The evolution of strong reproductive isolation between sympatric intertidal snails

S. Stankowski, A.M. Westram, Z.B. Zagrodzka, I. Eyres, T. Broquet, K. Johannesson, R.K. Butlin, Philosophical Transactions of the Royal Society. Series B: Biological Sciences 375 (2020).


Journal Article | Published | English

Scopus indexed
Author
Stankowski, SeanIST Austria; Westram, Anja MIST Austria ; Zagrodzka, Zuzanna B.; Eyres, Isobel; Broquet, Thomas; Johannesson, Kerstin; Butlin, Roger K.
Department
Abstract
The evolution of strong reproductive isolation (RI) is fundamental to the origins and maintenance of biological diversity, especially in situations where geographical distributions of taxa broadly overlap. But what is the history behind strong barriers currently acting in sympatry? Using whole-genome sequencing and single nucleotide polymorphism genotyping, we inferred (i) the evolutionary relationships, (ii) the strength of RI, and (iii) the demographic history of divergence between two broadly sympatric taxa of intertidal snail. Despite being cryptic, based on external morphology, Littorina arcana and Littorina saxatilis differ in their mode of female reproduction (egg-laying versus brooding), which may generate a strong post-zygotic barrier. We show that egg-laying and brooding snails are closely related, but genetically distinct. Genotyping of 3092 snails from three locations failed to recover any recent hybrid or backcrossed individuals, confirming that RI is strong. There was, however, evidence for a very low level of asymmetrical introgression, suggesting that isolation remains incomplete. The presence of strong, asymmetrical RI was further supported by demographic analysis of these populations. Although the taxa are currently broadly sympatric, demographic modelling suggests that they initially diverged during a short period of geographical separation involving very low gene flow. Our study suggests that some geographical separation may kick-start the evolution of strong RI, facilitating subsequent coexistence of taxa in sympatry. The strength of RI needed to achieve sympatry and the subsequent effect of sympatry on RI remain open questions.
Publishing Year
Date Published
2020-07-12
Journal Title
Philosophical Transactions of the Royal Society. Series B: Biological Sciences
Acknowledgement
Funding was provided by the Natural Environment Research Council (NERC) and the European Research Council. We thank Rui Faria, Nicola Nadeau, Martin Garlovsky and Hernan Morales for advice and/or useful discussion during the project. Richard Turney, Graciela Sotelo, Jenny Larson, Stéphane Loisel and Meghan Wharton participated in the collection and processing of samples. Mark Dunning helped with the development of bioinformatic pipelines. The analysis of genomic data was conducted on the University of Sheffield High-performance computer, ShARC. Jeffrey Feder and an anonymous reviewer provided comments that improved the manuscript.
Volume
375
Issue
1806
Article Number
20190545
eISSN
IST-REx-ID

Cite this

Stankowski S, Westram AM, Zagrodzka ZB, et al. The evolution of strong reproductive isolation between sympatric intertidal snails. Philosophical Transactions of the Royal Society Series B: Biological Sciences. 2020;375(1806). doi:10.1098/rstb.2019.0545
Stankowski, S., Westram, A. M., Zagrodzka, Z. B., Eyres, I., Broquet, T., Johannesson, K., & Butlin, R. K. (2020). The evolution of strong reproductive isolation between sympatric intertidal snails. Philosophical Transactions of the Royal Society. Series B: Biological Sciences, 375(1806). https://doi.org/10.1098/rstb.2019.0545
Stankowski, Sean, Anja M Westram, Zuzanna B. Zagrodzka, Isobel Eyres, Thomas Broquet, Kerstin Johannesson, and Roger K. Butlin. “The Evolution of Strong Reproductive Isolation between Sympatric Intertidal Snails.” Philosophical Transactions of the Royal Society. Series B: Biological Sciences 375, no. 1806 (2020). https://doi.org/10.1098/rstb.2019.0545.
S. Stankowski et al., “The evolution of strong reproductive isolation between sympatric intertidal snails,” Philosophical Transactions of the Royal Society. Series B: Biological Sciences, vol. 375, no. 1806, 2020.
Stankowski S, Westram AM, Zagrodzka ZB, Eyres I, Broquet T, Johannesson K, Butlin RK. 2020. The evolution of strong reproductive isolation between sympatric intertidal snails. Philosophical Transactions of the Royal Society. Series B: Biological Sciences. 375(1806).
Stankowski, Sean, et al. “The Evolution of Strong Reproductive Isolation between Sympatric Intertidal Snails.” Philosophical Transactions of the Royal Society. Series B: Biological Sciences, vol. 375, no. 1806, 20190545, The Royal Society, 2020, doi:10.1098/rstb.2019.0545.
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