Using information in taxonomists’ heads to resolve hagfish and lamprey relationships and recapitulate craniate–vertebrate phylogenetic history

Abstract

In 1806, a hypothesis in which hagfishes and lampreys were classified as the taxon Cyclostomi was proposed on the basis of shared morphological traits. That ‘monophyletic cyclostome’ classification prevailed into the twentieth century and has persisted until the present. In 1958, a study involving coordinate grid transformations to analyse head ontogenies for living and fossil craniates was published. Results obtained in that evolutionary–developmental analysis revealed that extant hagfishes and extinct heterostracans developed substantially differently from closely related extant and extinct agnathans and warranted recognition as a distinct lineage. In 1977, a classification in which lampreys and jawed vertebrates formed a group exclusively from hagfishes was proposed on the basis of neontological, morphological and molecular traits. This ‘paraphyletic cyclostome’ classification garnered acceptance among some taxonomists and has persisted alongside the monophyletic cyclostome classification until the present. We applied geometric morphometrics to data obtained from the 1958 evolutionary–developmental analysis, to objectively test and confirm these overlooked and underappreciated results. We demonstrated that the paraphyletic cyclostome classification was conceived at least 19 years earlier than usually acknowledged. Our reanalysis emphasises that the debate on whether the Cyclostomata is monophyletic or paraphyletic must be resolved formally on the basis of principles and practices for phylogenetic systematic analysis including fossil data.

Keywords::

• coordinate grid transformation
• cyclostome classification
• evolutionary developmental biology
• geometric morphometrics
• history of ideas
• systematics

Acknowledgements

This study was developed with financial support from the Canadian Institutes of Health Research (postdoctoral fellowship to JRS), the Natural Sciences and Engineering Research Council of Canada (Discovery Grants 261590 to JRS and A5056 to BKH) and the resources from the Department of Biology, Origins Institute and Shared Hierarchical Academic Research Computing Network at McMaster University. The authors thank D. A. Elliott, anonymous Reviewer 2, D. Cantelmi, T. Domladovac, S. Faheim, W. Mok and M. Zdelar for intellectual assistance, M. G. B. Colangelo for overseeing and B. Pratt and Luz de Lourdes Vasquez Paz for inspiration.