Echoes of ancient introgression punctuate stable genomic lineages in the evolution of figs

Author:

Gardner Elliot M.123ORCID,Bruun-Lund Sam4ORCID,Niissalo Matti3ORCID,Chantarasuwan Bhanumas5,Clement Wendy L.6,Geri Connie7,Harrison Rhett D.8ORCID,Hipp Andrew L.9ORCID,Holvoet Maxime4,Khew Gillian3,Kjellberg Finn10ORCID,Liao Shuai91112,Pederneiras Leandro Cardoso13,Peng Yan-Qiong14ORCID,Pereira Joan T.15,Phillipps Quentin16ORCID,Ahmad Puad Aida Shafreena17ORCID,Rasplus Jean-Yves18ORCID,Sang Julia19,Schou Sverre Juul4ORCID,Velautham Elango3ORCID,Weiblen George D.2021ORCID,Zerega Nyree J. C.2223ORCID,Zhang Qian24ORCID,Zhang Zhen12,Baraloto Christopher1,Rønsted Nina24ORCID

Affiliation:

1. International Center for Tropical Botany at the Kampong, Institute of Environment, Florida International University, Miami, FL 33133

2. National Tropical Botanical Garden, Kalāheo, HI 96741

3. Singapore Botanic Gardens, National Parks Board, 259569, Singapore

4. Natural History Museum of Denmark, University of Copenhagen, 1123 Copenhagen, Denmark

5. Thailand National History Museum, National Science Museum, Klong Luang, Pathum Thani 12120, Thailand

6. Department of Biology, The College of New Jersey, Ewing, NJ 08618

7. Sarawak Forestry Corporation, 93250 Kuching, Sarawak, Malaysia

8. CIFOR-ICRAF, St Eugene Office Park, 10101 Lusaka, Zambia

9. The Morton Arboretum, Lisle, IL 60532

10. CEFE, CNRS, Université de Montpellier, EPHE, IRD, 34090 Montpellier, France

11. South China Botanical Garden, Chinese Academy of Sciences, 510650 Guangzhou, China

12. School of Life Sciences, East China Normal University, 200241 Shanghai, China

13. Instituto de Pesquisa do Jardim Botânico do Rio de Janeiro, Diretoria de Pesquisa Científica, 22460-030 Rio de Janeiro–RJ, Brazil

14. Chinese Academy of Sciences, Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, 666303 Mengla, China

15. Sabah Forest Research Centre, Sabah Forestry Department, 90175 Sandakan, Sabah, Malaysia

16. Borneo Research Consultants, W3 0HA London, United Kingdom

17. Faculty of Agriculture & Applied Sciences, i-CATS University College, 93350 Kuching, Sarawak, Malaysia

18. CBGP, INRAE, CIRAD, IRD, Montpellier SupAgro, Université de Montpellier, 34988 Montpellier, France

19. Sarawak Forest Department, 34988 Kuching, Sarawak, Malaysia

20. Bell Museum, University of Minnesota, St. Paul, MN 55113

21. Department of Plant Biology, University of Minnesota, St. Paul, MN 55108

22. Plant Biology and Conservation, Northwestern University, Evanston, IL 60208

23. Negaunee Institute for Plant Conservation and Action, Chicago Botanic Garden, Glencoe, IL 60022

24. State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, 100093 Beijing, China

Abstract

Studies investigating the evolution of flowering plants have long focused on isolating mechanisms such as pollinator specificity. Some recent studies have proposed a role for introgressive hybridization between species, recognizing that isolating processes such as pollinator specialization may not be complete barriers to hybridization. Occasional hybridization may therefore lead to distinct yet reproductively connected lineages. We investigate the balance between introgression and reproductive isolation in a diverse clade using a densely sampled phylogenomic study of fig trees (Ficus, Moraceae). Codiversification with specialized pollinating wasps (Agaonidae) is recognized as a major engine of fig diversity, leading to about 850 species. Nevertheless, some studies have focused on the importance of hybridization inFicus, highlighting the consequences of pollinator sharing. Here, we employ dense taxon sampling (520 species) throughout Moraceae and 1,751 loci to investigate phylogenetic relationships and the prevalence of introgression among species throughout the history ofFicus. We present a well-resolved phylogenomic backbone forFicus, providing a solid foundation for an updated classification. Our results paint a picture of phylogenetically stable evolution within lineages punctuated by occasional local introgression events likely mediated by local pollinator sharing, illustrated by clear cases of cytoplasmic introgression that have been nearly drowned out of the nuclear genome through subsequent lineage fidelity. The phylogenetic history of figs thus highlights that while hybridization is an important process in plant evolution, the mere ability of species to hybridize locally does not necessarily translate into ongoing introgression between distant lineages, particularly in the presence of obligate plant–pollinator relationships.

Funder

Danish Council for Independent Research

National Science Foundation

National Parks Board - Singapore

China Scholarship Council

Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro

Publisher

Proceedings of the National Academy of Sciences

Subject

Multidisciplinary

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