Evolutionary mechanisms of pheromone divergence in moths and butterflies – pheromone-mediated assortative mating and speciation

In order to coexist, biological species need to be reproductively isolated (Mallet, 1995) and the evolution of mechanisms ensuring efficient reproductive isolation barriers is an integrated part of the speciation process. The evolution of mechanisms involved in specific mate finding and mate choice may account for premating reproductive isolation. In the Lepidoptera, with the exception of butterflies, mate finding is primarily mediated by female-emitted sex pheromones and finely tuned male responses (Wyatt, 2003). Pheromone changes can drive species divergence and may account for many instances of successful speciation (Baker, 2002; Löfstedt et al., 1986). An intriguing question in the evolution of sexual communication is how signal and response are coordinated for mate recognition (and species specificity) and how signal and response may still change under speciation (Löfstedt, 1993; Bengtsson and Löfstedt, 2007).

The purpose of this research programme is to link molecular insight about the genetic and biochemical mechanisms underpinning the evolution of novel pheromones with ecological and evolutionary theories concerning the role of pheromones in reproductive isolation and speciation. Using molecular and genomic tools, functional assays and phylogenetic analysis we explore the gene families that control this system. We are particularly interested in unravelling the mechanisms - including gene duplications, point mutations and regulation of transcription - that allow the diverging sex pheromone systems to escape the stabilizing selection ruling under normal conditions.

Ongoing studies focus on several groups of moths, butterflies of the genus Bicyclus as well as caddisflies, the sister group of Lepidoptera. In vitro expression systems have allowed us to confirm the functional identities of many moth desaturases and reductases characterized from pheromone glands and involved in pheromone production. On the reception side, the antenna is the primary olfactory appendage in insects. Male antennae are morphologically distinct from those of females and contain various types of sensilla housing olfactory receptors, also encoded by a multigene family, and some of which are specifically tuned to interpret the species-specific pheromone stimuli.

Phylogenetic analysis has revealed that new types of pheromone components have evolved at least twice in the evolution of the Lepidoptera (Löfstedt and Kozlov, 1997). At the same time, female-produced pheromones were apparently lost at least once in the evolution of the day-active butterflies, which rely on visual cues for mate finding. Male-produced pheromones may mediate courtship in butterflies as well as moths (Lassance and Löfstedt, 2009). Moths and butterflies provide an excellent model for studies of the causes and consequences of mate signal-response divergence and the diversification of a sophisticated mate communication system.

References:

Baker, T. C. 2002. Mechanism for saltational shifts in pheromone communication systems. Proc. Natl. Acad. Sci. USA 99:13368-13370.

Bengtsson, B.O. and Löfstedt, C. 2007. Direct and indirect selection in moth pheromone evolution: Population genetical simulations of asymmetric sexual interactions. Biol. J. Linn. Soc. 90:117-123.

Lassance, J.-M., Groot, A.T., Liénard, M.A., Antony, B., Borgwardt, C., Andersson, F., Hedenström, E., Heckel, D.G. and Löfstedt, C. 2010. Allelic variation in a fatty-acyl reductase gene causes divergence in moth sex pheromones. Nature 466:486-489.

Lassance, J.-M. and Löfstedt C. 2009. Concerted evolution of male and female display traits in the European corn borer, Ostrinia nubilalis. BMC Biol. 7:10 (12 pp.).

Liénard, M., Strandh, M., Hedenström, E., Johansson, T. and Löfstedt, C. 2008. Key biosynthetic gene subfamily recruited for pheromone production prior to the extensive radiation of Lepidoptera. BMC Evol. Biol.8:270 (15 pp.).

Liénard, M.A., Hagström, Å.K, Lassance, J.M., and Löfstedt, C. 2010. Evolution of multi-component pheromone signals in small ermine moths involves a single fatty-acyl reductase gene. Proc. Natl. Acad. Sci. USA 107:10955-10960.

Löfstedt, C. 1990. Population variation and genetic control of pheromone communication systems in moths. Ent. exp. appl. 54:199-218.

Löfstedt, C. 1993. Moth pheromone genetics and evolution. Phil. Trans. R. Soc. Lond. B 340:167-177.

Löfstedt, C., Herrebout, W.M., and Du, J.-W. 1986. Evolution of the ermine moth pheromone tetradecyl acetate. Nature 323:621-623.

Löfstedt, C. and Kozlov. M. 1997. A phylogenetic analysis of pheromone communication in primitive moths, pp. 473-489 in R.T. Cardé and A.K. Minks (eds.). Insect Pheromone Research: New Directions. Chapman & Hall, New York.

Mallet, J. 1995. A species definition for the modern synthesis. Trends Ecol. Evol. 43, 294-299.

Nieberding, C.M., de Vos, H., Schneider, M.V, Lassance, J.-M., Estramil, N., Andersson, J., Bång, J., Hedenström, E., Löfstedt, C. and Brakefield, P.M. 2008. The male sex pheromone of the butterfly Bicyclus anynana: Towards an evolutionary analysis. PLoS ONE 3:e2751 (12 pp.).

Wyatt, T.D. 2003. Pheromones and Animal Behaviour (Cambridge University Press).

Photos: Jean-Marc Lassance


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Last modified 19 Jul 2013

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