A simple biophysical model predicts more rapid accumulation of hybrid incompatibilities in small populations

TL;DR

This study presents a biophysical model showing that smaller populations tend to develop reproductive incompatibilities faster due to greater initial drift load and specific divergence dynamics, providing insights into speciation processes.

Contribution

The paper introduces a biophysical model of speciation that predicts rapid incompatibility accumulation in small populations without relying on peak-shifts or positive selection.

Findings

Smaller populations develop incompatibilities more quickly.

Longer sequences lead to faster incompatibility in small populations.

In larger populations, divergence and incompatibility development slow down.

Abstract

Speciation is fundamental to the huge diversity of life on Earth. Evidence suggests reproductive isolation arises most commonly in allopatry with a higher speciation rate in small populations. Current theory does not address this dependence in the important weak mutation regime. Here, we examine a biophysical model of speciation based on the binding of a protein transcription factor to a DNA binding site, and how their independent co-evolution, in a stabilizing landscape, of two allopatric lineages leads to incompatibilities. Our results give a new prediction for the monomorphic regime of evolution, consistent with data, that smaller populations should develop incompatibilities more quickly. This arises as: 1) smaller populations having a greater initial drift load, as there are more sequences that bind poorly than well, so fewer substitutions are needed to reach incompatible regions of phenotype space; 2) slower divergence when the population size is larger than the inverse of discrete differences in fitness. Further, we find longer sequences develop incompatibilities more quickly at small population sizes, but more slowly at large population sizes. The biophysical model thus represents a robust mechanism of rapid reproductive isolation for small populations and large sequences, that does not require peak-shifts or positive selection.