University of Illinois Urbana-Champaign

Comparative and population genomics of secondarily temperate Paranotothenia angustata, New Zealand black cod

Rayamajhi, Niraj

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RAYAMAJHI-DISSERTATION-2024.pdf

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https://hdl.handle.net/2142/124358

Description

Title
Comparative and population genomics of secondarily temperate Paranotothenia angustata, New Zealand black cod
Author(s)
Rayamajhi, Niraj
Issue Date
2024-04-23
Director of Research (if dissertation) or Advisor (if thesis)
Catchen, Julian M
Doctoral Committee Chair(s)
Catchen, Julian M
Committee Member(s)
  • Cheng, Chi-Hing Christina
  • Fuller, Rebecca
  • Suarez, Andrew
Department of Study
Evolution Ecology Behavior
Discipline
Biology
Degree Granting Institution
University of Illinois at Urbana-Champaign
Degree Name
Ph.D.
Degree Level
Dissertation
Keyword(s)
  • notothenioids
  • RADseq
  • genome assembly
  • genomics
Abstract
Notothenioids are a group of teleost fish that have undergone at least two thermal transitions in their evolutionary history. Due to paleo-geological, -climatic, and -oceanographic changes, the environment of Antarctica transitioned from temperate to cold. Antifreeze glycoproteins became a key evolutionary innovation that enabled a group of temperate, bottom-dwelling notothenioids to adapt to increasingly cold waters. With the availability of vacant ecological niches, the cold-resistant notothenioids diversified over evolutionary time. Most of these derived lineages became cold-specialized (e.g., Trematomus borchgrevinki). Remarkably, a few of them readapted to a warmer environment, becoming secondarily temperate (e.g., Paranotothenia angustata); however, the genetic architecture of readaptation for these organisms remains largely unknown. In this dissertation, my first goal was to identify the optimal de novo genome assembly strategy for notothenioids, as robust assembly is required for genome-based projects (Chapter 2). I evaluated Illumina-, Nanopore-, and PacBio-based genome assembly strategies with T. borchgrevinki. My results suggest that the strategy based on long-reads only is the current best approach and can be optimized through a subsampling method. My results indicate that short-reads only and hybrid (short- and long-reads) based strategies produce low quality assemblies. My second goal was to identify genomic features associated with secondarily temperate adaptations of P. angustata (Chapter 3). My results suggest that I have produced high quality chromosome-level assemblies for P. angustata (a focal species) and T. borchgrevinki (an outgroup). They also indicate that the genome of P. angustata consists of lineage-specific DNA transposons, chromosomal fusion patterns, inversions (most of which co-localized with one to three protein-coding genes having signals of accelerated molecular evolution), and translocations. This line of evidence calls for a detailed future investigation on the role of lineage-specific repeats and chromosomal rearrangements in non-polar adaptations of P. angustata. Based on results related to the P. angustata-specific signatures of positive selection, I propose that genes under selection, mainly associated with protein chaperoning, circadian rhythm, vision, erythrocyte differentiation and development, heme metabolism, mitochondria, and ribosomes, may have contributed to the adaptations of P. angustata in a temperate environment. My third goal was to infer timing of origin of the P. angustata-specific adaptive loci (Chapter 4). I assessed genome-wide gene genealogical patterns from Restriction site-Associated DNA sequencing (RADseq)-based loci at homologous regions between P. angustata and T. borchgrevinki, as well as between McMurdo Station and Prydz Bay populations of T. borchgrevinki. Additionally, I estimated the time to the most recent common ancestor (TMRCA) of alleles across RAD-loci within and between species and populations. I was unable to find distinct local signatures of positive selection because most of the gene trees had reciprocally monophyletic patterns (i.e., haplotypes from one species clustered to the exclusion of haplotypes from the other species, resulting in a monophyletic clade per species). However, some genealogical trees with reciprocally monophyletic patterns were also located within a) 92 candidates (from a group of 317 genes exhibiting accelerated molecular evolution in P. angustata) and b) structural variations (specific to P. angustata) which were presented in Chapter 3. Additionally, the average time to the most recent common ancestor (TMRCA) of alleles between species appears to be lower than the time required for a genome-wide reciprocally monophyletic pattern to form under neutrality. These results are consistent with the idea that divergent selection contributed to the observed reciprocally monophyletic patterns. Moreover, I did not find distinct local peaks of inter-species TMRCA, suggesting that adaptations of P. angustata evolved after the divergence of the ancestral lineages of P. angusta and T. borchgrevinki. While one intra-species TMRCA outlier was found within the P. angustata-specific inversion, none were within the candidate loci. Also, intra-species TMRCA distributions within and outside of candidates (317 genes exhibiting accelerated molecular evolution) showed no significant difference, similar to those within and outside structural variations. These results further support a substantial contribution of de novo mutations in P. angustata’s temperate adaptations. Apart from these findings, I found incomplete lineage sorting between two populations of T. borchgrevinki (one from McMurdo Station and another from Prydz Bay). This result indicates high gene flow and no geography-specific selection between the populations. I found intra-species TMRCA outliers within two translocations specific to T. borchgrevinki (mentioned in Chapter 3). These results call for future investigation into the role of structural changes in the continuing cold adaptation of T. borchgrevinki. Overall, my results provide an overview of how and when the secondarily temperate adaptations of P. angustata may have evolved and provide genomic resources for future comparative and population genomic analyses in non-polar and polar notothenioids.
Graduation Semester
2024-05
Type of Resource
Thesis
Handle URL
https://hdl.handle.net/2142/124358
Copyright and License Information
Copyright 2024 Niraj Rayamajhi

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