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Explosive Radiation of Ant Parasitic Butterflies During the Miocene Aridification of Africa

54 Pages Posted: 5 Apr 2021 Publication Status: Review Complete

See all articles by Marianne Espeland

Marianne Espeland

Zoological Research Museum Alexander Koenig - Department of Anthropology

Nicolas Chazot

Swedish University of Agricultural Sciences (SLU) - Department of Ecology

Fabien L. Condamine

Institut des Sciences de l’Evolution de Montpellier

Alan R. Lemmon

Florida State University - Department of Scientific Computing

Emily Moriarty Lemmon

Florida State University - Department of Biological Science

Ernest Pringle

Lepidopterists' Society of Africa

Alan Heath

Lepidopterists' Society of Africa

Steve Collins

African Butterfly Research Institute

Wilson Tiren

Nature Kenya

Martha Mutiso

Nature Kenya

David C. Lees

Natural History Museum - Department of Life Sciences

Stewart Fisher

Lepidopterists' Society of Africa

Stephen Woodhall

Lepidopterists' Society of Africa

Robert Tropek

Charles University - Department of Ecology

Svenja Sabine Ahlborn

Zoological Research Museum Alexander Koenig - Department of Anthropology

Kevin Cockburn

Lepidopterists' Society of Africa

Jeremy Dobson

Lepidopterists' Society of Africa

Thierry Bouyer

B-4032

Zofia A. Kaliszewska

Harvard University - Department of Organismic and Evolutionary Biology

Christopher C. M. Baker

Harvard University - Department of Organismic and Evolutionary Biology

Gerard Talavera

Institut Botànic de Barcelona (IBB, CSIC-Ajuntament de Barcelona)

Roger Vila

Universitat Pompeu Fabra - Institute of Evolutionary Biology

Alan J. Gardiner

Southern African Wildlife College

Mark Williams

Lepidopterists' Society of Africa

Dino J. Martins

Mpala Research Centre

Szabolcs Sáfián

University of Sopron - Institute of Silviculture and Forest Protection

David A. Edge

Lepidopterists' Society of Africa

Naomi E. Pierce

Harvard University - Department of Organismic and Evolutionary Biology

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Abstract

Extremely spezialized life history strategies are sometimes  seen as evolutionary dead-ends. The Afrotropical butterfly genus Lepidochrysops exhibits such a life history. All 137 species are known or assumed to be phyto-predaceous, with caterpillars feeding on plants for the first few instars and later switching to  parasitizing ants in the Formicinae,  either by consuming ant brood or being fed by the ants through trophallaxis.  The only other butterflies that exhibit this phyto-predaceous life history are those in the Palaearctic genus Phengaris (= Maculinea), a group of only a bout  11 species whose caterpillars parasitize ants in the Myrmicinae. We hypothesize that the move into ant nests by species of Lepidochrysops was an adaptive response to the aridification of Africa during the Miocene that facilitated subsequent radiation. Ant colonies have the advantage of providing both shelter from threats like fire and desiccation, as well as a stable food source when vegetation is scarce or unpredictable. To evaluate this hypothesis, we inferred a time-calibrated phylogeny using >400 loci for Lepidochrysops and its closest, non-parasitic relatives. We  showed that this clade originated with the emerging Miombo woodlands about 22 million years ago (Mya), and spread to drier biomes as they became available. The diversity of the non-parasitic lineages decreased as aridification intensified around 10 Mya, culminating in an abrupt extinction. In contrast, the phyto-predaceous Lepidochrysops lineage radiated rapidly from around 6.5 Mya when phyto-predation likely evolved, showing the importance of this innovation for diversification and survival during the intensifying aridification of Africa.

Keywords: Climate change; hybrid enrichment; biogeography; diversification; Lycaenidae

Suggested Citation

Espeland, Marianne and Chazot, Nicolas and Condamine, Fabien L. and Lemmon, Alan R. and Moriarty Lemmon, Emily and Pringle, Ernest and Heath, Alan and Collins, Steve and Tiren, Wilson and Mutiso, Martha and Lees, David C. and Fisher, Stewart and Woodhall, Stephen and Tropek, Robert and Ahlborn, Svenja Sabine and Cockburn, Kevin and Dobson, Jeremy and Bouyer, Thierry and Kaliszewska, Zofia A. and Baker, Christopher C. M. and Talavera, Gerard and Vila, Roger and Gardiner, Alan J. and Williams, Mark and Martins, Dino J. and Sáfián, Szabolcs and Edge, David A. and Pierce, Naomi E., Explosive Radiation of Ant Parasitic Butterflies During the Miocene Aridification of Africa. Available at SSRN: https://ssrn.com/abstract=3820043 or http://dx.doi.org/10.2139/ssrn.3820043
This version of the paper has not been formally peer reviewed.

Marianne Espeland (Contact Author)

Zoological Research Museum Alexander Koenig - Department of Anthropology ( email )

Germany

Nicolas Chazot

Swedish University of Agricultural Sciences (SLU) - Department of Ecology ( email )

S-901 83 Umea
Sweden

Fabien L. Condamine

Institut des Sciences de l’Evolution de Montpellier ( email )

Alan R. Lemmon

Florida State University - Department of Scientific Computing

Tallahasse, FL 32306
United States

Emily Moriarty Lemmon

Florida State University - Department of Biological Science

Tallahasse, FL 32306
United States

Ernest Pringle

Lepidopterists' Society of Africa ( email )

Alan Heath

Lepidopterists' Society of Africa ( email )

Steve Collins

African Butterfly Research Institute

Wilson Tiren

Nature Kenya ( email )

Martha Mutiso

Nature Kenya ( email )

David C. Lees

Natural History Museum - Department of Life Sciences ( email )

Cromwell Road
London, SW7 5BD
United Kingdom

Stewart Fisher

Lepidopterists' Society of Africa ( email )

Stephen Woodhall

Lepidopterists' Society of Africa ( email )

Robert Tropek

Charles University - Department of Ecology

U Knize 8
Prague, 15800
Czech Republic

Svenja Sabine Ahlborn

Zoological Research Museum Alexander Koenig - Department of Anthropology ( email )

Germany

Kevin Cockburn

Lepidopterists' Society of Africa ( email )

Jeremy Dobson

Lepidopterists' Society of Africa ( email )

Thierry Bouyer

B-4032 ( email )

Zofia A. Kaliszewska

Harvard University - Department of Organismic and Evolutionary Biology

1875 Cambridge Street
Cambridge, MA 02138
United States

Christopher C. M. Baker

Harvard University - Department of Organismic and Evolutionary Biology

1875 Cambridge Street
Cambridge, MA 02138
United States

Gerard Talavera

Institut Botànic de Barcelona (IBB, CSIC-Ajuntament de Barcelona) ( email )

Roger Vila

Universitat Pompeu Fabra - Institute of Evolutionary Biology ( email )

Ramon Trias Fargas, 25-27
Barcelona, E-08005
Spain

Alan J. Gardiner

Southern African Wildlife College ( email )

Mark Williams

Lepidopterists' Society of Africa

Dino J. Martins

Mpala Research Centre ( email )

Szabolcs Sáfián

University of Sopron - Institute of Silviculture and Forest Protection

4. Bajcsy-Zsilinszky street
Sopron, 9400
Hungary

David A. Edge

Lepidopterists' Society of Africa ( email )

Naomi E. Pierce

Harvard University - Department of Organismic and Evolutionary Biology ( email )

1875 Cambridge Street
Cambridge, MA 02138
United States

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