Rapid radiation of ant parasitic butterflies during the Miocene aridification of Africa

Africa has undergone a progressive aridification during the last 20 My that presumably impacted organisms and fostered the evolution of life history adaptations. We test the hypothesis that shift to living in ant nests and feeding on ant brood by larvae of phyto-predaceous Lepidochrysops butterflies...

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Autores: Espeland, Marianne, Chazot, Nicolas, Condamine, Fabien L., Lemmon, Alan R., Moriarty Lemmon, Emily, Pringle, Ernest, Heath, Alan, Collins, Steve C., Tiren, Wilson, Mutiso, Martha, Lees, David C., Fisher, Stewart, Murphy, Raymond, Woodhall, Stephen, Tropek, Robert, Ahlborn, Svenja S., Cockburn, Kevin, Dobson, Jeremy, Bouyer, Thierry, Kaliszewska, Zofia A., Baker, Christopher C. M., Talavera, Gerard, Vila, Roger, Gardiner, Alan J., Williams, Mark, Martins, Dino J., Sáfián, Szabolcs, Edge, David A., Pierce, Naomi E.
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2023
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/308915
Acceso en línea:http://hdl.handle.net/10261/308915
https://doi.org/10.1002/ece3.10046
Access Level:acceso abierto
Palabra clave:Butterfly–ant interactions
Lepidochrysops
Lycaenidae
Myrmecophagy
Phytopredation
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network_name_str España
repository_id_str
dc.title.none.fl_str_mv Rapid radiation of ant parasitic butterflies during the Miocene aridification of Africa
title Rapid radiation of ant parasitic butterflies during the Miocene aridification of Africa
spellingShingle Rapid radiation of ant parasitic butterflies during the Miocene aridification of Africa
Espeland, Marianne
Butterfly–ant interactions
Lepidochrysops
Lycaenidae
Myrmecophagy
Phytopredation
title_short Rapid radiation of ant parasitic butterflies during the Miocene aridification of Africa
title_full Rapid radiation of ant parasitic butterflies during the Miocene aridification of Africa
title_fullStr Rapid radiation of ant parasitic butterflies during the Miocene aridification of Africa
title_full_unstemmed Rapid radiation of ant parasitic butterflies during the Miocene aridification of Africa
title_sort Rapid radiation of ant parasitic butterflies during the Miocene aridification of Africa
dc.creator.none.fl_str_mv Espeland, Marianne
Chazot, Nicolas
Condamine, Fabien L.
Lemmon, Alan R.
Moriarty Lemmon, Emily
Pringle, Ernest
Heath, Alan
Collins, Steve C.
Tiren, Wilson
Mutiso, Martha
Lees, David C.
Fisher, Stewart
Murphy, Raymond
Woodhall, Stephen
Tropek, Robert
Ahlborn, Svenja S.
Cockburn, Kevin
Dobson, Jeremy
Bouyer, Thierry
Kaliszewska, Zofia A.
Baker, Christopher C. M.
Talavera, Gerard
Vila, Roger
Gardiner, Alan J.
Williams, Mark
Martins, Dino J.
Sáfián, Szabolcs
Edge, David A.
Pierce, Naomi E.
author Espeland, Marianne
author_facet Espeland, Marianne
Chazot, Nicolas
Condamine, Fabien L.
Lemmon, Alan R.
Moriarty Lemmon, Emily
Pringle, Ernest
Heath, Alan
Collins, Steve C.
Tiren, Wilson
Mutiso, Martha
Lees, David C.
Fisher, Stewart
Murphy, Raymond
Woodhall, Stephen
Tropek, Robert
Ahlborn, Svenja S.
Cockburn, Kevin
Dobson, Jeremy
Bouyer, Thierry
Kaliszewska, Zofia A.
Baker, Christopher C. M.
Talavera, Gerard
Vila, Roger
Gardiner, Alan J.
Williams, Mark
Martins, Dino J.
Sáfián, Szabolcs
Edge, David A.
Pierce, Naomi E.
author_role author
author2 Chazot, Nicolas
Condamine, Fabien L.
Lemmon, Alan R.
Moriarty Lemmon, Emily
Pringle, Ernest
Heath, Alan
Collins, Steve C.
Tiren, Wilson
Mutiso, Martha
Lees, David C.
Fisher, Stewart
Murphy, Raymond
Woodhall, Stephen
Tropek, Robert
Ahlborn, Svenja S.
Cockburn, Kevin
Dobson, Jeremy
Bouyer, Thierry
Kaliszewska, Zofia A.
Baker, Christopher C. M.
Talavera, Gerard
Vila, Roger
Gardiner, Alan J.
Williams, Mark
Martins, Dino J.
Sáfián, Szabolcs
Edge, David A.
Pierce, Naomi E.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Research Council of Norway
German Research Foundation
Synthesys
Museum of Comparative Zoology (US)
Hintelmann Award for Zoological Systematics
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Butterfly–ant interactions
Lepidochrysops
Lycaenidae
Myrmecophagy
Phytopredation
topic Butterfly–ant interactions
Lepidochrysops
Lycaenidae
Myrmecophagy
Phytopredation
description Africa has undergone a progressive aridification during the last 20 My that presumably impacted organisms and fostered the evolution of life history adaptations. We test the hypothesis that shift to living in ant nests and feeding on ant brood by larvae of phyto-predaceous Lepidochrysops butterflies was an adaptive response to the aridification of Africa that facilitated the subsequent radiation of butterflies in this genus. Using anchored hybrid enrichment we constructed a time-calibrated phylogeny for Lepidochrysops and its closest, non-parasitic relatives in the Euchrysops section (Poloyommatini). We estimated ancestral areas across the phylogeny with process-based biogeographical models and diversification rates relying on time-variable and clade-heterogeneous birth-death models. The Euchrysops section originated with the emerging Miombo woodlands about 22 million years ago (Mya) and spread to drier biomes as they became available in the late Miocene. The diversification of the non-parasitic lineages decreased as aridification intensified around 10 Mya, culminating in diversity decline. In contrast, the diversification of the phyto-predaceous Lepidochrysops lineage proceeded rapidly from about 6.5 Mya when this unusual life history likely first evolved. The Miombo woodlands were the cradle for diversification of the Euchrysops section, and our findings are consistent with the hypothesis that aridification during the Miocene selected for a phyto-predaceous life history in species of Lepidochrysops, with ant nests likely providing caterpillars a safe refuge from fire and a source of food when vegetation was scarce.
publishDate 2023
dc.date.none.fl_str_mv 2023
2023
2023
2023
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/308915
https://doi.org/10.1002/ece3.10046
url http://hdl.handle.net/10261/308915
https://doi.org/10.1002/ece3.10046
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv https://doi.org/10.1002/ece3.10046

dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv John Wiley & Sons
publisher.none.fl_str_mv John Wiley & Sons
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
repository.name.fl_str_mv
repository.mail.fl_str_mv
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spelling Rapid radiation of ant parasitic butterflies during the Miocene aridification of AfricaEspeland, MarianneChazot, NicolasCondamine, Fabien L.Lemmon, Alan R.Moriarty Lemmon, EmilyPringle, ErnestHeath, AlanCollins, Steve C.Tiren, WilsonMutiso, MarthaLees, David C.Fisher, StewartMurphy, RaymondWoodhall, StephenTropek, RobertAhlborn, Svenja S.Cockburn, KevinDobson, JeremyBouyer, ThierryKaliszewska, Zofia A.Baker, Christopher C. M.Talavera, GerardVila, RogerGardiner, Alan J.Williams, MarkMartins, Dino J.Sáfián, SzabolcsEdge, David A.Pierce, Naomi E.Butterfly–ant interactionsLepidochrysopsLycaenidaeMyrmecophagyPhytopredationAfrica has undergone a progressive aridification during the last 20 My that presumably impacted organisms and fostered the evolution of life history adaptations. We test the hypothesis that shift to living in ant nests and feeding on ant brood by larvae of phyto-predaceous Lepidochrysops butterflies was an adaptive response to the aridification of Africa that facilitated the subsequent radiation of butterflies in this genus. Using anchored hybrid enrichment we constructed a time-calibrated phylogeny for Lepidochrysops and its closest, non-parasitic relatives in the Euchrysops section (Poloyommatini). We estimated ancestral areas across the phylogeny with process-based biogeographical models and diversification rates relying on time-variable and clade-heterogeneous birth-death models. The Euchrysops section originated with the emerging Miombo woodlands about 22 million years ago (Mya) and spread to drier biomes as they became available in the late Miocene. The diversification of the non-parasitic lineages decreased as aridification intensified around 10 Mya, culminating in diversity decline. In contrast, the diversification of the phyto-predaceous Lepidochrysops lineage proceeded rapidly from about 6.5 Mya when this unusual life history likely first evolved. The Miombo woodlands were the cradle for diversification of the Euchrysops section, and our findings are consistent with the hypothesis that aridification during the Miocene selected for a phyto-predaceous life history in species of Lepidochrysops, with ant nests likely providing caterpillars a safe refuge from fire and a source of food when vegetation was scarce.This work was funded by the Research Council of Norway (# 204308), the German Research Foundation (ES 522/1-1), Synthesys (GB-TAF-6197), the Putnam Exploration Fund of the Museum of Comparative Zoology, and the Hintelmann Prize for Zoological systematics to ME, and NSF DEB-0447244 and a Wetmore-Colles grant from the Museum of Comparative Zoology to NEP. ERC-EMARES (# 250325) funded fieldwork by DJL in Madagascar. Open Access funding enabled and organized by Projekt DEAL.1 INTRODUCTION 2 MATERIALS AND METHODS Taxon sampling Probe design 2.2.1 Selection of AHE target loci 2.2.2 Selection of anonymous target loci 2.2.3 Incorporation of legacy loci 2.2.4 Probe generation Molecular methods, data cleaning, and assembly Molecular data, phylogeny, and dating Historical biogeography Diversification dynamics 3 RESULTS AND DISCUSSION Diversification during the aridification of Africa Increasing occupation of drier biomes Extinction and rise of phyto-predation Aphytophagy: A rare and risky life history strategy in Lepidoptera Ant association and adaptation to the aridification of Africa 4 CONCLUSIONS AUTHOR CONTRIBUTIONS ACKNOWLEDGMENTS CONFLICT OF INTEREST STATEMENTPeer reviewedJohn Wiley & SonsResearch Council of NorwayGerman Research FoundationSynthesysMuseum of Comparative Zoology (US)Hintelmann Award for Zoological SystematicsConsejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2023202320232023info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/308915https://doi.org/10.1002/ece3.10046reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Ingléshttps://doi.org/10.1002/ece3.10046Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/3089152026-05-22T06:33:51Z
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