We investigate how ecology and sexual selection interact to shape the speciation process using threespine stickleback species pairs (Gasterosteus spp.). We examine both how reproductive isolation can evolve in the forward direction and how it can break down through reverse speciation. We first focus on one reproductive barrier, sexual isolation, which reduces gene flow between species through differences in mate preferences and mating signals and is likely important for species formation and maintenance. We provide the first evidence that sexual isolation has been lost in a species pair that has recently collapsed into a hybrid swarm. Furthermore, we show that preferences females have for conspecific mates and the traits they use to distinguish conspecific and heterospecific males contribute to this loss. This work highlights the fragility of reproductive isolation between young species pairs and considers the role of sexual isolation in speciation. Second, we explore how sexual selection and ecological differences can contribute to speciation via male competition. We find that selection via male competition in one habitat would promote trait divergence and reproductive isolation, while in another habitat, selection would hinder divergence. Other behavioral mechanisms in male competition that might promote divergence, such as avoiding aggression with heterospecifics, are insufficient to maintain separate species. This work emphasizes the importance of mating habitats in male competition for both sexual selection and speciation. Third, we explore how environmental differences might mediate the expression, and current maintenance, of sexual isolation. Surprisingly, we find that the expression of female discrimination was fairly insensitive to habitat, despite the significance of habitat differences for sexual isolation to evolve. Female sensitivity to habitat was only shown by the ecotype being subsumed by hybridization, suggesting this plasticity may have contributed to reverse speciation. Also, habitat sensitivity in the expression of male courtship would further erode sexual isolation. Thus, environmental differences may play very different roles in the evolution versus maintenance of sexual isolation and the forward versus reverse process of speciation. Lastly, we ask how patterns of reproductive isolation in stickleback species pairs that represent early to late stages of the speciation process reveal how isolation might evolve both in the forward and reverse directions. The types of barriers that contribute most to isolation differ along the speciation continuum, thus the primary barriers that initiate speciation differ from those that complete it. Premating isolation, especially habitat and sexual isolation, likely plays an especially important role in initiating speciation. The loss of sexual isolation in reverse speciation and absence in halted movement along the speciation continuum highlights its potential importance for general movement or lack thereof along the speciation continuum. Intrinsic postmating isolation is likely necessary to complete and maintain speciation. Asymmetrical barriers may reveal selection that acts differently on each taxon and could predict the likelihood of forward, halted, or reverse movement along the continuum as well as the direction of introgression if reversal does occur. This study, and others that look at most or all potential reproductive barriers in systems that span the speciation continuum, can generate important insights into how new species evolve, what maintains them, and when and how they might collapse.
Read
