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The Role of Wolbachia in Rhagoletis Fruit Fly Speciation

The Role of Wolbachia in Rhagoletis Fruit Fly Speciation

Hannes Schuler (ORCID: 0000-0001-8307-9831)
  • Grant DOI 10.55776/J3527
  • Funding program Erwin Schrödinger
  • Status ended
  • Start August 15, 2014
  • End March 14, 2017
  • Funding amount € 111,052
  • E-mail

Disciplines

Biology (65%); Agriculture and Forestry, Fishery (35%)

Keywords

    Wolbachia, Rhagoletis, Speciation

Abstract Final report

Speciation is a fundamental evolutionary process responsible for the great diversity of life on Earth. Main factors contributing to the evolution of reproductive isolation are geographic and ecological isolation. However, oft- forgotten and controversially discussed players in the speciation process of insects are reproduction-manipulating endosymbiotic bacteria of the genus Wolbachia that can form pre- and postzygotic barriers in infected insect populations. The multiply infected Rhagoletis fruit flies are an excellent system to study such effects as the evolutionary history of this genus involves a number radiations with different geographic modes, ranging from classic allopatric divergence to sympatric speciation via host plant shifting. Aim of this proposal is to evaluate the contribution of Wolbachia to speciation in different Rhagoletis species utilizing on-site research at the highly complex structured North American fruit fly populations. The research objective will be accomplished by analyzing Wolbachia strains from different Rhagoletis species groups that have undergone allopatric (e.g., R. suavis group) vs. sympatric (e.g., R. pomonella group) speciation. Following the broadly accepted theory that bacterial reproductive isolation almost always evolves in allopatry, I hypothesize that sympatrically derived species with extant gene flow will share the same strains of Wolbachia while allopatric species will possess different strains. I will test this hypothesis by the characterization of different Rhagoletis populations. Further, Wolbachia strains in parasitoid wasps attacking Rhagoletis flies will be characterized as possible vector of horizontal Wolbachia transmission between Rhagoletis species. This will give new insights into routes of horizontal transmission between different species and the evolution of Wolbachia in geographically separated populations with possible influences into speciation. Going beyond the capabilities of the established MLST system for strain discrimination, a combination of Sanger and next generation high throughput sequencing will be adapted to perform a high resolution characterization of this bacteria. Additionally the Rhagoletis species and their parasitoids will be screened for other bacterial endosymbionts influencing the host`s reproduction. Verifying an active role of Wolbachia in reproductive isolation and Rhagoletis speciation will ultimately require breeding of flies that are depleted of the bacteria to determine the extent that fertility is restored between flies. Thus, a secondary objective of the current proposal is to develop and establish protocols for curing Rhagoletis of Wolbachia, allowing follow-up manipulative studies in the future to confirm a direct connection of Wolbachia with fly reproductive isolation.

Bacterial endosymbionts have been hypothesized to play an important contributing role in the process of speciation. Cytoplasmic incompatibility between populations of organisms possessing different bacterial strains can contribute to postmating reproductive isolation. However, there is currently little direct evidence for this in nature, and the role of endosymbionts in speciation is still controversial. The goal of the Erwin Schrödinger Fellowship was to compare the genetic variation of Wolbachia among sympatric and allopatric Rhagoletis species to understand the potential role of the bacterial endosymbiont Wolbachia in speciation of Rhagoletis fruit flies. Specifically we focused on the characterization of different species and host races of the Rhagoletis pomonella species group and cherry infesting members of the Rhagoletis cingulata species group. We adapted the restriction site associated DNA sequencing (RADseq) approach to characterize Wolbachia (and potentially other endosymbionts) more efficiently. The enrichment of specific Wolbachia fragments, followed by ddRADseq and Illumina MiSeq sequencing enables the high-resolution characterization of Wolbachia in multiple individuals. With this approach we characterized Wolbachia in different Rhagoletis species. We characterized Wolbachia in Rhagoletis pomonella populations from the Midwestern US, Pacific Northwest and Mexico. Additionally we sequenced the endosymbiont from the sister taxa Rhagoletis mendax, Rhagoletis zephyria, the undescribed flowering dogwood fly and Rhagoletis cornivora. Based on the six different genes all members of the R. pomonella species group share the same Wolbachia strain. Populations from the central highlands of Mexico, however, are infected by a second Wolbachia strain. Similar, different populations of the two cherry attacking sister species Rhagoletis cingulata and Rhagoletis indifferens are all infected by the same Wolbachia strain. Populations from Southwestern US, however, are infected by an additional Wolbachia strain, while R. indifferens populations from Central Washington are additionally infected by a third Wolbachia strain. Crossings of individuals infected by different Wolbachia strains revealed unidirectional incompatibilities between males from Southwestern US with females from Eastern and Western US suggesting Wolbachia-induced cytoplasmic incompatibility. In this project we further described the Wolbachia spread in the European cherry fruit fly Rhagoletis cerasi, we characterized Wolbachia in parasitoids attacking different Rhagoletis species and we performed an initial characterization of the microbial community in different Rhagoletis species. We also described an additional Endosymbiont Spiroplasma in the R. pomonella species group and studied Wolbachia in the gall wasp Belonocnema traetae.

Research institution(s)
  • University of Notre Dame - 100%

Research Output

  • 249 Citations
  • 17 Publications
Publications
  • 2021
    Title Testing the potential contribution of Wolbachia to speciation when cytoplasmic incompatibility becomes associated with host-related reproductive isolation
    DOI 10.1111/mec.16157
    Type Journal Article
    Author Bruzzese D
    Journal Molecular Ecology
    Pages 2935-2950
    Link Publication
  • 2017
    Title Speciation, Process of
    DOI 10.1016/b978-0-12-809633-8.02366-9
    Type Book Chapter
    Author Feder J
    Publisher Elsevier
  • 2019
    Title The Apennines as a cryptic Pleistocene refugium of the bark beetle Pityogenes chalcographus (Coleoptera: Curculionidae)
    DOI 10.1093/biolinnean/blz012
    Type Journal Article
    Author Schebeck M
    Journal Biological Journal of the Linnean Society
    Pages 24-33
    Link Publication
  • 2019
    Title Dynamics of an Ongoing Wolbachia Spread in the European Cherry Fruit Fly, Rhagoletis cerasi (Diptera: Tephritidae)
    DOI 10.3390/insects10060172
    Type Journal Article
    Author Schebeck M
    Journal Insects
    Pages 172
    Link Publication
  • 2021
    Title Genomically correlated trait combinations and antagonistic selection contributing to counterintuitive genetic patterns of adaptive diapause divergence in Rhagoletis flies
    DOI 10.1111/jeb.13952
    Type Journal Article
    Author Calvert M
    Journal Journal of Evolutionary Biology
    Pages 146-163
  • 2019
    Title Geographic and Ecological Dimensions of Host Plant-Associated Genetic Differentiation and Speciation in the Rhagoletis cingulata (Diptera: Tephritidae) Sibling Species Group
    DOI 10.3390/insects10090275
    Type Journal Article
    Author Doellman M
    Journal Insects
    Pages 275
    Link Publication
  • 2019
    Title Host plant-related genomic differentiation in the European cherry fruit fly, Rhagoletis cerasi
    DOI 10.1111/mec.15239
    Type Journal Article
    Author Bakovic V
    Journal Molecular Ecology
    Pages 4648-4666
    Link Publication
  • 2018
    Title Diversity and distribution of Wolbachia in relation to geography, host plant affiliation and life cycle of a heterogonic gall wasp
    DOI 10.1186/s12862-018-1151-z
    Type Journal Article
    Author Schuler H
    Journal BMC Evolutionary Biology
    Pages 37
    Link Publication
  • 2020
    Title Wolbachia-Mitochondrial DNA Associations in Transitional Populations of Rhagoletis cerasi
    DOI 10.3390/insects11100675
    Type Journal Article
    Author Bakovic V
    Journal Insects
    Pages 675
    Link Publication
  • 2020
    Title Identification of Plant DNA in Adults of the Phytoplasma Vector Cacopsylla picta Helps Understanding Its Feeding Behavior
    DOI 10.3390/insects11120835
    Type Journal Article
    Author Barthel D
    Journal Insects
    Pages 835
    Link Publication
  • 2020
    Title Evidence for spatial clines and mixed geographic modes of speciation for North American cherry-infesting Rhagoletis (Diptera: Tephritidae) flies
    DOI 10.1002/ece3.6667
    Type Journal Article
    Author Doellman M
    Journal Ecology and Evolution
    Pages 12727-12744
    Link Publication
  • 2016
    Title Wolbachia endosymbionts in haplodiploid and diploid scolytine beetles (Coleoptera: Curculionidae: Scolytinae)
    DOI 10.1111/1758-2229.12425
    Type Journal Article
    Author Kawasaki Y
    Journal Environmental Microbiology Reports
    Pages 680-688
  • 2016
    Title Wolbachia in Parasitoids Attacking Native European and Introduced Eastern Cherry Fruit Flies in Europe
    DOI 10.1093/ee/nvw137
    Type Journal Article
    Author Schuler H
    Journal Environmental Entomology
    Link Publication
  • 2016
    Title The hitchhiker's guide to Europe: the infection dynamics of an ongoing Wolbachia invasion and mitochondrial selective sweep in Rhagoletis cerasi
    DOI 10.1111/mec.13571
    Type Journal Article
    Author Schuler H
    Journal Molecular Ecology
    Pages 1595-1609
    Link Publication
  • 2015
    Title Divergence and evolution of reproductive barriers among three allopatric populations of Rhagoletis cingulata across eastern North America and Mexico
    DOI 10.1111/eea.12331
    Type Journal Article
    Author Tadeo E
    Journal Entomologia Experimentalis et Applicata
    Pages 301-311
    Link Publication
  • 2016
    Title Modes and Mechanisms of speciation.
    Type Book Chapter
    Author Reviews In Cell Biology And Molecular Medicine (Ed. R. Meyers).
  • 2017
    Title Wolbachia: Ein bakterieller Endosymbiont zur Bekämpfung von Schadinsekten.
    Type Conference Proceeding Abstract
    Author Schuler H
    Conference Arbeitsgemeinschaft für Lebensmittel-, Veterinär- und Agrarwesen, Tagungsbericht 2017 Zukunft Obstbau

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