Convergent loss of chemoreceptors across independent origins of slave-making in ants

Abstract

The evolution of an obligate parasitic lifestyle often leads to the reduction of morphological and physiological traits, which may be accompanied by loss of genes and functions. Slave-maker ants are social parasites that exploit the work force of closely related ant species for social behaviours such as brood care and foraging. Recent divergence between these social parasites and their hosts enables comparative studies of gene family evolution. We sequenced the genomes of eight ant species, representing three independent origins of ant slavery. During the evolution of eusociality, chemoreceptor genes multiplied due to the importance of chemical communication in societies. We investigated evolutionary patterns of chemoreceptors in relation to slave-making in ants. We found that slave-maker ant genomes harboured only half as many gustatory receptors as their hosts, potentially mirroring the outsourcing of foraging tasks to host workers. In addition, parasites had fewer odorant receptors and their loss shows patterns of convergence across origins of parasitism, representing a rare case of convergent molecular evolution. This convergent loss of specific odorant receptors suggests that selective deprivation of receptors is adaptive. The 9-exon odorant receptor subfamily, previously linked to social evolution in insects, was significantly enriched for convergent loss across the three origins of slavery in our study, indicating that the transition to social parasitism in ants is accompanied by the loss of receptors that are likely important for mediating eusocial behaviour. Overall, gene loss in slave-maker ants suggests that a switch to a parasitic lifestyle accompanies relaxed selection on chemical perception.

The genomic basis of army ant chemosensory adaptations

“…While these were published too recently to be included in our in-depth comparative analyses, it is worth noting some striking similarities and differences in these ant groups relative to E. burchellii. Specifically, both studies found large contractions in the OR family in social parasites compared with their free-living relatives (Schrader et al, 2021, Jongepier et al, 2021. This suggests that olfactory system simplification is a common theme of ecological specialization in ants.…”

“…burchellii . Specifically, both studies found large contractions in the OR family in social parasites compared with their free‐living relatives (Schrader et al, 2021 , Jongepier et al, 2021 ). This suggests that olfactory system simplification is a common theme of ecological specialization in ants.…”

“…This suggests that there may be fundamental differences in the olfactory processes related to finding host colonies to parasitize vs. distinguishing between prey species during raids. Of note, most inquilines and kidnapping ants parasitize closely related ant species (Schrader et al, 2021 , Jongepier et al, 2021 ), and thus they may be ancestrally able to detect volatile host pheromones.…”

“…Recently, two studies have been published examining the genomic consequences of ecological specialization in socially parasitic inquiline (Schrader et al, 2021) and kidnapping (Jongepier et al, 2021) ant species. While these were published too recently to be included in our in-depth comparative analyses, it is worth noting some striking similarities and differences in these ant groups relative to E. burchellii.…”

The influence of parasite load on transcriptional activity and morphology of a cestode and its ant intermediate host

“…Subsequently, the quality of the reads was assessed using FastQC (Andrews, 2010). Filtered reads were mapped against the T. nylanderi genome assembly (Jongepier et al, 2022) using HISAT2 v2.1.0 (Kim et al, 2015) with the --dta parameter in preparation for genome-guided assembly. The resulting BAM files were sorted and indexed using Samtools v0.1.19 (Li et al, 2009) and used to generate a genome-guided transcriptome assembly using StringTie v1.3.6 (Pertea et al, 2015).…”