What Do We Really Know About Adaptation at Range Edges?

Abstract

Recent theory and empirical evidence have provided new insights regarding how evolutionary forces interact to shape adaptation at stable and transient range margins. Predictions regarding trait divergence at leading edges are frequently supported. However, declines in fitness at and beyond edges show that trait divergence has sometimes been insufficient to maintain high fitness, so identifying constraints to adaptation at range edges remains a key challenge. Indirect evidence suggests that range expansion may be limited by adaptive genetic variation, but direct estimates of genetic constraints at and beyond range edges are still scarce. Sequence data suggest increased genetic load in edge populations in several systems, but its causes and fitness consequences are usually poorly understood. The balance between maladaptive and positive effects of gene flow on fitness at range edges deserves further study. It is becoming increasingly clear that characterizations about degree of adaptation based solely on geographical peripherality are unsupported.

Adaptation across geographic ranges is consistent with strong selection in marginal climates and legacies of range expansion

“…4). Reinforcing the idea that range edges are not all alike (Hampe and Petit, 2005; Angert et al, 2020; Oldfather et al, 2020), peripherality itself–without consideration of direction or environment–did not strongly predict local adaptation or site quality (Fig. 3).…”

“…Genetic load has many possible sources, including immigration of maladaptive alleles (‘migration load’), genetic drift (‘drift load’), and allele surfing of deleterious mutations during spread (‘expansion load’) (Whitlock and Davis, 2011; Peischl et al, 2013). While our results cannot distinguish among these sources, accumulating evidence from genomics, field transplants, and experimental crosses suggests that range-edge populations might be particularly likely to harbor deleterious mutations and benefit from immigration (reviewed in Angert et al, 2020). This suggests that high genetic load at range edges is more likely due to expansion and drift than to migration.…”

“…It follows that if low-quality sites predominate at range edges (Fig. 1B), selection at edges will be stronger than in the range center (Crow, 1958; Caruso et al, 2017; Angert et al, 2020). However, if response to selection is constrained, individual fitness and population size will remain low in these low-quality sites.…”

“…Across large spatial scales, climate is often assumed to be the major ecological agent of divergent selection and a predominant factor limiting species’ ranges (Araújo and Rozenfeld, 2014; Cunningham et al, 2016). However, climate marginality is only one component of ecological marginality, and increasing evidence implicates biotic interactions as a key driver of selection even at broad geographic scales (Araújo and Rozenfeld, 2014; Belmaker et al, 2015; Armitage and Jones, 2020; Angert et al, 2020, and references therein). Additionally, it is not always the case that geographically peripheral populations inhabit climatically marginal conditions (Lira-Noriega and Manthey, 2014; Pironon et al, 2015; Oldfather et al, 2020).…”

Large-scale geography survey provides insights into the colonization history of a major aphid pest on its cultivated apple host in Europe, North America and North Africa

“…Understanding the evolutionary processes underlying the colonization of new environments and the range expansion of species is a key goal in evolutionary biology (Angert, Bontrager, & Ågren, 2020;Austerlitz, Jung-Muller, Godelle, & Gouyon, 1997;Excoffier, Foll, & Petit, 2009;Hoffmann & Courchamp, 2016;Rius & Darling, 2014). Crop parasites, with their frequent shifts in hosts involving the colonization of new hosts across large geographic ranges, are good models to study the mechanisms of rapid colonization and range expansion (Garnas et al, 2016;Gladieux et al, 2014;Stukenbrock & McDonald, 2008).…”