How to tuna fish: constraint, convergence, and integration in the neurocranium of pelagiarian fishes

Andrew Knapp; Gizéh  Rangel-de Lázaro; Matt Friedman; Zerina Johanson; Kory M Evans; Sam Giles; Hermione T. Beckett; Anjali Goswami

doi:10.1093/evolut/qpad056

How to tuna fish: constraint, convergence, and integration in the neurocranium of pelagiarian fishes

Andrew Knapp^*, Gizéh Rangel-de Lázaro, Matt Friedman, Zerina Johanson, Kory M Evans, Sam Giles, Hermione T. Beckett, Anjali Goswami

^*Corresponding author for this work

Geography, Earth and Environmental Sciences

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Abstract

Morphological evolution of the vertebrate skull has been explored across a wide range of tetrapod clades using geometric morphometrics, but the application of these methods to teleost fishes, accounting for roughly half of all vertebrate species, has been limited. Here we present the results of a study investigating 3D morphological evolution of the neurocranium across 114 species of Pelagiaria, a diverse clade of open-ocean teleost fishes that includes tuna and mackerel. Despite showing high shape disparity overall, taxa from all families fall into three distinct morphological clusters. Convergence in shape within clusters is high, and phylogenetic signal in shape data is significant but low. Neurocranium shape is significantly correlated with body elongation and significantly but weakly correlated with size. Diet and habitat depth are weakly correlated with shape, and nonsignificant after accounting for phylogeny. Evolutionary integration in the neurocranium is high, suggesting that convergence in skull shape and the evolution of extreme morphologies are associated with the correlated evolution of neurocranial elements. These results suggest that shape evolution in the pelagiarian neurocranium reflects the extremes in elongation found in body shape but is constrained along relatively few axes of variation, resulting in repeated evolution toward a restricted range of morphologies.

Original language	English
Pages (from-to)	1277-1288
Number of pages	12
Journal	Evolution; international journal of organic evolution
Volume	77
Issue number	6
Early online date	30 Mar 2023
DOIs	https://doi.org/10.1093/evolut/qpad056
Publication status	Published - Jun 2023

Bibliographical note

Acknowledgments:
For access to specimens, we are grateful to James Maclaine, Ollie Crimmen, and Emma Bernard (NHMUK); Peter Rask Möller (NHMD); Peter Bartsch and Edda Assel (MfN); Philippe Béarez and Jonathan Pfliger (MNHN); and Amanda Hay (AMS). For assistance with scanning, we thank Vincent Fernandez and Brett Clark (NHMUK), Kristen Mahlow (MfN), Marta Bellato (MNHN), and Jenny Gibson (Royal National Orthopaedic Hospital NHS Trust). We also thank current and past members of the Goswami Lab at the Natural History Museum, London, for valuable feedback and discussion, and two anonymous reviewers whose thoughtful comments and suggestions helped greatly improve our original manuscript. This study includes data produced in the CTEES facility at University of Michigan, supported by the Department of Earth and Environmental Sciences and College of Literature, Science, and the Arts, and from the Department of Earth Sciences, University of Oxford, Oxford, UK. This study was funded by a Leverhulme Trust grant, no. RPG-2019-113.

Publisher Copyright:
© The Author(s) 2023. Published by Oxford University Press on behalf of The Society for the Study of Evolution (SSE).

Keywords

geometric morphometrics
morphological evolution
Pelagiaria
teleost

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Genetics
General Agricultural and Biological Sciences

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KnappA2023tunaFinal published version, 18 MBLicence: Creative Commons: Attribution (CC BY)

Cite this

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title = "How to tuna fish: constraint, convergence, and integration in the neurocranium of pelagiarian fishes",

abstract = "Morphological evolution of the vertebrate skull has been explored across a wide range of tetrapod clades using geometric morphometrics, but the application of these methods to teleost fishes, accounting for roughly half of all vertebrate species, has been limited. Here we present the results of a study investigating 3D morphological evolution of the neurocranium across 114 species of Pelagiaria, a diverse clade of open-ocean teleost fishes that includes tuna and mackerel. Despite showing high shape disparity overall, taxa from all families fall into three distinct morphological clusters. Convergence in shape within clusters is high, and phylogenetic signal in shape data is significant but low. Neurocranium shape is significantly correlated with body elongation and significantly but weakly correlated with size. Diet and habitat depth are weakly correlated with shape, and nonsignificant after accounting for phylogeny. Evolutionary integration in the neurocranium is high, suggesting that convergence in skull shape and the evolution of extreme morphologies are associated with the correlated evolution of neurocranial elements. These results suggest that shape evolution in the pelagiarian neurocranium reflects the extremes in elongation found in body shape but is constrained along relatively few axes of variation, resulting in repeated evolution toward a restricted range of morphologies.",

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note = "Acknowledgments: For access to specimens, we are grateful to James Maclaine, Ollie Crimmen, and Emma Bernard (NHMUK); Peter Rask M{\"o}ller (NHMD); Peter Bartsch and Edda Assel (MfN); Philippe B{\'e}arez and Jonathan Pfliger (MNHN); and Amanda Hay (AMS). For assistance with scanning, we thank Vincent Fernandez and Brett Clark (NHMUK), Kristen Mahlow (MfN), Marta Bellato (MNHN), and Jenny Gibson (Royal National Orthopaedic Hospital NHS Trust). We also thank current and past members of the Goswami Lab at the Natural History Museum, London, for valuable feedback and discussion, and two anonymous reviewers whose thoughtful comments and suggestions helped greatly improve our original manuscript. This study includes data produced in the CTEES facility at University of Michigan, supported by the Department of Earth and Environmental Sciences and College of Literature, Science, and the Arts, and from the Department of Earth Sciences, University of Oxford, Oxford, UK. This study was funded by a Leverhulme Trust grant, no. RPG-2019-113. Publisher Copyright: {\textcopyright} The Author(s) 2023. Published by Oxford University Press on behalf of The Society for the Study of Evolution (SSE).",

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AU - Giles, Sam

AU - Beckett, Hermione T.

AU - Goswami, Anjali

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How to tuna fish: constraint, convergence, and integration in the neurocranium of pelagiarian fishes

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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