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![Life cycle of Ma. arion and its interaction with Myrmica ants and O. vulgare, indicated by this and previous [5,11-14] studies. (1) Female butterfly is attracted to flowers then, when close, by volatiles promoting oviposition (2) on flowerbuds of O. vulgare plants that co-occur with a nest of any Myrmica species; (3) final-instar larvae abandon O. vulgare and are adopted by Myrmica ants, in whose nests they live for 11 months, feeding on ant brood (4, 5) and acquiring more than 98% of their final biomass (5). Larval survival in the study race of Ma. arion is highest with Myrmica scabrinodis and Myrmica sabuleti and zero with ants of other genera [15].](publication/279916871/figure/fig1/AS:614317904900115@1523476210586/Life-cycle-of-Ma-arion-and-its-interaction-with-Myrmica-ants-and-O-vulgare-indicated.png)
Life cycle of Ma. arion and its interaction with Myrmica ants and O. vulgare, indicated by this and previous [5,11-14] studies. (1) Female butterfly is attracted to flowers then, when close, by volatiles promoting oviposition (2) on flowerbuds of O. vulgare plants that co-occur with a nest of any Myrmica species; (3) final-instar larvae abandon O. vulgare and are adopted by Myrmica ants, in whose nests they live for 11 months, feeding on ant brood (4, 5) and acquiring more than 98% of their final biomass (5). Larval survival in the study race of Ma. arion is highest with Myrmica scabrinodis and Myrmica sabuleti and zero with ants of other genera [15].
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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–predace...
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Context 1
... insect social parasites have evolved from phytophagous ancestors [6,8,9] and are constrained, during early larval development, by an obligate need to feed on specific plant tissues before infiltrating ant colonies for an extended final instar during which most of their ultimate biomass is acquired ( [8,10 -12]; figure 1). With average realized fecundities seldom exceeding 50 eggs laid per wild female [5,11], this lifestyle poses the logistical challenge of locating sufficient proximate hosts for a population to persist. ...
Context 2
... sabuleti and Myrmica scabrinodis colonies (primary host of Ma. arion, respectively, in west Europe and Italy) and O. vulgare seeds were collected in the Parco Fluviale Gesso e Stura, North Italy, where a previous study of Ma. arion oviposition behaviour had been made [15]. Twelve terraria (electronic supplementary material, figure S1) were established, each containing four O. vulgare plants grown from seedlings maintained at 268C, 60% humidity and 120 mmol m 22 s 21 light under a 16 L : 8 D regime. Six also contained one Myrmica colony each, while six controls did not. ...
Context 3
... consider that the described interactions are adaptive for all members of the Ma. arion community module ( figure 1). An ability, when ovipositing, indirectly to detect the presence of Myrmica presence causes a 10-fold induction for a monoterpene synthase gene (OvTPS2) that encodes a protein catalysing the formation of g-terpinene, a direct precursor for thymol and carvacrol. ...
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Coordinated social behaviour is fundamental for ant ecological success. However, even distantly-related organisms, such as plants, have evolved the ability to manipulate ant collective performances to their own advantage. In the parasitic system encompassing Maculinea butterflies, Myrmica ants, and Origanum vulgare plants, the ant-plant interaction...
Citations
... Studying Myrmica scabrinodis, the authors found that a blend of Origanum vulgare terpenoids, i.e., carvacrol and thymol, decreased the locomotor activity of ants and increased their aggressiveness by regulating the BA levels in workers' brains [24]. The release of carvacrol is triggered by the interaction between the plant and Myrmica ants, and this chemical signaling is eavesdropped by females of a myrmecophilous butterfly, Maculinea arion, to locate their optimal egg-laying site [93]. M. arion is an obligate social parasite of Myrmica ants and scent carvacrol to spot Origanum foodplants growing in the foraging range of a Myrmica colony, thus providing the offspring with their necessary host resources. ...
Eusociality represents the higher degree of interaction in insects. This complex social structure is maintained through a multimodal communication system that allows colony members to be flexible in their responses, fulfilling the overall society’s needs. The colony plasticity is supposedly achieved by combining multiple biochemical pathways through the neuromodulation of molecules such as biogenic amines, but the mechanisms through which these regulatory compounds act are far from being fully disentangled. Here, we review the potential function of major bioamines (dopamine, tyramine, serotine, and octopamine) on the behavioral modulation of principal groups of eusocial Hymenoptera, with a special focus on ants. Because functional roles are species- and context-dependent, identifying a direct causal relationship between a biogenic amine variation and behavioral changes is extremely challenging. We also used a quantitative and qualitative synthesis approach to summarize research trends and interests in the literature related to biogenic amines of social insects. Shedding light on the aminergic regulation of behavioral responses will pave the way for an entirely new approach to understanding the evolution of sociality in insects.
... The enhanced expression of these genes may be induced by an increase in the phenolic monoterpenes that these genes are known to produce. The absence or presence of ants near Origanum vulgare L. has been reported to induce an enhancement in the production and accumulation of phenolic monoterpenes, which is related to ants [58]. OvTPS2, CYP71D179/182, CYP71D180, and CYP71D178, among other genes involved in terpene biosynthesis, were found to be expressed more frequently when a Myrmica ant parasitized Origanum vulgare [58]. ...
... The absence or presence of ants near Origanum vulgare L. has been reported to induce an enhancement in the production and accumulation of phenolic monoterpenes, which is related to ants [58]. OvTPS2, CYP71D179/182, CYP71D180, and CYP71D178, among other genes involved in terpene biosynthesis, were found to be expressed more frequently when a Myrmica ant parasitized Origanum vulgare [58]. ...
The medicinal herb coriander (Coriandrum sativum L.), with a high linalool (LIN) content,
is widely recognized for its therapeutic benefits. As a novel report, the goals of this study
were to determine how methyl jasmonate (MeJA) affects total phenolic content (TPC), LIN content, flavonoid content (TFC), and changes in gene expression involved in the linalool biosynthesis pathway (CsgTRPS and CsLINS). Our findings showed that, in comparison to the control samples, MeJA treatment substantially enhanced the TPC, LIN, and TFC content in both ecotypes. Additionally, for both Iranian coriander ecotypes, treatment-induced increases in CsɣTRPS and CsLINS expression were connected to LIN accumulation in all treatments. A 24 h treatment with 150 μM MeJA substantially increased the LIN content in the Mashhad and Zanjan ecotypes, which was between 1.48 and 1.69 times greater than that in untreated plants, according to gas chromatography–mass spectrometry (GC-MS) analysis. Our findings demonstrated that MeJA significantly affects the accumulation of LIN, TPC, and TFC in Iranian C. sativum treated with MeJA, which is likely the consequence of gene activation from the monoterpene biosynthesis pathway. Our discoveries have improved the understanding of the molecular mechanisms behind LIN synthesis in coriander plants.
... The chemical composition of essential oils and extracts in plant species is generally affected by these variables. According to the research, MeJA and SA therapy stimulates secondary metabolism in many plant species, allowing plant hormones to control the synthesis of volatile chemicals, which is linked to plant protection and interactions with the environment [30][31][32]. ...
... Mohammadi et al. [1] investigated the impact of various environmental variables, such as drought, on increased amounts of several key components such as thymol, carvacrol, and linalool in T. kotschyanus and T. vulgaris, and they reported consistent findings. T. vulgaris and Origanum vulgare L. are two Lamiaceae species whose essential oil content and, as a result, thymol and carvacrol production and accumulation vary in various tissues or in response to distinct environmental variables and stressors [31,34]. ...
... Most of the time, these variables alter the chemical composition of essential oils in different plant species. MeJA and SA treatments have been shown to stimulate secondary metabolism in a variety of plant species, and it is probable that the synthesis of volatile chemicals is controlled by these plant hormones, which are involved in plant defense and interaction with the environment [24,31]. ...
Thyme species are a good source of thymol and carvacrol, which plays a key role in controlling diseases. For the first time, the expression patterns of γ -terpinene synthase (TPS2), CYP71D178, and CYP71D180 genes and phenolics compounds amount were evaluated in T. migricus and T. daenensis after different methyl jasmonate (MeJA) treatments. The highest thymol and carvacrol contents were observed in T. migricus (86.27%) and T. daenensis (17.87%) at MeJA 100µM, which was consistent with the expression patterns of the three investigated genes. All species treated showed high total phenolic and flavonoid content compared to control plants for which the highest amounts were observed in T. vulgaris treated with 100 µM and 10 µM MeJA. Further-more, in the 100 µM MeJA treatment, the relative expression of TPS2 and CYP71D178 in T. mi-gricus increased 7.47 and 9.86-fold compared with the control, respectively. The highest level of CYP71D180 transcripts (5.15-fold) was also observed for T. daenensis treated. This finding highlights the notion that thymol was known as the dominant component of the essential oil rather than carvacrol in diffident thyme species. This implies that MeJA at different concentrations in-fluenced metabolic pathways, induced expression changes, resulting in a rise in essential oil lev-els.
... Interestingly, the compound Germancrene D, observed in the majority of the samples, was not identified in sample A. Furthermore, sample A showed a relatively lower content of other comparable oil compounds. Carvacrol, as an aromatic oxygenated monoterpene, is known for being attractive to pollinators [18]. It also has antifungal and insecticidal properties [18,19] and since plants are more sensitive to herbivores and disease at an early vegetative stage, high quantities of Carvacrol can function as an allomone. ...
... Carvacrol, as an aromatic oxygenated monoterpene, is known for being attractive to pollinators [18]. It also has antifungal and insecticidal properties [18,19] and since plants are more sensitive to herbivores and disease at an early vegetative stage, high quantities of Carvacrol can function as an allomone. Increasing the content of Carvacrol in flowers and the flowering stage demonstrates the role of this phenolic monoterpene as a kairomone [19]. ...
The quality and content of essential oils extracted from medicinal and culinary plants can be affected by harvesting time conditions. This study focused on the antioxidant activity and chemical composition of Origanum dictamnus essential oils under different harvesting time conditions. Samples from the same area and different harvesting times were treated by hydrodistillation. Gas Chromatography (GC-FID) and gas chromatography-mass spectrometry (GC-MS) were used to determine the different compounds found in essential oils. In all the essential oil samples, the phenolic monoterpenoid Carvacrol was prevalent. Through different seasons, we could observe a relatively high yield ratio. However, the lowest and highest yield values were found in plants collected during winter and summer. These essential oils showed high level radical scavenging properties level, as exhibited in the DPPH assay. Essential oils from sample C (collected on 10/02/18) showed the highest antioxidant activity.
... Communication and its corruption are at the base of the evolution and maintenance of multiple interactions, and we believe that community context approaches are ideal to assess properly all the selective pressures shaping these complex systems. We discuss the hypothesis by FIGURE 1 | Life cycle of Maculinea arion and its interaction with Myrmica ants and Origanum vulgare following Patricelli et al. (2015). (1) Gravid female butterflies are visually attracted to the green-red buds of O. vulgare; when in their proximity, (2) by detecting the monoterpenoid volatile carvacrol emitted by plants co-occurring with ants of any Myrmica species (3) female lays eggs on phenologically suitable flower buds; (4) fourth-instar caterpillars leave the host plant and are "adopted" by Myrmica ants; (5) M. arion caterpillars spend 11 months within Myrmica colonies, feeding on ant brood and acquiring more than 98% of their final biomass. ...
... Therefore, some authors started to hypothesize that induced plant volatiles might work as indirect signals for the ant presence and provide hints for the egg-laying females (Van Dyck and Regniers, 2010;Wynhoff et al., 2015). Patricelli et al. (2015) provided the first evidence that Origanum vulgare plants, the LHP of M. arion, react to Myrmica workers by releasing a volatile organic compound (carvacrol), which in turn is used by gravid females to locate ideal food plants growing close to a Myrmica nest (Figure 1). Experimental O. vulgare plants grown with ants upregulate genes involved in the monoterpenes pathway thus releasing higher amounts of carvacrol than control plants (without ants). ...
... Using a multidisciplinary approach, authors shed light on the indirect mechanism used by M. arion females to detect the presence of the Myrmica ants by means of a very tiny variation in the LHP volatilome (Patricelli et al., 2015) and on the way a certain degree of overlap between the two butterfly resources, LHPs and Myrmica ants, can be maintained (Mannino et al., 2018). ...
Ant nests and their surrounding territories represent a hoard of trophic resources, as well as of stable and protected environments for many arthropods involved in commensal, mutualistic, or parasitic associations. Among these organisms, called myrmecophiles, several are butterflies. Here, we explore the amazing diversity of strategies developed by myrmecophilous butterflies to “cheat” or manipulate ants and to elude the tough defenses of the colony. During oviposition, female butterflies use visual or plant volatile signals to identify the presence of ants, whereas chemical and vibroacoustic cues, either isolated or combined, are used by larvae and pupae to attract, deceive, or appease workers. Examples of mimicry and eavesdropping on both intraspecific and interspecific signals are discussed, primarily referring to the obligate-parasitic interactions involving Maculinea butterflies and Myrmica ants. Multimodal communication is crucial to maintaining the strong cohesion and social structure of ant societies, but its corruption is at the base of the evolution and persistence of interspecific associations, which can be beneficial or detrimental for the colony's fitness. In this framework, the remarkable complexity of signaling could have prompted the evolution of specialized life cycles enhancing the extraordinary butterfly diversity.
... This fine team, led originally by Emilio Balletto at the University of Turin, has made remarkable advances in understanding Maculinea systems post-MacMan, several in collaboration with our UK group and many, as here, with Magda Witek and her outstanding group at the Polish Academy of Sciences. Striking examples include describing how the larvae and pupae of Maculinea broadcast acoustical signals that closely mimic the distinctive stridulations of (adult) Myrmica queens, thereby elevating their status within host societies after penetration through chemical mimicry (Barbero et al., 2009); and how ovipositing female Maculinea arion select Origanum plants growing in close proximity to a Myrmica nest through detecting an agonistic monoterpenoid volatile, carvacrol, that is released when their foodplant's roots are disturbed (Patricelli et al., 2015). The putative influence of Wolbachia on relationships was also explored by Patricelli et al. (2013) and, most recently, di Salvo et al. (2019) suggested that the bipartite Myrmica-Maculinea interaction might in fact be a tripartite one, with direct or indirect involvement of the Maculinea microbiome. ...
The six papers in this Special Issue of Insect Conservation and Diversity are presented as a gedenkschrift honouring ground‐breaking contributions made by the late Graham Elmes towards understanding the biology of Myrmica ants and their social parasites.
A common theme is that each research paper contributes new knowledge applicable to the future survival of Maculinea (= Phengaris ) species of butterflies, which have become flagships for insect conservation across Europe. All Maculinea species are highly specialised, with larvae that feed briefly on a specific foodplant before living underground for 11–23 months as social parasites of Myrmica colonies.
This introductory overview provides a brief history of the research that has led to the current collection, with emphasis on Graham Elmes' life and work. It is followed by three research papers that illustrate the diversity, socio‐biology and ecology of Myrmica ants. A fourth describes an extreme adaptation that increases the efficiency with which some populations of Maculinea larvae exploit the resources within Myrmica nests. A fifth, more theoretical, paper models the constraints that typically lead to host specificity among social parasites and explores why host switches are rare and quick.
... Only later is each young larva carried into the nest of the first foraging worker of any Myrmica species that encounters it, regardless of whether it is a host ant or one of up to four non-host Myrmica species that commonly forage beneath the initial foodplants (Thomas et al., 2005b). This assumption is not undermined by recent research that indicates that Ma. arion uses host-plant defence chemicals to root disturbance as cues to bias oviposition to plants growing in the vicinity of any Myrmica nest (Patricelli et al., 2015). Therefore, phenotypes of Maculinea teleius and Ma. ...
The link between multi‐host use and host switching in host–parasite interactions is a continuing area of debate. Lycaenid butterflies in the genus Maculinea , for example, exploit societies of different Myrmica ant species across their ranges, but there is only rare evidence that they simultaneously utilise multiple hosts at a local site, even where alternative hosts are present.
We present a simple population‐genetic model accounting for the proportion of two alternative hosts and the fitness of parasite genotypes on each host. In agreement with standard models, we conclude that simultaneous host use is possible whenever fitness of heterozygotes on alternative hosts is not too low.
We specifically focus on host‐shifting dynamics when the frequency of hosts changes. We find that (i) host shifting may proceed so rapidly that multiple host use is unlikely to be observed, (ii) back and forth transition in host use can exhibit a hysteresis loop, (iii) the parasites' host use may not be proportional to local host frequencies and be restricted to the rarer host under some conditions, and (iv) that a substantial decline in parasite abundance may typically precede a shift in host use.
We conclude that focusing not just on possible equilibrium conditions but also considering the dynamics of host shifting in non‐equilibrium situations may provide added insights into host–parasite systems.
... Caterpillars mimic the surface chemistry of the ant brood (Nash, Als, Maile, Jones, & Boomsma, 2008) and the acoustic signals of queen ants (Sala, Casacci, Balletto, Bonelli, & Barbero, 2014), and these features cause ants to carry them to their nest, where they spend the rest of their larval period as brood parasites. Females of Phengaris detect Myrmica presence through plant chemicals produced by ants or by plants in response to root tissue damage caused by ants (Patricelli et al., 2015;Van Dyck et al., 2000;Wynhoff & van Langevelde, 2017). Contrary to the majority of Phengaris species, which prey on ant brood, P. alcon is a "cuckoo" species (Als et al., 2004), and caterpillars feed primarily on regurgitants from ant workers, trophic eggs (i.e. ...
... Experimental studies have found Phengaris oviposition to be dependent on Myrmica ant presence, but found no effect of species identity (Patricelli et al., 2015;Wynhoff & van Langevelde, 2017). ...
The effects of consumers on fitness of resource organisms are a complex function of the spatio‐temporal distribution of the resources, consumer functional responses and trait preferences, and availability of other resources.
The ubiquitous variation in the intensity of species interactions has important consequences for the ecological and evolutionary dynamics of natural populations. Nevertheless, little is known about the processes causing this variation and their operational scales. Here, we examine how variation in the intensity of a consumer–resource interaction is related to resource timing, resource density and abundance of other resources.
Using the butterfly consumer Phengaris alcon and its two sequential resources, the host plant Gentiana pneumonanthe and the host ants Myrmica spp., we investigated how butterfly egg‐laying depended on focal host plant phenology, density and phenology of neighbouring host plants and host ant abundance.
Butterflies preferred plants that simultaneously maximized the availability of both larval resources in time and space, that is, they chose early‐flowering plants that were of higher nutritional quality for larvae where host ants were abundant. Both the probability of oviposition and the number of eggs were lower in plant individuals with a high neighbour density than in more isolated plants, and this dilution effect was stronger when neighbours flowered early.
Our results show that plant–herbivore interactions simultaneously depend on the spatio‐temporal distribution of a focal resource and on the small‐scale spatial variation in the abundance of other herbivore resources. Given that consumers have negative effects on fitness and prefer certain timing of the resource organisms, this implies that processes acting at the levels of individuals, populations and communities simultaneously contribute to variation in consumer‐mediated natural selection.
... Many other lycaenid butterflies that associate with specific ants use these ants as an oviposition cue [61][62][63], but the evidence for the use of ant-dependent oviposition in Maculinea has been controversial [24,[64][65][66][67][68]. The most recent evidence suggests that while Maculinea butterflies may lay their eggs in response to the presence of Myrmica ants, they do not distinguish between different species of Myrmica [69]. Hence our use of Myrmica distribution relative to overall host plant distribution as a measure of the encounter filter may underestimate the rate of encounters [35], but not the potential hosts that are encountered. ...
The range of hosts exploited by a parasite is determined by several factors, including host availability, infectivity and exploitability. Each of these can be the target of natural selection on both host and parasite, which will determine the local outcome of interactions, and potentially lead to coevolution. However, geographical variation in host use and specificity has rarely been investigated. Maculinea (= Phengaris ) butterflies are brood parasites of Myrmica ants that are patchily distributed across the Palæarctic and have been studied extensively in Europe. Here, we review the published records of ant host use by the European Maculinea species, as well as providing new host ant records for more than 100 sites across Europe. This comprehensive survey demonstrates that while all but one of the Myrmica species found on Maculinea sites have been recorded as hosts, the most common is often disproportionately highly exploited. Host sharing and host switching are both relatively common, but there is evidence of specialization at many sites, which varies among Maculinea species. We show that most Maculinea display the features expected for coevolution to occur in a geographic mosaic, which has probably allowed these rare butterflies to persist in Europe.
This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.
... Recently, it has been demonstrated that the interaction between Myrmica ants and O. vulgare plants leads to an increased production of the plant volatile monoterpene carvacrol [28]. The release of carvacrol is the indirect signal interpreted by M. arion gravid females to locate the food plant growing in the vicinity of its Myrmica host colonies, thus providing its brood with both sequential hosts (i.e., the source of food, shelter and care in the nest) [28,29]. ...
... Recently, it has been demonstrated that the interaction between Myrmica ants and O. vulgare plants leads to an increased production of the plant volatile monoterpene carvacrol [28]. The release of carvacrol is the indirect signal interpreted by M. arion gravid females to locate the food plant growing in the vicinity of its Myrmica host colonies, thus providing its brood with both sequential hosts (i.e., the source of food, shelter and care in the nest) [28,29]. Myrmica ants survive longer than other ant species when exposed to carvacrol, by upregulating specific genes coding for detoxifying enzymes [28]. ...
... The release of carvacrol is the indirect signal interpreted by M. arion gravid females to locate the food plant growing in the vicinity of its Myrmica host colonies, thus providing its brood with both sequential hosts (i.e., the source of food, shelter and care in the nest) [28,29]. Myrmica ants survive longer than other ant species when exposed to carvacrol, by upregulating specific genes coding for detoxifying enzymes [28]. Therefore, it seems that Myrmica ants benefit from being resistant to carvacrol by occupying a competitor-free spaces surrounding oregano plants, while parasite larvae increase their chance of encountering ants [28,29]. ...
Coordinated social behaviour is fundamental for ant ecological success. However, even distantly-related organisms, such as plants, have evolved the ability to manipulate ant collective performances to their own advantage. In the parasitic system encompassing Maculinea butterflies, Myrmica ants, and Origanum vulgare plants, the ant-plant interaction elicits the release of a volatile terpenoid compound (carvacrol) which is used by the gravid butterfly to locate the ideal oviposition site. Here we show that this ant-plant association is maintained by the effect of O. vulgare terpenoids on ant behaviour and that food plants might gain protection by Myrmica ants by chemically manipulating workers to forage in their surroundings. The variation in the locomotor ability of three ant species (Formica cinerea, Tetramorium caespitum, and Myrmica scabrinodis) was studied after treatment with the two major O. vulgare terpenoid volatile compounds (i.e., carvacrol and thymol). The brain levels of three biogenic amines (dopamine, tyramine and serotonin) were analysed in ants exposed to the O. vulgare terpenoids by HPLC-ESI-MS/MS. Carvacrol and thymol increased the locomotor activity of all ant species tested, but if blended reduced the movement propensity of Myrmica scabrinodis. Dopamine and tyramine production was positively correlated with the worker locomotor activity. In Myrmica ants, both brain biogenic ammines were negatively correlated with the aggressive behaviour. Blends of O. vulgare volatiles affected the locomotor ability while increased the aggressiveness of Myrmica workers by altering the aminergic regulation in the ant brains. This behavioural manipulation, might enhance partner fidelity and plant protection. Our findings provide new insights supporting a direct role of plant volatiles in driving behavioural changes in social insects through biogenic amine modulation.
