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
Author Information
Waring Trible: 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.
Vikram Chandra: 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.
Kip D Lacy: Laboratory of Social Evolution and Behavior, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA.
Gina Limón: 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.
Sean K McKenzie: Laboratory of Social Evolution and Behavior, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA; Oxford Nanopore Technologies, Oxford OX4 4DQ, UK.
Leonora Olivos-Cisneros: Laboratory of Social Evolution and Behavior, The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA.
Samuel V Arsenault: 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.
Daniel J C Kronauer: 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.
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.
