Lack of Spatial Immunogenetic Structure among Wolverine (Gulo gulo) Populations Suggestive of Broad Scale Balancing Selection.

Elucidating the adaptive genetic potential of wildlife populations to environmental selective pressures is fundamental for species conservation. Genes of the major histocompatibility complex (MHC) are highly polymorphic, and play a key role in the adaptive immune response against pathogens. MHC poly...

Full description

Bibliographic Details
Main Authors: Yessica Rico, James Morris-Pocock, Joanna Zigouris, Joseph J Nocera, Christopher J Kyle
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2015-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0140170
id doaj-f5f7d148f1194906967cbac0bdf7ed50
record_format Article
spelling doaj-f5f7d148f1194906967cbac0bdf7ed502021-03-03T19:58:43ZengPublic Library of Science (PLoS)PLoS ONE1932-62032015-01-011010e014017010.1371/journal.pone.0140170Lack of Spatial Immunogenetic Structure among Wolverine (Gulo gulo) Populations Suggestive of Broad Scale Balancing Selection.Yessica RicoJames Morris-PocockJoanna ZigourisJoseph J NoceraChristopher J KyleElucidating the adaptive genetic potential of wildlife populations to environmental selective pressures is fundamental for species conservation. Genes of the major histocompatibility complex (MHC) are highly polymorphic, and play a key role in the adaptive immune response against pathogens. MHC polymorphism has been linked to balancing selection or heterogeneous selection promoting local adaptation. However, spatial patterns of MHC polymorphism are also influenced by gene flow and drift. Wolverines are highly vagile, inhabiting varied ecoregions that include boreal forest, taiga, tundra, and high alpine ecosystems. Here, we investigated the immunogenetic variation of wolverines in Canada as a surrogate for identifying local adaptation by contrasting the genetic structure at MHC relative to the structure at 11 neutral microsatellites to account for gene flow and drift. Evidence of historical positive selection was detected at MHC using maximum likelihood codon-based methods. Bayesian and multivariate cluster analyses revealed weaker population genetic differentiation at MHC relative to the increasing microsatellite genetic structure towards the eastern wolverine distribution. Mantel correlations of MHC against geographical distances showed no pattern of isolation by distance (IBD: r = -0.03, p = 0.9), whereas for microsatellites we found a relatively strong and significant IBD (r = 0.54, p = 0.01). Moreover, we found a significant correlation between microsatellite allelic richness and the mean number of MHC alleles, but we did not observe low MHC diversity in small populations. Overall these results suggest that MHC polymorphism has been influenced primarily by balancing selection and to a lesser extent by neutral processes such as genetic drift, with no clear evidence for local adaptation. This study contributes to our understanding of how vulnerable populations of wolverines may respond to selective pressures across their range.https://doi.org/10.1371/journal.pone.0140170
collection DOAJ
language English
format Article
sources DOAJ
author Yessica Rico
James Morris-Pocock
Joanna Zigouris
Joseph J Nocera
Christopher J Kyle
spellingShingle Yessica Rico
James Morris-Pocock
Joanna Zigouris
Joseph J Nocera
Christopher J Kyle
Lack of Spatial Immunogenetic Structure among Wolverine (Gulo gulo) Populations Suggestive of Broad Scale Balancing Selection.
PLoS ONE
author_facet Yessica Rico
James Morris-Pocock
Joanna Zigouris
Joseph J Nocera
Christopher J Kyle
author_sort Yessica Rico
title Lack of Spatial Immunogenetic Structure among Wolverine (Gulo gulo) Populations Suggestive of Broad Scale Balancing Selection.
title_short Lack of Spatial Immunogenetic Structure among Wolverine (Gulo gulo) Populations Suggestive of Broad Scale Balancing Selection.
title_full Lack of Spatial Immunogenetic Structure among Wolverine (Gulo gulo) Populations Suggestive of Broad Scale Balancing Selection.
title_fullStr Lack of Spatial Immunogenetic Structure among Wolverine (Gulo gulo) Populations Suggestive of Broad Scale Balancing Selection.
title_full_unstemmed Lack of Spatial Immunogenetic Structure among Wolverine (Gulo gulo) Populations Suggestive of Broad Scale Balancing Selection.
title_sort lack of spatial immunogenetic structure among wolverine (gulo gulo) populations suggestive of broad scale balancing selection.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2015-01-01
description Elucidating the adaptive genetic potential of wildlife populations to environmental selective pressures is fundamental for species conservation. Genes of the major histocompatibility complex (MHC) are highly polymorphic, and play a key role in the adaptive immune response against pathogens. MHC polymorphism has been linked to balancing selection or heterogeneous selection promoting local adaptation. However, spatial patterns of MHC polymorphism are also influenced by gene flow and drift. Wolverines are highly vagile, inhabiting varied ecoregions that include boreal forest, taiga, tundra, and high alpine ecosystems. Here, we investigated the immunogenetic variation of wolverines in Canada as a surrogate for identifying local adaptation by contrasting the genetic structure at MHC relative to the structure at 11 neutral microsatellites to account for gene flow and drift. Evidence of historical positive selection was detected at MHC using maximum likelihood codon-based methods. Bayesian and multivariate cluster analyses revealed weaker population genetic differentiation at MHC relative to the increasing microsatellite genetic structure towards the eastern wolverine distribution. Mantel correlations of MHC against geographical distances showed no pattern of isolation by distance (IBD: r = -0.03, p = 0.9), whereas for microsatellites we found a relatively strong and significant IBD (r = 0.54, p = 0.01). Moreover, we found a significant correlation between microsatellite allelic richness and the mean number of MHC alleles, but we did not observe low MHC diversity in small populations. Overall these results suggest that MHC polymorphism has been influenced primarily by balancing selection and to a lesser extent by neutral processes such as genetic drift, with no clear evidence for local adaptation. This study contributes to our understanding of how vulnerable populations of wolverines may respond to selective pressures across their range.
url https://doi.org/10.1371/journal.pone.0140170
work_keys_str_mv AT yessicarico lackofspatialimmunogeneticstructureamongwolverinegulogulopopulationssuggestiveofbroadscalebalancingselection
AT jamesmorrispocock lackofspatialimmunogeneticstructureamongwolverinegulogulopopulationssuggestiveofbroadscalebalancingselection
AT joannazigouris lackofspatialimmunogeneticstructureamongwolverinegulogulopopulationssuggestiveofbroadscalebalancingselection
AT josephjnocera lackofspatialimmunogeneticstructureamongwolverinegulogulopopulationssuggestiveofbroadscalebalancingselection
AT christopherjkyle lackofspatialimmunogeneticstructureamongwolverinegulogulopopulationssuggestiveofbroadscalebalancingselection
_version_ 1714824764095201280