How species evolve collectively: implications of gene flow and selection for the spread of advantageous alleles

The traditional view that species are held together through gene flow has been challenged by observations that migration is too restricted among populations of many species to prevent local divergence. However, only very low levels of gene flow are necessary to permit the spread of highly advantageous alleles, providing an alternative means by which low-migration species might be held together. We re-evaluate these arguments given the recent and wide availability of indirect estimates of gene flow. Our literature review of F-ST values for a broad range of taxa suggests that gene flow in many taxa is considerably greater than suspected from earlier studies and often is sufficiently high to homogenize even neutral alleles. However, there are numerous species from essentially all organismal groups that lack sufficient gene flow to prevent divergence. Crude estimates on the strength of selection on phenotypic traits and effect sizes of quantitative trait loci (QTL) suggest that selection coefficients for leading QTL underlying phenotypic traits may be high enough to permit their rapid spread across populations. Thus, species may evolve collectively at major loci through the spread of favourable alleles, while simultaneously differentiating at other loci due to drift and local selection.