Gene expression of tandem-running in Temnothorax

Tandem-running in ants has been described as a form of teaching, where spatial information possessed by a leader is conveyed to a following nestmate. Within Temnothorax ants, tandem-running is used within a variety of contexts, from foraging and nest relocation to – in the case of slavemaking species – raiding parties. Here, we elucidate the transcriptomic basis of scouting, tandem-leading, and tandem-following behavior across two species with opposing lifestyles: the slavemaking Temnothorax americanus and its primary, non-parasitic host T. longispinosus. Analysis of gene expression data from brains revealed that only a small number of unique differentially-expressed genes are responsible for scouting and tandem-running behaviors. Comparison of orthologous genes between T. americanus and T. longispinosus suggests that tandem-running is characterized by species-specific patterns of gene usage. However, within both species, tandem-leaders showed gene expression patterns median to those of scouts and tandem-followers. This is not unexpected, as leaders can be recruited from either of the other two behavioral states. Most importantly, a number of differentially-expressed behavioral genes were found, with functions relating to learning and memory formation in other social and non-social insect species; including glutamate and tyramine receptor genes. Learning and memory genes were specifically upregulated within scouts and tandem-followers, which use spatial learning extensively to navigate novel environments. As such, results of our analyses suggest that tandem-running in Temnothorax ants involves learning of novel information by following individuals and possibly even teaching by leading individuals.