Résumé
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.