahner, Kozlovsky, Parchman, & Pravosudov, 2017;Kawecki & Ebert, 2004;Keller et al, 2013;Ohsawa & Ide, 2008).…”

Pre-adaptation to climate change through topography-driven evolution of traits and their plasticity

“…Fine-scale environmental variation has frequently been associated with high levels of adaptive phenotypic variation. In particular, the highly heterogeneous landscapes from mountain ranges provide ample opportunity for adaptive radiation at fine spatial scales (Halbritter et al 2018; Waterhouse et al 2018). Moreover, high-altitudinal secondary valleys and cold air sinks typical of topographically complex landscapes designate topographical factors other than altitude as contributing determinants of temperature and soil moisture levels (Körner 2007; Günther et al 2016; O’Brien et al 2017; Pfennigwerth et al 2017).…”