The metapleural gland (MG) is a complex glandular structure unique to ants, suggesting a critical role in their origin and ecological success. We synthesize the current understanding of the adaptive function, morphology, evolutionary history, and chemical properties of the MG. Two functions of the MG, sanitation and chemical defence, have received the strongest empirical support; two additional possible functions, recognition odour and territorial marking, are less well supported. The design of the MG is unusual for insects; glandular secretions are stored in a rigid, non-compressible invagination of the integument and the secretion is thought to ooze out passively through the non-closable opening of the MG or is groomed off by the legs and applied to target surfaces. MG loss has occurred repeatedly among the ants, particularly in the subfamilies Formicinae and Myrmicinae, and the MG is more commonly absent in males than in workers. MG chemistry has been characterized mostly in derived ant lineages with unique biologies (e.g. leafcutter ants, fire ants), currently precluding any inferences about MG chemistry at the origin of the ants. A synthetic approach integrating functional morphology, phylogenetic transitions and chemical ecology of the MGs of both the derived and the unstudied early-branching (basal) ant lineages is needed to elucidate the evolutionary origin and diversification of the MG of ants.
Sexual reproduction generally requires no more than two partners. Here, we show convergent evolution of social hybridogenesis, a reproductive system requiring three reproductive partners in harvester ants. In this unorthodox reproductive system, two distinct genetic lineages live in sympatry and queens have to mate with males of their own lineage to produce queens along with males of the alternative lineage to produce workers. Using a large transcriptomic data set of nine species, we show that social hybridogenesis evolved at least three times independently in the genus Messor. Moreover, a study of 13 populations of Messor barbarus revealed that this mode of reproduction is fixed in the whole range of this ecologically dominant species. Finally, we show that workers can produce males carrying genes of the two genetic lineages, raising the possibility of rare gene flow between lineages contributing to the long-term maintenance of pairs of interdependent lineages. These results emphasize the evolutionary importance of social hybridogenesis, a major transition possibly linked to the peculiar ecology of harvester ants.
Social insects in general and leaf-cutting ants in particular have increased selection pressures on their innate immune system due to their social lifestyle and monoclonality of the symbiotic fungal cultivar. As this symbiosis is obligate for both parties, prophylactic behavioural defences against infections are expected to increase either ant survival or fungus-garden survival, but also to possibly trade off when specific infections differ in potential danger. We examined the effectiveness of prophylactic behaviours and modulations of innate immune defences by a combination of inoculation bioassays and genome-wide transcriptomic studies (RNA-Seq), using an ant pathogen (Metarhizium brunneum) and a fungus-garden pathogen (Escovopsis weberi) and administering inoculations both directly and indirectly (via the symbiotic partner). Upon detection of pathogen conidia, ant workers responded by increasing both general activity and the frequency of specific defence behaviours (self-grooming, allo-grooming, garden-grooming) independent of the pathogen encountered. This trend was also evident in the patterns of gene expression change. Both direct and indirect (via fungus garden) inoculations with Metarhizium induced a general up-regulation of gene expression, including a number of well-known immune-related genes. In contrast, direct inoculation of the fungus garden by Escovopsis induced an overall down-regulation of ant gene expression, whereas indirect inoculation (via the ants) did not, suggesting that increased activity of ants to remove this fungus-garden pathogen is costly and involves trade-offs with the activation of other physiological pathways.
Ants have paired metapleural glands (MGs) to produce secretions for prophylactic hygiene. These exocrine glands are particularly well developed in leaf-cutting ants, but whether the ants can actively regulate MG secretion is unknown. In a set of controlled experiments using conidia of five fungi, we show that the ants adjust the amount of MG secretion to the virulence of the fungus with which they are infected. We further applied fixed volumes of MG secretion of ants challenged with constant conidia doses to agar mats of the same fungal species. This showed that inhibition halos were significantly larger for ants challenged with virulent and mild pathogens/weeds than for controls and Escovopsischallenged ants. We conclude that the MG defence system of leaf-cutting ants has characteristics reminiscent of an additional cuticular immune system, with specific and non-specific components, of which some are constitutive and others induced.
BackgroundThe obligate mutualism between fungus-growing ants and microbial symbionts offers excellent opportunities to study the specificity and stability of multi-species interactions. In addition to cultivating fungus gardens, these ants have domesticated actinomycete bacteria to defend gardens against the fungal parasite Escovopsis and possibly other pathogens. Panamanian Acromyrmex echinatior leaf-cutting ants primarily associate with actinomycetes of the genus Pseudonocardia. Colonies are inoculated with one of two vertically transmitted phylotypes (Ps1 or Ps2), and maintain the same phylotype over their lifetime. We performed a cross-fostering experiment to test whether co-adaptations between ants and bacterial phylotypes have evolved, and how this affects bacterial growth and ant prophylactic behavior after infection with Escovopsis.ResultsWe show that Pseudonocardia readily colonized ants irrespective of their colony of origin, but that the Ps2 phylotype, which was previously shown to be better able to maintain its monocultural integrity after workers became foragers than Ps1, reached a higher final cover when grown on its native host than on alternative hosts. The frequencies of major grooming and weeding behaviors co-varied with symbiont/host combinations, showing that ant behavior also was affected when cuticular actinomycete phylotypes were swapped.ConclusionThese results show that the interactions between leaf-cutting ants and Pseudonocardia bear signatures of mutual co-adaptation within a single ant population.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0308-2) contains supplementary material, which is available to authorized users.
Fungus-growing ants have interacted and partly coevolved with specialised microfungal parasites of the genusEscovopsissince the origin of ant fungiculture about 50 million years ago. Here, we review the recent progress in understanding the patterns of specificity of this ant-parasite association, covering both the colony/population level and comparisons between phylogenetic clades. We use a modified version of Tinbergen's four categories of evolutionary questions to structure our review in complementary approaches addressing both proximate questions of development and mechanism, and ultimate questions of (co)adaptation and evolutionary history. Using the same scheme, we identify future research questions that are likely to be particularly illuminating for understanding the ecology and evolution ofEscovopsisparasitism of the cultivar maintained by fungus-growing ants.
The mechanism by which palatable species take advantage of their similarity in appearance to those that are unpalatable, in order to avoid predation, is called Batesian mimicry. Several arthropods are thought to be Batesian mimics of social insects; however, social insects that are Batesian mimics among themselves are rare. In Malaysia we found a possible Batesian mimic in an arboreal ant species, Camponotus sp., which was exclusively observed on foraging trails of the myrmicine ant Crematogaster inflata. The bright yellow and black colouring pattern, as well as the walking behaviour, were very similar in both species. We observed general interactions between the two species, and tested their palatability and the significance of the remarkably similar visual colour patterns for predator avoidance. Prey offered to C. inflata was also eaten by Camponotus workers in spite of their being attacked by C. inflata, indicating that Camponotus sp. is a commensal of C. inflata. An experiment with chicks as potential predators suggests that Camponotus sp. is palatable whereas C. inflata is unpalatable. After tasting C. inflata, the chicks no longer attacked Camponotus sp., indicating that Camponotus sp. is a Batesian mimic of Crematogaster inflata.
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