Understanding the chemical cues and gene expressions that mediate herbivore–host-plant and parasite–host interactions can elucidate the ecological costs and benefits accruing to different partners in tight-knit community modules, and may reveal unexpected complexities. We investigated the exploitation of sequential hosts by the phytophagous–predaceous butterfly Maculinea arion, whose larvae initially feed on Origanum vulgare flowerheads before switching to parasitize Myrmica ant colonies for their main period of growth. Gravid female butterflies were attracted to Origanum plants that emitted high levels of the monoterpenoid volatile carvacrol, a condition that occurred when ants disturbed their roots: we also found that Origanum expressed four genes involved in monoterpene formation when ants were present, accompanied by a significant induction of jasmonates. When exposed to carvacrol, Myrmica workers upregulated five genes whose products bind and detoxify this biocide, and their colonies were more tolerant of it than other common ant genera, consistent with an observed ability to occupy the competitor-free spaces surrounding Origanum. A cost is potential colony destruction by Ma. arion, which in turn may benefit infested Origanum plants by relieving their roots of further damage. Our results suggest a new pathway, whereby social parasites can detect successive resources by employing plant volatiles to simultaneously select their initial plant food and a suitable sequential host.
In most metapopulation models dispersal is assumed to be a fixed species-specific trait, but in reality dispersal abilities are highly sensitive to various selective pressures. Strict isolation of a metapopulation, which precludes any influx of immigrants (and their genes) from outside and makes it impossible for emigrants to reach other localities with suitable habitat, thus reducing fitness benefits of long-distance dispersal to zero, may be expected to impose strong selection against dispersal. We tested the above prediction by comparing dispersal parameters derived with the Virtual Migration model for isolated and non-isolated metapopulations of two species of large blue Maculinea (= Phengaris) butterflies, surveyed with intensive mark-recapture. Mortality during dispersal was found to be twice (in M. teleius) to five times higher (in M. arion) in isolated metapopulations. Isolation also resulted in significantly reduced dispersal distances in isolated metapopulations, with the effect being particularly strong in M. arion females. Apart from its evolutionary and ecological consequences, dispersal depression in isolated butterfly metapopulations implied by our results has serious conservation implications. It provides a clear argument against using parameter values obtained in a different environmental setting in modelling applications, e.g., Population Viability Analyses or environmental impact assessment. Furthermore, it underlines the importance of establishing well-connected networks of suitable habitats prior to species release in areas where reintroductions are planned.
BackgroundClimatic oscillations are among the long-term factors shaping the molecular features of animals and plants and it is generally supposed that the rear edges (i.e., the low-latitude limits of distribution of any given specialised species) situated closer to glacial refugia are vital long-term stores of genetic diversity. In the present study, we compared the genetic structure of several populations of an endangered and obligate myrmecophilous butterfly (Maculinea arion) from two distinct and geographically distant parts of its European distribution (i.e., Italy and Poland), which fully represent the ecological and morphological variation occurring across the continent.ResultsWe sequenced the COI mitochondrial DNA gene (the ‘barcoding gene’) and the EF-1α nuclear gene and found substantial genetic differentiation among M. arion Italian populations in both markers. Eleven mtDNA haplotypes were present in Italy. In contrast, almost no mtDNA polymorphisms was found in the Polish M. arion populations, where genetic differentiation at the nuclear gene was low to moderate. Interestingly, the within-population diversity levels in the EF-1α gene observed in Italy and in Poland were comparable. The genetic data did not support any subspecies divisions or any ecological specialisations. All of the populations studied were infected with a single strain of Wolbachia and our screening suggested 100% prevalence of the bacterium.ConclusionsDifferences in the genetic structure of M. arion observed in Italy and in Poland may be explained by the rear edge theory. Although we were not able to pinpoint any specific evolutionarily significant units, we suggest that the Italian peninsula should be considered as a region of special conservation concern and one that is important for maintaining the genetic diversity of M. arion in Europe. The observed pattern of mtDNA differentiation among the populations could not be explained by an endosymbiotic infection.
Myrmica ant colonies host numerous insect species, including the larvae of Maculinea butterflies and Microdon myrmicae hoverflies. Little is known about the interspecific relationships among these social parasites and their host ants occurring in sympatric populations. We investigated communities of social parasites to assess the strategies allowing them to share the same pool of resources (i.e. Myrmica colonies). The present study was carried out at five sites inhabited by different social parasite communities, each comprising varying proportions of Maculinea teleius, Maculinea nausithous, Maculinea alcon, and Microdon myrmicae. We investigated their spatial distributions, host segregation, the degree of chemical similarity between social parasites and hosts, and temporal overlaps in colony resource exploitation. Spatial segregation among social parasites was found in two populations and it arises from microhabitat preferences and biological interactions. Local conditions can drive selection on one social parasite to use a Myrmica host species that is not exploited by other social parasites. Myrmica scabrinodis and Myrmica rubra nests infested by larvae of two social parasite species were found and the most common co‐occurrence was between Ma. teleius and Mi. myrmicae. The successful coexistence of these two species derives from their exploitation of the host colony resources at different times of the year. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 699–709.
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