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The evolution of social parasitism in Formica ants revealed by a global phylogeny

View ORCID ProfileMarek L. Borowiec, Stefan P. Cover, Christian Rabeling
doi: https://doi.org/10.1101/2020.12.17.423324
Marek L. Borowiec
aSchool of Life Sciences, Arizona State University, Tempe, AZ 85287, U.S.A.
bInstitute of Bioinformatics and Evolutionary Studies (IBEST), University of Idaho, Moscow, ID 83843, U.S.A.
cDepartment of Entomology, Plant Pathology and Nematology, University of Idaho, Moscow, ID 83844, U.S.A.
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  • For correspondence: mborowiec@uidaho.edu
Stefan P. Cover
dMuseum of Comparative Zoology, Harvard University, Cambridge, MA 02138, U.S.A.
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Christian Rabeling
aSchool of Life Sciences, Arizona State University, Tempe, AZ 85287, U.S.A.
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  • For correspondence: christian.rabeling@asu.edu
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Abstract

Studying the behavioral and life history transitions from a cooperative, eusocial life history to exploitative social parasitism allows for deciphering the conditions under which changes in behavior and social organization lead to diversification. The Holarctic ant genus Formica is ideally suited for studying the evolution of social parasitism because half of its 176 species are confirmed or suspected social parasites, which includes all three major classes of social parasitism known in ants. However, the life-history transitions associated with the evolution of social parasitism in this genus are largely unexplored. To test competing hypotheses regarding the origins and evolution of social parasitism, we reconstructed the first global phylogeny of Formica ants and representative formicine outgroups. The genus Formica originated in the Old World during the Oligocene (∼30 Ma ago) and dispersed multiple times to the New World. Within Formica, the capacity for dependent colony foundation and temporary social parasitism arose once from a facultatively polygynous, independently colony founding ancestor. Within this parasitic clade, dulotic social parasitism evolved once from a facultatively temporary parasitic ancestor that likely practiced colony budding frequently. Permanent social parasitism evolved twice from temporary social parasitic ancestors that rarely practiced colony budding, demonstrating that obligate social parasitism can originate from different facultative parasitic backgrounds in socially polymorphic organisms. In contrast to inquiline ant species in other genera, the high social parasite diversity in Formica likely originated via allopatric speciation, highlighting the diversity of convergent evolutionary trajectories resulting in nearly identical parasitic life history syndromes.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Revisions to the manuscript text; changed total Formica species number to 176, which better reflects current taxonomy. Included tenth, mononotypic species group for Formica uralensis. Added acknowledgments.

  • https://doi.org/10.5281/zenodo.4341310

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted February 15, 2021.
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The evolution of social parasitism in Formica ants revealed by a global phylogeny
Marek L. Borowiec, Stefan P. Cover, Christian Rabeling
bioRxiv 2020.12.17.423324; doi: https://doi.org/10.1101/2020.12.17.423324
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The evolution of social parasitism in Formica ants revealed by a global phylogeny
Marek L. Borowiec, Stefan P. Cover, Christian Rabeling
bioRxiv 2020.12.17.423324; doi: https://doi.org/10.1101/2020.12.17.423324

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