Complex Genomic Regions Under Selection in Atlantic Herring Resolved by Long-Read Sequencing

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dc.contributor.advisorAndersson, Leif
dc.contributor.committeeMemberCriscitiello, Michael
dc.contributor.committeeMemberKatju, Vaishali
dc.contributor.committeeMemberDavis, Brian W
dc.creatorJamsandekar, Minal Shrikant
dc.date.accessioned2024-07-30T23:01:20Z
dc.date.created2023-12
dc.date.issued2023-12-12
dc.date.submittedDecember 2023
dc.date.updated2024-07-30T23:01:21Z
dc.description.abstractEvolutionary genomic studies in non-model organisms are usually based on a limited number of genetic markers or short-read whole-genome sequencing (WGS) and a single reference assembly. These methods prevent us from exploring more complex regions of the genome and have also led to misinterpretation of results. Now with the recent progress in long-read sequencing technology, it is possible to study such regions in more detail and get a full account of their evolutionary role. This thesis has utilized the advancements in long-read sequencing to resolve some of the complex genomic regions under selection in Atlantic herring. Atlantic herring is one of the most abundant vertebrates on earth with a huge population size (Ne = 4.4x10^5 and Nc > 10^10), migratory behavior, adaptation to various ecological conditions, and minute genetic drift, thus an ideal model for population genomic studies. Our study based on pooled WGS of more than 50 population samples identified hundreds of loci showing highly significant genetic differentiation between populations across its species distribution. These loci underlie adaptation to various ecological conditions such as variation in salinity, spawning time, and water temperature. The genetic markers discovered in this study can be used to develop tools for stock assignments and monitor changes in allele frequencies at the loci under selection. The large shifts in allele frequencies (sometimes approaching fixation) are a deviation from Fisher’s infinitesimal model for polygenic variation that predicts that selection should not result in any large allele frequency changes because each locus has an infinitesimal small effect on phenotype. Four of the loci under selection were large chromosomal inversions that differentiated populations from the southern and northern part of the species distribution, which differ in water temperature. Inversions were first described 1913 but how they originate and evolve remains elusive due to a lack of molecular tools to study them. Our study sheds new light on their evolution as we discovered that they were formed via ectopic recombination between inverted duplicates and have been maintained under some form of balancing selection for more than 1 MY. Owing to their old age and the huge population size of Atlantic herring, these inversion polymorphisms show recombination between haplotypes and have not accumulated a mutation load. One of the major foci of this thesis is on the immune system genes. The migratory behavior and huge population size of Atlantic herring is expected to render them an attractive target for pathogens. To combat the pathogen pressure, the immune system of a species has to rapidly adapt to this threat. The Major Histocompatibility Complex (MHC) genes constitute an essential component of the vertebrate immune system. MHC genes are the most polymorphic genes in the vertebrate genome and show both high sequence diversity and multiple copies of closely related genes. Our long-read data on 29 haplotypes from different populations allowed us to characterize MHC class II genes in great detail. MHC class II genes in Atlantic herring maintain extensive genetic diversity at various levels such as high number of genes, high allelic diversity, non-random association between alpha-beta gene pairs, and non-random association between supertypes on a haplotype. Such immense MHC diversity has not been reported in any fish species before. A genome comparison of Atlantic and Pacific herring revealed that genomic regions harboring genes from the immune system are characterized by high nucleotide diversity within populations and copy number variation. The use of long-read sequencing in this thesis has contributed significantly to the characterization of the regions under strong selection in Atlantic herring.
dc.format.mimetypeapplication/pdf
dc.identifier.urihttps://hdl.handle.net/1969.1/203063
dc.language.isoen
dc.subjectAtlantic herring
dc.subjectecological adaptation
dc.subjectfishery
dc.subjectimmune system
dc.subjectinversion
dc.subjectlong-read
dc.subjectMHC
dc.subjectnatural selection
dc.subjectwhole genome sequencing
dc.titleComplex Genomic Regions Under Selection in Atlantic Herring Resolved by Long-Read Sequencing
dc.typeThesis
dc.type.materialtext
local.embargo.lift2025-12-01
local.embargo.terms2025-12-01
local.etdauthor.orcid0000-0001-8678-9329
thesis.degree.departmentVeterinary Integrative Biosciences
thesis.degree.disciplineBiomedical Sciences
thesis.degree.grantorTexas A&M University
thesis.degree.levelDoctoral
thesis.degree.nameDoctor of Philosophy

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