Faster speciation of fig-wasps than their host figs leads to decoupled speciation dynamics: Snapshots across the speciation continuum

Daniel Souto-Vilarós, Antonin Machac, Jan Michalek, Clive Terence Darwell, Mentap Sisol, Thomas Kuyaiva, Brus Isua, George D. Weiblen, Vojtech Novotny, Simon T. Segar

Research output: Contribution to journalArticlepeer-review

4 Scopus citations

Abstract

Even though speciation involving multiple interacting partners, such as plants and their pollinators, has attracted much research, most studies focus on isolated phases of the process. This currently precludes an integrated understanding of the mechanisms leading to cospeciation. Here, we examine population genetic structure across six species-pairs of figs and their pollinating wasps along an elevational gradient in New Guinea. Specifically, we test three hypotheses on the genetic structure within the examined species-pairs and find that the hypothesized genetic structures represent different phases of a single continuum, from incipient cospeciation to the full formation of new species. Our results also illuminate the mechanisms governing cospeciation, namely that fig wasps tend to accumulate population genetic differences faster than their figs, which initially decouples the speciation dynamics between the two interacting partners and breaks down their one-to-one matching. This intermediate phase is followed by genetic divergence of both partners, which may eventually restore the one-to-one matching among the fully formed species. Together, these findings integrate current knowledge on the mechanisms operating during different phases of the cospeciation process. They also reveal that the increasingly reported breakdowns in one-to-one matching may be an inherent part of the cospeciation process. Mechanistic understanding of this process is needed to explain how the extraordinary diversity of species, especially in the tropics, has emerged. Knowing which breakdowns in species interactions are a natural phase of cospeciation and which may endanger further generation of diversity seems critical in a constantly changing world.

Original languageEnglish (US)
Pages (from-to)3958-3976
Number of pages19
JournalMolecular ecology
Volume28
Issue number17
DOIs
StatePublished - Sep 1 2019

Bibliographical note

Funding Information:
We thank all our field assistants at each of the collection sites as well as camp managers and all staff at the New Guinea Binatang Research Centre. We thank the Papua New Guinea Forest Research Institute and the Department of Environment and Conservation for help in getting plant and insect export permits. We thank the National Grid and Infrastructure MetaCentrum for computing and storage facilities provided under the programme ?Projects of Large Research, Development and Innovations Infrastructures? (CESNET LM2015042). Thanks to the Workshop of Speciation and Population Genomics (2018) for in depth discussions and examples on the analysis of NGS data. We thank Finn Kjellberg, four anonymous reviewers and the handling editor for their constructive review towards the improvement of this manuscript. A.M. was supported by the European Union's Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement No. 785799 and by Charles University Research Centre program No. 204069. S.T.S. acknowledges funding from the Grant Agency of the Czech Republic (number 15-24511S) and departmental support from Harper Adams University. V.N. acknowledges ERC 669609 funding.

Keywords

  • Papua New Guinea
  • altitudinal gradient
  • cospeciation
  • fig and fig-wasp mutualism
  • population genomics
  • population structure

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