Development, Anatomy, and Phylogenetic Relationships of Jawless Vertebrates and Tests of Hypotheses about Early Vertebrate Evolution

• Author / Creator

  Miyashita, Tetsuto

• The origin and early evolution of vertebrates remain one of the central questions of comparative biology. This clade, which features a breathtaking diversity of complex forms, has generated profound, unresolved questions, including: How are major lineages of vertebrates related to one another? What suite of characters existed in the last common ancestor of all living vertebrates? Does information from seemingly ‘primitive’ groups — jawless vertebrates, cartilaginous fishes, or even invertebrate outgroups — inform us about evolutionary transitions to novel morphologies like the neural crest or jaw? Alfred Romer once likened a search for the elusive vertebrate archetype to a study of the Apocalypse: “That way leads to madness.” I attempt to address these questions using extinct and extant cyclostomes (hagfish, lampreys, and their kin). As the sole living lineage of jawless vertebrates, cyclostomes diverged during the earliest phases of vertebrate evolution. However, precise relationships and evolutionary scenarios remain highly controversial, due to their poor fossil record and specialized morphology. Through a comparative analysis of embryos, I identified significant developmental similarities and differences between hagfish and lampreys, and delineated specific problems to be explored. I attacked the first problem — whether cyclostomes form a clade or represent a grade — in a description and phylogenetic analyses of a new, nearly complete fossil hagfish from the Cenomanian of Lebanon. Aided by a detailed analysis of morphological characters, new phylogenetic trees recovered cyclostomes as a clade. This is the first morphological phylogeny to yield cyclostomes as monophyletic and therefore helps reconcile a major point of conflict between morphology- and molecule-based phylogenetics. I tested the second problem — the assumption that living lampreys pass through a filter-feeding larval stage resembling ancestors of vertebrates — using a growth series of a fossil lamprey from the Late Devonian of South Africa. Surprisingly, these fossil lamprey larvae bear little morphological resemblance to larvae of living lampreys. Instead, the growth series reveals ontogenetic transition of traits that are consistent with the predatory habit of modern lamprey adults. Through comparison to other Paleozoic stem lampreys, I suggest that the filter-feeding larval stage evolved independently within vertebrates. Under this new scenario, larvae of living lampreys are a poor model with which to reconstruct primitive vertebrate characters. For the third problem — how biting jaws evolved in vertebrates — I focused on one key feature of the jaw apparatus: the jaw joint. Using gene expression profiles and gene knockouts in lamprey and zebrafish embryos, I tested three hypotheses proposed to explain the origin of the jaw joint. Preliminary results suggest that a jaw joint may originate from a blood sinus pinched between two cartilages, or from a type of immature cartilaginous tissue. I describe a new genetic line of zebrafish that carries a mutation in the homeodomain-coding sequence of nkx3.2 — a jaw joint marker gene. Homozygous mutants have fused upper and lower jaw cartilages, replicating nkx3.2 morphants. At the adult stage, the mutants developed craniofacial phenotypes that resemble some of the jawless stem gnathostomes. Finally, I propose an analytical pipeline to address a number of remaining questions in early vertebrate phylogeny: supertrees as a platform for future modular analyses of morphological characters. By sorting individual characters by different biological attributes, I hope to illustrate a view on early vertebrate evolution through understanding the dynamics of character evolution.

• Subjects / Keywords

  • Vertebrates
  • Development
  • Evolution

• Graduation date

  Spring 2018

• Type of Item

  Thesis

• Degree

  Doctor of Philosophy

• DOI

  https://doi.org/10.7939/R3V40KF1B

• License

  This thesis is made available by the University of Alberta Libraries with permission of the copyright owner solely for non-commercial purposes. This thesis, or any portion thereof, may not otherwise be copied or reproduced without the written consent of the copyright owner, except to the extent permitted by Canadian copyright law.