A region of suppressed recombination misleads neoavian phylogenomics

Author:

Mirarab Siavash1ORCID,Rivas-González Iker2ORCID,Feng Shaohong34ORCID,Stiller Josefin5ORCID,Fang Qi6ORCID,Mai Uyen1,Hickey Glenn7ORCID,Chen Guangji34ORCID,Brajuka Nadolina8ORCID,Fedrigo Olivier8ORCID,Formenti Giulio8ORCID,Wolf Jochen B. W.9ORCID,Howe Kerstin10ORCID,Antunes Agostinho1112ORCID,Schierup Mikkel H.2ORCID,Paten Benedict7ORCID,Jarvis Erich D.8ORCID,Zhang Guojie3,Braun Edward L.13ORCID

Affiliation:

1. Electrical and Computer Engineering Department, University of California, San Diego, CA 95032

2. Bioinformatics Research Centre, Aarhus University, Aarhus 8000, Denmark

3. Center for Evolutionary & Organismal Biology, Zhejiang University School of Medicine, Hangzhou 310058, China

4. Liangzhu Laboratory, Zhejiang University, Hangzhou 311121, China

5. Section for Ecology & Evolution, Department of Biology, University of Copenhagen, København 2100, Denmark

6. BGI-Research, Shenzhen 518083, China

7. Genomics Institute, University of California, Santa Cruz, CA 96064

8. Vertebrate Genome Lab, Rockefeller University, New York, NY 10065

9. Division of Evolutionary Biology, Faculty of Biology, Ludwig-Maximillians-Universität, Munich 82152, Germany

10. Tree of Life Division, Wellcome Sanger Institute, Cambridge CB10 1RQ, United Kingdom

11. Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Porto 4099-002, Portugal

12. Department of Biology, Faculty of Sciences, University of Porto, Porto 4099-002, Portugal

13. Department of Biology, University of Florida, Gainesville, FL 32611

Abstract

Genomes are typically mosaics of regions with different evolutionary histories. When speciation events are closely spaced in time, recombination makes the regions sharing the same history small, and the evolutionary history changes rapidly as we move along the genome. When examining rapid radiations such as the early diversification of Neoaves 66 Mya, typically no consistent history is observed across segments exceeding kilobases of the genome. Here, we report an exception. We found that a 21-Mb region in avian genomes, mapped to chicken chromosome 4, shows an extremely strong and discordance-free signal for a history different from that of the inferred species tree. Such a strong discordance-free signal, indicative of suppressed recombination across many millions of base pairs, is not observed elsewhere in the genome for any deep avian relationships. Although long regions with suppressed recombination have been documented in recently diverged species, our results pertain to relationships dating circa 65 Mya. We provide evidence that this strong signal may be due to an ancient rearrangement that blocked recombination and remained polymorphic for several million years prior to fixation. We show that the presence of this region has misled previous phylogenomic efforts with lower taxon sampling, showing the interplay between taxon and locus sampling. We predict that similar ancient rearrangements may confound phylogenetic analyses in other clades, pointing to a need for new analytical models that incorporate the possibility of such events.

Funder

National Science Foundation

Howard Hughes Medical Institute

Deutsche Forschungsgemeinschaft

Publisher

Proceedings of the National Academy of Sciences

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