A Spatial Framework for Understanding Population Structure and Admixture

Geographic patterns of genetic variation within modern populations, produced by complex histories of migration, can be difficult to infer and visually summarize. A general consequence of geographically limited dispersal is that samples from nearby locations tend to be more closely related than samples from distant locations, and so genetic covariance often recapitulates geographic proximity. We use genome-wide polymorphism data to build “geogenetic maps,” which, when applied to stationary populations, produces a map of the geographic positions of the populations, but with distances distorted to reflect historical rates of gene flow. In the underlying model, allele frequency covariance is a decreasing function of geogenetic distance, and nonlocal gene flow such as admixture can be identified as anomalously strong covariance over long distances. This admixture is explicitly co-estimated and depicted as arrows, from the source of admixture to the recipient, on the geogenetic map. We demonstrate the utility of this method on a circum-Tibetan sampling of the greenish warbler (Phylloscopus trochiloides), in which we find evidence for gene flow between the adjacent, terminal populations of the ring species. We also analyze a global sampling of human populations, for which we largely recover the geography of the sampling, with support for significant histories of admixture in many samples. This new tool for understanding and visualizing patterns of population structure is implemented in a Bayesian framework in the program SpaceMix.Author Summary: In this paper, we introduce a statistical method for inferring, for a set of sequenced samples, a map in which the distances between population locations reflect genetic, rather than geographic, proximity. Two populations that are sampled at distant locations but that are genetically similar (perhaps one was recently founded by a colonization event from the other) may have inferred locations that are nearby, while two populations that are sampled close together, but that are genetically dissimilar (e.g., are separated by a barrier), may have inferred locations that are farther apart. The result is a “geogenetic” map in which the distances between populations are effective distances, indicative of the way that populations perceive the distances between themselves: the “organism’s-eye view” of the world. Added to this, “admixture” can be thought of as the outcome of unusually long-distance gene flow; it results in relatedness between populations that is anomalously high given the distance that separates them. We depict the effect of admixture using arrows, from a source of admixture to its target, on the inferred map. The inferred geogenetic map is an intuitive and information-rich visual summary of patterns of population structure.