A Dynamical Theory of Speciation on Holey Adaptive Landscapes.

A holey adaptive landscape is an adaptive landscape where relatively infrequent well-fit combinations of genes form a contiguous set that expands throughout the genotype space. 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 postmating reproductive isolation is a consequence of cumulative genetic change. I study possibilities for speciation according to allopatric, parapatric, peripatric, and vicariance scenarios. The results presented here, together with earlier numerical simulations, strongly suggest that rapid speciation, including simultaneous emergence of several new species, is a plausible outcome of the evolutionary dynamics of subdivided populations. Rapid speciation is most likely for populations that are subdivided into a large number of small subpopulations. Speciation is possible even when subpopulations exchange several individuals per generation. Selection for local adaptation is not necessary for rapid speciation. I briefly discuss implications of the dynamics on holey adaptive landscapes for the nearly neutral theory of molecular evolution and for the theory of evolution of genetic canalization.