Evolution and genetic architecture of sex-limited polymorphism in cuckoos

Author:

Merondun Justin12ORCID,Marques Cristiana I.345ORCID,Andrade Pedro35ORCID,Meshcheryagina Swetlana6ORCID,Galván Ismael7ORCID,Afonso Sandra35ORCID,Alves Joel M.3589ORCID,Araújo Pedro M.3510ORCID,Bachurin Gennadiy11,Balacco Jennifer12,Bán Miklós13ORCID,Fedrigo Olivier12ORCID,Formenti Giulio12ORCID,Fossøy Frode14ORCID,Fülöp Attila131516ORCID,Golovatin Mikhail6,Granja Sofia359ORCID,Hewson Chris17ORCID,Honza Marcel18,Howe Kerstin19ORCID,Larson Greger9ORCID,Marton Attila2021ORCID,Moskát Csaba22ORCID,Mountcastle Jacquelyn12ORCID,Procházka Petr18ORCID,Red’kin Yaroslav23ORCID,Sims Ying19ORCID,Šulc Michal18ORCID,Tracey Alan19ORCID,Wood Jonathan M. D.19ORCID,Jarvis Erich D.12ORCID,Hauber Mark E.24,Carneiro Miguel35ORCID,Wolf Jochen B. W.1ORCID

Affiliation:

1. Division of Evolutionary Biology, LMU Munich, Planegg-Martinsried, Germany.

2. Department of Ornithology, Max Planck Institute for Biological Intelligence, Seewiesen, Germany.

3. CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Universidade do Porto, Vairão, Portugal.

4. Departamento de Biologia, Faculdade de Ciências da Universidade do Porto, Porto, Portugal.

5. BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO, Vairão, Portugal.

6. Institute of Plant and Animal Ecology, Ural Branch, Russian Academy of Sciences, Yekaterinburg, Russia.

7. Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, Madrid, Spain.

8. Department of Genetics, University of Cambridge, Cambridge, CB2 3EH, UK.

9. Palaeogenomics and Bio-Archaeology Research Network, School of Archaeology, University of Oxford, Oxford, OX1 3QY, UK.

10. Department of Life Sciences, MARE–Marine and Environmental Sciences Centre/ARNET–Aquatic Research Network, University of Coimbra, Coimbra, Portugal.

11. Scientific and Practical Center of Biodiversity, Irbit, Russia.

12. The Vertebrate Genome Lab, Rockefeller University, New York, NY 10065, USA.

13. HUN-REN-UD Behavioral Ecology Research Group, Department of Evolutionary Zoology and Human Biology, University of Debrecen, Debrecen, Hungary.

14. Centre for Biodiversity Genetics, Norwegian Institute for Nature Research, Trondheim, Norway.

15. Evolutionary Ecology Group, Hungarian Department of Biology and Ecology, Babeş-Bolyai University, Cluj-Napoca, Romania.

16. STAR-UBB Institute of Advanced Studies in Science and Technology, Babeş-Bolyai University, Cluj-Napoca, Romania.

17. British Trust for Ornithology, Thetford, UK.

18. Institute of Vertebrate Biology, Czech Academy of Sciences, Brno, Czech Republic.

19. Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, UK.

20. Evolutionary Ecology Group, Faculty of Biology and Geology, Babeș-Bolyai University, Cluj-Napoca, Romania.

21. Department of Evolutionary Zoology and Human Biology, University of Debrecen, Debrecen, Hungary.

22. Hungarian Natural History Museum, Budapest, Hungary.

23. Zoological Museum, Moscow State University, Moscow, Russia.

24. Advanced Science Research Center and Program in Psychology, Graduate Center of the City University of New York, New York, NY 10031, USA.

Abstract

Sex-limited polymorphism has evolved in many species including our own. Yet, we lack a detailed understanding of the underlying genetic variation and evolutionary processes at work. The brood parasitic common cuckoo ( Cuculus canorus ) is a prime example of female-limited color polymorphism, where adult males are monochromatic gray and females exhibit either gray or rufous plumage. This polymorphism has been hypothesized to be governed by negative frequency-dependent selection whereby the rarer female morph is protected against harassment by males or from mobbing by parasitized host species. Here, we show that female plumage dichromatism maps to the female-restricted genome. We further demonstrate that, consistent with balancing selection, ancestry of the rufous phenotype is shared with the likewise female dichromatic sister species, the oriental cuckoo ( Cuculus optatus ). This study shows that sex-specific polymorphism in trait variation can be resolved by genetic variation residing on a sex-limited chromosome and be maintained across species boundaries.

Publisher

American Association for the Advancement of Science (AAAS)

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