Admixture of evolutionary rates across a butterfly hybrid zone
Abstract
Hybridization is a major evolutionary force that can erode genetic differentiation between species, whereas reproductive isolation maintains such differentiation. In studying a hybrid zone between the swallowtail butterflies Papilio syfanius and Papilio maackii (Lepidoptera: Papilionidae), we made the unexpected discovery that genomic substitution rates are unequal between the parental species. This phenomenon creates a novel process in hybridization, where genomic regions most affected by gene flow evolve at similar rates between species, while genomic regions with strong reproductive isolation evolve at species-specific rates. Thus, hybridization mixes evolutionary rates in a way similar to its effect on genetic ancestry. Using coalescent theory, we show that the rate-mixing process provides distinct information about levels of gene flow across different parts of genomes, and the degree of rate-mixing can be predicted quantitatively from relative sequence divergence (FST) between the hybridizing species at equilibrium. Overall, we demonstrate that reproductive isolation maintains not only genomic differentiation, but also the rate at which differentiation accumulates. Thus, asymmetric rates of evolution provide an additional signature of loci involved in reproductive isolation.
Data availability
Source code is available at:https://github.com/tzxiong/2021_Maackii_Syfanius_HybridZoneWhole-genome sequences are deposited in the National Center for Biotechnology Information, Sequence Read Archive (BioProject Accession Number: PRJNA765117).
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Hybridization between Papilio syfanius and Papilio maackiiNCBI Sequence Read Archive, PRJNA765117.
Article and author information
Author details
Funding
American Philosophical Society (The Lewis and Clark Fund for Exploration and Field Research (2017-2018))
- Tianzhu Xiong
The NSF-Simons Center for Mathematical and Statistical Analysis of Biology at Harvard (Award Number #1764269)
- Tianzhu Xiong
The Harvard Quantitative Biology Initiative (Graduate Student Fellowship)
- Tianzhu Xiong
Department of Organismic and Evolutionary Biology, Harvard University (Graduate Student Fellowship)
- Tianzhu Xiong
Department of Organismic and Evolutionary Biology, Harvard University (Faculty Start-up Fund)
- James Mallet
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Daniel R Matute, University of North Carolina, Chapel Hill, United States
Version history
- Preprint posted: September 28, 2021 (view preprint)
- Received: February 23, 2022
- Accepted: June 14, 2022
- Accepted Manuscript published: June 15, 2022 (version 1)
- Version of Record published: June 30, 2022 (version 2)
- Version of Record updated: April 2, 2024 (version 3)
Copyright
© 2022, Xiong et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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