Chemical communication for reproduction in the Tasmanian short-beaked echidna, Tachyglossus aculeatus setosus

Communication plays a key role in coordinating all social interactions in an individual's life, but is particularly crucial for coordinating reproduction. Although chemical (olfactory) signals are ubiquitous in sexual communication in mammals, a disproportionate reliance on laboratory-based studies using a limited range of species, along with several logistical and methodological limitations, limit our broader understanding of their functions in reproduction and as sexually selected traits. I addressed these shortcomings by using an integrated, multidisciplinary approach, combining organic chemical analyses, physiology, genetics and behaviour, to investigate chemical signals, reproduction and sexual selection in a terrestrial, egg-laying mammal (monotreme), the short-beaked echidna (Tachyglossus aculeatus). Although the monotreme and therian lines have been evolutionarily separate for over 150 million years, echidna scent gland secretions from the spur and cloaca showed a typical mammalian pattern in terms of high chemical diversity and complexity. I identified a large number of compounds of varying volatility, molecular weight, functional groups and aromaticity, suggesting a high reliance on olfactory communication. Similarities with other vertebrates can indicate evolutionary convergence on optimal chemicals as signals, although several obscure and even novel compounds were also identified. Consistent with other seasonal breeders, echidna chemical profiles varied between sexes and during the mating season. Profiles also differed between individuals, suggesting they could contain genetic information, although microsatellite markers were inadequate to confirm this hypothesis. Changes in male spur secretions during the mating season coincided with maximum annual plasma testosterone concentrations and could be sexually selected, functioning in mate choice or intra-sexual competition. Males were attracted to female scent, confirming male response to sex-specific scent differences is an important driver of echidna mating behaviour. Consequently, chemical sensory traits that influence the ability to locate mates seem to be favoured by natural and sexual selection.Behavioural responses to chemical signals can be complicated by sexual conflict, although this has rarely been investigated in mammals. Male echidnas locate and mate with hibernating females; however females showed no changes in chemical profiles during hibernation. These results suggest that females do not 'actively' signal to males while hibernating, but intense male-male competition for access to females has probably driven earlier male readiness to breed, even before females might otherwise emerge from hibernation and signal to males. In females, chemical cues and reproductive physiology were not closely linked, as females showed continued mating activity during pregnancy and no detectable changes in chemical profiles at the time of fertilization or during pregnancy. Therefore, female reproductive status appears undisclosed to males, and multi-male mating may function to confuse paternity and reduce infanticide risk. These results suggest chemical signals are used differently by males and females to increase their reproductive success, often at the expense of the other sex, resulting in an evolutionary 'arms race' between signalers and receivers. Overall, a complex interplay between chemical signals, behaviour, environmental and selective pressures is responsible for the mating behaviour observed in Tasmanian echidnas. My work highlights the benefit of using a comprehensive, multidisciplinary approach based on a free-living, 'non-model' mammalian species, representing a significant step towatrds understanding the influences of selective pressures, including selection and conflict, on animal communication.