Chemically armed mercenary ants protect fungus-farming societies

The ants are extraordinary in having evolved many lineages that exploit closely related ant societies as social parasites, but social parasitism by distantly related ants is rare. Here we document the interaction dynamics among a Sericomyrmex fungus-growing ant host, a permanently associated parasitic guest ant of the genus Megalomyrmex, and a raiding agro-predator of the genus Gnamptogenys. We show experimentally that the guest ants protect their host colonies against agro-predator raids using alkaloid venom that is much more potent than the biting defenses of the host ants. Relatively few guest ants are sufficient to kill raiders that invariably exterminate host nests without a cohabiting guest ant colony. We also show that the odor of guest ants discourages raider scouts from recruiting nestmates to host colonies. Our results imply that Sericomyrmex fungus-growers obtain a net benefit from their costly guest ants behaving as a functional soldier caste to meet lethal threats from agro-predator raiders. The fundamentally different life histories of the agro-predators and guest ants appear to facilitate their coexistence in a negative frequency-dependent manner. Because a guest ant colony is committed for life to a single host colony, the guests would harm their own interests by not defending the host that they continue to exploit. This conditional mutualism is analogous to chronic sickle cell anemia enhancing the resistance to malaria and to episodes in human history when mercenary city defenders offered either net benefits or imposed net costs, depending on the level of threat from invading armies.Ant societies retain much of their coherence through chemical nestmate recognition (1, 2), which allows resident workers to differentiate between friend and foe by colony-specific chemical signatures (3). This recognition system is not infallible, however; numerous species have evolved ways to evade detection so they can exploit ant colonies through invasion, usurpation, or thievery (2). One common route to social parasitism is shown convergently by many ant genera in which social parasites are their host’s closest relatives, a scenario that might have arisen through sympatric speciation (4, 5). At the other end of the spectrum are interactions with different insect orders, such as parasitic beetles and butterfly caterpillars, that drain host ant colonies of resources while remaining protected by crypsis or chemical mimicry (6).Intermediate types of parasitic interactions involving ants that exploit other, distantly related ants are rare (7). Several species of Megalomyrmex (Solenopsidini) belong to this category, associating in varying capacities with fungus-growing ant hosts (Attini), a clade of the same ant subfamily (8–12) (Fig. 1). Most details about the diversity and life history adaptations of these ants have been clarified only recently (11), and much of their biology remains to be discovered (SI Text: Study System and Tables S1 and S2). Free-living predatory Megalomyrmex are known to biosynthesize venom alkaloids that are used in defense (13, 14) whereas the fungus-growing ant associates seem to aggressively dispense these venoms when they attack host colonies (15). Some of these parasites are obligate or facultative thief ants consuming brood and fungus gardens (15), whereas others are specialized agro-predators that move from one host colony to the other after usurping fungus gardens and killing or chasing away the resident ants (10). Despite the often high densities of their attine hosts, these Megalomyrmex social parasites remain rare, with parasitism rates of ∼1.5–14% (10, 15), similar to the rates of many other social parasites (5).Open in a separate windowFig. 1.Subfamily and tribe-level tree after Brady et al. (8) indicating the different phylogenetic positions of the interacting ant species. (A) The fungus-growing ant host S. amabilis. (B) The guest ant social parasite M. symmetochus (in a stilted stance, emitting volatile alkaloids from its protruding sting). (C) The G. hartmani raiding agro-predator. M. symmetochus and G. hartmani have independently specialized on using S. amabilis fungus gardens and brood as food.Behaviorally derived lineages of Megalomyrmex have become guest ant parasites of the higher attine genera Trachymyrmex and Sericomyrmex (11, 16, 17) (Fig. 1A). The Trachymyrmex specialist, Megalomyrmex adamsae, appears to have remained as equally rare as the agro-predators and thief ants (11), but the Sericomyrmex specialist Megalomyrmex symmetochus (Fig. 1B) is surprisingly common, with a prevalence of >80% in some host populations (16). Newly mated guest ant queens of both species likely enter host colonies by stealth and establish themselves in the fungus garden, where their developing colony will consume host brood and fungus garden for years (11). Their presence slows host colony growth and also prevents or reduces host reproduction, because both guest ant species clip the wings of host gynes (virgin queens), but not males (11). Such mutilation reduces host reproduction and dispersal via mating flights, but likely increases guest ant fitness when these mutilated females adopt worker tasks (11, 18). Like all guest ant social parasites, M. symmetochus retains a fully functional worker caste (16, 19), in contrast to many social parasites that exploit the services of their phylogenetically similar host colony without the need to produce workers (5).The maintenance of a large worker caste despite permanent cohabitation with a host colony may have several purposes, all based on some specialized role for the parasite workers. First, it may be that the distantly related host workers are unable to feed the social parasite larvae (5) even though adult hosts and parasites are adapted to the same highly specific fungal diet. Another possibility is that the guest ant colony remains at risk of occasional attack by the host workers; such antagonism has been observed between M. symmetochus workers and host workers in older colonies (SI Text, Study System). But Sericomyrmex ants have only vestigial stings (20) and often feign death when attacked, and so this does not explain the large number of parasite workers. Thus, it seems reasonable to hypothesize that a large number of Megalomyrmex guest ant workers continue to remain essential for the survival and reproductive success of their own mother queen in ways other than merely reinforcing their dominance over Sericomyrmex host workers and caring for their own brood.Neither founding queens nor mature colonies of M. symmetochus guest ants are known to move to other host colonies later in life, implying that guest ant reproductive success is completely dependent on the continued well being (albeit not the reproduction) of host colonies (11). Thus, we conjectured that M. symmetochus guest ants might act as defenders when host colonies are attacked by natural enemies that are sufficiently effective to pose a significant threat. Such a specialized enemy, the unrelated agro-predator ant Gnamptogenys hartmani (Ectatomminae: Ectatommini) (Fig. 1C and Fig. S1A), was recently seen to raid colonies of Sericomyrmex in Panama and to usurp their gardens and nest structures with remarkable efficiency (21). This finding suggests that the enhanced mortality risk emanating from these raids might have produced an unusual secondary mutualism between the socially parasitic guest ants and their hosts. Rather than merely reducing worker production as ant social parasites normally do, the M. symmetochus guest ants produce a seemingly excess number of workers (Table S2) that constantly patrol the host nest. These guest ants’ potent alkaloid weaponry, which originally secured their establishment at a chronic cost to the host colony, potentially could also serve to protect the host from greater harm in the direct interest of the guest ant parasite.We tested this idea in a series of controlled laboratory experiments aimed at quantifying the damage by G. hartmani agro-predator parasites and the defense efficiency of Sericomyrmex hosts with and without guest ants (SI Text: Study System). We found that hosting even a moderate number of Megalomyrmex guest ants provides almost complete protection against G. hartmani raids, because (i) guest ants are much more efficient than host ants in killing intruding G. hartmani workers; (ii) guest ants reduce host ant mortality inflicted by the raiding agro-predators; and (iii) scouts of G. hartmani preferentially recruit nestmates to Sericomyrmex host colonies whose odor indicates an absence of guest ants.     

Effect of cyproterone acetate and conjugated estrogens on the human insulin receptor

It has recently been reported that prednisone increases whereas dexamethasone and cortisone decrease insulin binding to monocytes, thus suggesting that different steroids may exert opposite effects on the insulin receptor, depending on their chemical structure. In order to gain further insight into the modulations of the insulin receptor by other steroids, the effect in male patients of short- and long-term oral treatment with cyproterone acetate (100–150 mg/day) or conjugated estrogens (20 mg/day) was evaluated. Cyproterone acetate did not produce any statistical, evident change in insulin binding to monocytes after either short-term (5 days) or long-term (1 year) treatment. Short-term (5 days) administration of conjugated estrogens did not affect insulin binding; however, long-term (1 year) treatment produced a highly significant decrease in insulin binding due mainly to changes in receptor concentration. Thus, cyproterone acetate does not affect the insulin receptor, whereas conjugated estrogens reduce insulin receptors after long-term treatment, as with dexamethasone and cortisone. Estrogens probably play a role in the insulin binding impairment which occurs during the luteal phase of the menstrual cycle as well as in users of the “pill”.     

Cardiac denervation in mice infected with Trypanosoma cruzi

The neuronal features of the hearts of mice that were acutely or chronically infected with the Y strain of Trypanosoma cruzi were compared with those of control hearts from uninfected mice. Whole-mount preparations of the murine atria, isolated by microdissection, were stained to reveal neurons with NADH-diaphorase activity. Counts, by a microscopist who was blind to the infection status of the donor mouse, revealed that there were significantly (38%) fewer such neurons in the atria from the acutely infected mice than in the atria from the control hearts. The ganglia of the infected mice were also irregularly distributed, severely damaged ganglia being found beside slightly degenerated or morphologically normal ones. Although the ganglia contained small, medium and large neurons, the apparent destruction caused by T. cruzi was confined to the large ones. As neuron counts in preparations of hearts from mice with chronic infections were 32% lower than those in the control hearts, there appears to be no additional loss of cardiac neurons as the acute infection in mice progresses to the chronic phase.     

Cell cycle phase perturbations and apoptosis in tumour cells induced by aplidine

Aplidine, dehydrodidemnin B, is a marine depsipeptide isolated from the Mediterranean tunicate Aplidium albicans currently in phase II clinical trial. In human Molt-4 leukaemia cells Aplidine was found to be cytotoxic at nanomolar concentrations and to induce both a G(1) arrest and a G(2) blockade. The drug-induced cell cycle perturbations and subsequent cell death do not appear to be related to macromolecular synthesis (protein, RNA, DNA) since the effects occur at concentrations (e.g. 10 nM) in which macromolecule synthesis was not markedly affected. Ten nM Aplidine for 1 h inhibited ornithine decarboxylase activity, with a subsequently strong decrease in putrescine levels. This finding has questionable relevance since addition of putrescine did not significantly reduce the cell cycle perturbations or the cytotoxicity of Aplidine. The cell cycle perturbations caused by Aplidine were also not due to an effect on the cyclin-dependent kinases. Although the mechanism of action of Aplidine is still unclear, the cell cycle phase perturbations and the rapid induction of apoptosis in Molt-4 cells appear to be due to a mechanism different from that of known anticancer drugs.     

The incorporation of high pH euglobulin precipitation in the isolation of C1q

A one-step polyvalent counterimmunoelectrophoresis (PIE) method for the typing of pneumococci is described. Only one antiserum is used (omniserum, containing antibodies to > 80 pneumococcal types) and it is not necessary to stock large numbers of monospecific typing sera. By observing reactions of identity between the precipitin lines produced by the pneumococcus under test, and the specific capsular polysaccharide precipitin lines in a reference pattern produced by the polyvalent pneumococcal vaccine ‘Pneumovax’, a cumulative percentage of 64.6% of pneumococcal types isolated could be typed.The method is simple, reproducible, inexpensive and provides a permanent stained record.     

Structural changes in sheep antibody induced by interaction with polypeptide antigens

Certain glutamyl-containing polypeptides react with homologous sheep antibody only in the presence of divalent cations, and are dissociated with chelating agents. Near ultraviolet circular dichroism and hydrogen exchange studies show reversible conformational changes occurring in the antibody during specific interaction, but only at low antigen—antibody ratios.     

An HIV prevalence-based model for estimating urban risk populations of injection drug users and men who have sex with men

Issues of cost and complexity have limited the study of the population sizes of men who have sex with men (MSM) and injection drug users (IDUs), two groups at clearly increased risk for human immunodeficiency virus (HIV) and other acute and chronic diseases. We developed a prototypical, easily applied estimation model for these populations and applied it to Miami, Florida. This model combined HIV prevalence estimates, HIV seroprevalence rates, and census data to make plausible estimates of the number and proportion of MSM and IDUs under a number of assumptions. Sensitivity analyses were conducted to test the robustness of the model. The model suggests that approximately 9.5% (plausible range 7.7%–11.3%) of Miami males aged 18 years or older are MSM (point estimate, N=76,500), and 1.4% (plausible range 0.9%–1.9%) of the total population aged 18 years or older are IDUs (point estimate, N=23,700). Males may be about 2.5 times more likely than females to be IDUs. The estimates were reasonably robust to biases. The model was used to develop MSM and IDU population estimates in selected urban areas across Florida and should be replicable in other medium-to-large urban areas. Such estimates could be useful for behavioral surveillance and resource allocation, including enhanced targeting of community-based interventions for primary and secondary HIV prevention. Dr. Friedman is with National Development Research Institutes, Inc. Dr. Gates is with the Urban Institute.