Immunogenetic heterogeneity in a widespread ungulate: the European roe deer (Capreolus capreolus)

Abstract

Understanding how immune genetic variation is shaped by selective and neutral processes in wild populations is of prime importance in both evolutionary biology and epidemiology. The European roe deer (Capreolus capreolus) has considerably expanded its distribution range these last decades, notably by colonizing agricultural landscapes. This range shift is likely to have led to bottlenecks and increased roe deer exposure to a new range of pathogens that until recently predominantly infected humans and domestic fauna. We therefore investigated the historical and contemporary forces that have shaped variability in a panel of genes involved in innate and acquired immunity in roe deer, including Mhc-Drb and genes encoding cytokines or toll-like receptors (TLRs). Together, our results suggest that genetic drift is the main contemporary evolutionary force shaping immunogenetic variation within populations. However, in contrast to the classical view, we found that some innate immune genes involved in micropathogen recognition (e.g. Tlrs) continue to evolve dynamically in roe deer in response to pathogen-mediated positive selection. Most studied Tlrs (Tlr2, Tlr4 and Tlr5) had similarly high levels of amino acid diversity in the three studied populations including one recently established in southwestern France that showed a clear signature of genetic bottleneck. Tlr2 implicated in the recognition of Gram-positive bacteria in domestic ungulates, showed strong evidence of balancing selection. The high immunogenetic variation revealed here implies that roe deer are able to cope with a wide spectrum of pathogens and to respond rapidly to emerging infectious diseases.

Effects of invasion history on physiological responses to immune system activation in invasive Australian cane toads

“…Systemic mechanisms such as acute phase protein activity, anorexia, lethargy, and fever are highly inflammatory, and thus may be ‘costly’ (Klasing & Leshchinsky, 1999). These responses are predicted (Cornet et al, 2016; Lee & Klasing, 2004), and have been shown, to be down-regulated in invasive populations of invertebrates (Cornet, Sorci & Moret, 2010; Wilson-Rich & Starks, 2010), sparrows (Lee, Martin & Wikelski, 2005), trout (Monzon-Arguello et al, 2014), and deer (Quéméré et al, 2015). Although constitutive innate defences (such as whole-blood phagocytosis of bacteria or yeast) also require substantial energy to activate (McDade, Georgiev & Kuzawa, 2016), glucose metabolism does not increase during phagocytosis in human neutrophils (Borregaard & Herlin, 1982).…”

Eco‐immunology and bioinvasion: revisiting the evolution of increased competitive ability hypotheses

“…In addition to classical and nonspecific immune assays (e.g. cell count, enzymatic activity; Boughton, Joop, & Armitage, ), we noticed a growing interest in and use of diversified and modern immunology techniques applied to wild, nonmodel systems (Pedersen & Babayan, ) such as immuno‐genetic/genomic approaches in both invertebrate and vertebrate systems (Martin, Coon, Liebl, & Schrey, ; Monzon‐Arguello, de Leaniz, Gajardo, & Consuegra, ; Quéméré et al., ; Vilcinskas, Mukherjee, & Vogel, ; White, Perkins, Heckel, & Searle, ).…”

“…As these specialist parasites elicit, among other things, antibody‐mediated responses, invasive hosts that are no more in contact with them should take advantage of downregulating these adaptive responses. This may explain the lower genetic/functional diversity observed at Mhc genes in invasive populations when genetic drift alone cannot explain this pattern (Monzon‐Arguello et al., ; Quéméré et al., ). The loss of coevolved parasites during invasions may, however, come at a cost if the lack of exposure to immunosuppressive “old friends” substantially enhances the risk of suffering from immune disorders (Rook, ; Sorci, Cornet, & Faivre, ,b).…”

“…The maintenance of high levels of costly immune responses (e.g. inflammation) in natural populations at the invasion front (Diagne et al., in revision; Martin et al., ; Quéméré et al., ) could indicate that invaders are exposed to high pathogenic pressure, although not necessarily infected. Alternatively, maintaining an ability to mount an acute phase response could be essential to survive in any environment, and explain why this defence is not traded‐off (Hegemann, Matson, Versteegh, & Tieleman, ).…”

Drift, not selection, shapes toll‐like receptor variation among oceanic island populations

“…; Quéméré et al . ). Most of the sites identified as being under positive selection in these studies are located in the TLR extracellular domain which directly binds the PAMPs (reviewed in Mikami et al .…”