J Syst Evol

• Research Articles •    

The evolution of tachinid pollination in Neotinea ustulata is related to floral cuticular composition and the combined high relative production of (Z)-11-C23/C25enes

Carlos Martel1,2*, Demetra Rakosy3,4, Pedro E. Romero5, Jana Jersáková6, and Manfred Ayasse7   

  1. 1 Department of Biological Sciences, East Tennessee State University, Johnson City, TN 37614, USA
    2 Institute of Omics Sciences and Applied Biotechnology, Pontifical Catholic University of Peru, San Miguel, Lima 15088, Peru
    3 Department of Community Ecology, Helmholtz Centre for Environmental Research—UFZ, Halle (Saale) 06120, Germany
    4 German Centre for Integrative Biodiversity Research (iDiv), Halle‐Jena‐Leipzig, Leipzig 04103, Germany
    5 Laboratorios de Investigación y Desarrollo, Facultad de Ciencias y Filosofía, Universidad Peruana Cayetano Heredia, San Martín de Porres, Lima 15102, Peru
    6 Faculty of Science, University of South Bohemia, České Budějovice 37005, Czech Republic
    7 Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm 89081, Germany
  • Received:2021-08-19 Accepted:2021-10-17 Online:2021-10-21

Abstract: Among terrestrial orchids, and particularly among the subtribe Orchidinae, flies are underrepresented as pollinators. The European Neotinea ustulata, which developed specialized pollination by tachinid flies, is known to produce high relative concentrations of the floral cuticular alkenes (Z)-11-tricosene and (Z)-11-pentacosene (referred to as (Z)-11-C23/C25enes), which seem to be uncommon among orchid flowers. If the evolution of tachinid pollination is related to that of (Z)-11-C23/C25enes, we can expect that closely related species have a different floral chemical pattern and significantly small or no production of (Z)-11-C23/C25enes, independently of their pollinator guild identity (e.g., bees, flies, moths). We chemically compared the floral cuticular composition among Neotinea species, performed electrophysiological analyses, reconstructed the phylogenetic Orchidinae tree, and identified the evolutionary history of pollinator guild and (Z)-11-C23/C25enes production within the Orchidinae. Neotinea ustulata has evolved a markedly different floral cuticular composition compared to other Neotinea and produces both compounds ((Z)-11-C23/C25enes) in high relative quantities (i.e., above 8% in combination), which are detectable by tachinid antennae. Moreover, most Orchidinae taxa have minimal or no production of these alkenes, independently of the identity of their pollinator guild. Our ancestral reconstruction suggested that (Z)-11-C23/C25enes production was an evolutionary exaptation in Neotinea, whereas tachinid pollination was a unique evolutionary innovation for N. ustulata. Floral cuticular composition and, in particular, the combined production of (Z)-11-C23/C25enes at relatively high concentrations is intimately linked to the evolution of tachinid pollination within the Orchidinae.

Key words: alkenes, deceptive pollination, European orchids, exaptation, fly pollination