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Evolution of Cuticular Hydrocarbons in the Hymenoptera : a Metaanalysis

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Evolution of Cuticular Hydrocarbons in the Hymenoptera : a Metaanalysis Evolution of cuticular hydrocarbons in the hymenoptera : a meta-analysis Kather, R and Martin, SJ http://dx.doi.org/10.1007/s10886-015-0631-5 Title Evolution of cuticular hydrocarbons in the hymenoptera : a meta-analysis Authors Kather, R and Martin, SJ Type Article URL This version is available at: http://usir.salford.ac.uk/id/eprint/36247/ Published Date 2015 USIR is a digital collection of the research output of the University of Salford. Where copyright permits, full text material held in the repository is made freely available online and can be read, downloaded and copied for non-commercial private study or research purposes. Please check the manuscript for any further copyright restrictions. For more information, including our policy and submission procedure, please contact the Repository Team at: [email protected]. JChemEcol DOI 10.1007/s10886-015-0631-5 Evolution of Cuticular Hydrocarbons in the Hymenoptera: a Meta-Analysis Ricarda Kather1 & Stephen J. Martin 2 Received: 12 July 2015 /Revised: 30 August 2015 /Accepted: 1 September 2015 # The Author(s) 2015. This article is published with open access at Springerlink.com Abstract Chemical communication is the oldest form of social and solitary species, with some of the most complex communication, spreading across all forms of life. In insects, CHC profiles belonging to the Parasitica. This profile com- cuticular hydrocarbons (CHC) function as chemical cues for plexity has been maintained in the ants, but some specializa- the recognition of mates, species, and nest-mates in social tion in biosynthetic pathways has led to a simplification of insects. Although much is known about the function of indi- profiles in the aculeate wasps and bees. The absence of vidual hydrocarbons and their biosynthesis, a phylogenetic CHC classes in some taxa or species may be due to gene overview is lacking. Here, we review the CHC profiles of silencing or down-regulation rather than gene loss, as demon- 241 species of Hymenoptera, one of the largest and most im- strated by sister species having highly divergent CHC profiles, portant insect orders, which includes the Symphyta (sawflies), and cannot be predicted by their phylogenetic history. The the polyphyletic Parasitica (parasitoid wasps), and the presence of highly complex CHC profiles prior to the Aculeata (wasps, bees, and ants). We investigated whether vast radiation of the social Hymenoptera indicates a these taxonomic groups differed in the presence and absence ‘spring-loaded’ system where the diversity of CHC of CHC classes and whether the sociality of a species (solitar- needed for the complex communication systems of so- ily vs. social) had an effect on CHC profile complexity. We cial insects were already present for natural selection to found that the main CHC classes (i.e., n-alkanes, alkenes, and act upon, rather than having evolved independently. methylalkanes) were all present early in the evolutionary his- This diversity may have aided the multiple independent tory of the Hymenoptera, as evidenced by their presence in evolution of sociality within the Aculeata. ancient Symphyta and primitive Parasitica wasps. Throughout all groups within the Hymenoptera, the more complex a CHC Keywords Cuticular hydrocarbons . Communication . the fewer species that produce it, which may reflect the Sociality . Spring-loaded . Hymenoptera . Gene-silencing . Occam’s razor principle that insects’ only biosynthesize the Sanflies . Parasitoid wasps . Aculeate wasps . Ants . Bees most simple compound that fulfil its needs. Surprisingly, there was no difference in the complexity of CHC profiles between Introduction Electronic supplementary material The online version of this article (doi:10.1007/s10886-015-0631-5) contains supplementary material, Chemical communication is the oldest form of communica- which is available to authorized users. tion, spreading across all forms of life (Wilson 1970), and underlies almost all known behavior from genes to super-or- * Stephen J. Martin ganisms. Pheromones are one of the most important signals [email protected] perceived through the chemical sensory channel (Wyatt 2013), and are particularly complex and well studied in insects 1 Department of Animal and Plant Sciences, University of Sheffield, (Howard and Blomquist 2005), where 1000s of pheromones Sheffield S10 2TN, UK have been described. Short-range contact pheromones are 2 School of Environment and Life Sciences, The University of Salford, used by many insects to identify and potentially discriminate Manchester M5 4WT, UK against other individuals of the same or different species JChemEcol (Wyatt 2013). The best studied group of compounds are the underlie the production of all these CHC (Howard and cuticular hydrocarbons (CHC) that are embedded in the cutic- Blomquist 2005; Morgan 2010). Both types of pathways in- ular lipid layer of all insects and have been extensively volve the elongation and reduction of fatty acyl-CoAs precur- researched over the past 30 years. This has shown that CHC sors to aldehydes before oxidative decarbonylation to obtain differ greatly both quantitatively and qualitatively among as the correct carbon chain length (Qiu et al. 2012). The produc- well as within a species. More recently, CHC have been tion of n-alkanes and alkenes, involves malonyl-CoA and, in shown to convey information about an individual’s fertility, the case of alkenes, a fatty acyl-CoA desaturase inserting a sex, gender, caste, kin, etc. in numerous species (Blomquist double-bond into the carbon chain at a precise location; i.e., a and Bagnères 2010). The majority of CHC studies have con- Δ9 desaturase inserts a double bond in the 9th position, a Δ7 centrated on the Hymenoptera, one of the largest and most desaturase into the 7th position etc. In the production of diverse insect orders with over 130,000 described species, methylalkanes, it is methylmalonyl-CoA that helps to insert including many economically and environmentally important a methyl group at various positions along the carbon chain. species, especially among the social bees, wasps and ants There is increasing evidence that compound structure (i.e., (Wilson 1971). The combined hymenopteran biomass out- presence and position of double-bonds or methyl groups) rath- weighs that of all other terrestrial organisms, even the verte- er than chain length is the key factor when it comes to an brates, due to their evolutionary success, which is reflected in insect’s ability to detect and learn different hydrocarbons their vast abundance (Wilson 1971). Central to their success is (Châline et al. 2005;Danietal.2005; van Wilgenburg et al. their chemical ecology. 2010). These studies demonstrate that insects can easily dis- Within the Hymenoptera, a huge diversity of CHC is pres- criminate between compounds bearing moieties such as dou- ent with thousands of compounds already having been de- ble bond and methyl branches, but cannot discriminate linear scribed. This diversity is generated simply by either the inser- alkanes. Furthermore, insects are able to learn and distinguish tion of one or more double bonds (olefins) or one or more between compounds of the same chain length that vary in the methyl groups (methylalkanes) at various positions along a position of their double-bond or methyl group, but are unable chain of carbon atoms that typically varies from 21 to around to discriminate between different homologs, i.e., compounds 40 carbons in length. Very rarely do both biosynthetic path- that share the same structure but differ in chain length (van ways combine to produce methylalkenes, which are Wilgenburg et al. 2010). Hence, we have concentrated on the methylalkanes that also contain a double bond/s. divergence of CHC structural isomers among the Importantly, these small additions of a double bond or methyl Hymenoptera, and have omitted data on chain length in order group cause the molecules to bend via Van der Waals forces, to make the analysis of the dataset manageable. so giving each CHC a unique conformation (shape). Another factor that makes Hymenoptera a key system is Furthermore, most methylalkanes contain chiral centers and that the order contains both solitary and social species. perception depends on odorant chirality, although in 20 insect Solitary insects use CHC to identify mates of the correct spe- species from nine orders the methyl-branched hydrocarbons cies and gender (e.g., Bartelt et al. 2002;Böröczkyetal.2009; were in the (R)-configuration (Bello et al. 2015). Likewise the Steiner et al. 2006), whereas social insects use CHC to distin- vast majority of insect olefins are present in the (Z)-configu- guish individuals of different species, castes, colonies, domi- ration. It has been shown that insects detect these small differ- nance statuses, developmental stages, kin, etc.(e.g., Bonavita- ences in compound structure, i.e., the position, chirality, or Cougourdan et al. 1987; Ferreira-Caliman et al. 2010;Martin absence of double bonds or methyl groups, so insects can et al. 2008a;Monnin2006; Wagner et al. 2001). Given that distinguish between compounds of the same chain length that social insects have a much greater level of chemical commu- vary in the position of their double bond(s) (Dani et al. 2005) nication than solitary insects, it has long been assumed that or methyl group(s) (Châline et al. 2005). However, little is social insects will produce a greater variety of CHC compared known about the actual molecular mechanism at the basis of to solitary Hymenoptera;
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