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.
Highlights
The ecological success of social Hymenoptera is based on tight cooperation and an efficient division of labor in their colonies
For single-copy orthologous genes upregulated in the host T. longispinosus compared to the slave-making ant T. americanus and vice versa, we found the smallest difference in the number of differentially expressed genes (DEGs) between T. longispinosus and T. americanus workers (245, 0.8%)
More differences in gene expression were found between T. longispinosus and T. americanus queens, which differentially expressed 1,916 genes (6.23%), and especially between males, for which we found the strongest transcriptomic differences (3,103 genes, 10.09%)
Summary
The ecological success of social Hymenoptera is based on tight cooperation and an efficient division of labor in their colonies. Young slavemaker queens usurp a nest of another, closely related ant species (“Emery's rule,” Emery, 1909). Young slave-making workers participate in reproduction and lay unfertilized male-destined eggs even in the presence of the queen (Brunner, Trindl, Falk, Heinze, & d'Ettorre, 2005; Foitzik & Herbers, 2001; Franks & Scovell, 1983; Heinze, 1996), while host workers typically reproduce only in the queens' absence (Bourke, 1988). The aim of the present study is to identify characteristic expression patterns of larvae, worker pupae, workers, queens, and males and to search for commonalities and differences between the two ant species T. americanus and T. longispinosus. Queens of the two species are predicted to show strong transcriptomic correlates of reproduction and longevity (e.g., Negroni, Foitzik, & Feldmeyer, 2019) Due to their different life histories, worker and queen transcriptomes might show less interspecies commonalities in gene expression. The short-lived males are expected to strongly invest in sperm production and less in anti-aging mechanisms
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