Ant behaviour and brain gene expression of defending hosts depend on the ecological success of the intruding social parasite

Abstract

The geographical mosaic theory of coevolution predicts that species interactions vary between locales. Depending on who leads the coevolutionary arms race, the effectivity of parasite attack or host defence strategies will explain parasite prevalence. Here, we compare behaviour and brain transcriptomes of Temnothorax longispinosus ant workers when defending their nest against an invading social parasite, the slavemaking ant Temnothorax americanus . A full-factorial design allowed us to test whether behaviour and gene expression are linked to parasite pressure on host populations or to the ecological success of parasite populations. Albeit host defences had been shown before to covary with local parasite pressure, we found parasite success to be much more important. Our chemical and behavioural analyses revealed that parasites from high prevalence sites carry lower concentrations of recognition cues and are less often attacked by hosts. This link was further supported by gene expression analysis. Our study reveals that host–parasite interactions are strongly influenced by social parasite strategies, so that variation in parasite prevalence is determined by parasite traits rather than the efficacy of host defence. Gene functions associated with parasite success indicated strong neuronal responses in hosts, including long-term changes in gene regulation, indicating an enduring impact of parasites on host behaviour. This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.

Tandem‐running and scouting behaviour are characterized by up‐regulation of learning and memory formation genes within the ant brain

“…Another important learning gene is glutamate receptor ionotropic, NMDA 2B isoform X3 , which was up‐regulated in T. longispinosus scouts compared to followers (Table ). In an earlier study, we already found glutamate receptor NMDA to be up‐regulated in the brain of T. longispinosus workers, at that time in response to an attacking slavemaker (Kaur et al, ). Our findings are in line with previous investigations into honeybees, in which genes related to glutamate signalling were up‐regulated in scouts (Liang et al, ).…”

The coevolutionary biology of brood parasitism: a call for integration

“…Stoddard et al [56] Yang et al [57] Kaur et al [59] Hanley et al [60] McClelland et al [76] What cognitive rules do hosts use to distinguish kin from non-kin?…”

Defences against brood parasites from a social immunity perspective

“…Insect hosts of brood parasites, on the other hand, tend to have distinctive cuticular hydrocarbon profiles that can be used to discriminate kin or social partners [92 -95], leading to chemical mimicry [96] or camouflage [97]. Kaur et al [21] measured the aggressive responses displayed by hosts to slavemaking ants across a number of populations. Surprisingly, the best predictor of the host response, both behaviourally and in terms of gene expression in the brain, was the ecological success of the parasite.…”

“…In the most extreme cases, hosts can even abandon a nest that is heavily infected with parasites, as has been shown in ants [38] and termites [39], thus killing the parasite by depriving it of hosts. Similarly, brood parasite hosts can also show resistance by ejecting the parasite from the nest [98] or directly killing it [21]. There is also evidence that some hosts will abandon infected nests after brood parasites have been detected.…”

“…For example, brown-headed cowbird (Molothrus ater) hosts have been shown to desert parasitized nests [99] and mason bees (Osmia spp.) have been shown to abandon the tunnels they have been provisioning once one of the brood cells becomes parasitized [21]. Similarly, Myrmica ants have been shown to abandon nests where a virulent species of Maculinea caterpillar has become established [100].…”