Mechanisms of recognition are essential to the evolution of mutualistic and parasitic interactions between species. One such example is the larval mimicry that Maculinea butterfly caterpillars use to parasitize Myrmica ant colonies. We found that the greater the match between the surface chemistry of Maculinea alcon and two of its host Myrmica species, the more easily ant colonies were exploited. The geographic patterns of surface chemistry indicate an ongoing coevolutionary arms race between the butterflies and Myrmica rubra , which has significant genetic differentiation between populations, but not between the butterflies and a second, sympatric host, Myrmica ruginodis , which has panmictic populations. Alternative hosts may therefore provide an evolutionary refuge for a parasite during periods of counteradaptation by their preferred hosts.

The attine ant–fungus agricultural symbiosis evolved over tens of millions of years, producing complex societies with industrial-scale farming analogous to that of humans. Here we document reciprocal shifts in the genomes and transcriptomes of seven fungus-farming ant species and their fungal cultivars. We show that ant subsistence farming probably originated in the early Tertiary (55–60 MYA), followed by further transitions to the farming of fully domesticated cultivars and leaf-cutting, both arising earlier than previously estimated. Evolutionary modifications in the ants include unprecedented rates of genome-wide structural rearrangement, early loss of arginine biosynthesis and positive selection on chitinase pathways. Modifications of fungal cultivars include loss of a key ligninase domain, changes in chitin synthesis and a reduction in carbohydrate-degrading enzymes as the ants gradually transitioned to functional herbivory. In contrast to human farming, increasing dependence on a single cultivar lineage appears to have been essential to the origin of industrial-scale ant agriculture.

Eusocial hymenopteran males have exceptionally high levels of ejaculate quality, which are assumed to result from extreme selection pressures for pre- and postcopulatory male–male competition and the necessity to retain viable sperm after years of storage in female (queen) spermathecae. We hypothesized that the production of high-quality sperm carries substantial costs so that fertility of males may be compromised by stress factors when they are operating at their physiological limits. To test this, we performed a series of experiments using honeybees as our model system, to establish possible effects of male age on sperm quality and to evaluate effects of elevated temperatures, food deprivation during sexual maturation, and immune challenges. We found that sperm viability decreases with male age but that males of some colonies were better able to delay ejaculate senescence than others. Exposure to elevated temperatures and wounding both significantly decreased male fecundity, but protein deficiency after hatching did not. This suggests that investment in drones is completed at pupation and that sexual maturation does not require additional protein feeding. The sensitivity of drone fitness to stress factors related to temperature and immune system activation illustrates that hygienic monitoring and active thermoregulation by workers are essential for colony-level reproductive success. These results underline that honeybee drones have been under strong selection for extreme specialization on reproductive performance and that this precludes any exposure to the stressful conditions that foraging workers normally experience.

To combat disease, most fungus-growing ants (Attini) use antibiotics from mutualistic bacteria ( Pseudonocardia ) that are cultured on the ants' exoskeletons and chemical cocktails from exocrine glands, especially the metapleural glands (MG). Previous work has hypothesized that (i) Pseudonocardia antibiotics are narrow-spectrum and control a fungus ( Escovopsis ) that parasitizes the ants' fungal symbiont, and (ii) MG secretions have broad-spectrum activity and protect ants and brood. We assessed the relative importance of these lines of defence, and their activity spectra, by scoring abundance of visible Pseudonocardia for nine species from five genera and measuring rates of MG grooming after challenging ants with disease agents of differing virulence. Atta and Sericomyrmex have lost or greatly reduced the abundance of visible bacteria. When challenged with diverse disease agents, including Escovopsis , they significantly increased MG grooming rates and expanded the range of targets. By contrast, species of Acromyrmex and Trachymyrmex maintain abundant Pseudonocardia. When challenged, these species had lower MG grooming rates, targeted primarily to brood. More elaborate MG defences and reduced reliance on mutualistic Pseudonocardia are correlated with larger colony size among attine genera, raising questions about the efficacy of managing disease in large societies with chemical cocktails versus bacterial antimicrobial metabolites.