The effects of historical fragmentation on major histocompatibility complex class II β and microsatellite variation in the Aegean island reptile, Podarcis erhardii
Abstract:The major histocompatibility complex (MHC) plays a key role in disease resistance and is the most polymorphic gene region in vertebrates. Although habitat fragmentation is predicted to lead to a loss in MHC variation through drift, the impact of other evolutionary forces may counter this effect. Here we assess the impact of selection, drift, migration, and recombination on MHC class II and microsatellite variability in 14 island populations of the Aegean wall lizard Podarcis erhardii. Lizards were sampled from… Show more
“…The ecological and evolutionary impacts of long-term fragmentation on land-bridge island fauna has been studied in a number of systems (Karr, 1982;Aguilar et al, 2004;Hurston et al, 2009;Estrada-Villegas et al, 2010;Duryea et al, 2015;Belasen et al, 2016;Santonastaso et al, 2017). In a previous study examining immunogenetic diversity in island vertebrates, MHC diversity remained high while overall diversity dropped (Aguilar et al, 2004).…”
Habitat fragmentation and wildlife disease are two widespread drivers of biodiversity loss, yet few empirical studies have explored their interactions. In this study, we utilized a naturally fragmented island system to examine the impacts of fragmentation on genetic diversity and amphibian infection dynamics. We determined the impacts of fragmentation on genetic diversity at the immunity locus MHC IIB, a hypothesized predictor of disease susceptibility. Contrary to the expectation that MHC diversity would remain high due to balancing selection, island populations lost genetic diversity at this locus while simultaneously experiencing positive selection at MHC IIB. We then used Next-Generation Sequencing to identify a variety of potential eukaryotic parasites from amphibian skin swabs. Island populations exhibited higher potential parasite richness (proportion of eukaryotic microbe operational taxonomic units or OTUs from parasitic taxa) relative to mainland populations. MHC homozygotes hosted a lower diversity of potential parasites, and population-level MHC diversity was negatively associated with parasite richness. Our results show that genetic erosion can occur at the MHC IIB locus following fragmentation, which may contribute to increased susceptibility to parasites.
“…The ecological and evolutionary impacts of long-term fragmentation on land-bridge island fauna has been studied in a number of systems (Karr, 1982;Aguilar et al, 2004;Hurston et al, 2009;Estrada-Villegas et al, 2010;Duryea et al, 2015;Belasen et al, 2016;Santonastaso et al, 2017). In a previous study examining immunogenetic diversity in island vertebrates, MHC diversity remained high while overall diversity dropped (Aguilar et al, 2004).…”
Habitat fragmentation and wildlife disease are two widespread drivers of biodiversity loss, yet few empirical studies have explored their interactions. In this study, we utilized a naturally fragmented island system to examine the impacts of fragmentation on genetic diversity and amphibian infection dynamics. We determined the impacts of fragmentation on genetic diversity at the immunity locus MHC IIB, a hypothesized predictor of disease susceptibility. Contrary to the expectation that MHC diversity would remain high due to balancing selection, island populations lost genetic diversity at this locus while simultaneously experiencing positive selection at MHC IIB. We then used Next-Generation Sequencing to identify a variety of potential eukaryotic parasites from amphibian skin swabs. Island populations exhibited higher potential parasite richness (proportion of eukaryotic microbe operational taxonomic units or OTUs from parasitic taxa) relative to mainland populations. MHC homozygotes hosted a lower diversity of potential parasites, and population-level MHC diversity was negatively associated with parasite richness. Our results show that genetic erosion can occur at the MHC IIB locus following fragmentation, which may contribute to increased susceptibility to parasites.
“…A puzzling observation about MHC gene evolution is that some studies report that MHC diversity is primarily affected by drift 51 – 53 , whereas others show that the high polymorphism is maintained by balancing selection 54 , 55 . This contradiction is reconciled when realising that genetic drift (as well as selection) acts on the alleles, whereas balancing selection acts on the immunological function of the alleles, defined by their ST.…”
Red Queen host–parasite co-evolution can drive adaptations of immune genes by positive selection that erodes genetic variation (Red Queen arms race) or results in a balanced polymorphism (Red Queen dynamics) and long-term preservation of genetic variation (trans-species polymorphism). These two Red Queen processes are opposite extremes of the co-evolutionary spectrum. Here we show that both Red Queen processes can operate simultaneously by analysing the major histocompatibility complex (MHC) in guppies (Poecilia reticulata and P. obscura) and swamp guppies (Micropoecilia picta). Sub-functionalisation of MHC alleles into ‘supertypes’ explains how polymorphisms persist during rapid host–parasite co-evolution. Simulations show the maintenance of supertypes as balanced polymorphisms, consistent with Red Queen dynamics, whereas alleles within supertypes are subject to positive selection in a Red Queen arms race. Building on the divergent allele advantage hypothesis, we show that functional aspects of allelic diversity help to elucidate the evolution of polymorphic genes involved in Red Queen co-evolution.
“…This reflects the limited overlap of haplotypes between populations. In the Cycladic Archipelago in the Aegean Sea, Aegean wall lizard’s populations show little or no contemporary gene flow between different island populations ( Santonastaso et al, 2017 ). This is a group of continental islands comparable to the Andaman Islands as they were also formed due to rise in sea levels in the LGM.…”
Limited gene flow between populations due to geographic distance, presence of barriers or inherent low dispersal ability leads to the formation of genetically structured populations. Strong population structure indicates lowered levels or absence of gene flow which might lead to inbreeding and loss of genetic capacity to recuperate from anthropogenic stress and natural calamities. Terrestrial reptiles are generally known to have low dispersal abilities and few studies have explored drivers of their population structure on continental islands, where both anthropogenic stress and natural calamities are relatively common. We investigated the population structure and drivers of diversification of the Andaman keelback (Xenochrophis tytleri), an endemic, terrestrial and freshwater snake species in the Andaman archipelago, a continental group of islands in the Bay of Bengal. Data was collected from 86 individuals from seven islands and 78 individuals were sequenced for the gene Nuclear Dehydrogenase subunit 4 to identify the number of populations and distribution of genetic diversity across populations. We found 11 haplotypes on seven islands and observed high genetic differentiation between seven populations defined island-wise (FST = 0.82). We further tested the number of populations by incorporating spatial data into Bayesian Clustering Analysis (GENELAND) and identified six populations of the Andaman keelback. We tested for the influence of Isolation-by-distance on these populations. While the overall trend showed a positive correlation between geographic and genetic distance, a correlogram revealed that the positive correlation disappears beyond ∼20–40 km. We also tested for the presence of geographical barriers to gene flow using Monmonier’s algorithm (SPADS), which identified five barriers to dispersal confirming that there are oceanic barriers to dispersal for some island populations of the Andaman keelback. As the Andaman Islands are arranged almost in a straight line from North to South, our data are insufficient to tease apart the roles of geographical distance and barriers to gene flow. We conclude that salt waters between near islands are weak barriers and as the geographical distance between islands increases, so does the strength of the barrier.
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