The loss of nuptial gifts in sclerosomatid Opiliones coincides with an increase in sexual conflict-like behaviour

Description

Nuptial gifts serve to increase donor fitness through a variety of mechanisms, including securing additional copulations, increasing sperm transfer or storage, or increasing paternity share. Coercive mating behaviour can provide similar male benefits, potentially allowing for evolutionary transitions between solicitous and coercive strategies, wherein male behavioural antagonism 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 is elevated in nonsacculate harvesters by comparing 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.

Steps to reproduce

Leiobunum vittatum were collected in June and July 2021 at Rockburn Branch Park (39.219471, -76.761198) and UMBC (39.247397, -76.710568); L. aldrichi in June and July 2021 at Sugarloaf Mountain (39.261630, -77.395560) and Plummer’s Island (39.261630, -77.395560); L. euserratipalpe in April and May 2022 at Schooley Mill Park (39.166325, -76.961830); and L. bracchiolum in May and June 2021 and 2023 at Rockburn Branch Park. Trials consisted of pairing male and female conspecifics and recording mating behavior. We conducted trials in a 29.21cm x 29.21cm acrylic arena lined with white cardstock to reduce reflections. The arena was housed in a 24º C room illuminated with white light and we video recorded interactions dorsally and laterally with Microsoft LifeCam Studio cameras. We sterilized the arena with 95% ethanol before placing a male and female harvester in the arena. Harvesters were isolated for 5 minutes under transparent plastic containers to allow acclimation to the arena without contact with one another. Following this, we removed the containers and the trial began. Trials lasted for 20-minutes or until the mating interaction ended. Interactions were considered concluded when contact was broken between individuals and the male made no attempt to chase the female. If the interaction had not ended by the 60-minute mark, the trial was concluded. We used the automated tracking program TRex to score videos. To eliminate minor errors inherent to automated tracking, we averaged the per-frame centroid coordinates over 30-frame sections to create per-second coordinates. From these, we calculated the distance between individuals, time individuals were within one male leg span (using the longest leg specific to the male in each trial), and clasping time. We also used the centroid coordinates to calculate male and female trajectory vectors and magnitudes before using these to derive the angle between vectors. This describes the “pursuit angle” between males and females; values closer to 0 degrees indicate the individuals were moving in the same direction while values closer to 180 degrees indicate the individuals were moving in opposite directions. We additionally scored all trials with JWatcher. For attempted clasp trials, we scored the time the harvesters were in contact and the latency between first contact and first clasp attempt. For successful clasp trials, we additionally scored the time between first mating attempt and first successful clasp, the time the individuals were in contact, the time the male clasped the female, and the time the male guarded the female (post-copulatory contact lasting greater than 5 seconds). In attempted clasp trials, we used FIJI-ImageJ to measure the maximum angle the female’s genital operculum formed with the substrate. Due to mating pair movement during their interactions, we could not accurately obtain a continuous measure of the angle, thus we used the maximum angle reached during a clasp attempt.

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