Genetic, chemical and behavioral investigation of sexual signaling evolution in parasitoid wasps

• Applicant: Dr. Jan Büllesbach
• Subject Area: Ecology and Biodiversity of Animals and Ecosystems, Organismic Interactions ; Evolution, Anthropology
• Term: from 2019 to 2023
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 427879779

• Final Report Year: 2024

Final Report Abstract

The divergence of species- and sex-specific pheromone blends and their influence on reproductive behavior can be a major driving force of speciation. Cuticular hydrocarbons (CHCs) are an excellent example for this, as they have been demonstrated to encode and convey a vast array of differential chemical information, predominantly functioning in sexual and species-specific chemical communication. However, deciphering how exactly biologically relevant information is encoded and conveyed in complex pheromonal profiles has been notoriously difficult. Similarly, our knowledge of the genetic basis of CHC biosynthesis remains limited and heavily biased towards the insect model organism Drosophila melanogaster. The studies conducted through the obtained research grant were designed to jointly address these knowledge gaps, utilizing the prevalent model organisms for parasitoid wasps, the Nasonia species complex. Nasonia females use complex cuticular hydrocarbon (CHC) profiles as sex pheromones enticing males to perform courtship and copulation behavior. We elucidated the chemical pattern conveying sexual attractiveness in these wasps as specific methyl-branching patterns essential for the functionality in sexual communication. We achieved this by functionally characterizing three fatty acid synthase genes mainly responsible for biosynthesizing the methyl-branched hydrocarbons and upholding the integrity of the CHC profiles above a detection threshold for the males. This advances our understanding of how genetic information can be translated into biologically relevant chemical information and reveals that sexual attractiveness can have a comparably simple genetic basis. Furthermore, we pursued a comprehensive, complementary forward genomics approach to identify gene loci mediating species-specific mate preference between different Nasonia species. Taking advantage of their haplo-diploid sex determination and cross-species fertility, we mapped quantitative trait loci (QTL) for CHC variation in recombinant F2 hybrid males from Nasonia interspecific crosses that were also used to generate genetically identical daughters (‘clonal female sibships’) whose genetic variation stems solely from the respective fathers. Basically enabling us to perform haploid genetics for assessing phenotypic CHC variation in the diploid females, circumventing dominant/recessive effects, we discovered multiple genomic “hotspots” governing female CHC variation between the different Nasonia species. We also unveiled several methyl-branched CHC compounds either positively or negatively correlated with species-specific mating propensity of the parental males. Intriguingly, all of these research projects collectively hint at the little investigated methyl-branched alkanes as the main coding components conveying the main chemical information in CHC profiles. Transcending these valuable insights for evolutionary chemical ecology, prezygotic reproductive isolation, and genetics, furthering our knowledge on the exact mechanisms behind the complex mating system of this prominent parasitoid model organism bears considerable potential to optimize its rearing conditions and sustainability for integrated pest management. This very viable, ecofriendly alternative to the wide application of destructive and biodiversity-reducing pesticides constitutes an important stepstone towards a more sustainable, human-health driven and ecofriendly agriculture.

Publications

• Advances in deciphering the genetic basis of insect cuticular hydrocarbon biosynthesis and variation. Heredity, 126(2), 219-234.
  Holze, Henrietta; Schrader, Lukas & Buellesbach, Jan
  
• Genetic and genomic architecture of species-specific cuticular hydrocarbon variation in parasitoid wasps. Proceedings of the Royal Society B: Biological Sciences, 289.
  Buellesbach, Jan; Holze, Henrietta; Schrader, Lukas; Liebig, Jürgen; Schmitt, Thomas; Gadau, Juergen & Niehuis, Oliver
  
• Neglected Very Long-Chain Hydrocarbons and the Incorporation of Body Surface Area Metrics Reveal Novel Perspectives for Cuticular Profile Analysis in Insects. Insects, 13(1), 83.
  Golian, Marek; Bien, Tanja; Schmelzle, Sebastian; Esparza-Mora, Margy Alejandra; McMahon, Dino Peter; Dreisewerd, Klaus & Buellesbach, Jan
  
• Chemical and population genetic analysis show no evidence of ecotype formation in a European population of the parasitoid wasp Nasonia vitripennis. Frontiers in Ecology and Evolution, 11.
  Buellesbach, Jan; Lammers, Mark; van de Belt, José & Pannebakker, Bart A.
  
• Decoding the genetic and chemical basis of sexual attractiveness in parasitic wasps. eLife, 12.
  Sun, Weizhao; Lange, Michelle Ina; Gadau, Jürgen & Buellesbach, Jan