Host specificity pattern and chemical deception in a social parasite of ants

Luca Pietro Casacci,Francesca Barbero,Emilio Balletto,Simona Bonelli,Karsten Schönrogge,Jeremy Ambler Thomas

doi:10.1038/s41598-018-38172-4

Abstract

In natural ecosystems, relationships between organisms are often characterised by high levels of complexity, where vulnerabilities in multi-trophic systems are difficult to identify, yet variation in specific community modules can be traceable. Within the complex community interactions, we can shed new light on dynamics by which co-evolutionary outcomes can inform science-led conservation. Here we assessed host-ant use in six populations of the butterfly Phengaris (=Maculinea) rebeli, an obligate social parasite of Myrmica ants and a model system in evolutionary and conservation ecology. Starting from the initial distribution of eggs, we estimated the survival of the parasite in the wild in nests of seven Myrmica ant species, and analysed the chemical cues evolved by the parasites to subvert its host defences. We found local variations in host specificity that are consistent with similarities found in the chemical profiles of hosts and parasites on different sites. At some sites, only one ant species is successfully exploited; at others, multiple-host populations are used. Understanding how stable or adaptable these associations are is essential knowledge when devising conservation measures to maintain keystone species of ant and locally adapted populations of Phengaris butterfly species, which are rare, threatened and a high priority for conservation worldwide.

Highlights

Many generalist insect species can respond rapidly to environmental changes[1,2], closely-coupled assemblages of interacting specialists are often more vulnerable, because survival may depend upon the maintenance of obligate co-adaptations or interactions within the community[3]
For all sites the proportion of eggs found on gentian plants in late summer associated with each Myrmica species were compared to the proportion of P. rebeli full-grown larvae or pupae found in each Myrmica colony in the following spring
At Campitello, we found that estimated survival rates in nests of M. sabuleti and M. schencki were similar, but P. rebeli experienced significantly higher mortality when living with M. scabrinodis (Fig. 2)

Summary

Introduction

Many generalist insect species can respond rapidly to environmental changes[1,2], closely-coupled assemblages of interacting specialists are often more vulnerable, because survival may depend upon the maintenance of obligate co-adaptations or interactions within the community[3]. The European Phengaris (=Maculinea) (P. arion, P. teleius, P. nausithous, P. alcon, P. rebeli – we considered the two latter taxa as separate following7) are already the most studied ant-parasitic butterflies, and have become a model system in evolutionary and conservation ecology[8]. The low level of chemical similarity, coupled with poor discrimination by foraging workers, means that P. rebeli pre-adoption caterpillars are retrieved into nests by workers of any foraging Myrmica species that happen to encounter them[10,11,14,15]. To distinguish the two possibilities, we estimated the survival rates, rather than study the occurrence, of Phengaris rebeli caterpillars in Myrmica host colonies at six sites in Italy, and analysed similarities in the cuticular hydrocarbon signatures among host ants and parasites on which the chemical mimicry is based. How tight the relationships between the host ant and parasite are is central to understanding the evolution of widespread associations between butterflies and ants, and for the survival and conservation of Phengaris spp., especially when faced with additional threats such as rapid climate change that necessitate more intrusive land management[27]

Methods

Results

Conclusion