Skip to main content
SpringerLink
Log in

Reconstruction of Ancestral Genomes as a Key to Understanding the Early Evolution of Vertebrate Genotype

  • REVIEWS
  • Published:
Russian Journal of Developmental Biology Aims and scope Submit manuscript

Abstract

The hypothesis about whole-genome duplications as the most important driver of transformation of the structure plan and lifestyle of vertebrates at the early stages of their evolution is generally accepted today. At the same time, details such as the timing and mechanisms of these duplications still remain controversial. Research into issues of periodization, number, and in which evolutionary lineages rounds of whole-genome and/or local duplications occurred in vertebrates continues as methodology and technical capabilities develop. The role of high-throughput genomic sequencing and big data analysis is increasing, which makes it possible to identify and track the history of not only individual genes or their families but of large sections of the genome, including at the chromosomal level. New opportunities allow for considering the problem at the macro level and conduct a comparative analysis of the genomic characteristics of representatives of different evolutionary groups. In this article, which is a logical continuation of an earlier review article (in 2020), the authors make an attempt to review and summarize the data of recent years, largely related to the sequencing of genomes of representatives of evolutionarily ancient (basal) groups of vertebrates and to understand the contribution of this new information to our ideas about the early evolutionary history of the vertebrate genotype. According to new data, the divergence and observed significant differences in the morphological plans of the two evolutionary lineages of vertebrates could be ensured by different scenarios of polyploidization of their genomes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.

REFERENCES

  1. Aase-Remedios, M.E. and Ferrier, D.E.K., Improved understanding of the role of gene and genome duplications in chordate evolution with new genome and transcriptome sequences, Front. Ecol. Evol., 2021, vol. 9, p. 703163. https://doi.org/10.3389/fevo.2021.703163

    Article  Google Scholar 

  2. Bayramov, A.V., Ermakova, G.V., Kuchryavyy, A.V., et al., Genome duplications as the basis of vertebrates’ evolutionary success, Russ. J. Dev. Biol., 2021, vol. 52, pp. 141–163. https://doi.org/10.1134/S1062360421030024

    Article  Google Scholar 

  3. Bi, X., Wang, K., Yang, L., et al., Tracing the genetic footprints of vertebrate landing in non-teleost ray-finned fishes, Cell, 2021, vol. 184, no. 5, pp. 1377–1391. e14. https://doi.org/10.1016/j.cell.2021.01.046

  4. Braasch, I. and Schartl, M., Evolution of endothelin receptors in vertebrates, Gen. Comp. Endocrinol., 2014, vol. 209, pp. 21–34. https://doi.org/10.1016/j.ygcen.2014.06.028

    Article  CAS  PubMed  Google Scholar 

  5. Cardoso, J.C.R., Bergqvist, C.A., Felix, R.C., et al., Corticotropin-releasing hormone family evolution: five ancestral genes remain in some lineages, J. Mol. Endocrinol., 2016, vol. 57, pp. 73–86.

    Article  CAS  PubMed  Google Scholar 

  6. Chen, Z., Omori, Y., Koren, S., et al., Comparative Sequencing Program, Mullikin, J.C., and Burgess, S.M., De novo assembly of the goldfish (Carassius auratus) genome and the evolution of genes after whole-genome duplication, Sci. Adv., 2019, vol. 5, no. 6, p. eaav0547. https://doi.org/10.1126/sciadv.aav0547

  7. Cheng, P., Huang, Y., Lv, Y., et al., The American paddlefish genome provides novel insights into chromosomal evolution and bone mineralization in early vertebrates, Mol. Biol. Evol., 2021, vol. 38, no. 4, pp. 1595–1607. https://doi.org/10.1093/molbev/msaa326

    Article  CAS  PubMed  Google Scholar 

  8. David, K.T., Global gradients in the distribution of animal polyploids, Proc. Natl. Acad. Sci. U. S. A., 2022, vol. 119, no. 48, p. e2214070119. https://doi.org/10.1073/pnas.2214070119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Delsuc, F., Brinkmann, H., Chourrout, D., et al., Tunicates and not cephalochordates are the closest living relatives of vertebrates, Nature, 2006, vol. 439, no. 7079, pp. 965–968. https://doi.org/10.1038/nature04336

    Article  CAS  PubMed  Google Scholar 

  10. Du, K., Stöck, M., Kneitz, S., et al., The sterlet sturgeon genome sequence and the mechanisms of segmental rediploidization, Nat. Ecol. Evol., 2020, vol. 4, no. 6, pp. 841–852. https://doi.org/10.1038/s41559-020-1166-x

    Article  PubMed  PubMed Central  Google Scholar 

  11. Ermakova, G.V., Kucheryavyy, A.V., Zaraisky, A.G., et al., Discovery of four noggin genes in lampreys suggests two rounds of ancient genome duplication, Commun. Biol., 2020, vol. 3, no. 1, p. 532. https://doi.org/10.1038/s42003-020-01234-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Fontana, F., Congiu, L., Mudrak, V.A., et al., Evidence of hexaploid karyotype in shortnose sturgeon, Genome, 2008, vol. 51, no. 2, pp. 113–119. https://doi.org/10.1139/g07-112

    Article  CAS  PubMed  Google Scholar 

  13. Hess, J.E., Smith, J.J., Timoshevskaya, N., et al., Genomic islands of divergence infer a phenotypic landscape in pacific lamprey, Mol. Ecol., 2020, vol. 29, pp. 3841–3856. https://doi.org/10.1111/mec.15605

    Article  PubMed  Google Scholar 

  14. Huang, Z., Xu, L., Cai, C., et al., Three amphioxus reference genomes reveal gene and chromosome evolution of chordates, Proc. Natl. Acad. Sci. U. S. A., 2023, vol. 120, no. 10, p. e2201504120. https://doi.org/10.1073/pnas.2201504120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Ikuta, T. and Saiga, H., Organization of Hox genes in ascidians: present, past, and future, Dev. Dyn., 2005, vol. 233, no. 2, pp. 382–389. https://doi.org/10.1002/dvdy.20374

    Article  CAS  PubMed  Google Scholar 

  16. Janvier, P., The phylogeny of the Craniata, with particular reference to the significance of fossil “agnathans,” J. Vertebr. Paleontol., 1981, vol. 1, no. 2, p. 121–159. http://www.jstor.org/stable/4522845

    Article  Google Scholar 

  17. Kuraku, S. and Kuratani, S., Time scale for cyclostome evolution inferred with a phylogenetic diagnosis of hagfish and lamprey cDNA sequences, Zool. Sci., 2006, vol. 23, pp. 1053–1064.

    Article  CAS  Google Scholar 

  18. Lakiza, O., Miller, S., Bunce, A., et al., SoxE gene duplication and development of the lamprey branchial skeleton: Insights into development and evolution of the neural crest, Dev. Biol., 2011, vol. 359, no. 1, pp. 149–161. https://doi.org/10.1016/j.ydbio.2011.08.012

    Article  CAS  PubMed  Google Scholar 

  19. Li, J.T., Wang, Q., Huang Yang, M.D., et al., Parallel subgenome structure and divergent expression evolution of allo-tetraploid common carp and goldfish, Nat. Genet., 2021, vol. 53, no. 10, pp. 1493–1503. https://doi.org/10.1038/s41588-021-00933-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Mallik, R., Carlson, K.B., Wcisel, D.J., et al., A chromosome-level genome assembly of longnose gar, Lepisosteus osseus, G3 (Bethesda), 2023, vol. 13, no. 7, p. jkad095. https://doi.org/10.1093/g3journal/jkad095

  21. Marlétaz, F., Timoshevskaya, N., Timoshevskiy, V., et al., The hagfish genome and the evolution of vertebrates, bioRxiv, 2023a, vol. 18, p. 2023.04.17.537254. https://doi.org/10.1101/2023.04.17.537254

  22. Marlétaz, F., de la Calle-Mustienes, E., Acemel, R.D., et al., The little skate genome and the evolutionary emergence of wing-like fins, Nature, 2023b, vol. 616, no. 7957, pp. 495–503. https://doi.org/10.1038/s41586-023-05868-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Marra, N.J., Stanhope, M.J., Jue, N.K., et al., White shark genome reveals ancient elasmobranch adaptations associated with wound healing and the maintenance of genome stability, Proc. Natl. Acad. Sci. U. S. A., 2019, vol. 116, no. 10, pp. 4446–4455. https://doi.org/10.1073/pnas.1819778116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Mehta, T.K., Ravi, V., Yamasaki, S., et al., Evidence for at least six Hox clusters in the Japanese lamprey (Lethenteron japonicum), Proc. Natl. Acad. Sci. U. S. A., 2013, vol. 110, no. 40, pp. 16044–16049. https://doi.org/10.1073/pnas.1315760110

    Article  PubMed  PubMed Central  Google Scholar 

  25. Meulemans, D. and Bronner-Fraser, M., Insights from amphioxus into the evolution of vertebrate cartilage, PLoS One, 2007, vol. 2, no. 8, p. e787. https://doi.org/10.1371/journal.pone.0000787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Miyashita, T., Coates, M.I., Farrar, R., et al., Hagfish from the Cretaceous Tethys Sea and a reconciliation of the morphological-molecular conflict in early vertebrate phylogeny, Proc. Natl. Acad. Sci. U. S. A., 2019, vol. 116, no. 6, p. 2146–2151. https://doi.org/10.1073/pnas.1814794116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Nakatani, Y. and McLysaght, A., Genomes as documents of evolutionary history: a probabilistic macrosynteny model for the reconstruction of ancestral genomes, Bioinformatics, 2017, vol. 33, no. 14, pp. i369–i378. https://doi.org/10.1093/bioinformatics/btx259

  28. Nakatani, Y., Shingate, P., Ravi, V., et al., Reconstruction of proto-vertebrate, protocyclostome and proto-gnathostome genomes provides new insights into early vertebrate evolution, Nat. Commun., 2021, vol. 12, p. 4489. https://doi.org/10.1038/s41467-021-24573-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Nishimura, O., Yamaguchi, K., Hara, Y., et al., Inference of a genome-wide protein-coding gene set of the inshore hagfish Eptatretus burger, F1000Research, 2022a, vol. 11, p. 1270. https://doi.org/10.12688/f1000research.124719

    Article  CAS  Google Scholar 

  30. Nishimura, O., Rozewicki, J., Yamaguchi, K., et al., Squalomix: shark and ray genome analysis consortium and its data sharing platform, F1000Research, 2022b, vol. 11, p. 1077. https://doi.org/10.12688/f1000research.123591.1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Ota, K., Fujimoto, S., Oisi, Y., et al., Identification of vertebra-like elements and their possible differentiation from sclerotomes in the hagfish, Nat. Commun., 2011, vol. 2, p. 373. https://doi.org/10.1038/ncomms1355

    Article  CAS  PubMed  Google Scholar 

  32. Parker, H.J., Bronner, M.E., and Krumlauf, R., An atlas of anterior Hox gene expression in the embryonic sea lamprey head: Hox-code evolution in vertebrates, Dev. Biol., 2019, vol. 453, no. 1, pp. 19–33. https://doi.org/10.1016/j.ydbio.2019.05.001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Putnam, N.H., Butts, T., Ferrier, D.E., et al., The amphioxus genome and the evolution of the chordate karyotype, Nature, 2008, vol. 453, pp. 1064–1071. https://doi.org/10.1038/nature06967

    Article  CAS  PubMed  Google Scholar 

  34. Ray, L. and Medeiros, D., Linking vertebrate gene duplications to the new head hypothesis, Biology, 2023, vol. 12, no. 9, p. 1213. https://doi.org/10.3390/biology12091213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Redmond, A.K., Casey, D., Gundappa, M.K., et al., Independent rediploidization masks shared whole genome duplication in the sturgeon-paddlefish ancestor, Nat. Commun., 2023, vol. 14, p. 2879. https://doi.org/10.1038/s41467-023-38714-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Robertson, F.M., Gundappa, M.K., Grammes, F., et al., Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification, Genome Biol., 2017, vol. 18, no. 1, p. 111. https://doi.org/10.1186/s13059-017-1241-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Rothstein, M., Bhattacharya, D., and Simoes-Costa, M., The molecular basis of neural crest axial identity, Dev. Biol., 2018, vol. 444, suppl. 1, pp. S170–S180. https://doi.org/10.1016/j.ydbio.2018.07.026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Sacerdot, C., Louis, A., Bon, C., et al., Chromosome evolution at the origin of the ancestral vertebrate genome, Genome Biol., 2018, vol. 19, no. 1, p. 166. https://doi.org/10.1186/s13059-018-1559-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Session, A.M., Uno, Y., Kwon, T., et al., Genome evolution in the allotetraploid frog Xenopus laevis, Nature, 2016, vol. 538, no. 7625, pp. 336–343. https://doi.org/10.1038/nature19840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Shimeld, S.M. and Donoghue, P.C.J., Evolutionary crossroads in developmental biology: cyclostomes (lamprey and hagfish), Development, 2012, vol. 139, pp. 2091–2099. https://doi.org/10.1242/dev.074716

    Article  CAS  PubMed  Google Scholar 

  41. Simakov, O., Marlétaz, F., Yue, J.X., et al., Deeply conserved synteny resolves early events in vertebrate evolution, Nat. Ecol. Evol., 2020, vol. 4, no. 6, pp. 820–830. https://doi.org/10.1038/s41559-020-1156-z

    Article  PubMed  PubMed Central  Google Scholar 

  42. Smith, J.J., Kuraku, S., Holt, C., et al., Sequencing of the sea lamprey (Petromyzon marinus) genome provides insights into vertebrate evolution, Nat. Genet., 2013, vol. 45, pp. 415–421. https://doi.org/10.1038/ng.2568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Smith, J.J., Timoshevskaya, N., Ye, C., et al., The sea lamprey germline genome provides insights into programmed genome rearrangement and vertebrate evolution, Nat. Genet., 2018, vol. 50, pp. 270–277. https://doi.org/10.1038/s41588-017-0036-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Song, X., Tang, Y., and Wang, Y., Genesis of the vertebrate FoxP subfamily member genes occurred during two ancestral whole genome duplication events, Gene, 2016, vol. 588, no. 2, pp. 156–162. https://doi.org/10.1016/j.gene.2016.05.019

    Article  CAS  PubMed  Google Scholar 

  45. Soshnikova, N., Dewaele, R., Janvier, P., et al., Duplications of hox gene clusters and the emergence of vertebrates, Dev. Biol., 2013, vol. 378, no. 2, pp. 194–199. https://doi.org/10.1016/j.ydbio.2013.03.004

    Article  CAS  PubMed  Google Scholar 

  46. Square, T.A., Jandzik, D., Massey, J.L., et al., Evolution of the endothelin pathway drove neural crest cell diversification, Nature, 2020, vol. 585, pp. 563–568. https://doi.org/10.1038/s41586-020-2720-z

    Article  CAS  PubMed  Google Scholar 

  47. Tai, A., Cheung, M., Huang, Y.H., et al., SOXE neofunctionalization and elaboration of the neural crest during chordate evolution, Sci. Rep., 2016, vol. 6, p. 34964. https://doi.org/10.1038/srep34964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Thompson, A.W., Hawkins, M.B., Parey, E., et al., The bowfin genome illuminates the developmental evolution of ray-finned fishes, Nat. Genet., 2021, vol. 53, no. 9, pp. 1373–1384. https://doi.org/10.1038/s41588-021-00914-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Timoshevskaya, N., Eşkut, K.I., Timoshevskiy, V.A., et al., An improved germline genome assembly for the sea lamprey Petromyzon marinus illuminates the evolution of germline-specific chromosomes, Cell Rep., 2023, vol. 42, no. 3, p. 112263. https://doi.org/10.1016/j.celrep.2023.112263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Timoshevskiy, V.A., Timoshevskaya, N.Y., and Smith, J.J., Germline-specific repetitive elements in programmatically eliminated chromosomes of the sea lamprey (Petromyzon marinus), Genes, 2019, vol. 10, p. 832. https://doi.org/10.3390/genes10100832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Wertheim, B., Beukeboom, L.W., and van de Zande, L., Polyploidy in animals: effects of gene expression on sex determination, evolution and ecology, Cytogenet. Genome Res., 2013, vol. 140, nos. 2–4, pp. 256–269. https://doi.org/10.1159/000351998

    Article  CAS  PubMed  Google Scholar 

  52. Yamaguchi, K., Uno, Y., Kadota, M., et al., Elasmobranch genome sequencing reveals evolutionary trends of vertebrate karyotypic organization, Genome Res., 2023, p. gr.276840.122. https://doi.org/10.1101/gr.276840.122

  53. Yu, D., Ren, Y., Uesaka, M., et al., Hagfish genome illuminates vertebrate whole genome duplications and their evolutionary consequences, bioRxiv, 2023. https://doi.org/10.1101/2023.04.08.536076

  54. Zhu, T., Li, Y., Pang, Y., et al., Chromosome-level genome assembly of Lethenteron reissneri provides insights into lamprey evolution, Mol. Ecol. Resour., 2021, vol. 21, pp. 448–463. https://doi.org/10.1111/1755-0998.13279

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

The research was carried out and the publication was prepared with the financial support of the Russian Science Foundation, grant no. 23-74-30005.

Author information

Authors and Affiliations

  1. Shemyakin–Ovchinnikova Institute of Bioorganic Chemistry, Russian Academy of Sciences, 117997, Moscow, Russia

    A. V. Bayramov, G. V. Ermakova & A. G. Zaraisky

Authors
  1. A. V. Bayramov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. V. Ermakova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. G. Zaraisky
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. V. Bayramov.

Ethics declarations

CONFLICT OF INTEREST

The authors of this work declare that they have no conflicts of interest.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

This work does not contain any studies involving human and animal subjects.

Additional information

Publisher’s Note.

Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bayramov, A.V., Ermakova, G.V. & Zaraisky, A.G. Reconstruction of Ancestral Genomes as a Key to Understanding the Early Evolution of Vertebrate Genotype. Russ J Dev Biol 54 (Suppl 1), S1–S9 (2023). https://doi.org/10.1134/S1062360423070020

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062360423070020

Keywords:

Search

Navigation