Evolution of choosiness dictates whether search costs of mate choice enhance speciation by sexual selection

Abstract

The role of sexual selection in speciation is implicated in both empirical case studies and larger comparative works. However, sexual selection faces two major problems in driving speciation. First, because females with novel preferences search for their initially rare males, search costs are expected to curtail initial sexual divergence. Second, if these populations come back into sympatry, sexual divergence may be erased due to hybridization. A major goal is to understand which conditions increase the likelihood of overcoming these problems. Here we generated a diploid population genetic model of how female search costs and evolution of female 'choosiness' (i.e. preference strength) interact to drive speciation in allopatry and secondary contact. We studied the model using numerical simulations in the context of two different male traits, ecologically 'arbitrary' versus 'magic' traits. First, in allopatry, without female search costs only minor and fluctuating sexual isolation evolved. In contrast, with female search costs, sexual isolation was highly curtailed with arbitrary male traits but was greatly facilitated with magic traits. However, because search costs selected for reduced choosiness, sexual isolation with magic traits was eventually eroded, the rate determined by the genetic architecture of choosiness. These factors also played a key role in secondary contact; with evolvable choosiness and female search costs, pure sexual selection models collapsed upon secondary contact. However, when we added selection against hybrids (i.e. reinforcement) to this model, we found that speciation could be maintained under a wide range of conditions with arbitrary male traits, but not with magic male traits. This surprisingly suggests that arbitrary male traits are in some cases more likely to aid speciation than magic male traits. We discuss these findings and relate them to empirical literature on female choosiness within species and in hybrids.