Hermógenes Fernández-Marín

Active use of the metapleural glands by ants in controlling fungal infection

Insect societies face constant challenges from disease agents. Ants deploy diverse antimicrobial compounds against pathogens and the key sources are metapleural glands (MGs). Are MG products passively secreted and used indiscriminately or are they selectively used when ants are challenged by pathogens? In 26 species from five subfamilies, ants use foreleg movements to precisely groom the MG opening. In the absence of experimental infection, MG grooming rates are low and workers groom themselves after contacting the MGs. The derived leaf-cutter ants (Atta and Acromyrmex) also groom their fungal gardens, substrata (leaves), queens and nest-mates after MG grooming. Atta respond to a challenge by fungal conidia by increasing the rate of MG grooming, but do not do so when an inert powder is applied. This increase occurs in the first hour after a potential infection, after which it returns to baseline levels. Ants with open MGs produce more infrabuccal pellets (IP) than ants with sealed MGs and conidia within pellets from the former are less likely to germinate. Thus, ants selectively groom their MGs when disease agents are present, suggesting that they also selectively use their MG secretions, which has important implications for understanding the evolution of hygienic behaviour in social groups.

Dynamic Disease Management in Trachymyrmex Fungus-Growing Ants (Attini: Formicidae)

Multipartner mutualisms have potentially complex dynamics, with compensatory responses when one partner is lost or relegated to a minor role. Fungus-growing ants (Attini) are mutualistic associates of basidiomycete fungi and antibiotic-producing actinomycete bacteria; the former are attacked by specialized fungi (Escovopsis) and diverse generalist microbes. Ants deploy biochemical defenses from bacteria and metapleural glands (MGs) and express different behaviors to control contaminants. We studied four Trachymyrmex species that differed in relative abundance of actinomycetes to understand interactions among antimicrobial tactics that are contingent on the nature of infection. MG grooming rate and actinomycete abundance were negatively correlated. The two species with high MG grooming rates or abundant actinomycetes made relatively little use of behavioral defenses. Conversely, the two species with relatively modest biochemical defenses relied heavily on behavior. Trade-offs suggest that related species can evolutionarily diverge to rely on different defense mechanisms against the same threat. Neither bacterial symbionts nor MG secretions thus appear to be essential for mounting defenses against the specialized pathogen Escovopsis, but reduced investment in one of these defense modes tends to increase investment in the other.

Ephemeral windows of opportunity for horizontal transmission of fungal symbionts in leaf-cutting ants.

Evolutionary theory predicts that hosts are selected to prevent mixing of genetically different symbionts when competition among lineages reduces the productivity of a mutualism. The symbionts themselves may also defend their interests: recent studies of Acromyrmex leaf-cutting ants showed that somatic incompatibility enforces single-clone gardens within mature colonies, thereby constraining horizontal transmission of fungal symbionts. However, phylogenetic analyses indicate that symbiont switches occur frequently enough to remove most signs of host-symbiont cocladogenesis. Here we resolve this paradox by showing that transmission among newly founded Acromyrmex colonies is not constrained. All tested queens of sympatric A. octospinosus and A. echinatior offered a novel fragment of fungus garden accepted the new symbiont. The outcome was unaffected by genetic distance between the novel and the original symbiont, and by the ant species the novel symbiont came from. The colony founding stage may thus provide an efficient but transient window for horizontal transmission, in which the fungus is unable to actively defend its partnership position before the host feeds on it, so that host fecal droplets remain compatible with alternative strains during the early stage of colony founding. We discuss how brief stages of low commitment between partners may increase the evolutionary stability of ancient coevolved mutualisms.

AN EVALUATION OF THE POSSIBLE ADAPTIVE FUNCTION OF FUNGAL BROOD COVERING BY ATTINE ANTS

Fungus‐growing ants (Myrmicinae: Attini) live in an obligate symbiotic relationship with a fungus that they rear for food, but they can also use the fungal mycelium to cover their brood. We surveyed colonies from 20 species of fungus‐growing ants and show that brood‐covering behavior occurs in most species, but to varying degrees, and appears to have evolved shortly after the origin of fungus farming, but was partly or entirely abandoned in some genera. To understand the evolution of the trait we used quantitative phylogenetic analyses to test whether brood‐covering behavior covaries among attine ant clades and with two hygienic traits that reduce risk of disease: mycelial brood cover did not correlate with mutualistic bacteria that the ants culture on their cuticles for their antibiotics, but there was a negative relationship between metapleural gland grooming and mycelial cover. A broader comparative survey showed that the pupae of many ant species have protective cocoons but that those in the subfamily Myrmicinae do not. We therefore evaluated the previously proposed hypothesis that mycelial covering of attine ant brood evolved to provide cocoon‐like protection for the brood.

Production of Minima Workers by Gynes of Atta colombica Guerin-Meneville (Hymenoptera: Formicidae: Attini) that Lack a Fungal Pellet

Abstract Early studies of Atta nest founding showed that gynes exhibit claustral nest foundation, cultivate fungal gardens with fecal secretions, and nourish their larvae with eggs. These studies also showed that gynes sometimes lose their fungal pellets, or the fungal garden fails before workers emerge, apparently dooming the incipient colony. Here we report that Atta colombica foundresses maintained in the laboratory can produce workers even though they lack fungal pellets to initiate gardens. If such behavior occurs in nature, it raises the possibility that workers might re-acquire a fungal symbiont after nest establishment, and potentially rescue failing colonies.

Eggs of the Blind Snake, Liotyphlops albirostris, Are Incubated in a Nest of the Lower Fungus-Growing Ant, Apterostigma cf. goniodes

Parental care is rare in most lower vertebrates. By selecting optimal oviposition sites, however, mothers can realize some benefits often associated with parental care. We found three ovoid reptilian eggs within a mature nest of a relatively basal fungus-growing ant, Apterostigma cf. goniodes (Attini), in central Panama. In laboratory colonies, A. cf. goniodes workers attended and cared for the eggs. Two blind snakes, Liotyphlops albirostris (Anomalepididae), successfully hatched, which is the first rearing record for this species. The ants did not disturb the snakes, and the snakes did not eat the ants; we found no ants in the dissected stomachs of the snakes. We review other associations between nesting fungus-growing ants and egg-laying vertebrates, which together suggest that attine nests may provide a safe, environmentally buffered location for oviposition, even in basal attine taxa with relatively small colony sizes.

A New Ectoparasitoid Species of Pseudogaurax Malloch, 1915 (Diptera: Chloropidae), Attacking the Fungus-Growing Ant, Apterostigma dentigerum Wheeler, 1925 (Hymenoptera: Formicidae)

Abstract Fungus-growing ants (Attini) are abundant and diverse, yet only one taxon of flies (Phoridae) and one of wasps (Diapriinae) are known parasitoids, and the biology of most species is not well known. Here we describe the first evidence for an ant parasitoid in the family Chloropidae (Diptera), in which larvae of Pseudogaurax paratolmos Wheeler, new species, parasitize larvae of the ant, Apterostigma dentigerum Wheeler, 1925. Larval flies are solitary ectoparasitoids, each of which attaches to a single ant larva and develops from larva to pupa in ~2 wk, consuming nearly the entire host, and then ecloses as an adult ~1 wk later. Overall parasitism prevalence was 6.8% of 203 nests, and flies were active during both the dry and rainy seasons. Intensity of parasitism ranged from 18.2 to 100% of larvae attacked per parasitized nest. No other species of Apterostigma that nested in the same localities were parasitized by the flies, including A. pilosum (Mayr, 1865) (n = 93 nests) and A. auriculatum (Wheeler, 1925) (n = 10 nests). All immature ants, parasitized or not, as well as immature stages of Pseudogaurax paratolmos, were attended by adult ants that exhibited normal brood care behavior, including covering immatures with mycelia, grooming, and maintaining brood in the fungus garden.

Use of Communal Nests by Male and Female Trachypus petiolatus (Hymenoptera: Sphecidae)

Abstract The nesting behavior of Trachypus petiolatus is described from central Panamá. Females nested within aggregations in bare soil; they re-used nests from a prior generation, and provisioned their nests with small bees, mainly Apidae and Halictidae. These nests had a communal social organization among resident females, and also included one or more males. At least some males left the nest in the morning on a daily basis, and then returned later in the day. Based on limited nest excavations, we did not observe any parasitized cells, which may be associated with communal nesting.

Slowing them down will make them lose: a role for attine ant crop fungus in defending pupae against infections?

Summary Fungus‐growing ants (Attini) have evolved an obligate dependency upon a basidiomycete fungus that they cultivate as their food. Less well known is that the crop fungus is also used by many attine species to cover their eggs, larvae and pupae. The adaptive functional significance of this brood covering is poorly understood. One hypothesis to account for this behaviour is that it is part of the pathogen protection portfolio when many thousands of sister workers live in close proximity and larvae and pupae are not protected by cells, as in bees and wasps, and are immobile. We performed behavioural observations on brood covering in the leaf‐cutting ant Acromyrmex echinatior, and we experimentally manipulated mycelial cover on pupae and exposed them to the entomopathogenic fungus Metarhizium brunneum to test for a role in pathogen resistance. Our results show that active mycelial brood covering by workers is a behaviourally plastic trait that varies temporally, and across life stages and castes. The presence of a fungal cover on the pupae reduced the rate at which conidia appeared and the percentage of pupal surface that produced pathogen spores, compared to pupae that had fungal cover experimentally removed or naturally had no mycelial cover. Infected pupae with mycelium had higher survival rates than infected pupae without the cover, although this depended upon the time at which adult sister workers were allowed to interact with pupae. Finally, workers employed higher rates of metapleural gland grooming to infected pupae without mycelium than to infected pupae with mycelium. Our results imply that mycelial brood covering may play a significant role in suppressing the growth and subsequent spread of disease, thus adding a novel layer of protection to their defence portfolio.