IDEAS home Printed from https://ideas.repec.org/a/plo/pgen00/1003125.html
   My bibliography  Save this article

A New Isolation with Migration Model along Complete Genomes Infers Very Different Divergence Processes among Closely Related Great Ape Species

Author

Listed:
  • Thomas Mailund
  • Anders E Halager
  • Michael Westergaard
  • Julien Y Dutheil
  • Kasper Munch
  • Lars N Andersen
  • Gerton Lunter
  • Kay Prüfer
  • Aylwyn Scally
  • Asger Hobolth
  • Mikkel H Schierup

Abstract

We present a hidden Markov model (HMM) for inferring gradual isolation between two populations during speciation, modelled as a time interval with restricted gene flow. The HMM describes the history of adjacent nucleotides in two genomic sequences, such that the nucleotides can be separated by recombination, can migrate between populations, or can coalesce at variable time points, all dependent on the parameters of the model, which are the effective population sizes, splitting times, recombination rate, and migration rate. We show by extensive simulations that the HMM can accurately infer all parameters except the recombination rate, which is biased downwards. Inference is robust to variation in the mutation rate and the recombination rate over the sequence and also robust to unknown phase of genomes unless they are very closely related. We provide a test for whether divergence is gradual or instantaneous, and we apply the model to three key divergence processes in great apes: (a) the bonobo and common chimpanzee, (b) the eastern and western gorilla, and (c) the Sumatran and Bornean orang-utan. We find that the bonobo and chimpanzee appear to have undergone a clear split, whereas the divergence processes of the gorilla and orang-utan species occurred over several hundred thousands years with gene flow stopping quite recently. We also apply the model to the Homo/Pan speciation event and find that the most likely scenario involves an extended period of gene flow during speciation. Author Summary: Next-generation sequencing technology has enabled the generation of whole-genome data for many closely related species. For population genetic inference we have sequenced many loci, but only in a few individuals. We present a new method that allows inference of the divergence process based on two closely related genomes, modelled as gradual isolation in an isolation with migration model. This allows estimation of the initial time of restricted gene flow, the cessation of gene flow, as well as the population sizes, migration rates, and recombination rates. We show by simulations that the parameter estimation is accurate with genome-wide data and use the model to disentangle the divergence processes among three sets of closely related great ape species: bonobo/chimpanzee, eastern/western gorillas, and Sumatran/Bornean orang-utans. We find allopatric speciation for bonobo and chimpanzee and non-allopatric speciation for the gorillas and orang-utans. We also consider the split between humans and chimpanzees/bonobos and find evidence for non-allopatric speciation, similar to that within gorillas and orang-utans.

Suggested Citation

  • Thomas Mailund & Anders E Halager & Michael Westergaard & Julien Y Dutheil & Kasper Munch & Lars N Andersen & Gerton Lunter & Kay Prüfer & Aylwyn Scally & Asger Hobolth & Mikkel H Schierup, 2012. "A New Isolation with Migration Model along Complete Genomes Infers Very Different Divergence Processes among Closely Related Great Ape Species," PLOS Genetics, Public Library of Science, vol. 8(12), pages 1-19, December.
  • Handle: RePEc:plo:pgen00:1003125
    DOI: 10.1371/journal.pgen.1003125
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1003125
    Download Restriction: no

    File URL: https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1003125&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pgen.1003125?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Heng Li & Richard Durbin, 2011. "Inference of human population history from individual whole-genome sequences," Nature, Nature, vol. 475(7357), pages 493-496, July.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Kevin J Liu & Jingxuan Dai & Kathy Truong & Ying Song & Michael H Kohn & Luay Nakhleh, 2014. "An HMM-Based Comparative Genomic Framework for Detecting Introgression in Eukaryotes," PLOS Computational Biology, Public Library of Science, vol. 10(6), pages 1-13, June.
    2. Costa, Rui J. & Wilkinson-Herbots, Hilde M., 2021. "Inference of gene flow in the process of speciation: Efficient maximum-likelihood implementation of a generalised isolation-with-migration model," Theoretical Population Biology, Elsevier, vol. 140(C), pages 1-15.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Ya-Mei Ding & Xiao-Xu Pang & Yu Cao & Wei-Ping Zhang & Susanne S. Renner & Da-Yong Zhang & Wei-Ning Bai, 2023. "Genome structure-based Juglandaceae phylogenies contradict alignment-based phylogenies and substitution rates vary with DNA repair genes," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    2. Romain Fournier & Zoi Tsangalidou & David Reich & Pier Francesco Palamara, 2023. "Haplotype-based inference of recent effective population size in modern and ancient DNA samples," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Guangping Huang & Lingyun Song & Xin Du & Xin Huang & Fuwen Wei, 2023. "Evolutionary genomics of camouflage innovation in the orchid mantis," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    4. Legried, Brandon & Terhorst, Jonathan, 2022. "Rates of convergence in the two-island and isolation-with-migration models," Theoretical Population Biology, Elsevier, vol. 147(C), pages 16-27.
    5. Jörn Bethune & April Kleppe & Søren Besenbacher, 2022. "A method to build extended sequence context models of point mutations and indels," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    6. Carmi, Shai & Wilton, Peter R. & Wakeley, John & Pe’er, Itsik, 2014. "A renewal theory approach to IBD sharing," Theoretical Population Biology, Elsevier, vol. 97(C), pages 35-48.
    7. Aoki, Kenichi & Wakano, Joe Yuichiro, 2022. "Hominin forager technology, food sharing, and diet breadth," Theoretical Population Biology, Elsevier, vol. 144(C), pages 37-48.
    8. Yupeng Sang & Zhiqin Long & Xuming Dan & Jiajun Feng & Tingting Shi & Changfu Jia & Xinxin Zhang & Qiang Lai & Guanglei Yang & Hongying Zhang & Xiaoting Xu & Huanhuan Liu & Yuanzhong Jiang & Pär K. In, 2022. "Genomic insights into local adaptation and future climate-induced vulnerability of a keystone forest tree in East Asia," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    9. Kimmel, Marek & Wojdyła, Tomasz, 2016. "Genetic demographic networks: Mathematical model and applications," Theoretical Population Biology, Elsevier, vol. 111(C), pages 75-86.
    10. Jason Flannick & Joshua M Korn & Pierre Fontanillas & George B Grant & Eric Banks & Mark A Depristo & David Altshuler, 2012. "Efficiency and Power as a Function of Sequence Coverage, SNP Array Density, and Imputation," PLOS Computational Biology, Public Library of Science, vol. 8(7), pages 1-13, July.
    11. Yee Wen Low & Sitaram Rajaraman & Crystal M. Tomlin & Joffre Ali Ahmad & Wisnu H. Ardi & Kate Armstrong & Parusuraman Athen & Ahmad Berhaman & Ruth E. Bone & Martin Cheek & Nicholas R. W. Cho & Le Min, 2022. "Genomic insights into rapid speciation within the world’s largest tree genus Syzygium," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    12. José Cerca & Bent Petersen & José Miguel Lazaro-Guevara & Angel Rivera-Colón & Siri Birkeland & Joel Vizueta & Siyu Li & Qionghou Li & João Loureiro & Chatchai Kosawang & Patricia Jaramillo Díaz & Gon, 2022. "The genomic basis of the plant island syndrome in Darwin’s giant daisies," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    13. Rong Wang & Chao-Nan Liu & Simon T. Segar & Yu-Ting Jiang & Kai-Jian Zhang & Kai Jiang & Gang Wang & Jing Cai & Lu-Fan Chen & Shan Chen & Jing Cheng & Stephen G. Compton & Jun-Yin Deng & Yuan-Yuan Din, 2024. "Dipterocarpoidae genomics reveal their demography and adaptations to Asian rainforests," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    14. Jerome Kelleher & Alison M Etheridge & Gilean McVean, 2016. "Efficient Coalescent Simulation and Genealogical Analysis for Large Sample Sizes," PLOS Computational Biology, Public Library of Science, vol. 12(5), pages 1-22, May.
    15. Deng, Yun & Song, Yun S. & Nielsen, Rasmus, 2021. "The distribution of waiting distances in ancestral recombination graphs," Theoretical Population Biology, Elsevier, vol. 141(C), pages 34-43.
    16. Ran Tian & Yaolei Zhang & Hui Kang & Fan Zhang & Zhihong Jin & Jiahao Wang & Peijun Zhang & Xuming Zhou & Janet M. Lanyon & Helen L. Sneath & Lucy Woolford & Guangyi Fan & Songhai Li & Inge Seim, 2024. "Sirenian genomes illuminate the evolution of fully aquatic species within the mammalian superorder afrotheria," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    17. Ait Kaci Azzou, S. & Larribe, F. & Froda, S., 2016. "Inferring the demographic history from DNA sequences: An importance sampling approach based on non-homogeneous processes," Theoretical Population Biology, Elsevier, vol. 111(C), pages 16-27.
    18. Gideon S Bradburd & Peter L Ralph & Graham M Coop, 2016. "A Spatial Framework for Understanding Population Structure and Admixture," PLOS Genetics, Public Library of Science, vol. 12(1), pages 1-38, January.
    19. Juraj Bergman & Rasmus Ø. Pedersen & Erick J. Lundgren & Rhys T. Lemoine & Sophie Monsarrat & Elena A. Pearce & Mikkel H. Schierup & Jens-Christian Svenning, 2023. "Worldwide Late Pleistocene and Early Holocene population declines in extant megafauna are associated with Homo sapiens expansion rather than climate change," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    20. Per Unneberg & Mårten Larsson & Anna Olsson & Ola Wallerman & Anna Petri & Ignas Bunikis & Olga Vinnere Pettersson & Chiara Papetti & Astthor Gislason & Henrik Glenner & Joan E. Cartes & Leocadio Blan, 2024. "Ecological genomics in the Northern krill uncovers loci for local adaptation across ocean basins," Nature Communications, Nature, vol. 15(1), pages 1-29, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pgen00:1003125. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plosgenetics (email available below). General contact details of provider: https://journals.plos.org/plosgenetics/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.