Year

2020

Degree Name

Doctor of Philosophy

Department

School of Earth, Atmospheric and Life Sciences

Abstract

Female mate choice is a powerful evolutionary force that can drive the diversification of reproductive traits. Despite female mate choice being pervasive among sexually reproducing animals, we still have a limited understanding of the mechanisms that underpin mate choice. Generally, direct material benefits of mate choice are well supported whereby choosy females gain immediate fitness benefits through increased fertilisation/fecundity, superior parental care, provision of resources or by promoting offspring quality and survival. Alternatively, females stand to gain from indirect genetic benefits of mate choice, which are derived from the contribution of genes alone. Despite sexual selection being a research focus over the past four decades, the importance of indirect genetic benefits remains unclear and highly controversial, in part due to a lack of robust empirical testing required to draw firm conclusions. Major criticisms of past studies have centred on there being limited attempt to; i) consider population-wide variation in breeding behaviours throughout breeding seasons, ii) use genetic approaches to elucidate the mating success of individuals (and resolve the genetic mating system), and iii) simultaneously test competing indirect benefit hypotheses for mate choice. These limitations have inhibited our ability to discern the relative importance of indirect benefits and its prevalence among animals, impeding our understanding of sexual selection. As such, the general aim of this thesis was to employ a comprehensive, bottom-up approach to investigate the breeding biology and mating system of the red-backed toadlet (Pseudophryne coriacea), with a view towards unravelling patterns and benefits of female mate choice. My systematic approach aimed to; 1) gain fundamental insights into the species’ breeding ecology, 2) determine the species’ genetic mating system, 3) explore the potential for direct benefits of mate choice and 4) test competing hypotheses for indirect benefits of mate choice. Critically, this study focused on an entire population of P. coriacea, that spanned multiple reproductive events over a prolonged breeding season (115 days). In Chapter two, I used a multivariate approach to explore the social and climatic correlates of breeding, and to gain a general understanding of the species’ reproductive ecology. This work revealed that males respond strongly to climatic cues, while females were found to predominately use male calling activity (a social cue), in conjunction with climatic conditions, to inform breeding decisions. Accordingly, I developed an understanding of the specific environmental conditions that promote opportunities for mate choice in P. coriacea. In Chapter three, I quantified the genetic mating system of the population using single-nucleotide polymorphisms (SNPs) to assign parentage to offspring among all adults in the population. Females predominately mated with a single male, providing evidence for genetic monandry (one of only two cases in an amphibian), highlighting the potential for female mate choice. In support of this inference, mating success was skewed towards a subset of males, with only one third securing multiple females. Importantly, genetic analysis also revealed evidence for male nest-takeover, male sneaking, and the occurrence of hybridisation within the population. Considered together, chapters two and three demonstrated that there are strong opportunities for sexual selection in the system, and provided the foundations for teasing apart the specific mechanisms driving choice. Subsequently, my investigations in Chapter four focused on female preferences for nest-sites using a multivariate analysis which accounted for the inter-relationship between nest traits on male sexual display. Females were found to preferentially deposit eggs in nests with wetter, less acidic substrates, conditions that are known to improve embryonic survival (indicative of a direct reproductive benefit) in toadlets. The same nest characteristics also influenced the capacity of resident males to acoustically advertise and defend nests. Together, these findings highlight the importance of male defended resources (nests) to both male-male competition and female mate choice. Only at this point, with a thorough understanding of the model system, was it appropriate to test for indirect genetic benefit hypotheses, and place my findings in an ecological context. In Chapter five, I conducted a simultaneous test of two competing indirect benefit hypotheses for the evolution of mate choice. I found that females were significantly more related to their mates than expected under random mating during the main breeding event, drawing attention to the possibility that mate choice for genetic compatibility serves to reduce fitness costs associated with outbreeding. While this result provides the first population-wide evidence for non-random preferential inbreeding in a wild amphibian, there are multiple lines of inquiry which indicate that mate choice for genetic compatibility may be widespread among amphibians. This finding also calls into question the long-standing belief that mating with closely related mates should be avoided and promotes consideration that inbreeding might actually yield significant fitness benefits in certain animal groups. Overall, my findings indicate that females may benefit from mate choice both directly and indirectly, which provides evidence that multiple mechanisms may be simultaneously driving mate choice in this system. In conclusion, my research highlights the value of combining observational and genetic approaches to elucidate a species mating system, and comprehensively testing multiple, competing hypotheses for the evolution of mate choice. Moreover, it contributes to a rapidly growing body of evidence that female mate choice is highly complex.

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Unless otherwise indicated, the views expressed in this thesis are those of the author and do not necessarily represent the views of the University of Wollongong.