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Abstract Mating in ants often occurs on the wing during nuptial flights or on the ground when scattered female sexuals attract males by pheromones. In both scenarios, there is little opportunity for males to engage in prolonged aggressive competition or elaborate courtship displays. Male morphology is therefore adapted to locating female sexuals and mating, and it lacks specific weapons or other traits associated with courtship. In contrast, sexuals of the ant genus Cardiocondyla typically mate in their natal nests. As a consequence, in many species winged males have been replaced by wingless fighter or territorial males, which kill or expel rival males with their strong mandibles and show complex mating behavior. However, no wingless males are known from Cardiocondyla zoserka from West Africa, and instead, winged males have evolved a bizarre secondary sexual trait: uniquely shaped antennae with spoon‐like tips that show heavily sculptured ventral surfaces with numerous invaginations. We here report on the courtship behavior of C. zoserka males and describe antennal glands with class 3 gland cells, which presumably secrete a close range sex pheromone. Antennal glands have not yet been found in males of other ant species, including a close relative of C. zoserka, suggesting that in ants with intranidal mating sexual selection can rapidly lead to highly divergent adaptations and the evolution of novel structures.

Abstract Workers of the ant Cardiocondyla elegans drop female sexuals into the nest entrance of other colonies to promote outbreeding with unrelated, wingless males. Corroborating the results from previous years, we document that carrier and carried female sexuals are typically related and that the transfer initially occurs mostly from their joint natal colonies to unrelated colonies. Female sexuals mate multiply with up to seven genetically distinguishable males. Contrary to our expectation, the colony growth rate of multiple‐mated and outbred female sexuals was lower than that of inbred or single‐mated females, leading to the question of why female sexuals mate multiply at all. Despite the obvious costs, multiple mating might be a way for female sexuals to “pay rent” for hibernation in an alien nest. We argue that in addition to evade inbreeding depression from regular sibling mating over many generations, assisted dispersal might also be a strategy for minimizing the risk of losing all reproductive investment when nests are flooded in winter.

Abstract Workers in many species of social insects are capable of laying unfertilized eggs, which can develop into haploid males. This causes a conflict about male parentage between queens and workers. In a few species, this may result in matricide, that is, workers kill the colony's queen. Queen killing has so far been observed mainly in multi‐queen colonies or in annual species, when the queen's fecundity declines at the end of the reproductive period. Here, we report queen expulsion and matricide in a monogynous, monandrous ant with perennial societies. Workers were seen to aggressively expel both related and unrelated queens from their nest shortly after the end of hibernation. Queen expulsion and matricide led to a significant decrease in the number of workers and brood, but eventually increased the direct fitness of workers through significant male production. Long‐term observations revealed a short lifespan of queens, while workers in orphaned colonies survived and produced male offspring over several years.

Abstract Social insects dominate arthropod communities worldwide due to cooperation and division of labor in their societies. This, however, makes them vulnerable to exploitation by social parasites, such as slave‐making ants. Slave‐making ant workers pillage brood from neighboring nests of related host ant species. After emergence, host workers take over all nonreproductive colony tasks, whereas slavemakers have lost the ability to care for themselves and their offspring. Here, we compared transcriptomes of different developmental stages (larvae, pupae, and adults), castes (queens and workers), and sexes of two related ant species, the slavemaker Temnothorax americanus and its host Temnothorax longispinosus. Our aim was to investigate commonalities and differences in group‐specific transcriptomes, whereupon across‐species differences possibly can be explained by their divergent lifestyles. Larvae and pupae showed the highest similarity between the two species and upregulated genes with enriched functions of translation and chitin metabolism, respectively. Workers commonly upregulated oxidation‐reduction genes, possibly indicative of their active lifestyle. Host workers, but not workers of the slavemaker, upregulated a “social behavior” gene. In slavemaker queens and workers, genes associated with the regulation of transposable elements were upregulated. Queens of both species showed transcriptomic signals of anti‐aging mechanisms, with hosts upregulating various DNA repair pathways and slavemaker queens investing in trehalose metabolism. The transcriptomes of males showed enriched functions for quite general terms realized in different genes and pathways in each species. In summary, the strong interspecific commonalities in larvae, pupae, and workers were reflected in the same enriched Gene Ontology (GO) terms. Less commonalities occurred in the transcriptomes of queens and males, which apparently utilize different pathways to achieve a long life and sperm production, respectively. We found that all analyzed groups in this study show characteristic GO terms, with similar patterns in both species.