Gstoettl C, Stoldt M, Jongepier E, Bornberg-Bauer E , Feldmeyer B, Heinze J, Foitzik S
Comparative analysis of caste, sex and developmental stage-specific transcriptomes of a slavemaking ant and its ant host sheds light onto slavemaker evolution
Molecula Ecololgy, 2019

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Abstract

One of the most fascinating life histories of social insects are exhibited by slavemaking ants, which parasitize the social behavior of their ant hosts. Slavemaking queens usurp host colonies and force emerging young workers to care for their brood. Slavemaker workers never work. Instead, some of them produce males from unfertilized eggs, while others conduct raids and pillage brood from neighboring host nests. Slavemaking ants evolved from non-parasitic ancestors and enslave related species. This allows studying how gene expression changed during this lifestyle transition. To elucidate the molecular basis of slavemaker evolution we compared transcriptomes of different developmental stages (larvae, pupae, adults), castes (queens, workers), and sexes (females, males) of two related ant species, the slavemaker Temnothorax americanus (= Protomognathus americanus) and its host T. longispinosus. While the phenotypes of slavemaker males, larvae, and pupae resemble those of their host, queens and workers show lifestyle-specific morphologies and behavior. In particular, larvae and pupae showed similarities across species, upregulating genes with enriched functions of translation and chitin metabolism, respectively. Workers of both species upregulated oxidation-reduction genes, but only host workers upregulated genes assigned to the GO-term ‘social behavior.’ Gene expression patterns differed less between slavemaker queens and workers than between these two castes in the host, indicating that caste differences diminished during slavemaker evolution. This matches differences in phenotype, as slavemaker workers resemble queens in fertility and reluctance to work.