The coupling hypothesis: why genome scans may fail to map local adaptation genes

Abstract

Genomic scans of multiple populations often reveal marker loci with greatly increased differentiation between populations. Often this differentiation coincides in space with contrasts in ecological factors, forming a genetic-environment association (GEA). GEAs imply a role for local adaptation, and so it is tempting to conclude that the strongly differentiated markers are themselves under ecologically based divergent selection, or are closely linked to loci under such selection. Here, we highlight an alternative and neglected explanation: intrinsic (i.e. environment-independent) pre-or post-zygotic genetic incompatibilities rather than local adaptation can be responsible for increased differentiation. Intrinsic genetic incompatibilities create endogenous barriers to gene flow, also known as tension zones, whose location can shift over time. However, tension zones have a tendency to become trapped by, and therefore to coincide with, exogenous barriers due to ecological selection. This coupling of endogenous and exogenous barriers can occur easily in spatially subdivided populations, even if the loci involved are unlinked. The result is that local adaptation explains where genetic breaks are positioned, but not necessarily their existence, which can be best explained by endogenous incompatibilities. More precisely, we show that (i) the coupling of endogenous and exogenous barriers can easily occur even when ecological selection is weak; (ii) when environmental heterogeneity is fine-grained, GEAs can emerge at incompatibility loci, but only locally, in places where habitats and gene pools are sufficiently intermingled to maintain linkage disequilibria between genetic incompatibilities, local-adaptation genes and neutral loci. Furthermore, the association between the locally adapted and intrinsically incompatible alleles (i.e. the sign of linkage disequilibrium between endogenous and exogenous loci) is arbitrary and can form in either direction. Reviewing results from the literature, we find that many predictions of our model are supported, including endogenous genetic barriers that coincide with environmental boundaries, local GEA in mosaic hybrid zones, and inverted or modified GEAs at distant locations. We argue that endogenous genetic barriers are often more likely than local adaptation to explain the majority of Fst-outlying loci observed in genome scan approaches -even when these are correlated to environmental variables.

The challenge of separating signatures of local adaptation from those of isolation by distance and colonization history: The case of two white pines

“…The endogenous barrier formed after secondary contact between two genetic backgrounds often colocates with an exogenous barrier due to the buildup of linkage disequilibrium between endogenous and exogenous loci. In summary, barriers to gene flow are often both endogenous and exogenous, and inferring the possible role of local adaptation in creating or maintaining them is very difficult (Bierne et al., 2011). …”

“…Postglacial recolonization can also generate allele frequency gradients similar to IBE or IBD as a result of repeated founder events and “allele surfing” along the colonization front (de Lafontaine, Ducousso, Lefèvre, Magnanou, & Petit, 2013) because colonization routes often covary with environmental gradients. Furthermore, postglacial recolonization from different glacial refugia followed by secondary contact can also create genetic barriers (hereafter referred to as isolation by colonization, IBC) that often coincide with environmental clines (e.g., Bierne, Welch, Loire, Bonhomme, & David, 2011; Richardson, Rehfeldt, & Kim, 2009). Hence, because the selective climatic gradients, geography, and postglacial recolonization routes are often spatially correlated in natural populations, it is extremely difficult to separate the relative effects of IBE from those of IBD and IBC.…”

Adaptive genetic variation distinguishes Chilean blue mussels (Mytilus chilensis) from different marine environments

“…In our study, some F ST outlier SNPs may be interpreted as genetic variation in response to adaptation to local environmental conditions (Beaumont 2005), but other alternative explanations are also possible (Gosset and Bierne 2013) such as the examples of different cohorts described above or other endogenous barriers (Bierne et al. 2011) and introgression (Fraïsse et al. 2015).…”

Unexpected mosaic distribution of two hybridizing sibling lineages in the teleplanically dispersing snail Stramonita haemastoma suggests unusual postglacial redistribution or cryptic invasion

“…Postglacial secondary contact zones between Atlantic and Mediterranean lineages have always been detected at the Almeria–Oran front in planktonic dispersing marine species (Patarnello et al., 2007). One explanation is that the barrier to larval dispersal and/or the environmental boundary at the Almeria–Oran front have acted as a trap for hybrid zones (Bierne et al., 2011). The Spanish hybrid zone of S. haemastoma is therefore at an unusual place.…”