Are assortative mating and genital divergence driven by reinforcement?

Abstract

The evolution of assortative mating is a key part of the speciation process. Stronger assortment, or greater divergence in mating traits, between species pairs with overlapping ranges is commonly observed, but possible causes of this pattern of reproductive character displacement are difficult to distinguish. We use a multidisciplinary approach to provide a rare example where it is possible to distinguish among hypotheses concerning the evolution of reproductive character displacement. We build on an earlier comparative analysis that illustrated a strong pattern of greater divergence in penis form between pairs of sister species with overlapping ranges than between allopatric sister‐species pairs, in a large clade of marine gastropods (Littorinidae). We investigate both assortative mating and divergence in male genitalia in one of the sister‐species pairs, discriminating among three contrasting processes each of which can generate a pattern of reproductive character displacement: reinforcement, reproductive interference and the Templeton effect. We demonstrate reproductive character displacement in assortative mating, but not in genital form between this pair of sister species and use demographic models to distinguish among the different processes. Our results support a model with no gene flow since secondary contact and thus favor reproductive interference as the cause of reproductive character displacement for mate choice, rather than reinforcement. High gene flow within species argues against the Templeton effect. Secondary contact appears to have had little impact on genital divergence.

Hybridization patterns between two marine snails, Littorina fabalis and L. obtusata

“…A comparative analysis across Littorininae revealed greater male genital shape divergence between sympatric/parapatric sister species when compared with allopatric pairs (Hollander, Smadja, Butlin, & Reid, 2013), with flat periwinkles standing out as a strong candidate for prezygotic isolation to have evolved as a consequence of hybridization. However, similar patterns could have resulted from reproductive interference to reduce direct costs associated with interspecific mating after reproductive isolation was complete (Hollander et al, 2018). Thus, the comparisons between populations with different levels of hybridization is a prerequisite for further tests of reinforcement or other processes leading to completion of reproductive isolation in this system.…”

The evolution of female genitalia

“…This finding suggests a widespread pattern of lock‐and‐key genital evolution across the Littorininae. Interestingly, a recent study (Hollander et al., ) on one of the sister‐pair species ( Littoraria cingulata and L. filosa ) included in the same comparative analysis found contradictory results in that there was no evidence for RCD in penial form. Unfortunately, these data are limited insofar as the corresponding female genital trait, vaginal length, was not examined.…”

Speciation in marine environments: Diving under the surface

“…The comparison of hybridization rates between allopatric and sympatric species pairs offers a generally useful strategy to test for reinforcement in marine systems (e.g. Hollander et al., 2018). In this special issue, Tatarenkov et al.’s (2021) study of hermaphroditic Rivulus mangrove killifish that reproduce mainly by self‐fertilization revealed higher hybridization and introgression between sympatric than allopatric populations of divergent lineages, a pattern that is opposite to that predicted by reinforcement.…”

“…The comparison of hybridization rates between allopatric and sympatric species pairs offers a generally useful strategy to test for reinforcement in marine systems (e.g. Hollander et al, 2018). In this special issue, Tatarenkov et al's (2021)…”