Incomplete lineage sorting and phenotypic evolution in marsupials

Publikation: Bidrag til tidsskriftTidsskriftartikelForskningfagfællebedømt

  • Shaohong Feng
  • Ming Bai
  • Iker Rivas-González
  • Cai Li
  • Shiping Liu
  • Yijie Tong
  • Haidong Yang
  • Guangji Chen
  • Duo Xie
  • Karen E. Sears
  • Lida M. Franco
  • Juan Diego Gaitan-Espitia
  • Roberto F. Nespolo
  • Warren E. Johnson
  • Huanming Yang
  • Parice A. Brandies
  • Carolyn J. Hogg
  • Katherine Belov
  • Marilyn B. Renfree
  • Kristofer M. Helgen
  • Mikkel Heide Schierup

Incomplete lineage sorting (ILS) makes ancestral genetic polymorphisms persist during rapid speciation events, inducing incongruences between gene trees and species trees. ILS has complicated phylogenetic inference in many lineages, including hominids. However, we lack empirical evidence that ILS leads to incongruent phenotypic variation. Here, we performed phylogenomic analyses to show that the South American monito del monte is the sister lineage of all Australian marsupials, although over 31% of its genome is closer to the Diprotodontia than to other Australian groups due to ILS during ancient radiation. Pervasive conflicting phylogenetic signals across the whole genome are consistent with some of the morphological variation among extant marsupials. We detected hundreds of genes that experienced stochastic fixation during ILS, encoding the same amino acids in non-sister species. Using functional experiments, we confirm how ILS may have directly contributed to hemiplasy in morphological traits that were established during rapid marsupial speciation ca. 60 mya.

OriginalsprogEngelsk
TidsskriftCell
Vol/bind185
Udgave nummer10
Sider (fra-til)1646-1660.e18
ISSN0092-8674
DOI
StatusUdgivet - 2022

Bibliografisk note

Funding Information:
We thank Yun Ding (University of Pennsylvania) for helpful discussions of the transgenic experiments in mice. This work was supported by grants from the Strategic Priority Research Program of the Chinese Academy of Sciences ( XDB31020000 ); the International Partnership Program of the Chinese Academy of Sciences ( 152453KYSB20170002 ); the Carlsberg Foundation ( CF16-0663 ); the Villum Foundation ( 25900 ) to G.Z.; a National Natural Science Foundation of China grant ( 31901214 ) to S.F.; grants from the National Natural Science Foundation of China ( 31961143002 ), Bureau of International Cooperation, Chinese Academy of Sciences , the First-class discipline of Prataculture Science of Ningxia University ( NXYLXK2017A01 ), Hainan Yazhou Bay Seed Lab ( B21HJ0102 ), and Guizhou Science and Technology Planning Project (General support-2022-173 ) to M.B.; GDAS Special Project of Science and Technology Development ( 2020GDASYL-20200301003 ) to H.Y.; a NIH grant ( OD022988 ) to K.E.S.; a FONDECYT grant ( 1180917 ) to R.F.N.; and a grant from the Novo Nordisk Foundation ( NNF18OC0031004 ) to M.H.S. We thank the Beijing Synchrotron Radiation Facility (BSRF) and Shanghai Synchrotron Radiation Facility (SSRF) for beam time, staff 4W1A and 4W1B of the BSRF, and staff BL13W1 of the SSRF for analytical assistance. Parts of this manuscript were prepared while Warren E. Johnson held a National Research Council Research Associateship Award at the Walter Reed Army Institute of Research (WRAIR). The material has been reviewed by WRAIR and there is no objection to its presentation and/or publication. The opinions and assertions contained herein are the private views of the authors and are not to be construed as official or as reflecting true views of the Department of the Army or the Department of Defense. We thank Associate Professor Stephen Johnston (University of Queensland), the Queensland Museum, and the Australian Museum for making photographs of marsupial skeletal material available.

Funding Information:
We thank Yun Ding (University of Pennsylvania) for helpful discussions of the transgenic experiments in mice. This work was supported by grants from the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB31020000); the International Partnership Program of the Chinese Academy of Sciences (152453KYSB20170002); the Carlsberg Foundation (CF16-0663); the Villum Foundation (25900) to G.Z.; a National Natural Science Foundation of China grant (31901214) to S.F.; grants from the National Natural Science Foundation of China (31961143002), Bureau of International Cooperation, Chinese Academy of Sciences, the First-class discipline of Prataculture Science of Ningxia University (NXYLXK2017A01), Hainan Yazhou Bay Seed Lab (B21HJ0102), and Guizhou Science and Technology Planning Project (General support-2022-173) to M.B.; GDAS Special Project of Science and Technology Development (2020GDASYL-20200301003) to H.Y.; a NIH grant (OD022988) to K.E.S.; a FONDECYT grant (1180917) to R.F.N.; and a grant from the Novo Nordisk Foundation (NNF18OC0031004) to M.H.S. We thank the Beijing Synchrotron Radiation Facility (BSRF) and Shanghai Synchrotron Radiation Facility (SSRF) for beam time, staff 4W1A and 4W1B of the BSRF, and staff BL13W1 of the SSRF for analytical assistance. Parts of this manuscript were prepared while Warren E. Johnson held a National Research Council Research Associateship Award at the Walter Reed Army Institute of Research (WRAIR). The material has been reviewed by WRAIR and there is no objection to its presentation and/or publication. The opinions and assertions contained herein are the private views of the authors and are not to be construed as official or as reflecting true views of the Department of the Army or the Department of Defense. We thank Associate Professor Stephen Johnston (University of Queensland), the Queensland Museum, and the Australian Museum for making photographs of marsupial skeletal material available. Conceptualization, G.Z.; software, S.F. M.B. I.R.-G. Y.T. and Haidong Yang; formal analysis, S.F. I.R.-G. C.L. G.C. D.X. and M.H.S.; investigation, M.B. C.L. K.E.S. Y.T. and Haidong Yang; resources, L.M.F. R.F.N. J.D.G.-E. K.B. W.E.J. P.A.B. C.J.H. M.B.R. and K.M.H.; data curation, S.F. and G.C.; writing—original draft, S.F. M.B. C.L. and S.L.; writing—review & editing, G.Z. M.H.S. J.J.B. R.F.N. J.D.G.-E. M.B.R. K.M.H. and W.E.J.; visualization, S.F. M.B. Haidong Yang, Y.T. and G.C.; supervision, G.Z. and Huanming Yang; funding acquisition, G.Z. The authors declare no competing interests.

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© 2022 Elsevier Inc.

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