Parasitic behavioural manipulation reflected as an extended epigenotype in a naturalistic population

Abstract

Historically, the behavioural manipulation hypothesis is relentlessly challenged by inconsistent phenotypic profiles trying to coalesce molecules to behaviours in the laboratory. Yet, exploring the phenomena in naturalistic settings exposes the study to myriad confounders and stochasticity, making empirical evidence difficult to obtain. Herein, these challenges are addressed from a serendipitous intervention at Kangaroo Island accompanied by a longitudinal study design, allowing the dissection of the behavioural phenomenon, ‘fatal attraction’, observed in rodents infected with Toxoplasma gondii. Comparable to laboratory findings, parasitic infection in wild mice coincides with significant epigenetic changes within the paraventricular nucleus of the hypothalamus and the posterodorsal medial amygdala. The latter of which, is previously demonstrated to sufficiently reproduce the loss of aversion towards predators in laboratory rodents. We posit that Toxoplasma gondii remarkably alters the epigenotype of mice in the natural wild environment, with the extension of this epigenotype steering the loss of aversion towards predatory felids, augmenting parasitic transmission. We further explore the implications of infection on other facets of mice physiology derived from Kangaroo Island and deduce plausible connotations. The ‘extended epigenotype’ may provide a much-needed contemporary perspective on future parasite-host associations and broad, inter-intraspecies relationships.