Genealogies of rapidly adapting populations

TL;DR

This paper develops a new framework to understand the genealogical structures of rapidly adapting populations, revealing distinctive genetic signatures like multiple mergers and non-monotonic frequency spectra, which differ from neutral models.

Contribution

It introduces a novel genealogical model for continuous adaptation in asexual populations, highlighting the prevalence of multiple mergers and their genetic footprints.

Findings

Genealogies show small pools of highly fit ancestors with multiple mergers.

Site frequency spectrum peaks at high frequencies in adapting populations.

Tajima's D becomes increasingly negative with larger samples.

Abstract

The genetic diversity of a species is shaped by its recent evolutionary history and can be used to infer demographic events or selective sweeps. Most inference methods are based on the null hypothesis that natural selection is a weak or infrequent evolutionary force. However, many species, particularly pathogens, are under continuous pressure to adapt in response to changing environments. A statistical framework for inference from diversity data of such populations is currently lacking. Toward this goal, we explore the properties of genealogies in a model of continual adaptation in asexual populations. We show that lineages trace back to a small pool of highly fit ancestors, in which almost simultaneous coalescence of more than two lineages frequently occurs. While such multiple mergers are unlikely under the neutral coalescent, they create a unique genetic footprint in adapting populations. The site frequency spectrum of derived neutral alleles, for example, is non-monotonic and has a peak at high frequencies, whereas Tajima's D becomes more and more negative with increasing sample size. Since multiple merger coalescents emerge in many models of rapid adaptation, we argue that they should be considered as a null-model for adapting populations.