Ecological and Mutation-Order Speciation in Senecio.

Abstract

Natural selection shapes how new species arise, yet the mechanisms that generate reproductive barriers remain actively debated. Although ecological divergence in contrasting environments and mutation-order processes in similar environments are often viewed as distinct speciation mechanisms, we show they can occur simultaneously and act as part of a continuum of selective pressures. In the Senecio lautus species complex, Dune and Headland ecotypes have evolved repeatedly along the Australian coastline. Through crossing experiments and field studies, we find that divergent natural selection promotes strong reproductive isolation between the Dune and Headland ecotypes. While uniform selection maintains reproductive compatibility among ecologically similar Dune populations, geographically distant Headland populations have evolved reproductive barriers despite their convergent prostrate phenotypes, likely driven by adaptation to subtle environmental differences between each Headland location. To understand how this habitat heterogeneity contributes to patterns of reproductive isolation, we extend previous theoretical work on the accumulation of hybrid incompatibilities to account for environmental gradients and polygenic adaptation. We show that the probability of reproductive isolation depends on three factors: how similar the environments are, how complex the genetic architecture is and how selection coefficients are distributed among beneficial mutations. These theoretical findings explain how reproductive isolation arises in systems like Senecio, where multiple forms of selection jointly drive speciation.