Effects of the social environment on the survival and fungal resistance of ant brood (original) (raw)

Foster carers influence brood pathogen resistance in ants

Proceedings. Biological sciences / The Royal Society, 2014

Social organisms face a high risk of epidemics, and respond to this threat by combining efficient individual and collective defences against pathogens. An intriguing and little studied feature of social animals is that individual pathogen resistance may depend not only on genetic or maternal factors, but also on the social environment during development. Here, we used a cross-fostering experiment to investigate whether the pathogen resistance of individual ant workers was shaped by their own colony of origin or by the colony of origin of their carers. The origin of care-giving workers significantly influenced the ability of newly eclosed cross-fostered Formica selysi workers to resist the fungal entomopathogen Beauveria bassiana. In particular, carers that were more resistant to the fungal entomopathogen reared more resistant workers. This effect occurred in the absence of post-infection social interactions, such as trophallaxis and allogrooming. The colony of origin of eggs signifi...

Colony take-over and brood survival in temporary social parasites of the ant genus Formica

Behavioral Ecology and Sociobiology, 2013

ABSTRACT Parasites reduce host fitness, and so instigate counter adaptations by their hosts. In temporary social parasitism, usurpers must not only enter the colony unharmed, but also have their eggs reared by the host workers. We introduced parasitic Formica lugubris and Formica aquilonia queens into queen right and orphaned fragments of three host species, Formica cinerea, Formica picea and Formica fusca, and show that workers of all three host species kill over 40 % of the introduced queens within 10 days, regardless of the presence/absence of a resident queen, and parasite species. More parasite queens died in F. cinerea than in F. picea and F. fusca. There were no major differences in survival between the parasite species (except that F. lugubris survived longer than F. aquilonia in F. fusca colonies compared to F. picea colonies), but parasite queens survived longer in orphaned than in queen right fragments of F. fusca. Experimental introduction of parasite (F. aquilonia) eggs into orphaned colonies of F. fusca showed that none of the parasite eggs were reared until pupation; whereas on average, 12 % of the con-specific hetero-colonial eggs introduced in the same manner were reared until pupation. In all colonies that received parasite brood, all offspring consisted of worker-laid males, whereas the corresponding value was 50 % for colonies that received con-specific hetero-colonial brood. Thus, when the risks of entering host colonies and brood failure are combined, the rate of successful colony take-over is very low. Moreover, the host workers can to some extent alleviate the costs of parasitism by producing a final batch of own offspring.

Covariation between colony social structure and immune defences of workers in the ant Formica selysi

Insectes Sociaux, 2010

Several ant species vary in the number of queens per colony, yet the causes and consequences of this variation remain poorly understood. In previous experiments, we found that Formica selysi workers originating from multiple-queen (=polygyne) colonies had a lower resistance to a fungal pathogen than workers originating from single-queen (=monogyne) colonies. In contrast, group diversity improved disease resistance in experimental colonies. This discrepancy between field and experimental colonies suggested that variation in social structure in the field had antagonistic effects on worker resistance, possibly through a down-regulation of the immune system balancing the positive effect of genetic diversity. Here, we examined if workers originating from field colonies with alternative social structure differed in three major components of their immune system. We found that workers from polygyne colonies had a lower bacterial growth inhibitory activity than workers from monogyne colonies. In contrast, workers from the two types of colonies did not differ significantly in bacterial cell wall lytic activity and prophenoloxidase activity. Overall, the presence of multiple queens in a colony correlated with a slight reduction in one inducible component of the immune system of individual workers. This reduced level of immune defence might explain the lower resistance of workers originating from polygyne colonies despite the positive effect of genetic diversity. More generally, these results indicate that social changes at the group level can modulate individual immune defences.

Ant queens (Hymenoptera: Formicidae) are attracted to fungal pathogens during the initial stage of colony founding

Ant queens that attempt to disperse and found new colonies independently face high mortality risks. The exposure of queens to soil entomopathogens during claustral colony founding may be particularly harmful, as founding queens lack the protection conferred by mature colonies. Here, we tested the hypotheses that founding queens (I) detect and avoid nest sites that are contaminated by fungal pathogens, and (II) tend to associate with other queens to benefit from social immunity when nest sites are contaminated. Surprisingly, in nest choice assays, young Formica selysi BONDROIT, 1918 queens had an initial preference for nest sites contaminated by two common soil entomopathogenic fungi, Beauveria bassiana and Metarhizium brunneum. Founding queens showed a similar preference for the related but non-entomopathogenic fungus Fusarium graminearum. In contrast, founding queens had no significant preference for the more distantly related nonentomopathogenic fungus Petromyces alliaceus, nor for heat-killed spores of B. bassiana. Finally, founding queens did not increase the rate of queen association in presence of B. bassiana. The surprising preference of founding queens for nest sites contaminated by live entomopathogenic fungi suggests that parasites manipulate their hosts or that the presence of specific fungi is a cue associated with suitable nesting sites.

Report Maternal Effect on Female Caste Determination in a Social Insect

2000

Caste differentiation and division of labor are the hallmarks of social insect colonies [1, 2]. The current dogma for female caste differentiation is that female eggs are totipotent, with morphological and physiological differences between queens and workers stemming from a developmental switch during the larval stage controlled by nutritional and other environmental factors (e.g., [3-8]). In this study, we tested whether maternal effects influence caste differentiation in Pogonomyrmex harvester ants. By conducting crossfostering experiments we identified two key factors in the process of caste determination. New queens were produced only from eggs laid by queens exposed to cold. Moreover, there was a strong age effect, with development into queens occurring only in eggs laid by queens that were at least two years old. Biochemical analyses further revealed that the level of ecdysteroids was significantly lower in eggs developing into queens than workers. By contrast, we found no significant effect of colony size or worker exposure to cold, suggesting that the trigger for caste differentiation may be independent of the quantity and quality of resources provided to larvae. Altogether these data demonstrate that the developmental fate of female brood is strongly influenced by maternal effects in ants of the genus Pogonomyrmex. Results and Discussion Effect of Cold Exposure, Queen Age, and Colony Size on Queen Production in Pogonomyrmex Lineages Some Pogonomyrmex lineages produce queens and workers that differ genetically [9-14]. In these lineages, queen-destined eggs abort at periods when only workers are raised [15, 16], whereas the same eggs hatch and develop into adult queens at periods of reproduction. We conducted crossfostering

Evolution of social parasitism in ants: size of sexuals, sex ratio and mechanisms of caste determination

1999

Social parasitism, one of the most intriguing phenomena in ants, has evolved to various levels, the most extreme form being parasites that have lost the worker caste and rely completely on the host's worker force to raise their brood. A remarkable feature of workerless social parasites is the small size of sexuals. It has been suggested that reduced size evolved as a means to take advantage of the host's caste-determination system, so that parasite larvae develop into sexuals with less food than is required to produce host workers. An important consequence of size reduction is that it might restrict the host workers' ability to discriminate between the brood of the social parasite and their own brood and might protect parasite sexuals from elimination. We found that sexuals of the workerless inquiline ant Plagiolepis xene were signi¢cantly smaller than the sexuals of their host Plagiolepis pygmaea, but remarkably similar to the host workers. The size variance of parasite sexuals was much lower than that of their host; this result possibly suggests that there is very stabilizing selection acting on size of the parasite sexuals. Comparison of the primary (egg) and secondary (adult) sex ratios of the parasite and host showed that miniaturization of P. xene sexuals has been accompanied by their ability to develop into sexuals even when the host P. pygmaea actively prevents production of its own sexuals. These results suggest that the inquiline's size and caste threshold have been reduced such that all individuals in a parasite brood will develop into sexuals. We also found that the adult sex ratio of P. xene was heavily female-biased. This bias probably stems from local mate competition that arises from sexuals mating within the nest. There was no signi¢cant di¡erence between the proportion of haploid eggs and adult males produced; this observation indicates that a female-biased sex ratio is achieved by queens producing a higher proportion of diploid eggs rather than by a higher mortality of haploid males.

Social insect colonies are more likely to accept unrelated queens when they come with workers

Behavioral Ecology

Relatedness underlies the evolution of reproductive altruism, yet eusocial insect colonies occasionally accept unrelated reproductive queens. Why would workers living in colonies with related queens accept unrelated ones, when they do not gain indirect fitness through their reproduction? To understand this seemingly paradox, we investigated whether acceptance of unrelated queens by workers is an incidental phenomenon resulting from failure to recognize non-nestmate queens, or whether it is adaptively favored in contexts where cooperation is preferable to rejection. Our study system is the socially polymorphic Alpine silver ant, Formica selysi. Within populations, some colonies have a single queen, and others have multiple, sometimes unrelated, breeding queens. Social organization is determined by a supergene with two haplotypes. In a first experiment, we investigated whether the number of reproductive queens living in colonies affects the ability of workers at rejecting alien queens...

Egg Recognition and Social Parasitism in Formica Ants

2011

Nests of social insects are an attractive resource in terms of nutrition and shelter and therefore targeted by a variety of pathogens and parasites that harness the resources of a host colony in their own reproductive interests. Colonies of the ants Formica fusca and F. lemani serve as hosts for mound-building Formica species, the queens of which use host colonies during colony founding. Here, we investigate whether workers of the host species can mitigate the costs imposed on them by invading parasite queens by recognizing and selectively removing eggs laid by these queens. We used behavioural assays, allowing host workers to choose between con-colonial eggs and eggs laid by the parasite species F. truncorum. We show that workers of both host species discriminate between the two types of eggs in favour of con-colonial eggs. Moreover, workers of F. fusca rejected more con-colonial eggs than F. lemani. This higher rate of error in F. fusca may reflect a greater selectivity or a greater difficulty in discriminating between the two egg types. Nevertheless, both host species removed parasite eggs at a similar rate, when these were artificially introduced into the colonies, although some eggs remained after 10 d. In addition, upon receiving parasite eggs, host workers started to lay unfertilized male-destined eggs within 6 d, thus employing an alternative pathway to gain direct fitness when the resident queen is no longer present and the colony is parasitized.

Sociogenetic responses to ecological variation in the ant Myrmica punctiventris are context dependent

Behavioral Ecology and Sociobiology, 2001

Models of social evolution predict a strong relationship between ecological factors and sociogenetic organization in social insects (e.g. queen number, nestmate relatedness and population structure). Despite a large body of coherent theory, empirical support for these predictions is weak. Here we report the results of an experiment that manipulated two ecological parameters, food and nestsite availability, thought to be important for a population of the forest ant Myrmica punctiventris. Earlier work had shown that the sociogenetic structure varies between two populations of this species, and an ecological experiment in one of the populations (in Vermont) revealed that food supplementation had the strongest effects on nestmate relatedness. We repeated the experiment in the second population (in New York) and obtained strikingly different results. We show that nestsite supplementation had the strongest effect in the New York population, and that adding both food and nestsites affected nestmate relatedness in a direction opposite to that reported from the Vermont study. These results show that the ecological context is critically important for understanding the determinants of colony structure in ants. Furthermore, comparison of our data with that of a previous study shows that social organization in New York is temporally unstable. Thus, not only do ecological factors strongly influence social organization, but their influence can vary over time. Our study underscores the need for detailed information on the natural history and ecology of social species.