Invoking adaptation to decipher the genetic legacy of past climate change

Abstract

Persistence of natural populations during periods of climate change is likely to depend on migration (range shifts) or adaptation. These responses were traditionally considered discrete processes and conceptually divided into the realms of ecology and evolution. In a milestone paper, Davis and Shaw (2001) Science 292:673 argued that the interplay of adaptation and migration was central to biotic responses to Quaternary climate, but since then there has been no synthesis of efforts made to set up this research program. Here we review some of the salient findings from molecular genetic studies assessing ecological and evolutionary responses to Quaternary climate change. These studies have revolutionized our understanding of population processes associated with past species migration. However, knowledge remains limited about the role of natural selection for local adaptation of populations to Quaternary environmental fluctuations and associated range shifts, and for the footprints this might have left on extant populations. Next-generation sequencing technologies, high-resolution paleoclimate analyses, and advances in population genetic theory offer an unprecedented opportunity to test hypotheses about adaptation through time. Recent population genomics studies have greatly improved our understanding of the role of contemporary adaptation to local environments in shaping spatial patterns of genetic diversity across modern-day landscapes. Advances in this burgeoning field provide important conceptual and methodological bases to decipher the historical role of natural selection and assess adaptation to past environmental variation. We suggest that a process called "temporal conditional neutrality" has taken place: some alleles favored in glacial environments become selectively neutral in modern-day conditions, whereas some alleles that had been neutral during glacial periods become under selection in modern environments. Building on this view, we present a new integrative framework for addressing the interplay of demographic and adaptive evolutionary responses to Quaternary climate dynamics, the research agenda initially envisioned by Davis and Shaw (2001) Science 292:673.

Integrating three comprehensive data sets shows that mitochondrial DNA variation is linked to species traits and paleogeographic events in European butterflies

“…Recent evidence proved that these mitochondrial‐derived traits are involved, among others, in local adaptation to climatic conditions (Toews et al, ). Under this perspective, the strong variation in mtDNA sequences among populations and the relatively fast shifts in their distributions demonstrated by direct and indirect evidence, indicate that spatial mtDNA variation represents a source of differential adaptive optima, which can sweep across populations and preserve species in a rapidly changing environment (de Lafontaine, Napier, Petit, & Hu, ). The macroscopic consequence is the preservation of species diversity and of the related ecosystem functioning.…”

Ice‐age persistence and genetic isolation of the disjunct distribution of larch in Alaska

“…Our understanding of the relative importance of ice-age refugial persistence versus postglacial long-distance migration in the development of modern species distributions has advanced greatly with recent integrative studies combining fossil, genetic, and modeling analyses (e.g., Gavin et al, 2014;Wang et al, 2015). These studies have called into question the role of long-distance migration as the dominant species response to shifting climates (Christmas, Breed, & Lowe, 2016;Corlett & Westcott, 2013;de Lafontaine, Napier, Petit, & Hu, 2018). In particular, a growing number of phylogeographic surveys have demonstrated populations persisted in situ, in refugia closer to the ice sheets during the LGM than previously discernible from other lines of evidence (e.g., Anderson, Hu, Nelson, Petit, & Paige, 2006;de Lafontaine, Ducousso, Lefèvre, Magnanou, & Petit, 2013;McLachlan, Clark, & Manos, 2005;Napier, de Lafontaine, Heath, & Hu, 2019).…”

Climatic niche predicts the landscape structure of locally adaptive standing genetic variation

“…Our approach fills an important gap in identifying geographic regions where adaptive genomic diversity is concentrated within the range, while also revealing the relative importance of historic and selective processes shaping the current distribution of SGV 13,29,61,62 . Our findings in a widespread forest tree species suggest that adaptive SGV clusters non-randomly along geographic and climatic gradients, with decreasing alpha diversity and increasing compositional turnover (i.e., beta diversity) with distance away from the center of the current climatic niche ( Fig.…”

“…While proximity to the rear range edge may predict if SGV for ancestral polymorphism has been reduced by colonization bottlenecks, it may not adequately capture how SGV has been shaped by spatially-varying selection after expansion 29 . In this context, populations inhabiting ecologically marginal environments are of particular interest 13,30 .…”