Inbreeding in a dioecious plant has sex- and population origin-specific effects on its interactions with pollinators

Abstract

We study the effects of inbreeding in a dioecious plant on its interaction with pollinating insects and test whether the magnitude of such effects is shaped by plant individual sex and the evolutionary histories of plant populations. We recorded spatial, scent, colour and rewarding flower traits as well as pollinator visitation rates in experimentally inbred and outbred, male and female Silene latifolia plants from European and North American populations differing in their evolutionary histories. We found that inbreeding specifically impairs spatial flower traits and floral scent. Our results support that sex-specific selection and gene expression may have partially magnified these inbreeding costs for females, and that divergent evolutionary histories altered the genetic architecture underlying inbreeding effects across population origins. Moreover, the results indicate that inbreeding effects on floral scent may have a huge potential to disrupt interactions among plants and nocturnal moth pollinators, which are mediated by elaborate chemical communication.

Data availability

All datasets and analyses supporting this article have been deposited to Dryad, under the DOI 10.5061/dryad.612jm643d

The following data sets were generated

Article and author information

Author details

  1. Karin Schrieber

    Geobotany, Institute for Ecosystem Research, Kiel University, Kiel, Germany
    For correspondence
    kschrieber@ecology.uni-kiel.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7181-2741
  2. Sarah Catherine Paul

    Department of Chemical Ecology, Faculty of Biology, Bielefeld University, Bielefeld, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Levke Valena Höche

    Geobotany, Institute for Ecosystem Research, Kiel University, Kiel, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Andrea Cecilia Salas

    Geobotany, Institute for Ecosystem Research, Kiel University, Kiel, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Rabi Didszun

    Geobotany, Institute for Ecosystem Research, Kiel University, Kiel, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Jakob Mößnang

    Geobotany, Institute for Ecosystem Research, Kiel University, Kiel, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Caroline Müller

    Department of Chemical Ecology, Bielefeld University, Bielefeld, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Alexandra Erfmeier

    Geobotany, Institute for Ecosystem Research, Kiel University, Kiel, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1002-9216
  9. Elisabeth Eilers

    Department of Chemical Ecology, Faculty of Biology, Bielefeld University, Bielefeld, Germany
    Competing interests
    The authors declare that no competing interests exist.

Funding

Kiel University, Faculty of Mathematics and Natural Sciences, program for promotion of young female scientists

  • Karin Schrieber
  • Alexandra Erfmeier

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Youngsung Joo, Chungbuk National University, Republic of Korea

Publication history

  1. Received: December 9, 2021
  2. Accepted: May 9, 2021
  3. Accepted Manuscript published: May 14, 2021 (version 1)
  4. Version of Record published: May 27, 2021 (version 2)
  5. Version of Record updated: June 3, 2021 (version 3)

Copyright

© 2021, Schrieber et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 2,871
    Page views
  • 128
    Downloads
  • 2
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Karin Schrieber
  2. Sarah Catherine Paul
  3. Levke Valena Höche
  4. Andrea Cecilia Salas
  5. Rabi Didszun
  6. Jakob Mößnang
  7. Caroline Müller
  8. Alexandra Erfmeier
  9. Elisabeth Eilers
(2021)
Inbreeding in a dioecious plant has sex- and population origin-specific effects on its interactions with pollinators
eLife 10:e65610.
https://doi.org/10.7554/eLife.65610
  1. Further reading

Further reading

    1. Ecology
    2. Microbiology and Infectious Disease
    Aileen Berasategui, Hassan Salem
    Insight

    Honeybees rely on their microbial gut symbionts to overcome a potent toxin found in pollen and nectar.

    1. Ecology
    2. Microbiology and Infectious Disease
    Noa Barak-Gavish, Bareket Dassa ... Assaf Vardi
    Research Article

    Unicellular algae, termed phytoplankton, greatly impact the marine environment by serving as the basis of marine food webs and by playing central roles in the biogeochemical cycling of elements. The interactions between phytoplankton and heterotrophic bacteria affect the fitness of both partners. It is becoming increasingly recognized that metabolic exchange determines the nature of such interactions, but the underlying molecular mechanisms remain underexplored. Here, we investigated the molecular and metabolic basis for the bacterial lifestyle switch, from coexistence to pathogenicity, in Sulfitobacter D7 during its interaction with Emiliania huxleyi, a cosmopolitan bloom-forming phytoplankter. To unravel the bacterial lifestyle switch, we analyzed bacterial transcriptomes in response to exudates derived from algae in exponential growth and stationary phase, which supported the Sulfitobacter D7 coexistence and pathogenicity lifestyles, respectively. In pathogenic mode, Sulfitobacter D7 upregulated flagellar motility and diverse transport systems, presumably to maximize assimilation of E. huxleyi-derived metabolites released by algal cells upon cell death. Algal dimethylsulfoniopropionate (DMSP) was a pivotal signaling molecule that mediated the transition between the lifestyles, supporting our previous findings. However, the coexisting and pathogenic lifestyles were evident only in the presence of additional algal metabolites. Specifically, we discovered that algae-produced benzoate promoted the growth of Sulfitobacter D7 and hindered the DMSP-induced lifestyle switch to pathogenicity, demonstrating that benzoate is important for maintaining the coexistence of algae and bacteria. We propose that bacteria can sense the physiological state of the algal host through changes in the metabolic composition, which will determine the bacterial lifestyle during interaction.