The Evolution of Orthopteran Mating Systems and the Reproductive Ecology of New Zealand Cave Wētā

Abstract

Sexual selection has long been recognised as driving the evolution of diverse morphological and behavioural traits in animals. Decades of concerted research into the topic has uncovered reproductive adaptations ranging from the beautiful to the horrific, and insects provide some of the most striking examples from all parts of that spectrum. The diversity of insects, their mating systems, and their reproductive adaptations has made them crucial to our understanding of sexual selection and the evolution of sexual reproduction itself. Their natural amenability to observation and experimentation has granted us many useful and informative model systems for that endeavour. In particular, the Orthoptera (crickets, grasshoppers, katydids, wētā and their allies) have provided many model species for the study of acoustic mate calling, nuptial provisioning, intrasexual combat, the economics of reproduction that contribute to sexual conflict, and countless other topics in the realm of reproductive ecology. The current research delves into the diversity of mating system traits exhibited by the order, with a comprehensive review of the literature, as well as targeted evolutionary hypothesis testing via the phylogenetic comparative method. I then investigate in detail the reproductive ecology of New Zealand cave wētā, which are fascinating representatives of a globally distributed but hardly-studied orthopteran family, the Rhaphidophoridae. Firstly I investigate orthopteran reproductive ecology with analyses of sexual evolution across the order. I test for phylogenetic signal, ancestral character states and correlated evolution with data derived from a comprehensive literature search, using a synthetic supertree assembled for that purpose by tree grafting. The results of this approach indicated trends of strong evolutionary conservatism in orthopteran sexual traits, and a probable ancestral mating system that involved protandry, male-male combat and mate-guarding, acoustic mate-calling, and female-biased sexual size dimorphism, but without coercive mating or exaggerated weaponry. Although I was able to model the evolution of these traits, phylogenetic comparisons did not provide evidence in support of correlated evolution between them. I then move from broad questions to detailed examination of sexually dimorphic antennal structures in New Zealand cave wētā (Rhaphidophoridae: Pachyrhamma sp). Using scanning electron microscopy, I describe the morphology of microsensory hairs (sensilla) in P. waitomoensis and P. acanthocera and test for sexual dimorphism in the length, as well as presence and absence of these. This reveals numerous sensilla with unique morphology that may be particular to the group, and suggests possible sensory functions based on their individual characteristics. In addition, I provide the first detailed examination of intriguing, horn-like antennal cuticular structures that are restricted to males of these species. The two kinds of protrusive structure have some qualities that suggest a secretory function, indicating that male pheromonal communication may be an important aspect of those species' ecology. Subsequently, I investigate New Zealand cave wētā behavioural ecology with field-based approaches to observing P. waitomoensis. I examine the role of sexually dimorphic, elongated hind-legs in that species in the context of mate guarding, a central topic in the study of sexual selection. Interestingly, although males doggedly guard their mates with their exaggerated hind-legs, the limbs do not appear to function in warding off rivals. Because of that observation, I tested the novel hypothesis that the mate guarding behaviour and morphology of male P. waitomoensis instead serves to reduce disturbance to females by organisms other than sexual rivals of the male. Through several simple experiments with the wētā in their natural environment, I show a reduction in pair duration when females are disturbed, a disturbance-protection effect of male presence, a mating advantage to males that can guard their mates for longer, and a negative correlation between male hind-leg length and the likelihood of disturbance to the female. Taken together, these results provide an example of a mate guarding role in exaggerated trait evolution, and a novel function of mate guarding that may occur in other taxa. In addition, this highlights the importance of considering environmental context when examining behaviour, as well as raising the possibility that more potential female benefits of mate guarding may be observed if study organisms are observed in nature. After examining mate guarding, I continue the investigation of exaggerated trait evolution in P. waitomoensis by looking at the additional role of their elongated hind-legs in male-male-combat and competitive assessment. By comparing morphometric data with video recordings of intrasexual contest behaviour in the field, I showed that males with longer legs have greater chances of victory in combat. In addition, when the difference in leg-length between contestants was greater, fights escalated to a lesser degree. The observed relationship between contestant leg-length and contest escalation matched the predictions of the selfonly model of assessment, according to current contest theory. The results highlight the fact that fighting and weaponry are an important part of cave wētā reproductive ecology, and indicate that other Rhaphidophoridae with similar morphology may represent an overlooked trove of examples for exaggerated weaponry research in the Orthoptera. Lastly I approach the question of exaggerated weapon evolution from a different angle. Using software designed for entertainment war-gaming, I edited matches in order to pitch artificial intelligence contestants against one another under varied experimental conditions. By doing so, I was able to test the hypothesis that one-on-one duel scenarios favour arms superiority, a potential explanatory factor in the presence of extreme weaponry among various taxa, and in the occurrence of arms races in non-animal systems. I found that strong contestants enjoyed a greater advantage when fighting head-to-head, in contrast to the lack of any advantage in more chaotic skirmishes with multiple opponents. The advantage of superior weaponry showed the same pattern, in two different forms of contest. This suggests that conflict scenarios that are restricted to duels may contribute to weaponry escalation, in diverse systems. I thereby demonstrate a novel technique for approaching a difficult-to-test, broad evolutionary question, and show the potential for widely available and user-friendly consumer software to provide simulators for approaching scientific questions. Overall, this thesis summarises sexual selection research in the Orthoptera offers a hypotheses regarding ancestral mating systems in the order, provides new data on a poorly studied family, and tests a general hypothesis in a novel way. As well as reviewing and analysing existing knowledge and providing new discoveries in an overlooked group, this research opens and highlights novel avenues for investigation of orthopteran reproductive ecology, the examination of sexual selection, and the evolution of extreme weaponry.