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.

Keywords: Littorinidae, reproductive interference, assortative mating; gene‐flow; genitalia; reinforcement; reproductive character displacement; speciation.

Figure 1

(A) Map of the sampling sites from the north and west coasts of Australia. Coloured regions describe the snail species distribution areas. Colours correspond with Fig. 2. Arrows designate combinations between pairs of populations for which mating trials where conducted, while the bar plot shows the mating trials outcomes in terms of mounting duration (minutes). Error bars represent SE. (B) Camera lucida drawings of the penes of L. filosa and L. cingulata, showing the elongated filament of the penis together with the penial glandular disc attached to the wrinkled base (after Reid 1986).

Figure 2

The top left panel gives Nei's estimator of pairwise F_ST values; locality names in red and blue represent allopatric populations of L. cingulata and L. filosa, respectively; those in green represent sympatric populations of both species. The following panels show principal component scores from the first three axes of an analysis based on 1878 loci in 113 individuals. Circles (allopatric) and triangles (sympatric). Each point represents a single individual.