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 172 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 a global phylogeny of Formica ants. The genus originated in the Old World ∼30 Ma ago and dispersed multiple times to the New World and back. Within Formica , obligate dependent colony-founding behavior arose once from a facultatively polygynous common ancestor practicing independent and facultative dependent colony foundation. Temporary social parasitism likely preceded or arose concurrently with obligate dependent colony founding, and dulotic social parasitism evolved once within the obligate dependent colony-founding clade. Permanent social parasitism evolved twice from temporary social parasitic ancestors that rarely practiced colony budding, demonstrating that obligate social parasitism can originate from a facultative parasitic background in socially polymorphic organisms. In contrast to permanently socially parasitic ants in other genera, the high parasite diversity in Formica likely originated via allopatric speciation, highlighting the diversity of convergent evolutionary trajectories resulting in nearly identical parasitic life history syndromes.
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This content will become publicly available on May 25, 2024
Biogeography and evolution of social parasitism in Australian Myrmecia bulldog ants revealed by phylogenomics
Studying the historical biogeography and life history transitions from eusocial colony life to social parasitism
contributes to our understanding of the evolutionary mechanisms generating biodiversity in eusocial insects. The
ants in the genus Myrmecia are a well-suited system for testing evolutionary hypotheses about how their species
diversity was assembled through time because the genus is endemic to Australia with the single exception of the
species M. apicalis inhabiting the Pacific Island of New Caledonia, and because at least one social parasite species
exists in the genus. However, the evolutionary mechanisms underlying the disjunct biogeographic distribution of
M. apicalis and the life history transition(s) to social parasitism remain unexplored. To study the biogeographic
origin of the isolated, oceanic species M. apicalis and to reveal the origin and evolution of social parasitism in the
genus, we reconstructed a comprehensive phylogeny of the ant subfamily Myrmeciinae. We utilized Ultra
Conserved Elements (UCEs) as molecular markers to generate a molecular genetic dataset consisting of 2,287 loci
per taxon on average for 66 out of the 93 known Myrmecia species as well as for the sister lineage Nothomyrmecia
macrops and selected outgroups. Our time-calibrated phylogeny inferred that: (i) stem Myrmeciinae originated
during the Paleocene ~ 58 Ma ago; (ii) the current disjunct biogeographic distribution of M. apicalis was driven
by long-distance dispersal from Australia to New Caledonia during the Miocene ~ 14 Ma ago; (iii) the single
social parasite species, M. inquilina, evolved directly from one of the two known host species, M. nigriceps, in
sympatry via the intraspecific route of social parasite evolution; and (iv) 5 of the 9 previously established
taxonomic species groups are non-monophyletic. We suggest minor changes to reconcile the molecular phylogenetic
results with the taxonomic classification. Our study enhances our understanding of the evolution and
biogeography of Australian bulldog ants, contributes to our knowledge about the evolution of social parasitism in
ants, and provides a solid phylogenetic foundation for future inquiries into the biology, taxonomy, and classification
of Myrmeciinae.
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- Award ID(s):
- 1943626
- NSF-PAR ID:
- 10478012
- Publisher / Repository:
- https://doi.org/10.1016/j.ympev.2023.107825
- Date Published:
- Journal Name:
- Molecular phylogenetics and evolution
- Volume:
- 186
- ISSN:
- 1055-7903
- Page Range / eLocation ID:
- 107825
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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