Does investment into “expensive” tissue compromise anti-parasitic defence? Testes size, brain size and parasite diversity in rodent hosts

Abstract

Species richness of parasite assemblages varies among host species. Earlier studies that searched for host-related determinants of parasite diversity mainly considered host traits that affect the probability of host encounter with parasites, whereas host traits related to defensibility against parasites have rarely been investigated. From the latter perspective, evolutionary investment in "expensive" tissue or organs (like testes or brain) may trade off against energetically costly anti-parasitic defences. If so, richer parasite assemblages are expected in hosts with larger testes and brains. We studied the relationships between testes and brain size and diversity of parasites (fleas, gamasid mites and helminths) in 55 rodent species using a comparative approach and application of two methods, namely the method of independent contrasts and generalized least-squares (GLS) analysis. Both phylogenetically correct methods produced similar results for flea and helminth species richness. Testes size positively correlated with flea and helminth species richness but not gamasid mite species richness. No correlation between brain size and species richness of any parasite group was found by the method of independent contrasts. However, GLS analysis indicated negative correlation between brain size and mite species richness. Our results cast doubt on the validity of the expensive tissue hypothesis, but suggest instead that larger testes are associated with higher parasite diversity via their effect on mobility and/or testosterone-mediated immunosuppression.

Immunological Sex Differences in Socially Promiscuous African Ground Squirrels

“…A similar relationship between testes size and flea and helminth species richness has been found in other rodents which was possibly attributed to testosterone-mediated immunosuppression [40]. However, as our data show, the relationship between testosterone and parasites also depends on the parasite [16], [40], [41]. Similarly, a recent study in spiny lizards ( Sceloporus jarrovi ) demonstrated a positive association between plasma testosterone levels and mites but a negative association with endoparasites [16].…”

“…This hypothesis was supported by our data which showed a negative association between testes size and immune function as well as a significant positive association between testes investment and number of lice, despite a low sample size. A similar relationship between testes size and flea and helminth species richness has been found in other rodents which was possibly attributed to testosterone-mediated immunosuppression [40]. However, as our data show, the relationship between testosterone and parasites also depends on the parasite [16], [40], [41].…”

Evolutionary co-variation of host and parasite diversity—the first test of Eichler’s rule using parasitic lice (Insecta: Phthiraptera)

“…In the wide taxonomic range presented by this study, host body mass does not seem a key factor shaping louse richness, as is also suggested by several earlier studies (Bordes et al 2011;Hughes and Page 2007;Krasnov et al 2004;Poulin 2007). We found, however, that body mass had a strong effect on the generic richness of Ricinids.…”

“…However, research on the interaction between host body size and parasite richness yielded contradictory results (see e.g. Poulin and Morand (2004), Poulin (2007) for reviews), suggesting that host body mass may not act as a general predictor of parasite diversity (Bordes et al 2011;Hughes and Page 2007;Krasnov et al 2004;). …”

Global parasite and Rattus rodent invasions: The consequences for rodent‐borne diseases

“…Fourth, as the immunocompetence should be linked to parasite diversity (Ponlet et al 2011), trade-offs between levels of immunocompetence and expensive life history traits are expected (Bordes et al 2011;Morand 2015) as well as decreased immunocompetence with the loss of parasites and lower local biodiversity (Møller & Cassey 2004). A re-allocation of resources away from costly defences should be particularly pronounced at the wave-front of the invasion during the range expansion stage (White & Perkings 2012).…”