A comprehensive phylogeny and revised taxonomy illuminate the origin and diversification of the global radiation of Papilio (Lepidoptera: Papilionidae)

Fabien L. Condamine; Rémi Allio; Eliette L. Reboud; Julian R. Dupuis; Emmanuel F.A. Toussaint; Nathan Mazet; Shao Ji Hu; Delano S. Lewis; Krushnamegh Kunte; Adam M. Cotton; Felix A.H. Sperling

doi:10.1016/j.ympev.2023.107758

A comprehensive phylogeny and revised taxonomy illuminate the origin and diversification of the global radiation of Papilio (Lepidoptera: Papilionidae)

Fabien L. Condamine, Rémi Allio, Eliette L. Reboud, Julian R. Dupuis, Emmanuel F.A. Toussaint, Nathan Mazet, Shao Ji Hu, Delano S. Lewis, Krushnamegh Kunte, Adam M. Cotton, Felix A.H. Sperling

Research output: Contribution to journal › Article › peer-review

8 Scopus citations

Abstract

The swallowtail genus Papilio (Lepidoptera: Papilionidae) is species rich, distributed worldwide, and has broad morphological habits and ecological niches. Because of its elevated species richness, it has been historically difficult to reconstruct a densely sampled phylogeny for this clade. Here we provide a taxonomic working list for the genus, resulting in 235 Papilio species, and assemble a molecular dataset of seven gene fragments representing ca. 80% of the currently described diversity. Phylogenetic analyses reconstructed a robust tree with highly supported relationships within subgenera, although a few nodes in the early history of the Old World Papilio remain unresolved. Contrasting with previous results, we found that Papilio alexanor is sister to all Old World Papilio and that the subgenus Eleppone is no longer monotypic. The latter includes the recently described Fijian Papilio natewa with the Australian Papilio anactus and is sister to subgenus Araminta (formerly included in subgenus Menelaides) occurring in Southeast Asia. Our phylogeny also includes rarely studied (P. antimachus, P. benguetana) or endangered species (P. buddha, P. chikae). Taxonomic changes resulting from this study are elucidated. Molecular dating and biogeographic analyses indicate that Papilio originated ca. 30 million years ago (Oligocene), in a northern region centered on Beringia. A rapid early Miocene radiation in the Paleotropics is revealed within Old World Papilio, potentially explaining their low early branch support. Most subgenera originated in the early to middle Miocene followed by synchronous southward biogeographic dispersals and repeated local extirpations in northern latitudes. This study provides a comprehensive phylogenetic framework for Papilio with clarification of subgeneric systematics and species taxonomic changes enumerated, which will facilitate further studies to address questions on their ecology and evolutionary biology using this model clade.

Original language	English
Article number	107758
Journal	Molecular Phylogenetics and Evolution
Volume	183
DOIs	https://doi.org/10.1016/j.ympev.2023.107758
State	Published - Jun 2023

Bibliographical note

Publisher Copyright:
© 2023 Elsevier Inc.

Funding

This project has received funding from the European Research Council (ERC) under the European Union's Horizon 2020 research and innovation programme (project GAIA, agreement no. 851188), and an ‘Investissement d'Avenir’ grant from the Agence Nationale de la Recherche (project CASMA, CEBA, ref. ANR-10-LABX-25-01) to F.L.C.; a Ramanujan Fellowship from the Dept. of Science and Technology, Govt. of India, to K.K. and support of the Dept. of Atomic Energy, Govt. of India, under project nos. 12-RandD-TFR-5.04-0800 and 12-RandD-TFR-5.04-0900 to TIFR/NCBS; a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant to F.A.H.S. Sequencing of most Indian Papilio was done at NCBS under research and voucher specimen collection permits issued to K.K. by the state forest departments in Kerala (permit no. WL 10-3781/2012 dated 18/12/2012, and GO (RT) No. 376/2012/FandWLD dated 26/07/2012) and Nagaland (permit no. CWL/GEN/240/522-39 dated 14 August 2012). Alberto Fracasso (Italy) and Laurie Wills (New Zealand) are thanked for providing samples of some hard to obtain taxa. This project has received funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (project GAIA, agreement no. 851188), and an ‘Investissement d’Avenir’ grant from the Agence Nationale de la Recherche (project CASMA, CEBA, ref. ANR-10-LABX-25-01) to F.L.C.; a Ramanujan Fellowship from the Dept. of Science and Technology, Govt. of India, to K.K., and support of the Dept. of Atomic Energy, Govt. of India, under project nos. 12-RandD-TFR-5.04-0800 and 12-RandD-TFR-5.04-0900 to TIFR/NCBS; a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant to F.A.H.S. Sequencing of most Indian Papilio was done at NCBS under research and voucher specimen collection permits issued to K.K. by the state forest departments in Kerala (permit no. WL 10-3781/2012 dated 18/12/2012, and GO (RT) No. 376/2012/FandWLD dated 26/07/2012) and Nagaland (permit no. CWL/GEN/240/522-39 dated 14 August 2012). Alberto Fracasso (Italy) and Laurie Wills (New Zealand) are thanked for providing samples of some hard to obtain taxa.

Funders	Funder number
Dept. of Atomic Energy
Horizon 2020 Framework Programme
Natural Sciences and Engineering Research Council of Canada	CWL/GEN/240/522-39, WL 10-3781/2012, 376/2012/FandWLD
H2020 European Research Council
Department of Science and Technology, Ministry of Science and Technology, India	12-RandD-TFR-5.04-0900, 12-RandD-TFR-5.04-0800
Agence Nationale de la Recherche	ANR-10-LABX-25-01
Horizon 2020	851188

Keywords

Butterflies
Historical biogeography
Macroevolution
Paleotropics
Systematics
Taxonomy

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Molecular Biology
Genetics

Access to Document

10.1016/j.ympev.2023.107758

Cite this

Condamine, F. L., Allio, R., Reboud, E. L., Dupuis, J. R., Toussaint, E. F. A., Mazet, N., Hu, S. J., Lewis, D. S., Kunte, K., Cotton, A. M., & Sperling, F. A. H. (2023). A comprehensive phylogeny and revised taxonomy illuminate the origin and diversification of the global radiation of Papilio (Lepidoptera: Papilionidae). Molecular Phylogenetics and Evolution, 183, Article 107758. https://doi.org/10.1016/j.ympev.2023.107758

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title = "A comprehensive phylogeny and revised taxonomy illuminate the origin and diversification of the global radiation of Papilio (Lepidoptera: Papilionidae)",

abstract = "The swallowtail genus Papilio (Lepidoptera: Papilionidae) is species rich, distributed worldwide, and has broad morphological habits and ecological niches. Because of its elevated species richness, it has been historically difficult to reconstruct a densely sampled phylogeny for this clade. Here we provide a taxonomic working list for the genus, resulting in 235 Papilio species, and assemble a molecular dataset of seven gene fragments representing ca. 80% of the currently described diversity. Phylogenetic analyses reconstructed a robust tree with highly supported relationships within subgenera, although a few nodes in the early history of the Old World Papilio remain unresolved. Contrasting with previous results, we found that Papilio alexanor is sister to all Old World Papilio and that the subgenus Eleppone is no longer monotypic. The latter includes the recently described Fijian Papilio natewa with the Australian Papilio anactus and is sister to subgenus Araminta (formerly included in subgenus Menelaides) occurring in Southeast Asia. Our phylogeny also includes rarely studied (P. antimachus, P. benguetana) or endangered species (P. buddha, P. chikae). Taxonomic changes resulting from this study are elucidated. Molecular dating and biogeographic analyses indicate that Papilio originated ca. 30 million years ago (Oligocene), in a northern region centered on Beringia. A rapid early Miocene radiation in the Paleotropics is revealed within Old World Papilio, potentially explaining their low early branch support. Most subgenera originated in the early to middle Miocene followed by synchronous southward biogeographic dispersals and repeated local extirpations in northern latitudes. This study provides a comprehensive phylogenetic framework for Papilio with clarification of subgeneric systematics and species taxonomic changes enumerated, which will facilitate further studies to address questions on their ecology and evolutionary biology using this model clade.",

keywords = "Butterflies, Historical biogeography, Macroevolution, Paleotropics, Systematics, Taxonomy",

author = "Condamine, {Fabien L.} and R{\'e}mi Allio and Reboud, {Eliette L.} and Dupuis, {Julian R.} and Toussaint, {Emmanuel F.A.} and Nathan Mazet and Hu, {Shao Ji} and Lewis, {Delano S.} and Krushnamegh Kunte and Cotton, {Adam M.} and Sperling, {Felix A.H.}",

note = "Publisher Copyright: {\textcopyright} 2023 Elsevier Inc.",

year = "2023",

month = jun,

doi = "10.1016/j.ympev.2023.107758",

language = "English",

volume = "183",

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Condamine, FL, Allio, R, Reboud, EL, Dupuis, JR, Toussaint, EFA, Mazet, N, Hu, SJ, Lewis, DS, Kunte, K, Cotton, AM & Sperling, FAH 2023, 'A comprehensive phylogeny and revised taxonomy illuminate the origin and diversification of the global radiation of Papilio (Lepidoptera: Papilionidae)', Molecular Phylogenetics and Evolution, vol. 183, 107758. https://doi.org/10.1016/j.ympev.2023.107758

TY - JOUR

T1 - A comprehensive phylogeny and revised taxonomy illuminate the origin and diversification of the global radiation of Papilio (Lepidoptera: Papilionidae)

AU - Condamine, Fabien L.

AU - Allio, Rémi

AU - Reboud, Eliette L.

AU - Dupuis, Julian R.

AU - Toussaint, Emmanuel F.A.

AU - Mazet, Nathan

AU - Hu, Shao Ji

AU - Lewis, Delano S.

AU - Kunte, Krushnamegh

AU - Cotton, Adam M.

AU - Sperling, Felix A.H.

PY - 2023/6

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N2 - The swallowtail genus Papilio (Lepidoptera: Papilionidae) is species rich, distributed worldwide, and has broad morphological habits and ecological niches. Because of its elevated species richness, it has been historically difficult to reconstruct a densely sampled phylogeny for this clade. Here we provide a taxonomic working list for the genus, resulting in 235 Papilio species, and assemble a molecular dataset of seven gene fragments representing ca. 80% of the currently described diversity. Phylogenetic analyses reconstructed a robust tree with highly supported relationships within subgenera, although a few nodes in the early history of the Old World Papilio remain unresolved. Contrasting with previous results, we found that Papilio alexanor is sister to all Old World Papilio and that the subgenus Eleppone is no longer monotypic. The latter includes the recently described Fijian Papilio natewa with the Australian Papilio anactus and is sister to subgenus Araminta (formerly included in subgenus Menelaides) occurring in Southeast Asia. Our phylogeny also includes rarely studied (P. antimachus, P. benguetana) or endangered species (P. buddha, P. chikae). Taxonomic changes resulting from this study are elucidated. Molecular dating and biogeographic analyses indicate that Papilio originated ca. 30 million years ago (Oligocene), in a northern region centered on Beringia. A rapid early Miocene radiation in the Paleotropics is revealed within Old World Papilio, potentially explaining their low early branch support. Most subgenera originated in the early to middle Miocene followed by synchronous southward biogeographic dispersals and repeated local extirpations in northern latitudes. This study provides a comprehensive phylogenetic framework for Papilio with clarification of subgeneric systematics and species taxonomic changes enumerated, which will facilitate further studies to address questions on their ecology and evolutionary biology using this model clade.

AB - The swallowtail genus Papilio (Lepidoptera: Papilionidae) is species rich, distributed worldwide, and has broad morphological habits and ecological niches. Because of its elevated species richness, it has been historically difficult to reconstruct a densely sampled phylogeny for this clade. Here we provide a taxonomic working list for the genus, resulting in 235 Papilio species, and assemble a molecular dataset of seven gene fragments representing ca. 80% of the currently described diversity. Phylogenetic analyses reconstructed a robust tree with highly supported relationships within subgenera, although a few nodes in the early history of the Old World Papilio remain unresolved. Contrasting with previous results, we found that Papilio alexanor is sister to all Old World Papilio and that the subgenus Eleppone is no longer monotypic. The latter includes the recently described Fijian Papilio natewa with the Australian Papilio anactus and is sister to subgenus Araminta (formerly included in subgenus Menelaides) occurring in Southeast Asia. Our phylogeny also includes rarely studied (P. antimachus, P. benguetana) or endangered species (P. buddha, P. chikae). Taxonomic changes resulting from this study are elucidated. Molecular dating and biogeographic analyses indicate that Papilio originated ca. 30 million years ago (Oligocene), in a northern region centered on Beringia. A rapid early Miocene radiation in the Paleotropics is revealed within Old World Papilio, potentially explaining their low early branch support. Most subgenera originated in the early to middle Miocene followed by synchronous southward biogeographic dispersals and repeated local extirpations in northern latitudes. This study provides a comprehensive phylogenetic framework for Papilio with clarification of subgeneric systematics and species taxonomic changes enumerated, which will facilitate further studies to address questions on their ecology and evolutionary biology using this model clade.

KW - Butterflies

KW - Historical biogeography

KW - Macroevolution

KW - Paleotropics

KW - Systematics

KW - Taxonomy

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ER -

A comprehensive phylogeny and revised taxonomy illuminate the origin and diversification of the global radiation of Papilio (Lepidoptera: Papilionidae)

Abstract

Bibliographical note

Funding

Keywords

ASJC Scopus subject areas

Access to Document

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