Genetic variation for rectal gland volatiles among recently collected isofemale lines and a domesticated strain of Queensland fruit fly, Bactrocera tryoni (Diptera: Tephritidae)

PLoS One. 2023 Apr 28;18(4):e0285099. doi: 10.1371/journal.pone.0285099. eCollection 2023.

Abstract

Divergence between populations in mating behaviour can function as a potent premating isolating mechanism and promote speciation. However, very few cases of inherited intraspecific variation in sexual signalling have been reported in tephritid fruit flies, despite them being a highly speciose family. We tested for such variation in one tephritid, the Queensland fruit fly, Bactrocera tryoni (Qfly). Qfly mating behaviour depends on volatiles secreted from male rectal glands but no role for the volatiles from female rectal glands has yet been reported. We previously detected over 100 volatile compounds in male rectal glands and identified over 30 of them. Similar numbers were recorded in females. However, many compounds showed presence/absence differences between the sexes and many others showed quantitative differences between them. Here we report inherited variation among 24 Qfly lines (23 isofemale lines established from recent field collections and one domesticated line) in the abundance of three esters, two alcohols, two amides, an aldehyde and 18 unidentified volatiles in male rectal glands. We did not find any compounds in female rectal glands that varied significantly among the lines, although this may at least partly reflect lower female sample numbers. Most of the 26 male compounds that differed between lines were more abundant in the domesticated line than any of the recently established isofemale lines, which concurs with other evidence for changes in mating behaviour during domestication of this species. There were also large differences in several of the 26 compounds among the isofemale lines, and some of these differences were associated with the regions from which the lines were collected. While some of the variation in different compounds was correlated across lines, much of it was not, implicating involvement of multiple genes. Our findings parallel reports of geographic variation in other Qfly traits and point to inherited differences in reproductive physiology that could provide a basis for evolution of premating isolation between ecotypes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Domestication
  • Drosophila
  • Female
  • Genetic Variation
  • Male
  • Salt Gland
  • Tephritidae* / genetics

Grants and funding

This research was supported by the Australian Research Council Industrial Transformation Training Centre (ITTC) for Fruit Fly Biosecurity Innovation (Project IC50100026), funded by the Australian Government, including a fellowship to S.J.P. and PhD scholarship to C.C-V. This research was also conducted as part of the SITplus collaborative fruit fly program. Project Raising Q-fly Sterile Insect Technique to World Standard (HG14033) is funded by the Hort Frontiers Fruit Fly Fund, part of the Hort Frontiers strategic partnership initiative developed by Hort Innovation, with coinvestment from Macquarie University and contributions from the Australian Government. We also acknowledge CSIRO for its generous support of this project. Australian Research Council, https://www.arc.gov.au/ Hort Innovation, https://www.horticulture.com.au/ Macquarie University, https://www.mq.edu.au/ CSIRO, https://www.csiro.au/ The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.