Biases in demographic modeling affect our understanding of recent divergence

Abstract

Testing among competing demographic models of divergence has become an important component of evolutionary research in model and non-model organisms. However, the effect of unaccounted demographic events on model choice and parameter estimation remains largely unexplored. Using extensive simulations, we demonstrate that under realistic divergence scenarios, failure to account for population size (Ne) changes in daughter and ancestral populations leads to strong biases in divergence time estimates as well as model choice. We illustrate these issues reconstructing the recent demographic history of North Sea and Baltic Sea turbots (Scophthalmus maximus) by testing 16 isolation with migration (IM) and 16 secondary contact (SC) scenarios, modeling changes in Ne as well as the effects of linked selection and barrier loci. Failure to account for changes in Ne resulted in selecting SC models with long periods of strict isolation and divergence times preceding the formation of the Baltic Sea. In contrast, models accounting for Ne changes suggest recent (<6 kya) divergence with constant gene flow. We further show how interpreting genomic landscapes of differentiation can help discerning among competing models. For example, in the turbot data, islands of differentiation show signatures of recent selective sweeps, rather than old divergence resisting secondary introgression. The results have broad implications for the study of population divergence by highlighting the potential effects of unmodeled changes in Ne on demographic inference. Tested models should aim at representing realistic divergence scenarios for the target taxa, and extreme caution should always be exercised when interpreting results of demographic modeling.