Accounting for Gene Flow from Unsampled `Ghost' Populations while Estimating Evolutionary History under the Isolation with Migration Model

Abstract

Unsampled or extinct ghost populations leave signatures on the genomes of individuals from extant, sampled populations, especially if they have exchanged genes with them over evolutionary time. This gene flow from ghost populations can introduce biases when estimating evolutionary history from genomic data, often leading to data misinterpretation and ambiguous results. Here we assess these biases while accounting, or not accounting for gene flow from ghost populations under the Isolation with Migration (IM) model. We perform extensive simulations under five scenarios with no gene flow (Scenario A), to extensive gene flow to- and from- an unsampled ghost population (Scenarios B, C, D, and E). Estimates of evolutionary history across all scenarios A-E (effective population sizes, divergence times, and migration rates) indicate consistent a) under-estimation of divergence times between sampled populations, (b) over-estimation of effective population sizes of sampled populations, and (c) under-estimation of migration rates between sampled populations, with increased gene flow from the unsampled ghost population. Without accounting for an unsampled ghost, summary statistics like FST are under-estimated, and{pi} is over-estimated with increased gene flow from the ghost. To show this persistent issue in empirical data, we use a 355 locus dataset from African Hunter-Gatherer populations and discuss similar biases in estimating evolutionary history while not accounting for unsampled ghosts. Considering the large effects of gene flow from these ghosts, we propose a multi-pronged approach to account for the presence of unsampled ghost populations in population genomics studies to reduce erroneous inferences.