Variability of whipworm infection and humoral immune response in a wild population of mole voles (Ellobius talpinus Pall.)

Abstract

Restricted mobility and spatial isolation of social units in gregarious subterranean mammals ensure good defence mechanisms against parasites, which in turn allows for a reduction of immunity components. In contrast, a parasite invasion may cause an increased adaptive immune response. Therefore, it can be expected that spatial and temporal distribution of parasites within a population will correlate with the local variability in the host's immunocompetence. To test this hypothesis, the intra-population variability of a whipworm infestation and the humoral immune response to non-replicated antigens in mole voles (Ellobius talpinus Pall.), social subterranean rodents, was estimated. Whipworm prevalence in mole voles increased from spring to autumn, and this tendency was more pronounced in settlements living in natural meadows compared to settlements in man-made meadows. However, humoral immune response was lowest in animals from natural meadows trapped in autumn. Since whipworm infestation does not directly affect the immunity of mole voles, the reciprocal tendencies in seasonal dynamics and spatial distribution of whipworm abundance and host immunocompetence may be explained by local deterioration of habitat conditions, which increases the probability of an infestation.

Acute-Phase Immune Response Involves Fever, Sickness Behavior, and an Elevated Metabolic Rate in the Subterranean RodentCtenomys talarum

“…Ctenomys talarum (Talas tuco-tucos, Thomas 1898) is a South American subterranean rodent that lives solitarily in permanently sealed burrows, where most of their activities take place (Busch et al 1989;2000). The relatively low parasite richness of gastrointestinal helminths observed in this species (Rossin and Malizia 2002) and other subterranean rodents has been related to their solitary existence underground (Novikov et al 2016). Besides limiting convective heat loss, the moist and stagnant conditions of the subterranean environment are hypothesized to have favored the low basal metabolic rate (BMR) observed in C. talarum (Busch 1989;Luna et al 2009) and other subterranean rodents (McNab 1966).…”

“…costly adaptive defenses, subterranean rodents live in habitats characterized by high prevalence but low diversity of parasite infections, which may facilitate innate immunity to reduce resource allocation towards more expensive adaptive immunity (Novikov et al 2016). In fact, low polymorphism at Major Histocompatibility Complex (MHC) genes, involved in foreign antigen recognition and destruction (Klein et al 1998), have been reported for different subterranean rodents (Nižetić et al 1988;Kundu and Faulkes 2004), and in particular for ctenomyids (Hambuch and Lacey 2002;Cutrera and Lacey 2006;Cutrera and Mora 2017), relative to surface-dwelling rodents, presumably associated with low levels of parasite exposure in the subterranean habitat.…”

Social interaction, and not group size, predicts parasite burden in mammals

“…Parasitism is capable of affecting host survival and reproduction (Møller et al 2001), and larger group sizes, higher population densities, a promiscuous sexual system, social contact and colonialism are each associated with higher levels of exposure to, or transmission of, parasites (Altizer et al 2003;Arneberg et al 1998;Hoogland 1979;Hoogland and Sherman 1976;Johnson et al 2004;Rifkin et al 2012;Tella 2002). However, several studies have found that parasitism is not significantly affected by group size (Arnold and Anja 1993;Hillegass et al 2008;Novikov et al 2016;Zhang et al 2010). In a comparative study, Watve and Sukumar (1995) found that among 12 species of mammals, the solitary species had higher levels of parasitism than did the gregarious ones.…”

Transcriptomic analyses reveal tissue-specific selection on genes related to apoptotic processes in the subterranean rodent,Ctenomys sociabilis

“…While the larger set of transcripts identified using the branch-site model for GO enrichment did not reveal statistically significant enrichment of GO terms for C. sociabilis genes under positive selection, it did reveal that many of the GO terms identified corresponded to processes of cell proliferation control, DNA damage response, immune response, and ion transport. These findings are intriguing in light of evidence suggesting that burrowing rodents may be exposed to heavy metals or other toxins in the soils that they inhabit (De Vleeschouwer et al, 2014; Fernández-Cadena et al, 2014) and recent studies characterizing the immunogenetics of subterranean rodents (Cutrera et al, 2010; Merlo, Cutrera & Zenuto, 2016; Novikov et al, 2016). Particularly exciting is the identification of transcripts involved in the control of cell proliferation, which has potential ties to susceptibility to cancer (Tian et al, 2013).…”