Social alliances are rare. Only in a handful of species, such as fiddler crabs and chipping sparrows, do unrelated neighbours team-up when a member of the same species invades their territory. Near-by residents will aid their harassed compatriots and help to ward off the assailant, so long as the invader presents a threat to the neighbourhood. Posing a threat can really amount to being ‘sexier’ than the neighbour: having a larger claw or a prettier song. However, past studies focused solely on the point of view of the animals leaping to a neighbour's defence, and less often included how the resident under siege responded.
To capture both perspectives – that of the threatened animal and its allies – neuroscientist Chelsea Weitekamp and colleagues in Hans Hofmann’s lab at the University of Texas, USA, compared how an intruder elicits different behavioural and biological responses depending on the social role of a cooperative territorial teleost fish, the African cichlid (Astatotilapia burtoni).
Initially, Weitekamp set up two fish tanks next to each other, each tank containing one male and two female cichlids, and allowed the neighbouring fish tank communities to acclimate to one another over the next 4 days. On the fifth day, Weitekamp placed an intruder fish into one of the tanks (the ‘residents’ tank), and noted how aggressively the residents and their neighbours responded to the interloper. Following harassment by the intruder, Weitekamp then measured how the encounter changed hormone levels in the blood and gene expression in the brain in both the resident and neighbouring males.
During the intrusion, the residents lashed out more often at the intruder than did their neighbours. And, although the resident and neighbouring males pumped similar amounts of the sex hormone testosterone and the stress hormone cortisol into their systems, only testosterone levels in neighbours, but not residents, predicted how aggressively a fish would respond.
Focusing on the effects of the intruder on the brains of the fish from the neighbouring tank, the team found that expression of the egr-1 gene (which occurs when neurons are activated) in the amygdala region of the brain, which mediates social behaviour, increased as the fish became more aggressive. In addition, Weitekamp realised that as the concerned neighbours became increasingly aggressive, they expressed more genes that mediate social behaviours [such as the serotonin (5-htr2c) and dopamine (d1r) receptors] in the amygdala, in addition to producing more testosterone.
In contrast, Weitekamp found no evidence of any other changes in the brains or bodies of the resident fish, aside from soaring levels of testosterone as they lashed out. Further, resident fish's aggression didn't relate to any changes in gene expression or hormone levels.
These intriguing findings – that harassed residents become more aggressive during an intrusion while their neighbours enhance the social side of their characters – are beginning to shape our understanding of how social roles mediate divergent behavioural and biological responses to a territorial threat. In cichlids at least, a fellow territorial fish next door makes for the most vigilant and responsive neighbourhood watch.
