Evidence for high-performance suction feeding in the Pennsylvanian stem-group holocephalan Iniopera

Richard P Dearden; Anthony Herrel; Alan Pradel

doi:10.1073/pnas.2207854119

Evidence for high-performance suction feeding in the Pennsylvanian stem-group holocephalan Iniopera

Richard P Dearden^*, Anthony Herrel, Alan Pradel

^*Corresponding author for this work

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Abstract

The Carboniferous (358.9 to 298.9 Ma) saw the emergence of marine ecosystems dominated by modern vertebrate groups, including abundant stem-group holocephalans (chimaeras and relatives). Compared with the handful of anatomically conservative holocephalan genera alive today-demersal durophages all-these animals were astonishingly morphologically diverse, and bizarre anatomies in groups such as iniopterygians hint at specialized ecological roles foreshadowing those of the later, suction-feeding neopterygians. However, flattened fossils usually obscure these animals' functional morphologies and how they fitted into these important early ecosystems. Here, we use three-dimensional (3D) methods to show that the musculoskeletal anatomy of the uniquely 3D-preserved iniopterygian Iniopera can be best interpreted as being similar to that of living holocephalans rather than elasmobranchs but that it was mechanically unsuited to durophagy. Rather, Iniopera had a small, anteriorly oriented mouth aperture, expandable pharynx, and strong muscular links among the pectoral girdle, neurocranium, and ventral pharynx consistent with high-performance suction feeding, something exhibited by no living holocephalan and never clearly characterized in any of the extinct members of the holocephalan stem-group. Remarkably, in adapting a distinctly holocephalan anatomy to suction feeding, Iniopera is more comparable to modern tetrapod suction feeders than to the more closely related high-performance suction-feeding elasmobranchs. This raises questions about the assumed role of durophagy in the evolution of holocephalans' distinctive anatomy and offers a rare glimpse into the breadth of ecological niches filled by holocephalans in a pre-neopterygian world.

Original language	English
Article number	e2207854119
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	120
Issue number	4
Early online date	17 Jan 2023
DOIs	https://doi.org/10.1073/pnas.2207854119
Publication status	Published - 24 Jan 2023

Bibliographical note

Acknowledgments
We thank Florent Goussard for assistance with 3D datasets. We also thank Paul Tafforeau and the European Synchrotron Radiation Facility for help in scanning the original specimens. We are grateful to the two anonymous reviewers who gave valuable and highly constructive feedback on the manuscript. This work was funded by a Paris Île-de-France Region grant (Domaine d'intérêt majeur [DIM] “Matériaux anciens et patrimoniaux”) awarded for the DIM PHARE (Pharyngeal Evolution: illuminating its formed function in early jawed vertebrates) project. R.P.D. is now supported by Leverhulme Trust Grant RPG-2021-271 “Feeding without jaws.” A.P. is supported by the Agence nationale de la recherche (Grant CE02) Terre vivante, jeunes chercheurs ou des jeunes chercheuses, MACHER (Mechanical Adaptation to Crushing in the Holocephalan Evolutionary Radiation). We would like to thank Megan Sims (Kansas University Natural History Museum) for help with specimens.

Keywords

Animals
Suction
Ecosystem
Skull/anatomy & histology
Vertebrates/anatomy & histology
Fishes/anatomy & histology
Feeding Behavior

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1073/pnas.2207854119Licence: Creative Commons: Attribution (CC BY)

DeardenRP2023EvidenceFinal published version, 1.44 MBLicence: Creative Commons: Attribution (CC BY)

Feeding without jaws - innovations in early vertebrates
Lautenschlager, S., Sansom, I. & Giles, S.
Leverhulme Trust
1/12/21 → 30/11/24
Project: Research

Cite this

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abstract = "The Carboniferous (358.9 to 298.9 Ma) saw the emergence of marine ecosystems dominated by modern vertebrate groups, including abundant stem-group holocephalans (chimaeras and relatives). Compared with the handful of anatomically conservative holocephalan genera alive today-demersal durophages all-these animals were astonishingly morphologically diverse, and bizarre anatomies in groups such as iniopterygians hint at specialized ecological roles foreshadowing those of the later, suction-feeding neopterygians. However, flattened fossils usually obscure these animals' functional morphologies and how they fitted into these important early ecosystems. Here, we use three-dimensional (3D) methods to show that the musculoskeletal anatomy of the uniquely 3D-preserved iniopterygian Iniopera can be best interpreted as being similar to that of living holocephalans rather than elasmobranchs but that it was mechanically unsuited to durophagy. Rather, Iniopera had a small, anteriorly oriented mouth aperture, expandable pharynx, and strong muscular links among the pectoral girdle, neurocranium, and ventral pharynx consistent with high-performance suction feeding, something exhibited by no living holocephalan and never clearly characterized in any of the extinct members of the holocephalan stem-group. Remarkably, in adapting a distinctly holocephalan anatomy to suction feeding, Iniopera is more comparable to modern tetrapod suction feeders than to the more closely related high-performance suction-feeding elasmobranchs. This raises questions about the assumed role of durophagy in the evolution of holocephalans' distinctive anatomy and offers a rare glimpse into the breadth of ecological niches filled by holocephalans in a pre-neopterygian world.",

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note = "Acknowledgments We thank Florent Goussard for assistance with 3D datasets. We also thank Paul Tafforeau and the European Synchrotron Radiation Facility for help in scanning the original specimens. We are grateful to the two anonymous reviewers who gave valuable and highly constructive feedback on the manuscript. This work was funded by a Paris {\^I}le-de-France Region grant (Domaine d'int{\'e}r{\^e}t majeur [DIM] “Mat{\'e}riaux anciens et patrimoniaux”) awarded for the DIM PHARE (Pharyngeal Evolution: illuminating its formed function in early jawed vertebrates) project. R.P.D. is now supported by Leverhulme Trust Grant RPG-2021-271 “Feeding without jaws.” A.P. is supported by the Agence nationale de la recherche (Grant CE02) Terre vivante, jeunes chercheurs ou des jeunes chercheuses, MACHER (Mechanical Adaptation to Crushing in the Holocephalan Evolutionary Radiation). We would like to thank Megan Sims (Kansas University Natural History Museum) for help with specimens.",

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N2 - The Carboniferous (358.9 to 298.9 Ma) saw the emergence of marine ecosystems dominated by modern vertebrate groups, including abundant stem-group holocephalans (chimaeras and relatives). Compared with the handful of anatomically conservative holocephalan genera alive today-demersal durophages all-these animals were astonishingly morphologically diverse, and bizarre anatomies in groups such as iniopterygians hint at specialized ecological roles foreshadowing those of the later, suction-feeding neopterygians. However, flattened fossils usually obscure these animals' functional morphologies and how they fitted into these important early ecosystems. Here, we use three-dimensional (3D) methods to show that the musculoskeletal anatomy of the uniquely 3D-preserved iniopterygian Iniopera can be best interpreted as being similar to that of living holocephalans rather than elasmobranchs but that it was mechanically unsuited to durophagy. Rather, Iniopera had a small, anteriorly oriented mouth aperture, expandable pharynx, and strong muscular links among the pectoral girdle, neurocranium, and ventral pharynx consistent with high-performance suction feeding, something exhibited by no living holocephalan and never clearly characterized in any of the extinct members of the holocephalan stem-group. Remarkably, in adapting a distinctly holocephalan anatomy to suction feeding, Iniopera is more comparable to modern tetrapod suction feeders than to the more closely related high-performance suction-feeding elasmobranchs. This raises questions about the assumed role of durophagy in the evolution of holocephalans' distinctive anatomy and offers a rare glimpse into the breadth of ecological niches filled by holocephalans in a pre-neopterygian world.

AB - The Carboniferous (358.9 to 298.9 Ma) saw the emergence of marine ecosystems dominated by modern vertebrate groups, including abundant stem-group holocephalans (chimaeras and relatives). Compared with the handful of anatomically conservative holocephalan genera alive today-demersal durophages all-these animals were astonishingly morphologically diverse, and bizarre anatomies in groups such as iniopterygians hint at specialized ecological roles foreshadowing those of the later, suction-feeding neopterygians. However, flattened fossils usually obscure these animals' functional morphologies and how they fitted into these important early ecosystems. Here, we use three-dimensional (3D) methods to show that the musculoskeletal anatomy of the uniquely 3D-preserved iniopterygian Iniopera can be best interpreted as being similar to that of living holocephalans rather than elasmobranchs but that it was mechanically unsuited to durophagy. Rather, Iniopera had a small, anteriorly oriented mouth aperture, expandable pharynx, and strong muscular links among the pectoral girdle, neurocranium, and ventral pharynx consistent with high-performance suction feeding, something exhibited by no living holocephalan and never clearly characterized in any of the extinct members of the holocephalan stem-group. Remarkably, in adapting a distinctly holocephalan anatomy to suction feeding, Iniopera is more comparable to modern tetrapod suction feeders than to the more closely related high-performance suction-feeding elasmobranchs. This raises questions about the assumed role of durophagy in the evolution of holocephalans' distinctive anatomy and offers a rare glimpse into the breadth of ecological niches filled by holocephalans in a pre-neopterygian world.

KW - Animals

KW - Suction

KW - Ecosystem

KW - Skull/anatomy & histology

KW - Vertebrates/anatomy & histology

KW - Fishes/anatomy & histology

KW - Feeding Behavior

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SN - 1091-6490

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JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

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Evidence for high-performance suction feeding in the Pennsylvanian stem-group holocephalan Iniopera

Abstract

Bibliographical note

Keywords

UN SDGs

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Feeding without jaws - innovations in early vertebrates

Cite this