Cuticular Lipids As a Cross-Talk Among Ants, Plants and Butterflies
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International Journal of Molecular Sciences Review Cuticular Lipids as a Cross-Talk among Ants, Plants and Butterflies Francesca Barbero Department of Life Sciences and Systems Biology, University of Turin, Via Accademia Albertina 13, 10123 Turin, Italy; [email protected]; Tel.: +39-011-670-4538 Academic Editor: Kun Yan Zhu Received: 7 August 2016; Accepted: 17 November 2016; Published: 24 November 2016 Abstract: Even though insects and plants are distantly related organisms, they developed an integument which is functionally and structurally similar. Besides functioning as a physical barrier to cope with abiotic and biotic stress, this interface, called cuticle, is also a source of chemical signaling. Crucial compounds with this respect are surface lipids and especially cuticular hydrocarbons (CHCs). This review is focused on the role of CHCs in fostering multilevel relationships among ants, plants and Lepidoptera (primarily butterflies). Indeed, particular traits of ants as eusocial organisms allowed the evolution and the maintenance of a variety of associations with both plants and animals. Basic concepts of myrmecophilous interactions and chemical deception strategies together with chemical composition, biosynthetic pathways and functions of CHCs as molecular cues of multitrophic systems are provided. Finally, the need to adopt a multidisciplinary and comprehensive approach in the survey of complex models is discussed. Keywords: ants; plants; butterflies; interaction; chemical signaling; cuticular hydrocarbons; waxes; symbiosis; lipids 1. Introduction and Outlines The evolutionary success of organisms relies on their adaptability to various environmental conditions. The integument represents the outer, functional and structured interface between an organism and its habitat [1,2]. It functions as a physical barrier to pathogens or predators, provides protection against wounding and injuries [3,4], regulates the exchanges of water, primarily, but also plays a role in respiration, determination of inner temperature, body movements [5–7], and intra- and interspecific communications or sensing [1,2,8]. Curiously, and despite being phylogenetically unrelated, plants and arthropods share a very similar external tegument, which, in both cases, is called “cuticle” and is made of a stratified deposits of organic compounds on the epidermal cells (Figure1). The challenging need to maintain the water balance in aerial habitats could explain this remarkable case of parallel evolution [1]. In both taxa, the primary function of the cuticle is the prevention of water loss, a feature that is mainly determined by the physical arrangement of surface lipids [6,7,9,10]. More in general, terrestrial organisms have to cope with a “changing” environment, where temperatures, humidity and sun radiations are not constant. Thanks to the cuticle, acting as a plastic barrier able to respond to outer variations by modulating its characteristics (not exclusively its waterproofing), some plants and arthropods survive also in extreme conditions [7,9,11]. The cuticular chemical variability found among species, but also in distinct part of the same insect or plant, suggests a wide range of ecological functions played by this barrier [12]. This review explores the role of the cuticle, acting as a source of chemical signaling, in fostering multilevel relationships between plants and insects. Pivotal elements of the cuticle with this respect are undoubtedly its surface lipids and especially the long-chained, saturated, unsaturated, and branched hydrocarbons. Int. J. Mol. Sci. 2016, 17, 1966; doi:10.3390/ijms17121966 www.mdpi.com/journal/ijms Int.Int. J.J. Mol.Mol. Sci.Sci. 20162016,, 1717,, 19661966 22 ofof 1919 branched hydrocarbons. Cuticular hydrocarbons (CHCs) have been intensely investigated in social Cuticularinsects as hydrocarbons they are known (CHCs) to be have involved been intenselyin nestmate investigated recognition in social[13], whereas insects as in they plants are their known main to befunction involved is in in the nestmate limitation recognition of water [13 loss], whereas [14], as ina barrier plants theirto plant main pathogens function is[4] in or the as limitationtaxonomical of watermarkers loss [15]. [14], asIn a barriercontrast, to plantthere pathogensis a lack [4 ]of or asinformation taxonomical about markers the[ 15CHC]. In contrast,contribution there isas acommunication lack of information signals about or thecues CHC in multitrophic contribution interactions. as communication CHCs signalsare multifarious or cues in multitrophicmediators in interactions.plant–insect CHCsassociations are multifarious (see Section mediators 5), which in can plant–insect be secondarily associations exploited (see by Section eavesdroppers5), which can(see beSection secondarily 6). However, exploited the by evaluation eavesdroppers of benefits (see Section for the6). emitter However, or the evaluationreceiver (or of both) benefits is far for from the emitterbeing straightforward or the receiver (or or both) conclusive, is far from therefore being straightforward here CHCs are or conclusive,treated generically therefore hereas stimuli, CHCs areirrespectively treated generically of whether as stimuli, they are irrespectively true signals or of cues whether [16]. they are true signals or cues [16]. FigureFigure 1.1.Cuticle Cuticle scheme scheme of: of: ( A(A)) insects; insects; and and (B ()B plants.) plants. (A ()A a,) a, glandular glandular duct; duct; b, cement;b, cement; c, wax;c, wax; d, epicuticle;d, epicuticle; e, exocuticle; e, exocuticle; f, endocuticle; f, endocuticle; g, glandular g, glandular cell; and cell; h, epidermal and h, epidermal cell with nucleus; cell with i, trichogen nucleus; celli, trichogen (B) a, epicuticular cell (B) a, waxes; epicuticular b, proper waxes; cuticle; b, proper c, pectine cuticle; cuticle c, layer;pectine d, cuticle cell wall; layer; and d, e, cell vacuole. wall; Chemicaland e, vacuole. structure Chemical of insect structure chitin and of insect plant chitin cutin isand also plant reported. cutin is also reported. Since symbioses between insects and plants may concern several distantly related taxa, this Since symbioses between insects and plants may concern several distantly related taxa, this survey is narrowed to systems involving ants, plants and Lepidoptera as: (i) ideal models to study survey is narrowed to systems involving ants, plants and Lepidoptera as: (i) ideal models to study co-evolutionary dynamics; and (ii) taxa for which bulk of eco-ethological, molecular and co-evolutionary dynamics; and (ii) taxa for which bulk of eco-ethological, molecular and physiological physiological information exists. information exists. After concisely describing myrmecophilous interactions, a synthesis beyond the current state of After concisely describing myrmecophilous interactions, a synthesis beyond the current state of the literature on chemical composition, biosynthetic pathways and functions of CHCs as molecular the literature on chemical composition, biosynthetic pathways and functions of CHCs as molecular signals in these multitrophic systems is provided. Finally, the opportunity to follow a signals in these multitrophic systems is provided. Finally, the opportunity to follow a comprehensive comprehensive approach in the inspection of multiple level associations is discussed, suggesting approach in the inspection of multiple level associations is discussed, suggesting new pathways for new pathways for future research. future research. WhyWhy Ants?Ants? AmongAmong insects,insects, antsants areare oneone ofof thethe richestrichest animalanimal groupsgroups inin termsterms ofof abundance,abundance, biomass,biomass, andand diversity.diversity. The evolutionary success of of ants ants is is likely likely due due to to their their so socialcial organization organization enhanced enhanced by by a acomplex complex communication communication system, system, as aswell well as asto totheir their morphology, morphology, physiology physiology and and ecology ecology [17]. [17 In]. Inseveral several terrestrial terrestrial ecosystems, ecosystems, a aconsiderable considerable amount amount of of individuals, individuals, coordinated coordinated by meansmeans ofof chemicalchemical cues cues in in collective-decision collective-decision making, making, represents represents a key a key factor factor for theirfor their ecological ecological dominance dominance [18]. Ants[18]. lackAnts in lack a hierarchical in a hierarchical control, control, but their but structured their structured labor system labor as system well as as the well colony as the plasticity colony plasticity to respond to internal and external environmental variations, by regulating the number of workers involved in distinct tasks, have proven to be a rewarding strategy [19,20]. Int. J. Mol. Sci. 2016, 17, 1966 3 of 19 to respond to internal and external environmental variations, by regulating the number of workers involved in distinct tasks, have proven to be a rewarding strategy [19,20]. Ants also show a wide geographical range, they are found in virtually all existing lands, with a few exceptions such as Iceland, Greenland and the Antarctic region. They are adapted to colonize even extreme habitats, and deeply shape the environment in which they live, by moving soils or conveying energy and cycles of nutrients [21]. In addition, ants often represent the main predators of other insects or small invertebrates, the primary seed-disperse organisms or even