Genomic basis of adaptation to climate and parasite prevalence and the importance of odorant perception in the ant Temnothorax longispinosus.

A co-evolutionary arms race ensues when parasites exhibit exploitative behaviour, which prompts adaptations in their hosts, in turn triggering counter-adaptations by the parasites. To unravel the genomic basis of this coevolution from the host's perspective, we collected ants of the host species Temnothorax longispinosus, parasitized by the social parasite Temnothorax americanus, from 10 populations in the northeastern United States exhibiting varying levels of parasite prevalence and living under different climatic conditions. We conducted a genome-wide association study (GWAS) to identify single nucleotide polymorphisms (SNPs) associated with both prevalence and climate. Our investigation highlighted a multitude of candidate SNPs associated with parasite prevalence, particularly in genes responsible for sensory perception of smell including odorant receptor genes. We further focused on population-specific compositions of cuticular hydrocarbons, a complex trait important for signalling, communication and protection against desiccation. The relative abundances of n-alkanes were correlated with climate, while there was only a trend between parasite prevalence and the relative abundances of known recognition cues. Furthermore, we identified candidate genes likely involved in the synthesis and recognition of specific hydrocarbons. In addition, we analysed the population-level gene expression in the antennae, the primary organ for odorant reception, and established a strong correlation with parasite prevalence. Our comprehensive study highlights the intricate genomic patterns forged by the interplay of diverse selection factors and how these are manifested in the expression of various phenotypes.

Brain and antennal transcriptomes of host ants reveal potential links between behaviour and the functioning of socially parasitic colonies.

Insect social parasites are characterized by exploiting the hosts' social behaviour. Why exactly hosts direct their caring behaviour towards these parasites and their offspring remains largely unstudied. One hypothesis is that hosts do not perceive their social environment as altered and accept the parasitic colony as their own. We used the ant Leptothorax acervorum, host of the dulotic, obligate social parasite Harpagoxenus sublaevis, to shed light on molecular mechanisms underlying behavioural exploitation by contrasting tissue-specific transcriptomes in young host workers. Host pupae were experimentally (re-)introduced into fragments of their original, another conspecific, heterospecific or parasitic colony. Brain and antennal mRNA was extracted and sequenced from adult ants after they had lived in the experimental colony for at least 50 days after eclosion. The resulting transcriptomes of L. acervorum revealed that ants were indeed affected by their social environment. Host brain transcriptomes were altered by the presence of social parasites, suggesting that the parasitic environment influences brain activity, which may be linked to behavioural changes. Transcriptional activity in the antennae changed most with the presence of unrelated individuals, regardless of whether they were conspecifics or parasites. This suggests early priming of odour perception, which was further supported by sensory perception of odour as an enriched function of differentially expressed genes. Furthermore, gene expression in the antennae, but not in the brain corresponded to ant worker behaviour before sampling. Our study demonstrated that the exploitation of social behaviours by brood parasites correlates with transcriptomic alterations in the central and peripheral nervous systems.

Molecular (co)evolution of hymenopteran social parasites and their hosts.

Social parasitism describes a fascinating way of life in which species exploit the altruistic behaviour of closely related, social species. Social parasites have repeatedly evolved in the social Hymenoptera, including ants, bees, and wasps. The common ancestry and shared (social) environment with their hosts facilitates the study of molecular adaptations to the parasitic lifestyle. Moreover, when social parasites are widespread and virulent, they exert strong selection pressure on their hosts, leading to the evolution of defense mechanisms and triggering a coevolutionary arms race. Recent advances in sequencing technology now make it possible to study the molecular basis of this coevolutionary process. In addition to describing the latest developments, we highlight open research questions that could be tackled with genomic, transcriptomic, or epigenetic data.

Molecular regulation of lifespan extension in fertile ant workers.

The evolution of sociality in insects caused a divergence in lifespan between reproductive and non-reproductive castes. Ant queens can live for decades, while most workers survive only weeks to a few years. In most organisms, longevity is traded-off with reproduction, but in social insects, these two life-history traits are positively linked. Once fertility is induced in workers, e.g. by queen removal, worker lifespan increases. The molecular regulation of this positive link between fecundity and longevity and generally the molecular underpinnings of caste-specific senescence are not well understood. Here, we investigate the transcriptomic regulation of lifespan and reproduction in fat bodies of three worker groups in the ant Temnothorax rugatulus. In a long-term experiment, workers that became fertile in the absence of the queen showed increased survival and upregulation of genes involved in longevity and fecundity pathways. Interestingly, workers that re-joined their queen after months exhibited intermediate ovary development, but retained a high expression of longevity and fecundity genes. Strikingly, the queen's presence causes a general downregulation of genes in worker fat bodies. Our findings point to long-term consequences of fertility induction in workers, even after re-joining their queen. Moreover, we reveal longevity genes and pathways modulated during insect social evolution. This article is part of the theme issue 'Ageing and sociality: why, when and how does sociality change ageing patterns?'