Balancing selection and genetic drift create unusual patterns of <scp>MHCII</scp>β variation in Galápagos mockingbirds

Vlček, Jakub; Hoeck, Paquita E. A.; Keller, Lukas F.; Wayhart, Jessica P; Dolinová, Iva; Štefka, Jan

doi:10.1111/mec.13807

Cited by 17 publications

(25 citation statements)

References 88 publications

(226 reference statements)

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“…Furthermore, despite the loss of allelic diversity, Iberian lynx conserved a similar number of segregating sites and maintained high average levels of divergence between alleles, with most supertypes being represented by at least one allele. In fact, the retention of variation- especially of a non-random highly-divergent subset of alleles- following a bottleneck has been observed in several other studies (e.g., [53–56]). In these cases, this has been interpreted as the consequence of balancing selection favouring the retention of more divergent vs. less divergent alleles (divergent allele selection [14]).…”

Section: Discussionmentioning

confidence: 67%

Retention of functional variation despite extreme genomic erosion: MHC allelic repertoires in the Lynx genus

Marmesat

Schmidt

Saveljev³

et al. 2017

BMC Evol Biol

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BackgroundDemographic bottlenecks erode genetic diversity and may increase endangered species’ extinction risk via decreased fitness and adaptive potential. The genetic status of species is generally assessed using neutral markers, whose dynamic can differ from that of functional variation due to selection. The MHC is a multigene family described as the most important genetic component of the mammalian immune system, with broad implications in ecology and evolution. The genus Lynx includes four species differing immensely in demographic history and population size, which provides a suitable model to study the genetic consequences of demographic declines: the Iberian lynx being an extremely bottlenecked species and the three remaining ones representing common and widely distributed species. We compared variation in the most variable exon of the MHCI and MHCII-DRB loci among the four species of the Lynx genus.ResultsThe Iberian lynx was characterised by lower number of MHC alleles than its sister species (the Eurasian lynx). However, it maintained most of the functional genetic variation at MHC loci present in the remaining and genetically healthier lynx species at all nucleotide, amino acid, and supertype levels.ConclusionsSpecies-wide functional genetic diversity can be maintained even in the face of severe population bottlenecks, which caused devastating whole genome genetic erosion. This could be the consequence of divergent alleles being retained across paralogous loci, an outcome that, in the face of frequent gene conversion, may have been favoured by balancing selection.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-017-1006-z) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 67%

Retention of functional variation despite extreme genomic erosion: MHC allelic repertoires in the Lynx genus

Marmesat

Schmidt

Saveljev³

et al. 2017

BMC Evol Biol

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“…Some degree of differentiation in supertypes present in different invasive sampling sites may be due to contrasting pathogen pressures in these sites, but may also reflect interpopulation differentiation due to demographic processes. Still, taking into account high levels Godoy, 2017;Oosterhout et al, 2006;Vlček et al, 2016) and was interpreted as the footprint of balancing selection in the form of divergent allele advantage.…”

Section: Mhc-drb Diversitymentioning

confidence: 99%

Comparing raccoon major histocompatibility complex diversity in native and introduced ranges: Evidence for the importance of functional immune diversity for adaptation and survival in novel environments

Biedrzycka

Konopiński

Hoffman

et al. 2019

Evolutionary Applications

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The adaptive potential of invasive species is related to the genetic diversity of the invader, which is influenced by genetic drift and natural selection. Typically, the genetic diversity of invaders is studied with neutral genetic markers; however, the expectation of reduced diversity has not been consistently supported by empirical studies. Here, we describe and interpret genetic diversity at both neutral microsatellite loci and the immune‐related MHC‐DRB locus of native and invasive populations of raccoon to better understand of how drift and selection impact patterns of genetic diversity during the invasion process. We found that despite the loss of many MHC (major histocompatibility complex) alleles in comparison with native populations, functional MHC supertypes are preserved in the invasive region. In the native raccoon population, the number of supertypes within individuals was higher than expected under a neutral model. The high level of individual functional divergence may facilitate the adaptation to local conditions in the invasive range. In the invasive populations, we also detected increased population structure at microsatellites compared to the MHC locus, further suggesting that balancing selection is acting on adaptively important regions of the raccoon genome. Finally, we found that alleles known to exhibit resistance to rabies in the native range, Prlo‐DRB*4, Prlo‐DRB*16 and Prlo‐DRB*102, were the most common alleles in the European populations, suggesting directional selection is acting on this locus. Our research shows empirical support for the importance of functional immune diversity for adaptation and survival in novel environments.

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“…We also performed linear models as aforementioned to test the predictive value of population size and distance from the mainland on MHC variation (e.g. Vlček et al 2016). Estimates of MHC genetic diversity were used as response variables and population of origin as a random effect.…”

Section: Effects Of Insularity On Adaptive Diversitymentioning

confidence: 99%

“…Miller et al 2010;Strand et al 2012), others fail to find such an effect in spite of strong bottlenecks (e.g. Aguilar et al 2004;Oliver and Piertney 2012;Vlček et al 2016). Introgression, which may occur when closely related, occasionally hybridizing, species occur in sympatry, also affects MHC diversity (Nadachowska-Brzyska et al 2012;Hedrick 2013).…”

Section: Introductionmentioning

confidence: 99%

“…Furthermore, we predicted that the geographically isolated island populations will have lower MHC diversity and greater MHC structure compared to mainland populations due to restricted gene flow. Lower MHC allele polymorphism on islands may also be the result of weaker pathogen-mediated selection pressure due to the lower pathogen diversity prevailing on islands (Wikelski et al 2004;Roca et al 2009;Vlček et al 2016). To address this, we directly compared the effects of insularity on the diversity of the adaptively and neutrally evolving loci.…”

Section: Introductionmentioning

confidence: 99%

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Selection, drift, and introgression shape MHC polymorphism in lizards

et al. 2018

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The major histocompatibility complex (MHC) has long served as a model for the evolution of adaptive genetic diversity in wild populations. Pathogen-mediated selection is thought to be a main driver of MHC diversity, but it remains elusive to what degree selection shapes MHC diversity in complex biogeographical scenarios where other evolutionary processes (e.g. genetic drift and introgression) may also be acting. Here we focus on two closely related green lizard species, Lacerta trilineata and L. viridis, to address the evolutionary forces acting on MHC diversity in populations with different biogeographic structure. We characterized MHC class I exon 2 and exon 3, and neutral diversity (microsatellites), to study the relative importance of selection, drift, and introgression in shaping MHC diversity. As expected, positive selection was a significant force shaping the high diversity of MHC genes in both species. Moreover, introgression significantly increased MHC diversity in mainland populations, with a primary direction of gene flow from L. viridis to L. trilineata. Finally, we found significantly fewer MHC alleles in island populations, but maintained MHC sequence and functional diversity, suggesting that positive selection counteracted the effect of drift. Overall, our data support that different evolutionary processes govern MHC diversity in different biogeographical scenarios: positive selection occurs broadly while introgression acts in sympatry and drift when the population sizes decrease.

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Balancing selection and genetic drift create unusual patterns of MHCIIβ variation in Galápagos mockingbirds

Cited by 17 publications

References 88 publications

Retention of functional variation despite extreme genomic erosion: MHC allelic repertoires in the Lynx genus

Retention of functional variation despite extreme genomic erosion: MHC allelic repertoires in the Lynx genus

Comparing raccoon major histocompatibility complex diversity in native and introduced ranges: Evidence for the importance of functional immune diversity for adaptation and survival in novel environments

Selection, drift, and introgression shape MHC polymorphism in lizards

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