The origin of the chemical profiles of fungal symbionts and their significance for nestmate recognition in Acromyrmex leaf-cutting ants

Abstract

Cuticular hydrocarbon profiles are essential for nestmate recognition in insect societies, and quantitative variation in these recognition cues is both environmentally and genetically determined. Environmental cues are normally derived from food or nest material, but an exceptional situation may exist in the fungus-growing ants where the symbiotic fungus garden may be an independent source of recognition compounds. To investigate this hypothesis, we quantified the chemical profiles of the fungal symbionts of 18 sympatric colonies of Acromyrmex echinatior and Acromyrmex octospinosus and evaluated the quantitative variation of the 47 compounds in a multivariate analysis. Colony-specific chemical profiles of fungal symbionts were highly distinct and significantly different between the two ant species. We also estimated the relative genetic distances between the fungal symbionts using amplified fragment length polymorphism (AFLP) and correlated these with the overall (Mahalanobis) chemical distances between the colony-specific profiles. Despite the standardized laboratory conditions, the correlations were generally weak, but a statistically significant portion of the total variation in chemical profiles could be explained by genetic differences between the fungal symbionts. However, there was no significant effect of ant species in partial analyses because genetic differences between symbionts tend to coincide with being reared by different ant species. However, compound groups differed significantly with amides, aldehydes, and methyl esters contributing to the correlations, but acetates, alkanes, and formates being unrelated to genetic variation among symbionts. We show experimentally that workers that are previously exposed to and fed with the fungal symbiont of another colony are met with Behav Ecol Sociobiol (2007) less aggression when they are later introduced into that colony. It appears, therefore, that fungus gardens are an independent and significant source of chemical compounds, potentially contributing a richer and more abundant blend of recognition cues to the colony "gestalt" than the innate chemical profile of the ants alone.

Diet-Mediated Pheromones and Signature Mixtures Can Enforce Signal Reliability

“…Similar observations have been recorded in other ants, including Formica aquilonia (Sorvari et al, 2008) and Linepithema humile (Liang and Silverman, 2000). In some of these systems, diet is so crucial to the nest-mate recognition system that the converse pattern also occurs: previously hostile colonies experience decreased aggression when reared on the same diet (Buczkowski et al, 2005;Richard et al, 2007). Intriguingly, the cuticular hydrocarbon profile of the myrmecophile spider Cosmophasis bitaeniata, which feeds on the larval stages of the ant Oecophylla smaragdina, changes with diet (Elgar and Allan, 2004), presumably allowing the spider to mimic the colony profile and thus remain undetected by its prey (Elgar and Allan, 2006).…”

Symbiont recognition of mutualistic bacteria by Acromyrmex leaf-cutting ants

“…This would mirror the ant-fungus mutualism, where ants can differentiate between different cultivar strains (Bot et al, 2001;Viana et al, 2001), presumably by recognizing clone-specific chemical signatures (Richard et al, 2007). Furthermore, both the forage that the ants use to manure their cultivar (Richard et al, 2004), and the chemical signatures of the fungal cultivar (Richard et al, 2007), affect Acromyrmex workers so that ants from different colonies adapted to the same forage or cultivar clone exhibit reduced aggression when introduced. While it is unknown whether Pseudonocardia affects the ant nest-mate recognition, the location of Pseudonocardia on the ant cuticle , and the ability for very precise ant-actinomycete recognition, make it conceivable that the bacterial symbiont also plays a role in this aspect of the symbiosis.…”

Brood adoption in the leaf-cutting ant Acromyrmex echinatior: adaptation or recognition noise?

“…The data points indicate the mean values and the vertical lines the standard error Brood adoption in the leaf-cutting ant A. echinatior 483 non-nestmate in the beginning of the experiment, the chance of mistaking allocolonial brood for nestmate may have increased with time because the label of allocolonial brood was aligned to that of the discriminator colony. It has been shown that the cuticular chemical profiles of brood of leafcutting ants, including A. echinatior, are rather simple as compared to that of adult workers (Viana et al, 2001;Richard et al, 2007), in that they consist of less substances and mainly of saturated alkanes, which are generally assumed to play a minor role in nestmate recognition (reviewed in d'Ettorre and Lenoir, 2010;van Zweden and d'Ettorre, 2010). It is therefore possible that the brood is chemically transparent (Schönrogge et al, 2004, Martin et al, 2008, i.e.…”

“…We can exclude a total chemical transparency of A. echinatior brood because initially nonnestmate brood is detected; the colony-specific profile may, however, be very weak and thus fade away or be replaced fairly quickly during our experiments, which would assist the unintended adoption process. The alignment of cuticular profiles could also have been facilitated by workers replacing the brood's fungal cover, as the fungus possesses a colony-specific chemical profile that allows workers to discriminate against non-nestmate fungus (Viana et al, 2001;Richard et al, 2007). Little is known about the exchange of odours between workers or fungus and brood, but it seems that there is a relation between fungus and brood chemical profiles since the two are similar to each other (Viana et al, 2001;Richard et al, 2007).…”

“…The alignment of cuticular profiles could also have been facilitated by workers replacing the brood's fungal cover, as the fungus possesses a colony-specific chemical profile that allows workers to discriminate against non-nestmate fungus (Viana et al, 2001;Richard et al, 2007). Little is known about the exchange of odours between workers or fungus and brood, but it seems that there is a relation between fungus and brood chemical profiles since the two are similar to each other (Viana et al, 2001;Richard et al, 2007). It has been noted before that leafcutter brood is often covered by fungal hyphae, which nurse workers plant on the surface of larvae and pupae (Lopes et al, 2005).…”