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• W2082208233 abstract "When others show sexy tails or sing elaborate songs, many animals use the language of chemistry to attract potential mates. A study provides insights into the evolutionary conundrum of how new chemical signals can evolve in an established communication system. When others show sexy tails or sing elaborate songs, many animals use the language of chemistry to attract potential mates. A study provides insights into the evolutionary conundrum of how new chemical signals can evolve in an established communication system. The chemical senses — smell and taste — have evolved in a wide range of organisms from bacteria to vertebrates and have enabled them to sense the surrounding environment and benefit from information carried by external chemical cues [1Wyatt T.D. Pheromones and Animal Behaviour: Communication by Smell and Taste. Cambridge University Press, Cambridge2003Crossref Google Scholar]. While organisms can perceive only a fraction of the chemical compounds present in their surroundings, they also contribute to the global olfactory cacophony by — intentionally or not — emitting molecules, such as waste products or biosynthetic by-products [2Steiger S. Schmitt T. Schaefer H.M. The origin and dynamic evolution of chemical information transfer.Proc. R. Soc. B-Biol. Sci. 2011; 278: 970-979Crossref PubMed Scopus (124) Google Scholar]. Urine, for example, appears to be an endless source of chemical signals in mammals [3Ferrero D.M. Liberles S.D. The secret codes of mammalian scents.WIREs Syst. Biol. Med. 2010; 2: 23-33Crossref Scopus (39) Google Scholar]. Chemical cues convey information to those who can detect them, which can have great fitness consequences for both the emitter and the receiver and can provide the bases for the evolution of communication systems [4Bradbury J.W. Vehrencamp S.L. Principles of Animal Communication. Sinauer Associates, Sunderland, MA1998Google Scholar]. In a recent study in Nature, Niehuis et al. [5Niehuis O. Buellesbach J. Gibson J.D. Pothmann D. Hanner C. Mutti N.S. Judson A.K. Gadau J. Ruther J. Schmitt T. Behavioural and genetic analyses of Nasonia shed light on the evolution of sex pheromones.Nature. 2013; 494: 345-348Crossref PubMed Scopus (98) Google Scholar] show how a new chemical cue evolved and was integrated into the communication system of the jewel wasp Nasonia vitripennis. Sexual reproduction usually entails the encounter of the sexes, and the use of sex pheromones — chemical signals that mediate interactions between individuals of the same species — is commonplace. Sex pheromones can be used to mediate attraction, to trigger sophisticated courtship displays and acceptance of the suitor or to repel competitors and incompatible mates. For example, the (Z7,Z11)-heptacosadiene produced by Drosophila melanogaster females acts as an aphrodisiac on conspecific males but deters males of other fruitfly species [6Billeter J.-C. Atallah J. Krupp J.J. Millar J.G. Levine J.D. Specialized cells tag sexual and species identity in Drosophila melanogaster.Nature. 2009; 461: 987-991Crossref PubMed Scopus (270) Google Scholar]. Accordingly, the emergence of new species is often accompanied by a divergence in the pheromones used by the forming species [7Symonds M.R.E. Elgar M.A. The evolution of pheromone diversity.Trends Ecol. Evol. 2008; 23: 220-228Abstract Full Text Full Text PDF PubMed Scopus (283) Google Scholar, 8Smadja C. Butlin R.K. On the scent of speciation: the chemosensory system and its role in premating isolation.Heredity. 2009; 102: 77-97Crossref PubMed Scopus (307) Google Scholar]. Since the first pheromone was identified in the silkworm Bombyx mori in 1959 [9Butenandt A. Beckmann R. Stamm D. Hecker E. Uber den Sexual-Lockstoff des Seidenspinners Bombyx mori - Reindarstellung und Konstitution.Z. Naturforsch. 1959; 14: 283-284Google Scholar], a tremendous diversity of chemical signals have been identified, many of them in insects. How the evolutionary diversification of sexual communication signals can take place poses a conundrum: normally, selections would act against senders that send a deviant message or receivers that respond inappropriately, thus maintaining the integrity of signal and response and the coordination of the mate-recognition system [7Symonds M.R.E. Elgar M.A. The evolution of pheromone diversity.Trends Ecol. Evol. 2008; 23: 220-228Abstract Full Text Full Text PDF PubMed Scopus (283) Google Scholar, 8Smadja C. Butlin R.K. On the scent of speciation: the chemosensory system and its role in premating isolation.Heredity. 2009; 102: 77-97Crossref PubMed Scopus (307) Google Scholar, 10Butlin R. Genetic variation in mating signals and responses.in: Lambert D.M. Spencer H.G. Speciation and the Recognition Concept: Theory and Application. Johns Hopkins University Press, Baltimore1995: 327-366Google Scholar]. Recently, molecular studies have demonstrated that a single amino acid change can produce a new pheromone blend or change the ligand specificity from one pheromone component to another in Ostrinia moths [11Lassance J.-M. Liénard M.A. Antony B. Qian S. Fujii T. Tabata J. Ishikawa Y. Löfstedt C. Functional consequences of sequence variation in the pheromone biosynthetic gene pgFAR for Ostrinia moths.Proc. Natl. Acad. Sci. USA. 2013; 110: 3967-3972Crossref PubMed Scopus (73) Google Scholar, 12Leary G.P. Allen J.E. Bunger P.L. Luginbill J.B. Linn C.E. Macallister I.E. Kavanaugh M.P. Wanner K.W. Single mutation to a sex pheromone receptor provides adaptive specificity between closely related moth species.Proc. Natl. Acad. Sci. USA. 2012; 109: 14081-14086Crossref PubMed Scopus (146) Google Scholar]. Also, Li et al. [13Li Q. Korzan W.J. Ferrero D.M. Chang R.B. Roy D.S. Buchi M.l. Lemon J.K. Kaur A.W. Stowers L. Fendt M. et al.Synchronous evolution of an odor biosynthesis pathway and behavioral response.Curr. Biol. 2013; 23: 11-20Abstract Full Text Full Text PDF PubMed Scopus (132) Google Scholar] described the parallel evolution of an odor biosynthesis pathway and odor-evoked behaviors mediated by an evolutionarily conserved chemosensory receptor. Studying acoustic communication, Shaw and Lesnick [14Shaw K.L. Lesnick S.C. Genomic linkage of male song and female acoustic preference QTL underlying a rapid species radiation.Proc. Natl. Acad. Sci. USA. 2009; 106: 9737-9742Crossref PubMed Scopus (88) Google Scholar] reported the colocalization of the QTL underlying variation in song and song preference in Laupala crickets. So far, however, no such example is known from chemical communication systems, whereby a single locus would change both signal and response at the same time. Thus, either the signal or the response (receptor) has to change first, and the causal mutation has to escape negative selection to allow a matching change to eventually evolve. In their recent study, Niehuis and colleagues [5Niehuis O. Buellesbach J. Gibson J.D. Pothmann D. Hanner C. Mutti N.S. Judson A.K. Gadau J. Ruther J. Schmitt T. Behavioural and genetic analyses of Nasonia shed light on the evolution of sex pheromones.Nature. 2013; 494: 345-348Crossref PubMed Scopus (98) Google Scholar] shed light on how new signals might emerge and avoid being immediately selected against. Using the parasitoid wasps Nasonia they show that some males of a derived wasp species use a new component that makes their pheromone bouquet irresistible to females of the same species. However, females of related ancestral species seem to be either unable to smell the new male fragrance or they ignore it. In Nasonia, females are guided to their mates by the pheromones males produce. All species use a blend of two molecules, here named RS and MQ (4(R), 5(S)-5-hydroxy-4-decanolide and 4-methylquinazoline, respectively), but in the cosmopolitan N. vitripennis males have added a third component to the mix, RR (4(R), 5(R)-5-hydroxy-4-decanolide). In their behavioral assay, the authors show that RR appears to be necessary in addition to RS and MQ to elicit robust attraction of N. vitripennis females, whereas females of the close relative N. giraulti could not care less: they are happy as long as RS and MQ are present but are neither attracted further nor repelled when RR is added. Based on a series of behavioral experiments, Niehuis et al. [5Niehuis O. Buellesbach J. Gibson J.D. Pothmann D. Hanner C. Mutti N.S. Judson A.K. Gadau J. Ruther J. Schmitt T. Behavioural and genetic analyses of Nasonia shed light on the evolution of sex pheromones.Nature. 2013; 494: 345-348Crossref PubMed Scopus (98) Google Scholar] bring convincing evidence that the ancestral state of N. vitripennis consisted of females just like N. giraulti: not selectively preferring RR, but rather partial to it as a new cue and eventually allowing it to evolve as a new pheromone component (Figure 1). In other terms, the evolution of the preference did not predate the emergence of the new trait as seen in many other biological systems [15Grether G.F. The evolution of mate preferences, sensory biases, and indicator traits.in: Brockmann H.J. Roper T.J. Naguib M. Wynne-Edwards K.E. Mitani J.C. Simmons L.W. Advances in the Study of Behavior. Vol 41. Academic Press, 2010: 35-76Google Scholar]. But how do you make a new pheromone component when you are a jewel wasp? Well, after quick examination of the chemical structure, RR does not appear that different from RS. Indeed, the two molecules only differ by the stereochemistry of the hydroxyl group. Of course, whether it is S or R can make a big difference in the chemical love world of insects [16Tumlinson J.H. Klein M.G. Doolittle R.E. Ladd T.L. Proveaux A.T. Identification of the female Japanese beetle sex pheromone: inhibition of male response by an enantiomer.Science. 1977; 197: 789-792Crossref PubMed Scopus (248) Google Scholar], but the two molecules may share a common biosynthetic pathway regardless. To unravel the pathway leading to the production of the novel pheromone compound, Niehuis and his colleagues [5Niehuis O. Buellesbach J. Gibson J.D. Pothmann D. Hanner C. Mutti N.S. Judson A.K. Gadau J. Ruther J. Schmitt T. Behavioural and genetic analyses of Nasonia shed light on the evolution of sex pheromones.Nature. 2013; 494: 345-348Crossref PubMed Scopus (98) Google Scholar] took advantage of the palette of tools that makes Nasonia an outstanding model to study the genetics of complex traits, including pheromone evolution [17Werren J.H. Richards S. Desjardins C.A. Niehuis O. Gadau J. Colbourne J.K. Group T.N.G.W. Functional and evolutionary insights from the genomes of three parasitoid Nasonia species.Science. 2010; 327: 343-348Crossref PubMed Scopus (660) Google Scholar, 18Werren J.H. Loehlin D.W. The parasitoid wasp Nasonia: an emerging model system with haploid male genetics.Cold Spring Harb. Protoc. 2009; 2009 (pdb.emo134)Google Scholar]. The analysis of the offspring of interspecies crosses between N. vitripennis and gaulti allowed them to identify one quantitative trait locus explaining over 80% of the total variance in pheromone phenotype. Using fine-scale mapping and RNAi gene knockdown, they could narrow down the list of causative loci to a cluster of three genes encoding putative short-chain dehydrogenases. These enzymes catalyze the synthesis of RR using RS as substrate. Because the three genes are present in the N. gaulti genome and expressed in N. gaulti wasps, one may speculate that mutations affecting the substrate preference of the enzymes are responsible for the rise of a novel pheromone compound. Future functional characterization will certainly provide much-needed answers. Gene duplication followed by neo-functionalization of one or several of the paralogues combined is a possible mechanism that could have promoted the emergence of a new function in N. vitripennis [19Soskine M. Tawfik D.S. Mutational effects and the evolution of new protein functions.Nat. Rev. Genet. 2010; 11: 572-582Crossref PubMed Scopus (284) Google Scholar]. This awaits further confirmation, but one thing is already certain: male wasps found a way to turn an old scent into an acclaimed perfume, which may represent a common strategy for modifying the qualitative properties of pheromones. The study by Niehuis and coworkers [5Niehuis O. Buellesbach J. Gibson J.D. Pothmann D. Hanner C. Mutti N.S. Judson A.K. Gadau J. Ruther J. Schmitt T. Behavioural and genetic analyses of Nasonia shed light on the evolution of sex pheromones.Nature. 2013; 494: 345-348Crossref PubMed Scopus (98) Google Scholar] exemplifies how a new signal can be produced and recruited to serve in the communication channel of one species. However, we still know little about the circumstances and evolutionary force that would favor the maintenance and fixation of a new signal, and nothing about the evolution of the matching changes that are necessary at the level of the receiver for the evolution of a new preference. There is a limit on what we can learn about evolutionary processes by mechanistic studies and phylogenetic reconstructions. Discussing the role of natural selection in speciation, Via [20Via S. Natural selection in action during speciation.Proc. Natl. Acad. Sci. USA. 2009; 106: 9939-9946Crossref PubMed Scopus (381) Google Scholar] contrasted two approaches: using the spyglass the process is studied by attempting to look back to see the details of speciation from today's vantage point, whereas using the magnifying glass the mechanisms of reproductive isolation are studied in populations that are used as models of an early stage of speciation. Likewise, it may be necessary to study model communication systems that are polymorphic and potentially undergoing evolutionary changes currently. Pheromones, like other sensory signals, are integrated and processed to generate appropriate behavioral responses. Neither the receptors for RR and RS nor the neural circuitry transducing their effects are known; these fundamental pieces of information are necessary to deepen our understanding of the bases of pheromone signal evolution in the perspective of the receiver. How changes in sensory representation lead to modification in stereotyped decision-making awaits further study. The jewel wasps have not yet revealed all their secrets, but they are definitely exciting emerging models to study the evolution of pheromone communication aside from fruit flies and moths." @default.
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• W2082208233 title "Chemical Communication: A Jewel Sheds Light on Signal Evolution" @default.
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