Maintaining microendemic primate species along an environmental gradient – parasites as drivers for species differentiation

Abstract

Understanding the drivers of species adaptations to changing environments on the one hand and the limits for hybridization on the other hand is among the hottest questions in evolutionary biology. Parasites represent one of the major selective forces driving host evolution and at least those with free-living stages are at the same time dependent on the ecological conditions of their host's habitat. Local immunological adaptations of host species to varying parasite pressure are therefore expected and might represent the genetic basis for ecological speciation and the maintenance of recently diverged species. Madagascar provides one of the rare examples where two partially sympatric primate species (Microcebus griseorufus, M. murinus) and their hybrids, as well as an allopatric species (M. cf rufus) live in close proximity along a very steep environmental gradient ranging from southern dry spiny bush to gallery forest to evergreen eastern humid rain forest, thus mimicking the situation encountered during extensions and retreats of vegetation formations under changing climatic conditions. This system was used to study parasite infection and immune gene (MHC) adaptations to varying parasite pressure that might provide selective advantages to pure species over hybrids. Parasite burdens increased with increasing humidity. M. griseorufus, M. murinus, and their hybrids but not M. rufus shared the same MHC alleles, indicating either retention of ancestral polymorphism or recent gene flow. The hybrids had much higher prevalence of intestinal parasites than either of the parent species living under identical environmental conditions. The different representation of parasites can indicate a handicap for hybrids that maintains species identities.

Shared evolutionary origin of major histocompatibility complex polymorphism in sympatric lemurs

“…griseorufus (Gligor et al, 2009;Sommer et al, 2014). We did not detect cross-specific sharing of identical DRB alleles among the four sympatric members of the Cheirogaleidae studied here, nor with sequences published previously, in line with other studies focusing on wild lemur populations (e.g., Schad et al, 2005;Schwensow, Dausmann et al, 2010;Huchard et al, 2012;Grogan, McGinnis, Sauther, Cuozzo, & Drea, 2016), except for one instance where hybridization is known to occur between two Microcebus sp.…”

“…For example, allelic introgression through hybridization, or gene conversion and recombination, may produce structurally and functionally similar alleles across species (Wegner & Eizaguirre, ). However, allelic introgression is rather unlikely to affect patterns observed in Cheirogaleidae because no recent hybridization is known to occur in the clade, except for the distant populations of M. murinus and M. griseorufus (Gligor et al., ; Sommer et al., ). We did not detect cross‐specific sharing of identical DRB alleles among the four sympatric members of the Cheirogaleidae studied here, nor with sequences published previously, in line with other studies focusing on wild lemur populations (e.g., Schad et al., ; Schwensow, Eberle et al, 2010; Schwensow, Dausmann et al, 2010; Huchard et al., ; Grogan, McGinnis, Sauther, Cuozzo, & Drea, ), except for one instance where hybridization is known to occur between two Microcebus sp.…”

“…We did not detect cross‐specific sharing of identical DRB alleles among the four sympatric members of the Cheirogaleidae studied here, nor with sequences published previously, in line with other studies focusing on wild lemur populations (e.g., Schad et al., ; Schwensow, Eberle et al, 2010; Schwensow, Dausmann et al, 2010; Huchard et al., ; Grogan, McGinnis, Sauther, Cuozzo, & Drea, ), except for one instance where hybridization is known to occur between two Microcebus sp. (Sommer et al., ). In contrast, a study based largely on a captive colony of lemurs described identical DRB alleles, both within genus and across families that diverged up to 40 Mya, and attributed this finding to trans‐species polymorphism (Go et al.…”

“…Third, the fluctuating selection hypothesis predicts spatio‐temporal variation of pathogen communities, which creates different selective landscapes in different host populations (see Spurgin & Richardson, ). Support for a pathogen‐mediated selection on MHC stems for instance from associations observed between certain MHC alleles and pathogen prevalence at the population or community level (e.g., Hill et al., ; Wegner, Reusch, & Kalbe, ; Prugnolle et al., ; Schwensow, Fietz, Dausmann, & Sommer, ; Schwensow, Eberle, & Sommer, 2010; Schwensow, Dausmann, Eberle, Fietz, & Sommer, 2010; Froeschke & Sommer, ; Sepil, Lachish, Hinks, & Sheldon, ; Sommer, Rakotondranary, & Ganzhorn, ; Pilosof et al., ), or from positive correlations between MHC polymorphism and parasite richness across species (Goüy de Bellocq, Charbonnel, & Morand, ; Garamszegi & Nunn, ).…”

Spatial pattern of adaptive and neutral genetic diversity across different biomes in the lesser anteater (Tamandua tetradactyla)

“…As MHC is known to respond to PMS, the factors that drive pathogen diversity in different environments could also represent important causal predictors for MHC diversity. In fact, contrasting local immunogenetic adaptations of hosts that inhabit habitats with different parasite and pathogen pressure have been reported (e.g., Eizaguirre & Lenz 2010;Lenz et al 2013;Froeschke and Sommer 2014;Sommer et al 2014).…”