Protozoan parasite Toxoplasma gondii manipulates mate choice in rats by enhancing attractiveness of males

Abstract

Females in various species typically avoid males infected with parasites, while parasite-free males advertise their status through conspicuous phenotypic traits. This process selects for heritable resistance and reduces direct exposure of the female to parasites. Coevolving parasites are likely to attempt to circumvent this obstacle. In this paper, we demonstrate a case of parasitic manipulation of host mate choice. We report that Toxoplasma gondii, a sexually transmitted infection of brown rats, enhances sexual attractiveness of infected males. Thus under some evolutionary niches, parasites can indeed manipulate host sexual signaling to their own advantage.

Figure 1. Toxoplasma gondii is transmitted through intercourse.

Toxoplasma gondii cysts were observed in epididymis of infected males (panel A), in vaginal lavage of naïve females mated with infected males (panel B) and in brain of pups derived from these mating (panel C). Scale bar = 10 µm. Parasites are stained red (anti-GFP antibody couples with fluorogenic detection using Cy3), cyst wall green (dolichos biflorus agglutinin coupled with fluorescein) and sperm nuclei in blue (DAPI).

Figure 2. Uninfected females preferred infected males.

Preference was quantified by comparing time spent by an estrus female in two opposing arms of an arena, each arm urine marked by either controls or males infected six weeks earlier (panel A; trial duration  = 1200 s). Ordinate depicts time spent in infected bisect divided by control bisect (ratio >5 assigned arbitrary value of 5). Each dot represents raw data from one female. Box plots depict median, 25^th percentile and 75^th percentile. Preference of females for males in each of the 12 unique pair was calculated by taking median of all females tested for that particular male (panel B; ordinate and abscissa depicts time spent in infected and control bisect, respectively). Mean and SEM of data used in scatter-plot are depicted in grey color. These results were confirmed using a different rat strain in a geographically distinct location (panel C; Long-Evans rats in SU, USA; in place of Wistar rats at NTU, Singapore). **, p<0.001; Chi² test. In a competitive paced mating, females chose to participate in more mounts and intromissions with infected males (panel D; ordinate and abscissa depicts number of intromissions by infected and control males, respectively). *, p<0.01; one-sample t-test against chance, i.e. 1. Intromission data exhibited one outlier that has been removed from the graph. Mean and SEM are depicted in grey color.