A Mosaic of Chemical Coevolution in a Large Blue Butterfly

Institute of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen, Denmark.
Science (Impact Factor: 33.61). 02/2008; 319(5859):88-90. DOI: 10.1126/science.1149180
Source: PubMed


Mechanisms of recognition are essential to the evolution of mutualistic and parasitic interactions between species. One such
example is the larval mimicry that Maculinea butterfly caterpillars use to parasitize Myrmica ant colonies. We found that the greater the match between the surface chemistry of Maculinea alcon and two of its host Myrmica species, the more easily ant colonies were exploited. The geographic patterns of surface chemistry indicate an ongoing coevolutionary
arms race between the butterflies and Myrmica rubra, which has significant genetic differentiation between populations, but not between the butterflies and a second, sympatric
host, Myrmica ruginodis, which has panmictic populations. Alternative hosts may therefore provide an evolutionary refuge for a parasite during periods
of counteradaptation by their preferred hosts.

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Available from: David Richard Nash
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    • "A field study ( Elmes et al . 2004 ) and an analysis of pre - adoption chemical profiles ( Nash et al . 2008 ) suggested that similar differentiation may have evolved between the main European form of M . alcon , which exploits Myrmica scabrinodis , and that of Scandinavia and the Netherlands , which is adapted to Myrmica rubra / M . ruginodis . Ant association is therefore a double - edged sword for the conservation of these lycaenid butterfl"
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    ABSTRACT: Abstract Although most conservationists claim to protect “species”, the conservation unit actually and practically managed is the individual population. As resources are not unlimited, we need to focus on a restricted number of populations. But how can we select them? The Evolutionarily Significant Unit (ESU), first conceptualised by Ryder in 1986, may offer some answer. Several definitions have been proposed for the ESU, but all make reference to units “whose divergence can be measured or evaluated by putting differential emphasis on the role of evolutionary forces at varied temporal scales”. Thus, an ESU might be fully identical with a “species”, or a “species” could be composed of multiple ESUs. On the other hand, an ESU might comprise single/multiple populations exchanging a degree of gene flow, such as meta-populations. In an attempt to show strengths and weaknesses of ESU concepts, we present here, among several others, some case studies on the myrmecophilous butterflies of the genus Maculinea. In particular, we analyse the apparently everlasting debate about Maculinea alcon and M. rebeli, whose separation into separate species has been accepted by many authors, on mainly ecological criteria, but has not been fully supported by molecular analyses. We also discuss how the tight association with host ants may have driven selection for increasingly more strictly adapted Maculinea populations, arguably deserving specific taxonomic identity. Finally we discuss how current DNA analyses may fail to detect critical information on differences between taxa recently originated by the action of separate adaptive processes, which non-molecular studies can sometimes reveal. We conclude by discussing some current and often conflicting taxonomic trends, in their relationships with conservation policies.
    Full-text · Article · Jun 2014 · Italian Journal of Zoology
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    • "Larvae of Maculinea alcon ([Denis & Schiffermüller], 1775) initially feed on the seeds of gentian plants for about a month and are later taken in and raised by Myrmica colonies (Thomas et al. 1989). They have a “cuckoo” strategy, in which they mimic the odour (Thomas and Settele 2004, Nash et al. 2008, Akino et al. 1999) and sound (Barbero et al. 2009) of the host ant species, and are therefore fed like an ant larva (Thomas and Elmes 1998), although they also sometimes prey directly on the ant brood (Tartally 2004). The caterpillars develop within the host ant nest during the autumn, winter and spring, and will then either pupate there, or continue development for an additional year (Schönrogge et al. 2000, Witek et al. 2006). "
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    ABSTRACT: AbstractThe taxonomy of the myrmecophilous Maculinea alcon group (Lepidoptera: Lycaenidae) is highly debated. The host-plant and host-ant usage of these butterflies have conventionally been important in their identification. Maculinea ‘rebeli’ has generally been considered to be the xerophilous form of Ma. alcon (Ma. alcon X hereafter) with Gentiana cruciata as initial food plant. However, the type locality and all other known sites of Ma. rebeli are found above the coniferous zone, and are well separated from the lower regions where Ma. alcon X sites are found. Furthermore, no food plant and host ant data for the nominotypic Ma. rebeli have yet been published. Our aim was therefore to identify the host ant(s) of Ma. rebeli around the type locality and compare this with the host ant usage of nearby Ma. alcon X. Nests of Myrmica spp. (Hymenoptera: Formicidae) close to the host plants were opened on one Ma. alcon X (host plant: Gentiana cruciata) and two Ma. rebeli (host plant: Gentianella rhaetica, first record, confirmed by oviposition and emerging larvae) sites just before the flying period, to find prepupal larvae and pupae. Three Myrmica species (My. lobulicornis, My. ruginodis, My. sulcinodis) were found on the two Ma. rebeli sites, which parasitized exclusively My. sulcinodis (22 individuals in 7 nests). On the Ma. alcon X site Myrmica sabuleti and My. lonae were found, with My. sabuleti the exclusive host (51 individuals in 10 nests). Ichneumon cf. eumerus parasitized both butterflies. The results highlight the differentiation of Maculinea rebeli from Ma. alcon X, from both conservation biological and ecological points of view. Thus, it should be concluded that Ma. rebeli does not simply represent an individual form of Ma. alcon but it can be considered as at least an ecological form adapted to high mountain conditions both in its initial food plant and host ant species. In addition, it should be emphasized that Ma. alcon X (= Ma. rebeli auct. nec Hirschke) cannot be synonymised with Ma. rebeli (Hirschke, 1904).
    Full-text · Article · Apr 2014 · ZooKeys
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    • "According to previous studies [22]–[23], the quick retrieval of Maculinea larvae is supposedly mediated only by the chemical mimicry of surface hydrocarbons existing on the epicuticle of Myrmica workers. Cuckoo larvae are commonly retrieved in a few minutes, thanks to the synthesis of specific epicuticular hydrocarbons [29]–[30]. However, this chemical mechanism has only been assessed for cuckoo species, while the only evidence for predatory species is that the adoption ritual is more durable than that of cuckoo species [53]–[54]. "
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    ABSTRACT: About 10,000 arthropods live as ants' social parasites and have evolved a number of mechanisms allowing them to penetrate and survive inside the ant nests. Many of them can intercept and manipulate their host communication systems. This is particularly important for butterflies of the genus Maculinea, which spend the majority of their lifecycle inside Myrmica ant nests. Once in the colony, caterpillars of Maculinea "predatory species" directly feed on the ant larvae, while those of "cuckoo species" are fed primarily by attendance workers, by trophallaxis. It has been shown that Maculinea cuckoo larvae are able to reach a higher social status within the colony's hierarchy by mimicking the acoustic signals of their host queen ants. In this research we tested if, when and how myrmecophilous butterflies may change sound emissions depending on their integration level and on stages of their life cycle. We studied how a Maculinea predatory species (M. teleius) can acoustically interact with their host ants and highlighted differences with respect to a cuckoo species (M. alcon). We recorded sounds emitted by Maculinea larvae as well as by their Myrmica hosts, and performed playback experiments to assess the parasites' capacity to interfere with the host acoustic communication system. We found that, although varying between and within butterfly species, the larval acoustic emissions are more similar to queens' than to workers' stridulations. Nevertheless playback experiments showed that ant workers responded most strongly to the sounds emitted by the integrated (i.e. post-adoption) larvae of the cuckoo species, as well as by those of predatory species recorded before any contact with the host ants (i.e. in pre-adoption), thereby revealing the role of acoustic signals both in parasite integration and in adoption rituals. We discuss our findings in the broader context of parasite adaptations, comparing effects of acoustical and chemical mimicry.
    Full-text · Article · Apr 2014 · PLoS ONE
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