A caste differentiation mutant elucidates the evolution of socially parasitic ants

Waring Trible; Vikram Chandra; Kip D Lacy; Gina Limón; Sean K McKenzie; Leonora Olivos-Cisneros; Samuel V Arsenault; Daniel J C Kronauer

doi:10.1016/j.cub.2023.01.067

A caste differentiation mutant elucidates the evolution of socially parasitic ants

Curr Biol. 2023 Mar 27;33(6):1047-1058.e4. doi: 10.1016/j.cub.2023.01.067. Epub 2023 Feb 28.

Authors

Waring Trible¹, Vikram Chandra², Kip D Lacy³, Gina Limón⁴, Sean K McKenzie⁵, Leonora Olivos-Cisneros³, Samuel V Arsenault⁶, Daniel J C Kronauer⁷

Affiliations

¹ Laboratory of Social Evolution and Behavior, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA; John Harvard Distinguished Science Fellowship Program, Harvard University, 52 Oxford Street, Cambridge, MA 02138, USA. Electronic address: bucktrible@g.harvard.edu.
² Laboratory of Social Evolution and Behavior, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA; Department of Organismic and Evolutionary Biology, Harvard University, 52 Oxford Street, Cambridge, MA 02138, USA.
³ Laboratory of Social Evolution and Behavior, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA.
⁴ Laboratory of Social Evolution and Behavior, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA; Department of Microbiology, New York University School of Medicine, 430 E. 29th Street, New York, NY 10016, USA.
⁵ Laboratory of Social Evolution and Behavior, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA; Oxford Nanopore Technologies, Oxford OX4 4DQ, UK.
⁶ John Harvard Distinguished Science Fellowship Program, Harvard University, 52 Oxford Street, Cambridge, MA 02138, USA; Department of Organismic and Evolutionary Biology, Harvard University, 52 Oxford Street, Cambridge, MA 02138, USA.
⁷ Laboratory of Social Evolution and Behavior, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA; Howard Hughes Medical Institute, New York, NY 10065, USA. Electronic address: dkronauer@rockefeller.edu.

Abstract

Most ant species have two distinct female castes-queens and workers-yet the developmental and genetic mechanisms that produce these alternative phenotypes remain poorly understood. Working with a clonal ant, we discovered a variant strain that expresses queen-like traits in individuals that would normally become workers. The variants show changes in morphology, behavior, and fitness that cause them to rely on workers in wild-type (WT) colonies for survival. Overall, they resemble the queens of many obligately parasitic ants that have evolutionarily lost the worker caste and live inside colonies of closely related hosts. The prevailing theory for the evolution of these workerless social parasites is that they evolve from reproductively isolated populations of facultative intermediates that acquire parasitic phenotypes in a stepwise fashion. However, empirical evidence for such facultative ancestors remains weak, and it is unclear how reproductive isolation could gradually arise in sympatry. In contrast, we isolated these variants just a few generations after they arose within their WT parent colony, implying that the complex phenotype reported here was induced in a single genetic step. This suggests that a single genetic module can decouple the coordinated mechanisms of caste development, allowing an obligately parasitic variant to arise directly from a free-living ancestor. Consistent with this hypothesis, the variants have lost one of the two alleles of a putative supergene that is heterozygous in WTs. These findings provide a plausible explanation for the evolution of ant social parasites and implicate new candidate molecular mechanisms for ant caste differentiation.

Keywords: Formicidae; Ooceraea biroi; ants; caste development; clonal raider ant; developmental plasticity; evolution; parasitism; social evolution.

Publication types

Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural

MeSH terms

Animals
Ants* / anatomy & histology
Female
Parasites*
Phenotype
Social Behavior

Abstract

Publication types

MeSH terms

Grants and funding