Balancing selection, genetic drift, and human‐mediated introgression interplay to shape MHC (functional) diversity in Mediterranean brown trout
Abstract The extraordinary polymorphism of major histocompatibility complex (MHC) genes is considered a paradigm of pathogen‐mediated balancing selection, although empirical evidence is still scarce. Furthermore, the relative contribution of balancing selection to shape MHC population structure and...
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doaj-d6bb466841a9498cb6a1921d14ac7bf62021-08-02T18:48:03ZengWileyEcology and Evolution2045-77582021-08-011115100261004110.1002/ece3.7760Balancing selection, genetic drift, and human‐mediated introgression interplay to shape MHC (functional) diversity in Mediterranean brown troutLorenzo Talarico0Silvio Marta1Anna Rita Rossi2Simone Crescenzo3Gerardo Petrosino4Marco Martinoli5Lorenzo Tancioni6Laboratory of Experimental Ecology and Aquaculture Department of Biology University of Rome “Tor Vergata” Rome ItalyDepartment of Environmental Science and Policy University of Milan Milan ItalyDepartment of Biology and Biotechnology C. Darwin University of Rome “La Sapienza” Rome ItalyDepartment of Biology and Biotechnology C. Darwin University of Rome “La Sapienza” Rome ItalyDepartment of Biology and Biotechnology C. Darwin University of Rome “La Sapienza” Rome ItalyLaboratory of Experimental Ecology and Aquaculture Department of Biology University of Rome “Tor Vergata” Rome ItalyLaboratory of Experimental Ecology and Aquaculture Department of Biology University of Rome “Tor Vergata” Rome ItalyAbstract The extraordinary polymorphism of major histocompatibility complex (MHC) genes is considered a paradigm of pathogen‐mediated balancing selection, although empirical evidence is still scarce. Furthermore, the relative contribution of balancing selection to shape MHC population structure and diversity, compared to that of neutral forces, as well as its interaction with other evolutionary processes such as hybridization, remains largely unclear. To investigate these issues, we analyzed adaptive (MHC‐DAB gene) and neutral (11 microsatellite loci) variation in 156 brown trout (Salmo trutta complex) from six wild populations in central Italy exposed to introgression from domestic hatchery lineages (assessed with the LDH gene). MHC diversity and structuring correlated with those at microsatellites, indicating the substantial role of neutral forces. However, individuals carrying locally rare MHC alleles/supertypes were in better body condition (a proxy of individual fitness/parasite load) regardless of the zygosity status and degree of sequence dissimilarity of MHC, hence supporting balancing selection under rare allele advantage, but not heterozygote advantage or divergent allele advantage. The association between specific MHC supertypes and body condition confirmed in part this finding. Across populations, MHC allelic richness increased with increasing admixture between native and domestic lineages, indicating introgression as a source of MHC variation. Furthermore, introgression across populations appeared more pronounced for MHC than microsatellites, possibly because initially rare MHC variants are expected to introgress more readily under rare allele advantage. Providing evidence for the complex interplay among neutral evolutionary forces, balancing selection, and human‐mediated introgression in shaping the pattern of MHC (functional) variation, our findings contribute to a deeper understanding of the evolution of MHC genes in wild populations exposed to anthropogenic disturbance.https://doi.org/10.1002/ece3.7760body conditionhybridizationmajor histocompatibility complexMHC supertypesrare allele advantageSalmo trutta complex |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Lorenzo Talarico Silvio Marta Anna Rita Rossi Simone Crescenzo Gerardo Petrosino Marco Martinoli Lorenzo Tancioni |
spellingShingle |
Lorenzo Talarico Silvio Marta Anna Rita Rossi Simone Crescenzo Gerardo Petrosino Marco Martinoli Lorenzo Tancioni Balancing selection, genetic drift, and human‐mediated introgression interplay to shape MHC (functional) diversity in Mediterranean brown trout Ecology and Evolution body condition hybridization major histocompatibility complex MHC supertypes rare allele advantage Salmo trutta complex |
author_facet |
Lorenzo Talarico Silvio Marta Anna Rita Rossi Simone Crescenzo Gerardo Petrosino Marco Martinoli Lorenzo Tancioni |
author_sort |
Lorenzo Talarico |
title |
Balancing selection, genetic drift, and human‐mediated introgression interplay to shape MHC (functional) diversity in Mediterranean brown trout |
title_short |
Balancing selection, genetic drift, and human‐mediated introgression interplay to shape MHC (functional) diversity in Mediterranean brown trout |
title_full |
Balancing selection, genetic drift, and human‐mediated introgression interplay to shape MHC (functional) diversity in Mediterranean brown trout |
title_fullStr |
Balancing selection, genetic drift, and human‐mediated introgression interplay to shape MHC (functional) diversity in Mediterranean brown trout |
title_full_unstemmed |
Balancing selection, genetic drift, and human‐mediated introgression interplay to shape MHC (functional) diversity in Mediterranean brown trout |
title_sort |
balancing selection, genetic drift, and human‐mediated introgression interplay to shape mhc (functional) diversity in mediterranean brown trout |
publisher |
Wiley |
series |
Ecology and Evolution |
issn |
2045-7758 |
publishDate |
2021-08-01 |
description |
Abstract The extraordinary polymorphism of major histocompatibility complex (MHC) genes is considered a paradigm of pathogen‐mediated balancing selection, although empirical evidence is still scarce. Furthermore, the relative contribution of balancing selection to shape MHC population structure and diversity, compared to that of neutral forces, as well as its interaction with other evolutionary processes such as hybridization, remains largely unclear. To investigate these issues, we analyzed adaptive (MHC‐DAB gene) and neutral (11 microsatellite loci) variation in 156 brown trout (Salmo trutta complex) from six wild populations in central Italy exposed to introgression from domestic hatchery lineages (assessed with the LDH gene). MHC diversity and structuring correlated with those at microsatellites, indicating the substantial role of neutral forces. However, individuals carrying locally rare MHC alleles/supertypes were in better body condition (a proxy of individual fitness/parasite load) regardless of the zygosity status and degree of sequence dissimilarity of MHC, hence supporting balancing selection under rare allele advantage, but not heterozygote advantage or divergent allele advantage. The association between specific MHC supertypes and body condition confirmed in part this finding. Across populations, MHC allelic richness increased with increasing admixture between native and domestic lineages, indicating introgression as a source of MHC variation. Furthermore, introgression across populations appeared more pronounced for MHC than microsatellites, possibly because initially rare MHC variants are expected to introgress more readily under rare allele advantage. Providing evidence for the complex interplay among neutral evolutionary forces, balancing selection, and human‐mediated introgression in shaping the pattern of MHC (functional) variation, our findings contribute to a deeper understanding of the evolution of MHC genes in wild populations exposed to anthropogenic disturbance. |
topic |
body condition hybridization major histocompatibility complex MHC supertypes rare allele advantage Salmo trutta complex |
url |
https://doi.org/10.1002/ece3.7760 |
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