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MHC diversity and expression in a songbird : Temporal and transgenerational variation

Mellinger, Samantha LU (2023)
Abstract
The immune system is of central importance to clear-off pathogens in order to keep an organism healthy. In vertebrates, the Major Histocompatibility Complex (MHC) is a genomic region that holds key genes involved in adaptive immunity and in particular in the antigen presenting process. The presentation relies on MHC class I (MHC-I) and MHC class II (MHC-II) molecules that are encoded by MHC-I and MHC-II genes, respectively. In passerine birds (songbirds; order Passeriformes), high MHC-I and MHC-IIB diversity (i.e., number of MHC alleles in an individual) has been reported compared to other avian orders. Each MHC molecule can present a limited number of antigens, therefore high MHC diversity could potentially be an advantage for presenting... (More)
The immune system is of central importance to clear-off pathogens in order to keep an organism healthy. In vertebrates, the Major Histocompatibility Complex (MHC) is a genomic region that holds key genes involved in adaptive immunity and in particular in the antigen presenting process. The presentation relies on MHC class I (MHC-I) and MHC class II (MHC-II) molecules that are encoded by MHC-I and MHC-II genes, respectively. In passerine birds (songbirds; order Passeriformes), high MHC-I and MHC-IIB diversity (i.e., number of MHC alleles in an individual) has been reported compared to other avian orders. Each MHC molecule can present a limited number of antigens, therefore high MHC diversity could potentially be an advantage for presenting various antigens from different pathogens. My aim was to gain a deeper understanding on what mechanisms have led to high MHC diversity in passerines, how much of this MHC diversity is expressed and whether it varies in time and across generation. In this thesis, I mainly focused on a particular passerine, the great reed warbler (GRW; Acrocephalus arundinaceus) for which high MHC diversity has been previously described. In chapter I, the MHC genomic region was characterized in the GRW and also in three additional passerine species from which long-read genome assemblies were available. The MHC region is extended in Passeriformes and the MHC diversity in the GRW has expanded through repeated and multiple gene duplication events of single and trios of MHC genes; these MHC paralogs are likely to have evolved under the birth-and death model process. In chapter II, I wanted to assess the correctness of the estimated haploid MHC diversity found in the GRW genome and to compare the resolution between the estimated diploid MHC diversity found with long- and short-read sequencing techniques. The haplotype resolution was improved using short-read amplicons and I found that two MHC-IIB scaffolds holding tandemly duplicated genes were most likely complementary haplotypes. In the last two chapters, I wanted to investigate the functional relevance of the MHC-I diversity in the GRW by looking at gene expression in individuals from our long-term monitored study population breeding at Lake Kvismaren in Sweden. I found that 71% of the MHC-I diversity is expressed in the GRW but the different MHC-I alleles are expressed at different levels with generally only one to two alleles being highly expressed in each individual. Therefore, I investigated temporal variation in MHC-I relative expression (chapter III) in individuals sampled both as nestlings and as breeding adults at our study site. I found that MHC-I relative expression in blood is highly stable throughout an individual lifetime. In chapter IV, I investigated transgenerational variation in MHC-I relative expression in 17 families. MHC-I relative expression in haplotypes in offspring is to a large extent genetically inherited from their parents and does not change with offspring age. I found a stronger relationship between mothers and offspring suggesting a maternal effect, but I have not found any epistasis effect. To conclude, a high proportion of the MHC diversity is expressed in the great reed warbler but only a small fraction is highly expressed. Additionally, MHC-I expression does not vary over time and is to a large extent inherited. (Less)
Please use this url to cite or link to this publication:
author
supervisor
opponent
  • Professor Lenz, Tobias, University of Hamburg, Germany
organization
publishing date
type
Thesis
publication status
published
subject
keywords
MHC diversity, MHC-I gene expression, songbirds, genome assembly, amplicon HTS, temporal variation, family data, great reed warbler (Acrocephalus arundinaceus)
pages
190 pages
publisher
Lund University
defense location
Blå hallen, Ekologihuset.
defense date
2023-09-29 09:30:00
ISBN
978-91-8039-766-7
978-91-8039-765-0
language
English
LU publication?
yes
id
8ef3d4c8-d534-4b9e-b15c-4c0d4b268bf8
date added to LUP
2023-09-05 12:10:19
date last changed
2023-09-07 07:29:59
@phdthesis{8ef3d4c8-d534-4b9e-b15c-4c0d4b268bf8,
  abstract     = {{The immune system is of central importance to clear-off pathogens in order to keep an organism healthy. In vertebrates, the Major Histocompatibility Complex (MHC) is a genomic region that holds key genes involved in adaptive immunity and in particular in the antigen presenting process. The presentation relies on MHC class I (MHC-I) and MHC class II (MHC-II) molecules that are encoded by MHC-I and MHC-II genes, respectively. In passerine birds (songbirds; order Passeriformes), high MHC-I and MHC-IIB diversity (i.e., number of MHC alleles in an individual) has been reported compared to other avian orders. Each MHC molecule can present a limited number of antigens, therefore high MHC diversity could potentially be an advantage for presenting various antigens from different pathogens. My aim was to gain a deeper understanding on what mechanisms have led to high MHC diversity in passerines, how much of this MHC diversity is expressed and whether it varies in time and across generation. In this thesis, I mainly focused on a particular passerine, the great reed warbler (GRW; Acrocephalus arundinaceus) for which high MHC diversity has been previously described. In chapter I, the MHC genomic region was characterized in the GRW and also in three additional passerine species from which long-read genome assemblies were available. The MHC region is extended in Passeriformes and the MHC diversity in the GRW has expanded through repeated and multiple gene duplication events of single and trios of MHC genes; these MHC paralogs are likely to have evolved under the birth-and death model process. In chapter II, I wanted to assess the correctness of the estimated haploid MHC diversity found in the GRW genome and to compare the resolution between the estimated diploid MHC diversity found with long- and short-read sequencing techniques. The haplotype resolution was improved using short-read amplicons and I found that two MHC-IIB scaffolds holding tandemly duplicated genes were most likely complementary haplotypes. In the last two chapters, I wanted to investigate the functional relevance of the MHC-I diversity in the GRW by looking at gene expression in individuals from our long-term monitored study population breeding at Lake Kvismaren in Sweden. I found that 71% of the MHC-I diversity is expressed in the GRW but the different MHC-I alleles are expressed at different levels with generally only one to two alleles being highly expressed in each individual. Therefore, I investigated temporal variation in MHC-I relative expression (chapter III) in individuals sampled both as nestlings and as breeding adults at our study site. I found that MHC-I relative expression in blood is highly stable throughout an individual lifetime. In chapter IV, I investigated transgenerational variation in MHC-I relative expression in 17 families. MHC-I relative expression in haplotypes in offspring is to a large extent genetically inherited from their parents and does not change with offspring age. I found a stronger relationship between mothers and offspring suggesting a maternal effect, but I have not found any epistasis effect. To conclude, a high proportion of the MHC diversity is expressed in the great reed warbler but only a small fraction is highly expressed. Additionally, MHC-I expression does not vary over time and is to a large extent inherited.}},
  author       = {{Mellinger, Samantha}},
  isbn         = {{978-91-8039-766-7}},
  keywords     = {{MHC diversity; MHC-I gene expression; songbirds; genome assembly; amplicon HTS; temporal variation; family data; great reed warbler (Acrocephalus arundinaceus)}},
  language     = {{eng}},
  month        = {{09}},
  publisher    = {{Lund University}},
  school       = {{Lund University}},
  title        = {{MHC diversity and expression in a songbird : Temporal and transgenerational variation}},
  url          = {{https://lup.lub.lu.se/search/files/157328011/Thesis_Samantha_Mellinger_without_papers.pdf}},
  year         = {{2023}},
}