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'.

Keywords: Temnothorax longispinosus; coevolution; parasite prevalence; slavemaking ants; social parasites; transcriptomics.

Figure 1.

(a) Proportion of host workers involved in defence against the intruding slavemaker was affected by an interaction between the success of the slavemaking population (parasite prevalence_PARASITE) and host colony size. Lines represent three different colony size classes (large = mean + 1 s.d.: solid line; midsized colonies = mean: long-dashed line; small colonies = mean − 1 s.d.: short-dashed line). (b) The percentage of slavemaker intruders that were immobilized or killed by host defenders (proportion of pinned SM) depended on the success of the slavemaking population (parasite prevalence_PARASITE, brown squares, dashed line), but not on parasite pressure (blue circles, dotted line). (c) Total proportion of cuticular recognition cues in T. americanus in relation to its success. Each data point (n = 40) represents the proportion of recognition cues in the CHC profile of one T. americanus worker (i.e. nine CHCs identified as relevant for nestmate recognition in T. longispinosus). The graph shows a linear regression line with 95% confidence interval. (d) T. americanus slavemaker worker (left) interacting with a smaller T. longispinosus host worker (drawing by Inon Scharf). (Online version in colour.)

Figure 2.

(a) Multi-dimensional scaling (MDS) plot showing sample distribution based on variance in gene expression including all contigs. Different shades of red denote variation in prevalence of the population of the parasite intruder (parasite prevalence_PARASITE). As parasite prevalence_PARASITE was negatively linked to whether or not an intruding slavemaker was immobilized or killed during host colony intrusion, the respective arrows point in the opposite direction. Distribution of samples did not vary with parasite prevalence in the host colony's source population (see Results for details). Plot created using the R package vegan v. 2.5-2. (b) Venn diagram showing the number of genes differentially expressed between hosts that do or do not attack the intruding slavemaker (right, bottom and top) and between hosts facing more or less successful slavemakers (left, top and bottom). Diagram created using the R package VennDiagram v. 1.6.20 (https://www.rdocumentation.org/packages/VennDiagram/versions/1.6.20).

Figure 3.

Heatmap based on the expression patterns found in all differentially expressed genes. Dendrogram showing relationships between samples based on similarities in gene expression. Colour bars above dendrogram show the parasite prevalence in the host population (blue), whether the slavemaker was immobilized/killed by the hosts (black) and the parasite prevalence of the population of the intruding slavemaker (orange). Heatmap created using R v. 3.4.4.

Figure 4.

Enriched GO terms in three WGCNA modules which were significantly associated with prevalence in the parasite population and whether or not a slavemaker was attacked/killed by host defenders. Genes in modules were either positively or negatively linked to parasite prevalence_PARASITE or under attack/no attack state of slavemakers, visualized using the R package tagcloud v. 0.6 (https://CRAN.R-project.org/package=tagcloud). The type size denotes the number of genes with this annotation (in green) found in the respective module. (Online version in colour.)