Section: Ecology
Topic: Ecology, Evolution, Population biology

Positive fitness effects help explain the broad range of Wolbachia prevalences in natural populations

Karisto, Petteri1, 2  ; Duplouy, Anne3 ; de Vries, Charlotte1, 4 ; Kokko, Hanna1, 5, 6 
1 Department of Evolutionary Biology and Environmental Studies, University of Zurich – Zurich, Switzerland
2 Current address: Plant Health, Natural Resources Institute Finland – Jokioinen, Finland
3 Insect Symbiosis Ecology and Evolution, Organismal and Evolutionary Biology Research Program, University of Helsinki – Helsinki, Finland
4 Current address: Department of Biological and Environmental Science, University of Jyväskylä – Jyväskylä, Finland
5 Konrad Lorenz Institute of Ethology, University of Veterinary Medicine – Vienna, Austria
6 Faculty of Biological and Environmental Sciences, University of Helsinki – Helsinki, Finland

Corresponding author(s): Karisto, Petteri (petteri.karisto@luke.fi)

10.24072/pcjournal.202 - Peer Community Journal, Volume 2 (2022), article no. e76.

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The bacterial endosymbiont Wolbachia is best known for its ability to modify its host’s reproduction by inducing cytoplasmic incompatibility (CI) to facilitate its own spread. Classical models predict either near-fixation of costly Wolbachia once the symbiont has overcome a threshold frequency (invasion barrier), or Wolbachia extinction if the barrier is not overcome. However, natural populations do not all follow this pattern: Wolbachia can also be found at low frequencies (below one half) that appear stable over time. Wolbachia is known to have pleiotropic fitness effects (beyond CI) on its hosts. Existing models typically focus on the possibility that these are negative. Here we consider the possibility that the symbiont provides direct benefits to infected females (e.g. resistance to pathogens) in addition to CI. We discuss an underappreciated feature of Wolbachia dynamics: that CI with additional fitness benefits can produce low-frequency (< 1/2) stable equilibria. Additionally, without a direct positive fitness effect, any stable equilibrium close to one half will be sensitive to perturbations, which make such equilibria unlikely to sustain in nature. The results hold for both diplodiploid and different haplodiploid versions of CI. We suggest that insect populations showing low-frequency Wolbachia infection might host CI-inducing symbiotic strains providing additional (hidden or known) benefits to their hosts, especially when classical explanations (ongoing invasion, source-sink dynamics) have been ruled out.

Published online:
DOI: 10.24072/pcjournal.202
Type: Research article

Karisto, Petteri 1, 2; Duplouy, Anne 3; de Vries, Charlotte 1, 4; Kokko, Hanna 1, 5, 6

1 Department of Evolutionary Biology and Environmental Studies, University of Zurich – Zurich, Switzerland
2 Current address: Plant Health, Natural Resources Institute Finland – Jokioinen, Finland
3 Insect Symbiosis Ecology and Evolution, Organismal and Evolutionary Biology Research Program, University of Helsinki – Helsinki, Finland
4 Current address: Department of Biological and Environmental Science, University of Jyväskylä – Jyväskylä, Finland
5 Konrad Lorenz Institute of Ethology, University of Veterinary Medicine – Vienna, Austria
6 Faculty of Biological and Environmental Sciences, University of Helsinki – Helsinki, Finland
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
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     title = {Positive fitness effects help explain the broad range of {\protect\emph{Wolbachia}} prevalences in natural populations},
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Karisto, Petteri; Duplouy, Anne; de Vries, Charlotte; Kokko, Hanna. Positive fitness effects help explain the broad range of Wolbachia prevalences in natural populations. Peer Community Journal, Volume 2 (2022), article  no. e76. doi : 10.24072/pcjournal.202. https://peercommunityjournal.org/articles/10.24072/pcjournal.202/

PCI peer reviews and recommendation, and links to data, scripts, code and supplementary information: 10.24072/pci.ecology.100104

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Arthofer, W.; Riegler, M.; Schneider, D.; Krammer, M.; Miller, W. J.; Stauffer, C. Hidden Wolbachia diversity in field populations of the European cherry fruit fly, Rhagoletis cerasi (Diptera, Tephritidae), Molecular Ecology, Volume 18 (2009) no. 18, pp. 3816-3830 | DOI

[2] Breeuwer, J. A.; Werren, J. H. Microorganisms associated with chromosome destruction and reproductive isolation between two insect species, Nature, Volume 346 (1990) no. 6284, pp. 558-560 | DOI

[3] Caspari, E.; Watson, G. On the evolutionary importance of cytoplasmic sterility in mosquitoes, Evolution, Volume 13 (1959) no. 4, pp. 568-570 | DOI

[4] Chrostek, E.; Marialva, M. S.; Esteves, S. S.; Weinert, L. A.; Martinez, J.; Jiggins, F. M.; Teixeira, L. Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: a phenotypic and phylogenomic analysis, PLoS Genet, Volume 9 (2013) no. 12, p. e1003896 | DOI

[5] Junchen Deng; Giacomo Assandri; Pallavi Chauhan; Ryo Futahashi; Andrea Galimberti; Bengt Hansson; Lesley Lancaster; Yuma Takahashi; Erik I Svensson; Anne Duplouy Wolbachia-driven selective sweep in a range expanding insect species,, Research Square (2021) | DOI

[6] Anne Duplouy; Oskar Brattström Wolbachia in the Genus Bicyclus: a Forgotten Player, Microbial ecology, Volume 75 (2018), pp. 255-263 | DOI

[7] Duplouy, A.; Couchoux, C.; Hanski, I.; van Nouhuys, S. Wolbachia infection in a natural parasitoid wasp population, PloS one, Volume 10 (2015) no. 8, p. e0134843 | DOI

[8] Duplouy, A.; Hurst, G. D.; O’NEILL, S. L.; Charlat, S. Rapid spread of male-killing Wolbachia in the butterfly Hypolimnas bolina, Journal of evolutionary biology, Volume 23 (2010) no. 1, pp. 231-235 | DOI

[9] Duplouy, A.; Nair, A.; Nyman, T.; van Nouhuys, S. Long-term spatio-temporal genetic structure of an accidental parasitoid introduction, and local changes in prevalence of its associated Wolbachia symbiont, Authorea Preprints (2021) | DOI

[10] Egas, M.; Vala, F.; Breeuwer, J. On the evolution of cytoplasmic incompatibility in haplodiploid species, Evolution, Volume 56 (2002) no. 6, pp. 1101-1109 | DOI

[11] Engelstädter, J.; Telschow, A. Cytoplasmic incompatibility and host population structure, Heredity, Volume 103 (2009) no. 3, pp. 196-207 | DOI

[12] Fine, P. E. On the dynamics of symbiote-dependent cytoplasmic incompatibility in culicine mosquitoes, Journal of Invertebrate Pathology, Volume 31 (1978) no. 1, pp. 10-18 | DOI

[13] Flor, M.; Hammerstein, P.; Telschow, A. Wolbachia-induced unidirectional cytoplasmic incompatibility and the stability of infection polymorphism in parapatric host populations, Journal of Evolutionary Biology, Volume 20 (2007) no. 2, pp. 696-706 | DOI

[14] Fry, A. J.; Palmer, M. R.; Rand, D. M. Variable fitness effects of Wolbachia infection in Drosophila melanogaster, Heredity, Volume 93 (2004) no. 4, pp. 379-389 | DOI

[15] Charles R. Harris; K. Jarrod Millman; Stéfan J. van der Walt; Ralf Gommers; Pauli Virtanen; David Cournapeau; Eric Wieser; Julian Taylor; Sebastian Berg; Nathaniel J. Smith; Robert Kern; Matti Picus; Stephan Hoyer; Marten H. van Kerkwijk; Matthew Brett; Allan Haldane; Jaime Fernández del Río; Mark Wiebe; Pearu Peterson; Pierre Gérard-Marchant; Kevin Sheppard; Tyler Reddy; Warren Weckesser; Hameer Abbasi; Christoph Gohlke; Travis E. Oliphant Array programming with NumPy, Nature, Volume 585 (2020) no. 7825, pp. 357-362 | DOI

[16] Hilgenboecker, K.; Hammerstein, P.; Schlattmann, P.; Telschow, A.; Werren, J. H. How many species are infected with Wolbachia?–a statistical analysis of current data, FEMS microbiology letters, Volume 281 (2008) no. 2, pp. 215-220 | DOI

[17] Hoffmann, A. A.; Turelli, M. Cytoplasmic incompatibility in insects, Influential passengers. Inherited microorganisms and arthropodreproduction, Oxford University Press, 1997, pp. 42-80

[18] Hoffmann, A. A.; Turelli, M.; Harshman, L. G. Factors affecting the distribution of cytoplasmic incompatibility in Drosophila simulans, Genetics, Volume 126 (1990) no. 4, pp. 933-948 | DOI

[19] Hughes, G.; Allsopp, P.; Brumbley, S.; Woolfit, M.; McGraw, E.; O'Neill, S. L. Variable infection frequency and high diversity of multiple strains of Wolbachia pipientis in Perkinsiella planthoppers, Applied and environmental microbiology, Volume 77 (2011) no. 6, pp. 2165-2168 | DOI

[20] Hunter, J. D. Matplotlib: A 2D graphics environment, Computing in science & engineering, Volume 9 (2007) no. 3, pp. 90-95 | DOI

[21] Jeong, G.; Kang, T.; Park, H.; Choi, J.; Hwang, S.; Kim, W.; Choi, Y.; Lee, K.; Park, I.; Sim, H.; others Wolbachia infection in the Korean endemic firefly, Luciola unmunsana (Coleoptera: Lampyridae), Journal of Asia-Pacific Entomology, Volume 12 (2009) no. 1, pp. 33-36 | DOI

[22] Karisto, P.; Duploy, A.; de Vries, C.; Kokko, H. Source code for figures and analysis for "Positive fitness effects help explain the broad range of Wolbachia prevalences in natural populations", Zenodo, 2022 | DOI

[23] Kriesner, P.; Hoffmann, A. A.; Lee, S. F.; Turelli, M.; Weeks, A. R. Rapid sequential spread of two Wolbachia variants in Drosophila simulans, PLoS Pathog, Volume 9 (2013) no. 9, p. e1003607 | DOI

[24] Laven, H. Cytoplasmic inheritance in Culex, Nature, Volume 177 (1956) no. 4499, pp. 141-142 | DOI

[25] Lehtonen, J.; Kokko, H. Positive feedback and alternative stable states in inbreeding, cooperation, sex roles and other evolutionary processes, Philosophical Transactions of the Royal Society B: Biological Sciences, Volume 367 (2012) no. 1586, pp. 211-221 | DOI

[26] Otto, S. P.; Day, T. A Biologist's Guide to Mathematical Modeling in Ecology and Evolution, Princeton University Press, 2007 | DOI

[27] Richardson, M. F.; Weinert, L. A.; Welch, J. J.; Linheiro, R. S.; Magwire, M. M.; Jiggins, F. M.; Bergman, C. M. Population genomics of the Wolbachia endosymbiont in Drosophila melanogaster, PLoS genetics, Volume 8 (2012) no. 12, p. e1003129 | DOI

[28] Russell, J. A.; Funaro, C. F.; Giraldo, Y. M.; Goldman-Huertas, B.; Suh, D.; Kronauer, D. J.; Moreau, C. S.; Pierce, N. E. A veritable menagerie of heritable bacteria from ants, butterflies, and beyond: broad molecular surveys and a systematic review, PLoS One, Volume 7 (2012) no. 12, p. e51027 | DOI

[29] Ryan, P. A.; Turley, A. P.; Wilson, G.; Hurst, T. P.; Retzki, K.; Brown-Kenyon, J.; Hodgson, L.; Kenny, N.; Cook, H.; Montgomery, B. L.; others Establishment of wMel Wolbachia in Aedes aegypti mosquitoes and reduction of local dengue transmission in Cairns and surrounding locations in northern Queensland, Australia, Gates open research, Volume 3 (2019) | DOI

[30] Sazama, E. J.; Ouellette, S. P.; Wesner, J. S. Bacterial endosymbionts are common among, but not necessarily within, insect species, Environmental entomology, Volume 48 (2019) no. 1, pp. 127-133 | DOI

[31] Sun, X.; Cui, L.; Li, Z. Diversity and phylogeny of Wolbachia infecting Bactrocera dorsalis (Diptera: Tephritidae) populations from China, Environmental entomology, Volume 36 (2007) no. 5, pp. 1283-1289 | DOI

[32] Tagami, Y.; Miura, K. Distribution and prevalence of Wolbachia in Japanese populations of Lepidoptera, Insect molecular biology, Volume 13 (2004) no. 4, pp. 359-364 | DOI

[33] Telschow, A.; Flor, M.; Kobayashi, Y.; Hammerstein, P.; Werren, J. H. Wolbachia-induced unidirectional cytoplasmic incompatibility and speciation: mainland-island model, PLoS one, Volume 2 (2007) no. 8, p. e701 | DOI

[34] Turelli, M. Evolution of incompatibility-inducing microbes and their hosts, Evolution, Volume 48 (1994) no. 5, pp. 1500-1513 | DOI

[35] Turelli, M.; Hoffmann, A. A. Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations., Genetics, Volume 140 (1995) no. 4, pp. 1319-1338 | DOI

[36] Vavre, F.; Fleury, F.; Varaldi, J.; Fouillet, P.; Bouleatreau, M. Evidence for female mortality in Wolbachia-mediated cytoplasmic incompatibility in haplodiploid insects: epidemiologic and evolutionary consequences, Evolution, Volume 54 (2000) no. 1, pp. 191-200 | DOI

[37] Weeks, A. R.; Turelli, M.; Harcombe, W. R.; Reynolds, K. T.; Hoffmann, A. A. From parasite to mutualist: rapid evolution of Wolbachia in natural populations of Drosophila, PLoS biology, Volume 5 (2007) no. 5, p. e114 | DOI

[38] Weinert, L. A.; Araujo-Jnr, E. V.; Ahmed, M. Z.; Welch, J. J. The incidence of bacterial endosymbionts in terrestrial arthropods, Proceedings of the Royal Society B: Biological Sciences, Volume 282 (2015) no. 1807, p. 20150249 | DOI

[39] Yen, J. H.; Barr, A. R. New hypothesis of the cause of cytoplasmic incompatibility in Culex pipiens L., Nature, Volume 232 (1971) no. 5313, pp. 657-658 | DOI

[40] Zug, R.; Hammerstein, P. Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected, PloS one, Volume 7 (2012) no. 6, p. e38544 | DOI

[41] Zug, R.; Hammerstein, P. Evolution of reproductive parasites with direct fitness benefits, Heredity, Volume 120 (2018) no. 3, pp. 266-281 | DOI

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