The loss of nuptial gifts in sclerosomatid Opiliones coincides with increased behavioural sexual conflict

Abstract

Nuptial gifts serve to increase donor fitness through a variety of pathways. Some nuptial gifts deliver benefits similar to those of antagonistic male behaviours: functioning to secure additional copulations, increase sperm transfer or storage, or increase paternity share. These commonalities may result in evolutionary transitions between solicitous and coercive strategies, wherein behavioural sexual conflict could function to secure mates in lieu of nuptial gifts. In temperate leiobunine harvesters (Arachnida: Opiliones), nuptial gifts have been repeatedly lost, resulting in two primary mating syndromes: an ancestral, sacculate state in which males endogenously produce high-investment nuptial gifts and females lack pregenital barriers, and a derived, nonsacculate state in which females have pregenital barriers and males produce significantly reduced, low-investment nuptial gifts. In this study, we investigated whether behavioural sexual conflict compensates for reduced nuptial gifts in nonsacculate harvesters by comparing the intensity of pre-, peri-, and postcopulatory mating behaviour between the nonsacculate species Leiobunum vittatum and L. euserratipalpe and the sacculate species L. aldrichi and L. bracchiolum. We additionally sought to establish an automated behavioural analysis pipeline by developing analogues for metrics traditionally scored manually. Our results revealed significantly different, potentially coercive, behaviour in nonsacculate species, indicating that the loss and reduction of pre- and pericopulatory nuptial gifts may contribute to increased behavioural antagonism. Mating behaviour also differed significantly between L. vittatum and L. euserratipalpe, indicating there are multiple suites of potentially antagonistic behaviours. Together, these results suggest that multiple behavioural strategies may be effective substitutes for nuptial gifts in leiobunine Opiliones, although the mechanisms through which male fitness is increased requires further research. HighlightsO_LITemperate Opiliones have repeatedly evolved reduced nuptial gift investment C_LIO_LIReduced-gift (nonsacculate) species possess morphology indicative of antagonism C_LIO_LIWe tested if mating behaviour differed between nonsacculate and sacculate species C_LIO_LINonsacculates displayed significantly higher behavioural antagonism than sacculates C_LIO_LINonsacculate species differed in their suites of antagonistic behaviours C_LI