Investigating the evolutionary impact of the teleost genome duplication through comparative genomics and phylogenetic analysis of homeobox genes in the Osteoglossomorpha

Martin, K

Abstract:: Multiple rounds of whole genome duplication (WGD) have played a pivotal role in the expansion, elaboration, and evolutionary diversification of vertebrate genomes. In addition to sharing two rounds of whole genome duplication with all other vertebrates, a teleost-specific genome duplication (TGD) occurred in the stem of the teleost lineage ∼350 million years ago (MYA) and is thus a genomic synapomorphy shared by all ∼26,000 extant species. The TGD has variously been i...
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APA Style

Martin, K. (2016). Investigating the evolutionary impact of the teleost genome duplication through comparative genomics and phylogenetic analysis of homeobox genes in the Osteoglossomorpha [PhD thesis]. University of Oxford.

MLA Style

Martin, K. Investigating the Evolutionary Impact of the Teleost Genome Duplication through Comparative Genomics and Phylogenetic Analysis of Homeobox Genes in the Osteoglossomorpha. 2016. University of Oxford, PhD thesis.

Chicago Style

Martin, K. 2016. “Investigating the Evolutionary Impact of the Teleost Genome Duplication through Comparative Genomics and Phylogenetic Analysis of Homeobox Genes in the Osteoglossomorpha.” PhD thesis, University of Oxford.
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Files:: KMARTIN_THESIS_MINOR_CORRECTIONS_HILARY2016.pdf

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Authors

+ Martin, K More by this author

Division:: MPLS
Department:: Zoology
Role:: Author

Contributors

+ Holland, PWH

Role:: Supervisor

+ Natural Sciences and Engineering Research Council of Canada More from this funder

Funding agency for:: Martin, K
Grant:: PGS-D award to Kyle J Martin

+ European Research Council More from this funder

Grant:: FP7/2007-2013/ERC grant 268513

DOI:: 10.5287/ora-rjj5b1wwb
Type of award:: DPhil
Level of award:: Doctoral
Awarding institution:: University of Oxford

Language:: English
Keywords:: Homeobox

Teleost

Genome Duplication

Evo-Devo

Homology

Phylogenetics
Subjects:: Genomics

Evolution (Biology)
UUID:: uuid:7c2df1c9-0aa6-4a63-a38b-757b3f12f664
Deposit date:: 2017-03-29
ARK identifier:: ark:/29072/ora_7c2df1c90aa64a63a38b757b3f12f664

Related item:: Enigmatic Orthology Relationships between Hox Clusters of the African Butterfly Fish and Other Teleosts Following Ancient Whole-Genome Duplication
Description:: Numerous ancient whole-genome duplications (WGD) have occurred during eukaryote evolution. In vertebrates, duplicated developmental genes and their functional divergence have had important consequences for morphological evolution. Although two vertebrate WGD events (1R/2R) occurred over 525 Ma, we have focused on the more recent 3R or TGD (teleost genome duplication) event which occurred approximately 350 Ma in a common ancestor of over 26,000 species of teleost fishes. Through a combination of whole genome and bacterial artificial chromosome clone sequencing we characterized all Hox gene clusters of Pantodon buchholzi, a member of the early branching teleost subdivision Osteoglossomorpha. We find 45 Hox genes organized in only five clusters indicating that Pantodon has suffered more Hox cluster loss than other known species. Despite strong evidence for homology of the five Pantodon clusters to the four canonical pre-TGD vertebrate clusters (one HoxA, two HoxB, one HoxC, and one HoxD), we were unable to confidently resolve 1:1 orthology relationships between four of the Pantodon clusters and the eight post-TGD clusters of other teleosts. Phylogenetic analysis revealed that many Pantodon genes segregate outside the conventional “a” and “b” post-TGD orthology groups, that extensive topological incongruence exists between genes physically linked on a single cluster, and that signal divergence causes ambivalence in assigning 1:1 orthology in concatenated Hox cluster analyses. Out of several possible explanations for this phenomenon we favor a model which keeps with the prevailing view of a single TGD prior to teleost radiation, but which also considers the timing of diploidization after duplication, relative to speciation events. We suggest that although the duplicated hoxa clusters diploidized prior to divergence of osteoglossomorphs, the duplicated hoxb, hoxc, and hoxd clusters concluded diploidization independently in osteoglossomorphs and other teleosts. We use the term “tetralogy” to describe the homology relationship which exists between duplicated sequences which originate through a shared WGD, but which diploidize into distinct paralogs from a common allelic pool independently in two lineages following speciation.
Related item:: Diversification of Hox Gene Clusters in Osteoglossomorph Fish in Comparison to Other Teleosts and the Spotted Gar Outgroup
Description:: An ancient genome duplication (TGD or 3R) occurred in teleost fish after divergence from the lineage leading to gar. This genome duplication is shared by the three extant teleost lineages: Osteoglossomorpha (bony-tongues), Elopomorpha (eels and tarpons), and Clupeocephala (a large clade including salmon, carp, medaka, zebrafish, cichlids, pufferfish, stickleback, and ∼26,000 other species). After TGD, different clupeocephalan species retained different gene duplicates; this is seen clearly in Hox gene clusters but extends to all genes. Since divergent resolution of TGD paralogs is a potential driving force for speciation, it is possible this contributed to diversification of this clade. The extent to which divergent resolution of TGD paralogs occurred within Osteoglossomorpha has not been investigated in detail, and Hox cluster organization has been reported for just two species: Pantodon buchholzi (Pantodontidae) and Scleropages formosus (Osteoglossidae). We applied survey-scale genome sequencing and de novo assembly to three further osteoglossomorph taxa: Osteoglossum bicirrhosum (Osteoglossidae), Chitala ornata (Notopteridae), and Gnathonemus petersii (Mormyridae). We find that each retained more Hox genes than clupeocephalan taxa (excluding those that underwent additional genome duplication), but fewer than eels. Several Hox genes are missing in all teleosts, including duplicates of two Hox genes present in the slow evolving pre-TGD genome of the spotted gar. We find divergent resolution through individual gene losses, and whole cluster losses have been rampant across osteoglossomorphs, despite their extant species paucity. We suggest that reciprocal gene loss following TGD was probably insufficient to drive the exceptional diversification of teleosts.

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Thesis

Investigating the evolutionary impact of the teleost genome duplication through comparative genomics and phylogenetic analysis of homeobox genes in the Osteoglossomorpha

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Investigating the evolutionary impact of the teleost genome duplication through comparative genomics and phylogenetic analysis of homeobox genes in the Osteoglossomorpha

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