Jointly representing long-range genetic similarity and spatially heterogeneous isolation-by-distance

Abstract Isolation-by-distance patterns in genetic variation are a widespread feature of the geo-graphic structure of genetic variation in many species, and many methods have been developed to illuminate such patterns in genetic data. However, long-range genetic similarities also exist, often as a result of rare or episodic long-range gene flow. Jointly characterizing patterns of isolation-by-distance and long-range genetic similarity in genetic data is an open data analysis challenge that, if resolved, could help produce more complete representations of the geographic structure of genetic data in any given species. Here, we present a computationally tractable method that identifies long-range genetic similarities in a background of spatially heterogeneous isolation-by-distance variation. The method uses a coalescent-based framework, and models long-range genetic similarity in terms of directional events with source fractions describing the fraction of ancestry at a location tracing back to a remote source. The method produces geographic maps annotated with inferred long-range edges, as well as maps of uncertainty in the geographic location of each source of long-range gene flow. We have implemented the method in a package called FEEMSmix (an extension to FEEMS from Marcus et al., 2021), and validated its implementation using simulations representative of typical data applications. We also apply this method to two empirical data sets. In a data set of over 4,000 humans (Homo sapiens) across Afro-Eurasia, we recover many known signals of long-distance dispersal from recent centuries. Similarly, in a data set of over 100 gray wolves (Canis lupus) across North America, we identify several previously unknown long-range connections, some of which were attributable to recording errors in sampling locations. Therefore, beyond identifying genuine long-range dispersals, our approach also serves as a useful tool for quality control in spatial genetic studies. Author Summary The movement of individuals across landscapes shapes genetic diversity and has significant implications for both evolutionary studies and conservation efforts. Advances in sequencing now allow researchers to analyze thousands of samples from broad geographic areas, helping to estimate local gene flow. However, long-range genetic flow can occur due to a host of reasons (e.g. natural weather patterns, migration for resources, etc.), and existing methods struggle to represent these patterns. In this study, we developed a method to identify and model these long-range genetic similarities as dispersals from a source to a destination over a landscape. In applying this method to over 4,000 human samples from Afro-Eurasia, we detected signatures of known long-distance dispersals from recent centuries. In applying this method to 100 gray wolf samples from North America, we found many unexpected long-range genetic connections, some of which turned out to be recording errors in sample locations. Thus, beyond detecting real long-range dispersal, our approach also serves as a useful tool for quality control in spatial genetic studies. Competing Interest Statement The authors have declared no competing interest. Footnotes The manuscript files have been updated to provide the supplemental information text.