A dynamical theory of speciation on holey adaptive landscapes

Abstract

The metaphor of holey adaptive landscapes provides a pictorial representation of the process of speciation as a consequence of genetic divergence. In this metaphor, biological populations diverge along connected clusters of well-fit genotypes in a multidimensional adaptive landscape and become reproductively isolated species when they come to be on opposite sides of a ``hole'' in the adaptive landscape. No crossing of any adaptive valleys is required. I formulate and study a series of simple models describing the dynamics of speciation on holey adaptive landscapes driven by mutation and random genetic drift. Unlike most previous models that concentrate only on some stages of speciation, the models studied here describe the complete process of speciation from initiation until completion. The evolutionary factors included are selection (reproductive isolation), random genetic drift, mutation, recombination, and migration. In these models, pre- and post-mating reproductive isolation is a consequence of cumulative genetic change. I study possibilities for speciation according to allopatric, parapatric, peripatric and vicariance scenarios. The analytic theory satisfactorily matches results of individual-based simulations reported by Gavrilets et al. (1998). It is demonstrated that rapid speciation including simultaneous emergence of several new species is a plausible outcome of the evolutionary dynamics of subdivided populations. I consider effects of population size, population subdivision, and local adaptation on the dynamics of speciation. I briefly discuss some implications of the dynamics on holey adaptive landscapes for molecular evolution.