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

Area of Science:

• Evolutionary genetics
• Population genetics
• Genomics

Background:

• Genome scans often reveal high genetic differentiation between populations, frequently associated with environmental contrasts (genetic-environment associations or GEAs).
• GEAs are typically interpreted as evidence for local adaptation, suggesting that differentiated markers are under divergent ecological selection or linked to such loci.

Purpose of the Study:

• To propose and explore an alternative explanation for increased genetic differentiation and GEAs: intrinsic genetic incompatibilities.
• To investigate how endogenous barriers (tension zones) can couple with exogenous environmental barriers.

Main Methods:

• Theoretical modeling of genetic incompatibilities and their interaction with ecological selection in subdivided populations.
• Analysis of linkage disequilibria between endogenous incompatibilities, local adaptation genes, and neutral loci under varying environmental heterogeneity.
• Review of existing literature to identify supporting evidence for the proposed model.

Main Results:

• Intrinsic genetic incompatibilities can drive population differentiation and create GEAs, even with weak ecological selection.
• Coupling of endogenous and exogenous barriers can occur easily, especially in spatially subdivided populations, irrespective of locus linkage.
• GEAs can emerge locally at incompatibility loci in fine-grained environments due to intermingled habitats and gene pools.

Conclusions:

• Endogenous genetic barriers, rather than local adaptation, are a more likely explanation for many Fst-outlying loci identified in genome scans.
• The observed spatial patterns of genetic differentiation and GEAs can be explained by the interaction of intrinsic incompatibilities and environmental factors.
• This framework provides a novel perspective on the evolutionary forces shaping genetic structure in natural populations.