Parasite-augmented mate choice and reduction in innate fear in rats infected byToxoplasma gondii

Abstract

SummaryTypically, female rats demonstrate clear mate choice. Mate preference is driven by the evolutionary need to choose males with heritable parasite resistance and to prevent the transmission of contagious diseases during mating. Thus, females detect and avoid parasitized males. Over evolutionary time scales, parasite-free males plausibly evolve to advertise their status. This arrangement between males and females is obviously detrimental to parasites, especially for sexually transmitted parasites. Yet Toxoplasma gondii, a sexually transmitted parasite, gets around this obstacle by manipulating mate choice of uninfected females. Males infected with this parasite become more attractive to uninfected females. The ability of T. gondii to not only advantageously alter the behavior and physiology of its host but also secondarily alter the behavior of uninfected females presents a striking example of the ʻextended phenotypeʼ of parasites. Toxoplasma gondii also abolishes the innate fear response of rats to cat odor; this likely increases parasite transmission through the trophic route. It is plausible that these two manipulations are not two distinct phenotypes, but are rather part of a single pattern built around testosterone-mediated interplay between mate choice, parasitism and predation.Key words: anti-predator behavior, behavioral manipulation, major urinary proteins, parasitism, sexual selection, sexual transmission, trophic transmission, testosterone. In many species, females provide greater parental care and investment than males. This leads to a biased operational sex ratio, manifested as more sexually receptive males than females. As a direct result of such bias, males compete between themselves for access to females and females have the opportunity to choose from many suitors. This leads to sexual selection, resulting in evolution of male traits that are useful in fighting competitor males (intrasexual selection) and influencing mate choice of females (intersexual selection) (Andersson, 1994; Andersson and Simmons, 2006). The intra-sexual selection often results in evolution of conspicuous male phenotypes that aim to advertise and attract females (e.g. bright plumage in birds).From the perspective of this review, mechanisms driving mate choice in rats are of special interest. Several mechanisms have been proposed to explain preference of females for certain male traits.It is possible that females choose males that provide a direct and immediate benefit to the female and/or their progeny (Møller and Jennions, 2001). Relevant examples include parental care or nuptial gifts (food or material tokens transferred by male during courtship or mating). Male rats provide neither parental care nor nuptial gifts. However, it is possible that female rats choose males in order to reduce the chances of direct associative transmission of parasites or diseases (Able, 1996). That will constitute a mate choice driven by direct benefit.It is also possible that mate choice is based on indirect benefits that hinge on the gre...

Host Manipulation by Parasites: Cases, Patterns, and Remaining Doubts

“…Virtually all infected animals show some kind of sickness behavior (Hart, 1988), which usually includes a general decrease in mobility and social activities. In addition, most animals discriminate against parasitized individuals as potential mating partners (Vyas, 2013;Adamo, 2014). Both behavioral changes are under the genetic control of the host and can reduce the transmission of horizontally transmitted parasites.…”

Toxoplasma gondiiinfection, from predation to schizophrenia: can animal behaviour help us understand human behaviour?

“…Members of the cat family (Felidae) are the only definitive hosts, within which the parasite undergoes full gametogenesis and mating within the intestinal epithelium, culminating in the generation of oocysts containing sporozoites that are shed in the cat's faeces (Hutchison et al, 1969). Infection of intermediate (such as rodents and birds) or other secondary (such as humans and domestic livestock) hosts can occur following ingestion of oocysts (via contaminated soil, water or food) or tissue cysts (through raw/undercooked infected meat, including via cannibalism), congenital transmission and also potentially, under certain conditions, by sexual transmission (Vyas, 2013). Within intermediate secondary hosts, the parasite undergoes asexual reproduction, characterized by rapidly dividing tachyzoites and the more slowly dividing bradyzoites.…”

302. Sleep Onset Insomnia, Daytime Sleepiness and Sleep Duration in Relationship to Toxoplasma gondii IgG Seropositivity and Serointensity

“…There are previous reports of an increased score of trait aggression in infected women compared to uninfected women, being also moderated by the phenylalanine:tyrosine ratio [78,80], and of a significantly lower score in self-control and higher vigilance in infected men vs. noninfected men [81]. Reproductive implications of T. gondii seropositivity have also been reported in rodents, with T. gondii-infected male rats being preferentially chosen as mates over the non-infected males by non-infected female rats, potentially due to changes in testosterone levels [82]. Testosterone levels have also been reported to be higher in T. gondii-infected men and decreased in T. gondii-infected women [83], and this may explain the increased impulsivity and reduced self-control findings in men.…”