Coevolution between multiple helminth infestations and basal immune investment in mammals: cumulative effects of polyparasitism?

Abstract

Animals often suffer from multiple parasite attacks in natural conditions (i.e., polyparasitism). The community of these parasites, which simultaneously or sequentially infest given host species, has rarely been investigated as a parasitic pressure per se. From this perspective, and despite the impressive number of immunoecological or comparative studies, the impacts of polyparasitism on immune responses are far from being appreciated. Focusing on helminths across a wide range of mammalian species and using a phylogenetic comparative method, we show, for the first time, that an increase in the number of helminth parasite species is positively correlated with an increase in basal immune investment (estimated by the counts of white blood cells) across mammal species. After discussing inherent limits of this comparative approach, we put this result in the evolutionary perspective of multiple parasitic infestations.

Parasite diversity of disease-bearing rodents of Southeast Asia: habitat determinants and effects on sexual size dimorphism and life-traits

“…The results of the few comparative studies that have investigated the effects of parasite species richness on the evolutionary ecology of their hosts have stressed four major findings (Morand, 2015): first, that host investment in immune defenses (i.e., immune cells, relative spleen size, immune genes) is related to parasite species richness or infection risk (Nunn et al, 2003;Pilosof et al, 2014Pilosof et al, , 2015; second, that increased parasite species diversity is linked to an increase in basal metabolism in mammals (Bordes and Morand, 2009) suggesting that increased basal metabolism may be related to an investment in immunity as a consequence of multiple infection; third, multi-parasitism affects life-history traits suggesting the existence of a trade-off between investment in reproduction or organs requiring high energy expenditure, and investment in defense ; fourth, a positive association between parasite diversity and sexual size dimorphism (SSD) has been observed in mammals, which suggests that multi-parasitism could drive sexual FIGURE 1 | Causal chain of relationships linking habitat specialization, parasite diversity, life-traits and sexual size dimorphism (see Introduction).…”

Landscape features and helminth co-infection shape bank vole immunoheterogeneity, with consequences for Puumala virus epidemiology

“…Multiparasitism may modulate the extent to which the organism invests in immunity as opposed to other life history traits (for example, Bordes and Morand, 2009) and the outcomes of immunological trade-offs (Cox, 2001;Graham et al, 2007). In vertebrates, the most heated debates have concerned the T helper-1 immune pathway, which is involved principally in the response to intracellular infections (for example, with viruses), and the T helper-2 immune pathway, which regulates infections with extracellular parasites, such as helminths (for a review, see Kidd, 2003).…”

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

“…The main parasites missing are those that require an intermediate host for transmission (for the house mice see Singleton et al 2005). Second, they have evolved strong immune defences in their natural range (Bordes & Morand 2009), which may subsequently confer a better capacity to control parasites that they may acquire by spill-back in the introduced range. Third, they do not lose all their parasites in the introduced range, any co-introduced parasites may be useful for the control of native hosts by spillover, which may have few opportunities for investment in defence, especially if living on islands (Hochberg & Møller 2001).…”