Immune Defense and Host Sociality: A Comparative Study of Swallows and Martins

Abstract

Sociality is associated with increased risks of parasitism, predation, and social competition, which may interact because social stress can reduce immunity, and parasitized individuals are more likely to fall prey to a predator. A mechanism allowing evolution of sociality in spite of high costs of parasitism is increased investment in antiparasite defenses. Here we show that the impact of parasites on host reproductive success was positively associated with the degree of sociality in the bird family Hirundinidae. However, the cost of parasitism in highly colonial species was countered by high levels of T- and B-cell immune responses. Investment in immune function among colonial species was particularly strong in nestlings, and among social species, this investment was associated with a relatively prolonged period of development, thereby leading to extended exposure to parasites. Thus, highly social species such as certain species of swallows and martins may cope with strong natural selection arising from parasites by heavy investment in immune function at the cost of a long exposure to nest parasites.

Immune responses to fleas in two rodent species differing in natural prevalence of infestation and diversity of flea assemblages

“…This is especially likely since fleas possess intracellular digestion, and lack a peritrophic membrane (Vatschenok 1988) that separates ingested food from the gut epithelium and, thus, may prevent penetration of ingested immune effector components (Eiseman and Binnengton 1994). In addition, different branches of immune defenses (e.g., humoral versus cell-mediated immunity) may differ in their costs for a host, and thus may compete for limiting resources, resulting in negatively correlated evolution and tradeoffs (Lochmiller and Deerenberg 2000;Blount et al 2003; but see Moller et al 2001).…”

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

“…Most immunoecological studies do not appreciate direct parasitic pressures (see Owen and Clayton (2007); Martin et al (2008)) as most of them have used indirect approaches of parasitism such as "parasite risk" (i.e., sociality, group size, densities, tropical latitude, or promiscuity). They have then linked stronger immune investment with a priori higher parasitic load (Møller 1998;Møller et al (2001) for birds ;Nunn 2002;Nunn et al 2000Nunn et al , 2003Semple et al (2002) for mammals, but see Preston et al (2009)). …”

Rodent sociality and parasite diversity

“…abundance, prevalence or parasite species richness (PSR)) for a variety of directly transmitted ectoparasites or helminths (Arneberg et al 1998;Stanko et al 2002), as well as for vector-borne arthropods ( Nunn & Heymann 2005). Other studies that focused on investment in immune function as an indirect measure of parasitic pressures have also found positive relationships between the group size and the level of immunological investment (Møller et al 2001;Brown & Brown 2002).…”