Local adaptation along smooth ecological gradients causes phylogeographic breaks and phenotypic clustering

Abstract

Coalescent theory has provided a basis for evolutionary biologists to build sophisticated methods for inferring population history from variation in genetic markers, but these methods leave out a major conceptual cornerstone of modern evolutionary theory: natural selection. I provide the first quantitative analysis of the effects of selection on genealogical patterns in a continuously distributed population in which the selective optimum for a trait linked to the marker varies gradually and continuously across the landscape. Simulations show that relatively weak selection for local adaptation can lead to strong phylogeographic structure, in which highly divergent genealogical groups (i.e., clades) are geographically localized and differentially adapted, and dramatically increased standing variation (e.g., coalescence time) compared to neutral expectations. This pattern becomes more likely with increasing population size and with decreasing dispersal distances, mutation rates, and mutation sizes. Under some conditions, the system alternates between a nearly neutral behavior and a behavior in which highly divergent clades are locally adapted. Natural selection on markers commonly used in phylogeographic studies (such as mitochondrial DNA) presents a major challenge to the inference of biogeographic history but also provides exciting opportunities to study how selection affects both between- and within-species biodiversity.