Wolbachia-driven selective sweep in a range expanding insect species

Junchen Deng, Giacomo Assandri, Pallavi Chauhan, Ryo Futahashi, Andrea Galimberti, Bengt Hansson, Lesley T. Lancaster, Yuma Takahashi, Erik Svensson, Anne Duplouy*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

7 Citations (Scopus)
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Background Evolutionary processes can cause strong spatial genetic signatures, such as local loss of genetic diversity, or conflicting histories from mitochondrial versus nuclear markers. Investigating these genetic patterns is important, as they may reveal obscured processes and players. The maternally inherited bacterium Wolbachia is among the most widespread symbionts in insects. Wolbachia typically spreads within host species by conferring direct fitness benefits, and/or by manipulating its host reproduction to favour infected over uninfected females. Under sufficient selective advantage, the mitochondrial haplotype associated with the favoured maternally-inherited symbiotic strains will spread (i.e. hitchhike), resulting in low mitochondrial genetic variation across the host species range. Method The common bluetail damselfly (Ischnura elegans: van der Linden, 1820) has recently emerged as a model organism for genetics and genomic signatures of range expansion during climate change. Although there is accumulating data on the consequences of such expansion on the genetics of I. elegans, no study has screened for Wolbachia in the damselfly genus Ischnura. Here, we present the biogeographic variation in Wolbachia prevalence and penetrance across Europe and Japan (including samples from 17 populations), and from close relatives in the Mediterranean area (i.e. I. genei: Rambur, 1842; and I. saharensis: Aguesse, 1958). Results Our data reveal (a) multiple Wolbachia-strains, (b) potential transfer of the symbiont through hybridization, (c) higher infection rates at higher latitudes, and (d) reduced mitochondrial diversity in the north-west populations, indicative of hitchhiking associated with the selective sweep of the most common strain. We found low mitochondrial haplotype diversity in the Wolbachia-infected north-western European populations (Sweden, Scotland, the Netherlands, Belgium, France and Italy) of I. elegans, and, conversely, higher mitochondrial diversity in populations with low penetrance of Wolbachia (Ukraine, Greece, Montenegro and Cyprus). The timing of the selective sweep associated with infected lineages was estimated between 20,000 and 44,000 years before present, which is consistent with the end of the last glacial period about 20,000 years. Conclusions Our findings provide an example of how endosymbiont infections can shape spatial variation in their host evolutionary genetics during postglacial expansion. These results also challenge population genetic studies that do not consider the prevalence of symbionts in many insects, which we show can impact geographic patterns of mitochondrial genetic diversity.

Original languageEnglish
Article number181
Number of pages17
JournalBmc ecology and evolution
Publication statusPublished - 25 Sept 2021

Bibliographical note

Thanks to F.F. Pan and S.W. Deng for their support over the course of this study. Thanks to C. Duplouy and S. Mäkelä for their assistance with collecting samples from France and Åland, and to H. Naraoka for providing samples from Rokkasho Japan. Thanks to C. Martel, Prof. N. Wahlberg and the members of the Systematic Biology Group at Lund University, to Prof. E. Svensson’s lab members, Prof. S. Bensch, Dr. C. Cornwallis and Prof. J-Å. Nilsson for fruitful discussions on the study. Diversity, Equality and Inclusion statement (https:// www.nature.com/articles/d41586-020-02429-8). The authors highly value equity, diversity and inclusion in science. We would like to acknowledge the international character of our team, which significantly contributed to the completion and quality of the present study. It includes researchers from different countries, backgrounds and career stages. The first author is from China, the last author is from France, other authors are from India, Italy, Japan, Sweden and USA. There are three female and seven male authors. We cite a large body of studies from many of our peers without checking whether the citations are equally distributed across groups. We thus acknowledge some shortcomings in our study and strive to address these issues in future work.

Open access funding provided by Lund University. JD was funded by the Lund University Master program in Evolutionary Biology. AD was funded by a Marie Curie Sklodowska Individual Fellowship to AD (#790531, HostSweetHome) and by the Academy of Finland to AD (#328944). BH was funded by the Swedish Research Council (consolidator grant #2016-689). EIS was funded by the Swedish Research Council (VR # 2016-03356), the Gyllenstiernska Krapperup- stiftelsen (#KR2018-0038) and Lunds Djurskyddsfond.

Data Availability Statement

The dataset supporting the conclusions of this article is available in the Zenodo repository https://doi.org/10.5281/zenodo.4445061; and in GenBank database (Accession #MZ463094-100; MZ501175-205; MZ508997-9001; MW509059-66; MZ893225-MZ893331) as stated in the text. The Illumina
raw reads are deposited at NCBI short read archive (SRA) under accession numbers Bioproject PRJNA575663 and Biosample SAMN12906381 and SAMN12920919–20.
The online version contains supplementary material available at https://doi. org/10.1186/s12862-021-01906-6.


  • Endosymbiosis
  • Phylogeography
  • Damselfly
  • Mitochondria
  • Genetic diversity


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