Factors shaping major histocompatibility complex diversity in an Australian dragon lizard

Author: Jessica Hacking

Hacking, Jessica, 2018 Factors shaping major histocompatibility complex diversity in an Australian dragon lizard, Flinders University, School of Biological Sciences

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The major histocompatibility complex (MHC) is a multigene family involved in pathogen recognition and immune response, and is one of the most diverse regions of the vertebrate genome. MHC genes encode cell surface glycoproteins that present self- and pathogen-derived peptides from a peptide binding region to circulating T-lymphocyte cells. Different MHC molecules bind to their own specific range of peptides. Hence, a population with high MHC diversity is less likely to be overcome by a particular pathogen.

The first aim of my thesis was to characterise the MHC in an Australian agamid, the tawny dragon lizard (Ctenophorus decresii), and investigate the mechanisms generating MHC polymorphism in Iguanian lizards. Six full-length C. decresii MHC class I transcripts were identified and were validated as likely to encode classical MHC molecules. Two partial transcripts were also identified and may represent non-classical MHC class I molecules, although truncation due to transcriptome assembly restrictions is more likely. I found evidence for both birth-and-death and concerted evolution generating MHC diversity within Iguanian lizards.

I used family group data to aid MHC genotyping, explore MHC allele segregation patterns and identify mechanisms maintaining MHC diversity (including MHC-associated mating). To obtain family group data I undertook a captive hatching program for a Flinders Ranges population of C. decresii. The second aim of my thesis was to determine the genetic mating system employed by C. decresii. A predominantly polygynous genetic mating system with a very low rate of multiple paternity was observed (4%), representing one of the lowest rates among squamates.

The third aim of my thesis was to describe polymorphism for previously characterised C. decresii MHC class I transcripts. I genotyped individuals across five populations at the MHC using a recently developed clustering method, which was aided by the analysis of family group data. This method allowed in-depth analysis of type I and II genotyping error rates. Varying numbers of alleles were observed among individuals within populations, and together with allele segregation patterns within family groups, suggested allele dropout and/or natural copy number variation. Sites under selection were identified, allowing the identification of putative peptide binding sites. High allele sharing among populations and low allelic diversity in an island population was uncovered.

Finally, the fourth aim of my thesis was to examine the mechanisms maintaining MHC class I diversity within a C. decresii population; specifically, sexual selection and parasite-mediated selection. I performed model selection analyses and discovered that parasite load was significantly lower in the presence of a specific MHC allele functional group (supertype), indicating that this supertype confers resistance. Furthermore, I uncovered trends suggesting that sexual selection may also play a role in maintaining MHC diversity through MHC-associated mating.

Overall, I was successful in identifying the factors influencing MHC class I diversity within an agamid lizard and addressed broad evolutionary ecology questions. The work presented in this thesis significantly broadens knowledge on squamate MHC class I genes. Future work includes investigating population differentiation using MHC markers and identifying the mechanisms operating to maintain MHC diversity among populations.

Keywords: major histocompatibility complex (MHC), Agamidae, gene characterisation, genetic mating system, genotyping, parasite-mediated selection, sexual selection

Subject: Biological Sciences thesis

Thesis type: Doctor of Philosophy
Completed: 2018
School: School of Biological Sciences
Supervisor: Michael Gardner