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Caste differentiation happens early in development to produce gynes as future colony germlines and workers as present colony soma. However, gynes need insemination to become functional queens, a transition that initiates reproductive role differentiation relative to unmated gynes. Here, we analyze the anatomy and transcriptomes of brains during this differentiation process within the reproductive caste of Monomorium pharaonis Insemination terminated brain growth, whereas unmated control gynes continued to increase brain volume. Transcriptomes revealed a specific gene regulatory network (GRN) mediating both brain anatomy changes and behavioral modifications. This reproductive role differentiation GRN hardly overlapped with the gyne-worker caste differentiation GRN, but appears to be also used by distantly related ants where workers became germline individuals after the queen caste was entirely or partially lost. The genes corazonin and neuroparsin A in the anterior neurosecretory cells were overexpressed in individuals with reduced or nonreproductive roles across all four ant species investigated., (Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).)

Queens of ants and bees normally obtain a lifetime supply of sperm on a single day of sexual activity, and sperm competition is expected to occur in lineages where queens receive sperm from multiple males. We compared singly mated (monandrous) and multiply mated (polyandrous) sister groups of ants and bees and show that seminal fluid of polyandrous species has a more positive effect on the survival of a male's own sperm than on other males' sperm. This difference was not observed in the monandrous species, suggesting that incapacitation of competing sperm may have independently evolved in both bees and ants. In Atta leafcutter ants, the negative effect of the seminal fluid of other males was negated by secretion from the queen sperm-storage organ, suggesting that queens may control ejaculate competition after sperm storage.

It is unclear how mutualistic relationships can be stable when partners disperse freely and have the possibility of forming associations with many alternative genotypes. Theory predicts that high symbiont relatedness should resolve this problem, but the mechanisms to enforce this have rarely been studied. We show that African fungus-growing termites propagate single variants of their Termitomyces symbiont, despite initiating cultures from genetically variable spores from the habitat. High inoculation density in the substrate followed by fusion among clonally related mycelia enhances the efficiency of spore production in proportion to strain frequency. This positive reinforcement results in an exclusive lifetime association of each host colony with a single fungal symbiont and hinders the evolution of cheating. Our findings explain why vertical symbiont transmission in fungus-growing termites is rare and evolutionarily derived.

Mechanisms of recognition are essential to the evolution of mutualistic and parasitic interactions between species. One such example is the larval mimicry that Maculinea butterfly caterpillars use to parasitize Myrmica ant colonies. We found that the greater the match between the surface chemistry of Maculinea alcon and two of its host Myrmica species, the more easily ant colonies were exploited. The geographic patterns of surface chemistry indicate an ongoing coevolutionary arms race between the butterflies and Myrmica rubra, which has significant genetic differentiation between populations, but not between the butterflies and a second, sympatric host, Myrmica ruginodis, which has panmictic populations. Alternative hosts may therefore provide an evolutionary refuge for a parasite during periods of counteradaptation by their preferred hosts.

Attine ants engage in a quadripartite symbiosis with fungi they cultivate for food, specialized garden parasites, and parasite-inhibiting bacteria. Molecular phylogenetic evidence supports an ancient host-pathogen association between the ant-cultivar mutualism and the garden parasite. Here we show that ants rear the antibiotic-producing bacteria in elaborate cuticular crypts, supported by unique exocrine glands, and that these structures have been highly modified across the ants' evolutionary history. This specialized structural evolution, together with the absence of these bacteria and modifications in other ant genera that do not grow fungus, indicate that the bacteria have an ancient and coevolved association with the ants, their fungal cultivar, and the garden parasite.

Leaf-cutting ants rear clonal fungi for food and transmit the fungi from mother to daughter colonies so that symbiont mixing and conflict, which result from competition between genetically different clones, are avoided. Here we show that despite millions of years of predominantly vertical transmission, the domesticated fungi actively reject mycelial fragments from neighboring colonies, and that the strength of these reactions are in proportion to the overall genetic difference between these symbionts. Fungal incompatibility compounds remain intact during ant digestion, so that fecal droplets, which are used for manuring newly grown fungus, elicit similar hostile reactions when applied to symbionts from other colonies. Symbiont control over new mycelial growth by manurial imprinting prevents the rearing of multiple crops in fungus gardens belonging to the same colony.