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European Black Grouse: MHC Genetic Diversity and Population Structure
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Ecology and Genetics, Population and Conservation Biology. (Jacob Höglund)
2011 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Black grouse Tetrao tetrix is a bird species composed of large, continuous as well as severely reduced and fragmented populations, making it an optimal species to investigate how genetic diversity is affected by habitat fragmentation. I have focused on genetic diversity in the Major Histocompatibility Complex (MHC) to measure the ability of the black grouse to respond to environmental changes.

I partly characterized MHC class II in black grouse and found striking similarities with chicken MHC class II. I demonstrated that black grouse possess a similar compact MHC as chicken with few MHC class II B (BLB) and Y (YLB) loci. I did not find evidence of balancing selection in YLB so I concentrated further studies on BLB.

I developed a PCR-based screening method for amplifying and separating expressed BLB alleles in European black grouse populations. Small fragmented populations had lost neutral genetic diversity (based on microsatellites and SNPs) compared to samples from the historical distribution and contemporary large populations. There was also a trend, albeit less pronounced, for reduced MHC diversity in these populations. Neutral markers in small isolated populations were affected by increased levels of genetic drift and were therefore genetically differentiated compared to other populations. MHC markers on the other hand, were not subjected to genetic drift to the same extent probably due a long historic process of balancing selection.

Inferences of heterozygosity and evolutionary patterns as well as detailed correlations to reproductive success and diseases cannot be performed until MHC can be amplified in a locus-specific manner. Therefore, I developed a single locus sequence-based typing method for independently amplifying MHC class II B loci (BLB1 and BLB2). I found that BLB1 and BLB2 were duplicated in a common ancestor to chickens and black grouse and that these loci are subjected to homogenizing concerted evolution due to inter-genetic exchange between loci after species divergence.  I could also verify that both BLB1 and BLB2 were transcribed in black grouse and under balancing selection.

This collection of work has significance for future conservation of black grouse as well as research and management of zoonotic diseases.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis , 2011. , p. 59
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 869
Keywords [en]
Major Histocompatibility Complex, BLB, balancing selection, concerted evolution, bottleneck, fragmentation, 3'UTR
National Category
Evolutionary Biology Ecology Genetics
Research subject
Biology with specialization in Population Biology
Identifiers
URN: urn:nbn:se:uu:diva-160042ISBN: 978-91-554-8188-9 (print)OAI: oai:DiVA.org:uu-160042DiVA, id: diva2:447876
Public defence
2011-11-25, Zootissalen, Evolutionary Biology Centre, Villavägen 9, Uppsala, 09:15 (English)
Opponent
Supervisors
Available from: 2011-11-04 Created: 2011-10-13 Last updated: 2011-11-10Bibliographically approved
List of papers
1. The MHC class II of the Black grouse (Tetrao tetrix) consists of low numbers of B and Y genes with variable diversity and expression
Open this publication in new window or tab >>The MHC class II of the Black grouse (Tetrao tetrix) consists of low numbers of B and Y genes with variable diversity and expression
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2007 (English)In: Immunogenetics, ISSN 0093-7711, E-ISSN 1432-1211, Vol. 59, no 9, p. 725-734Article in journal (Refereed) Published
Abstract [en]

We found that the Black grouse (Tetrao tetrix) possess low numbers of Mhc class II B (BLB) and Y (YLB) genes with variable diversity and expression. We have therefore shown, for the first time, that another bird species (in this case, a wild lek-breeding galliform) shares several features of the simple Mhc of the domestic chicken (Gallus gallus). The Black grouse BLB genes showed the same level of polymorphism that has been reported in chicken, and we also found indications of balancing selection in the peptide-binding regions. The YLB genes were less variable than the BLB genes, also in accordance with earlier studies in chicken, although their functional significance still remains obscure. We hypothesize that the YLB genes could have been under purifying selection, just as the mammal Mhc-E gene cluster.

Keywords
Mhc class II, YLB, Rfp-Y, BLB, Avian Mhc, Purifying selection
National Category
Evolutionary Biology Genetics
Identifiers
urn:nbn:se:uu:diva-14669 (URN)10.1007/s00251-007-0234-6 (DOI)000249503200004 ()17653538 (PubMedID)
Available from: 2008-01-31 Created: 2008-01-31 Last updated: 2017-12-11Bibliographically approved
2. Genotyping of black grouse MHC class II B using Reference Strand-Mediated Conformational Analysis (RSCA)
Open this publication in new window or tab >>Genotyping of black grouse MHC class II B using Reference Strand-Mediated Conformational Analysis (RSCA)
2011 (English)In: BMC Research Notes, ISSN 1756-0500, E-ISSN 1756-0500, Vol. 4, no 183Article in journal (Refereed) Published
Abstract [en]

Background

The Major Histocompatibility Complex (MHC) is a cluster of genes involved in the vertebrate immune system and includes loci with an extraordinary number of alleles. Due to the complex evolution of MHC genes, alleles from different loci within the same MHC class can be very similar and therefore difficult to assign to separate loci. Consequently, single locus amplification of MHC genes is hard to carry out in species with recently duplicated genes in the same MHC class, and multiple MHC loci have to be genotyped simultaneously. Since amplified alleles have the same length, accurate genotyping is difficult. Reference Strand-Mediated Conformational Analysis (RSCA), which is increasingly used in studies of natural populations with multiple MHC genes, is a genotyping method capable to provide high resolution and accuracy in such cases.

Findings

We adapted the RSCA method to genotype multiple MHC class II B (BLB) genes in black grouse (Tetrao tetrix), a non-model galliform bird species, using a 96-Capillary Array Electrophoresis, the MegaBACE™ 1000 DNA Analysing System (GE Healthcare). In this study we used fluorescently labelled reference strands from both black grouse and hazel grouse and observed good agreement between RSCA and cloning/sequencing since 71 alleles were observed by cloning/sequencing and 76 alleles by RSCA among the 24 individuals included in the comparison. At the individual level however, there was a trend towards more alleles scored with RSCA (1-6 per individual) than cloning/sequencing (1-4 per individual). In 63% of the pair-wise comparison, the identical allele was scored in RSCA as in cloning/sequencing. Nine out of 24 individuals had the same number of alleles in RSCA as in cloning/sequencing. Our RSCA protocol allows a faster RSCA genotyping than presented in many other RSCA studies.

Conclusions

In this study, we have developed the RSCA typing method further to work on a 96-Capillary Array Electrophoresis (MegaBACE™ 1000). Our RSCA protocol can be applied to fast and reliable screening of MHC class II B diversity of black grouse populations. This will facilitate future large-scale population studies of black grouse and other galliformes species with multiple inseparable MHC loci.

National Category
Genetics
Research subject
Population Biology
Identifiers
urn:nbn:se:uu:diva-159185 (URN)10.1186/1756-0500-4-183 (DOI)
Available from: 2011-10-13 Created: 2011-09-23 Last updated: 2017-12-08Bibliographically approved
3. Can balancing selection on MHC loci counteract genetic drift in small fragmented populations of black grouse?
Open this publication in new window or tab >>Can balancing selection on MHC loci counteract genetic drift in small fragmented populations of black grouse?
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2012 (English)In: Ecology and Evolution, ISSN 2045-7758, E-ISSN 2045-7758, Vol. 2, no 2, p. 341-353Article in journal (Refereed) Published
Abstract [en]

The ability of natural populations to adapt to new environmental conditions is crucial for their survival and partly determined by the standing genetic variation in each population. Populations with higher genetic diversity are more likely to contain individuals that are better adapted to new circumstances than populations with lower genetic diversity. Here we use both neutral and MHC markers to test whether small and highly fragmented populations hold lower genetic diversity than large ones. We use black grouse as it is distributed across Europe and found in populations with varying degrees of isolation and size. We sampled eleven different populations; five continuous, three isolated and three small and isolated. We tested patterns of genetic variation in these populations using three different types of genetic markers: nine microsatellites and 21 SNPs (Single Nucleotide Polymorphisms) which both were found to be neutral, and two functional MHC (Major Histocompatibility Complex) genes that are presumably under selection. The small isolated populations displayed significantly lower neutral genetic diversity compared to continuous populations. A similar trend, but not as pronounced, was found for genotypes at MHC class II loci. Populations were less divergent at MHC genes compared to neutral markers. Measures of genetic diversity and population genetic structure were positively correlated among microsatellites and SNPs, but none of them were correlated to MHC when comparing all populations. Our results suggest that balancing selection at MHC loci does not counteract the power of genetic drift when populations get small and fragmented. 

Keywords
Fragmentation; genetic drift; MHC; population isolation; SNP
National Category
Ecology Evolutionary Biology Genetics
Identifiers
urn:nbn:se:uu:diva-160034 (URN)10.1002/ece3.86 (DOI)000312442500006 ()22423328 (PubMedID)
Funder
Swedish Research Council
Available from: 2011-10-13 Created: 2011-10-13 Last updated: 2017-12-08Bibliographically approved
4. Historic and current populations of black grouse in central Europe – evidence for rapid loss of genetic diversity
Open this publication in new window or tab >>Historic and current populations of black grouse in central Europe – evidence for rapid loss of genetic diversity
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2011 (English)Article in journal (Other academic) Submitted
Abstract [en]

Black grouse (Tetrao tetrix) in central Europe have undergone a severe contraction of their range with only a few small isolated remaining populations. We here compare genetic diversity of two contemporary populations (Sallandse Heuvelrug, Netherlands and Lüneburger Heide, Germany) with historic samples from the same range collected decades ago. We use both neutral and MHC markers to test whether present small and highly fragmented populations hold lower genetic diversity compared to the former larger population. For this we applied three different types of genetic markers: nine microsatellites and 21 SNPs (Single Nucleotide Polymorphisms) which both have been found to be neutral, and two functional MHC (Major Histocompatibility Complex) genes that are presumably under selection. The contemporary small isolated populations displayed lower neutral genetic diversity compared to the historic samples. A similar trend was found for genotypes at MHC class II loci. Furthermore, population structure was more pronounced among contemporary populations compared to historic populations for microsatellites and SNPs. This effect was not as distinct for MHC which suggests that MHC has been subjected to balancing selection in the past, a process upholding genetic variation and minimizing population structure for such markers. As predicted from theory, drift is the most potent evolutionary processes affecting genetic variation at small population sizes. Genetic differentiation among present populations highlights the strong affects of population decline and habitat loss due to anthropogenic land use changes on genetic structure of natural populations. 

National Category
Ecology Evolutionary Biology Genetics
Identifiers
urn:nbn:se:uu:diva-160037 (URN)
Available from: 2011-10-13 Created: 2011-10-13 Last updated: 2015-06-24Bibliographically approved
5. Evolutionary history of black grouse BLB1 and BLB2 revealed through single locus sequence-based typing
Open this publication in new window or tab >>Evolutionary history of black grouse BLB1 and BLB2 revealed through single locus sequence-based typing
(English)Manuscript (preprint) (Other academic)
National Category
Evolutionary Biology Genetics
Identifiers
urn:nbn:se:uu:diva-160040 (URN)
Available from: 2011-10-13 Created: 2011-10-13 Last updated: 2011-11-10

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