Chromosome-length genome assemblies and cytogenomic analyses of pangolins reveal remarkable chromosome counts and plasticity

Authors

• Marlys L. Houck, San Diego Zoo Wildlife Alliance
• Klaus-Peter Koepfli, George Mason University; Smithsonian’s National Zoo and Conservation Biology Institute; ITMO University
• Taylor Hains, University of Chicago
• Ruqayya Khan, Baylor College of Medicine
• Suellen J. Charter, San Diego Zoo Wildlife Alliance
• Julie A. Fronczek, San Diego Zoo Wildlife Alliance
• Ann C. Misuraca, San Diego Zoo Wildlife Alliance
• Sergei Kliver, The University of Copenhagen
• Polina L. Perelman, Institute of Molecular and Cellular Biology SB RAS
• Violetta R. Beklemisheva, Institute of Molecular and Cellular Biology SB RAS
• Alexander Graphodatsky, Institute of Molecular and Cellular Biology SB RAS
• Shu-Jin Luo, Peking University
• Stephen J. O’Brien, ITMO University; Nova Southeastern UniversityFollow
• Norman T.-L. Lim, Nanyang Technological University
• Jason S. C. Chin, Taipei Zoo
• Vanessa Guerra, Simon Fraser University; Smithsonian Institution
• Gaik Tamazian, Peter the Great Saint Petersburg Polytechnic University
• Arina Omer, Baylor College of Medicine
• David Weisz, Baylor College of Medicine
• Kenneth Kaemmerer, Pittsburgh Zoo & Aquarium
• Ginger Sturgeon, Pittsburgh Zoo & Aquarium
• Joseph Gaspard, Pittsburgh Zoo & Aquarium
• Alicia Hahn, Pittsburgh Zoo & Aquarium
• Mark McDonough, Pittsburgh Zoo & Aquarium
• Isabel Garcia-Treviño, San Antonio Zoo
• Jordan Gentry, San Antonio Zoo
• Rob L. Coke, San Antonio Zoo
• Jan E. Janecka, Duquesne University
• Ryan J. Harrigan, University of California
• Jen Tinsman, University of California
• Thomas B. Smith, University of California
• Erez Lieberman Aiden, Baylor College of Medicine; Rice University; Broad Institute of Harvard and Massachusetts Institute of Technology (MIT)
• Olga Dudchenko, Baylor College of Medicine; Rice University

Document Type

Article

Publication Title

Chromosome Research

ISSN

1573-6849

Publication Date

4-12-2023

Keywords

chromosome number, karyotype, Pholidota, Phataginus tricuspis, genome assembly

Abstract

We report the first chromosome-length genome assemblies for three species in the mammalian order Pholidota: the white-bellied, Chinese, and Sunda pangolins. Surprisingly, we observe extraordinary karyotypic plasticity within this order and, in female white-bellied pangolins, the largest number of chromosomes reported in a Laurasiatherian mammal: 2n = 114. We perform the first karyotype analysis of an African pangolin and report a Y-autosome fusion in white-bellied pangolins, resulting in 2n = 113 for males. We employ a novel strategy to confirm the fusion and identify the autosome involved by finding the pseudoautosomal region (PAR) in the female genome assembly and analyzing the 3D contact frequency between PAR sequences and the rest of the genome in male and female white-bellied pangolins. Analyses of genetic variability show that white-bellied pangolins have intermediate levels of genome-wide heterozygosity relative to Chinese and Sunda pangolins, consistent with two moderate declines of historical effective population size. Our results reveal a remarkable feature of pangolin genome biology and highlight the need for further studies of these unique and endangered mammals.

DOI

10.1007/s10577-023-09722-y

Issue

13

Comments

Work was supported by grants from the National Geographic Society (NGS-418C-18) and US Gov. INLEC (S-INLEC-17-GR-1006). E.L.A. was supported by the Welch Foundation (Q-1866), a McNair Medical Institute Scholar Award, an NIH Encyclopedia of DNA Elements Mapping Center Award (UM1HG009375), a US-Israel Binational Science Foundation Award (2019276), the Behavioral Plasticity Research Institute (NSF DBI-2021795), an NSF Physics Frontiers Center Award (NSF PHY-2019745), and an NIH CEGS (RM1HG011016-01A1). A.S. Graphodatsky, P.L. Perelman, and V.R. Beklemisheva were supported by the Russian Science Foundation (Grant No. 19–14-00034p to A.S.G.). G. Tamazian was supported by Peter the Great St. Petersburg Polytechnic University in the framework of the Russian Federation’s Priority 2030 Strategic Academic Leadership Programme (Agreement 075–15-2021–1333).

Ethical approval The blood sample from the white-bellied pangolin, Jaziri, was collected opportunistically in April 2019 during a routine veterinary examination by the veterinary staf at the Pittsburgh Zoo & Aquarium, following all required and standard animal handling protocols and with approval by the Pittsburgh Zoo & Aquarium institutional animal care and use committee.

© The Author(s), under exclusive licence to Springer Nature B.V. 2023

NSUWorks Citation

Houck, Marlys L.; Klaus-Peter Koepfli; Taylor Hains; Ruqayya Khan; Suellen J. Charter; Julie A. Fronczek; Ann C. Misuraca; Sergei Kliver; Polina L. Perelman; Violetta R. Beklemisheva; Alexander Graphodatsky; Shu-Jin Luo; Stephen J. O’Brien; Norman T.-L. Lim; Jason S. C. Chin; Vanessa Guerra; Gaik Tamazian; Arina Omer; David Weisz; Kenneth Kaemmerer; Ginger Sturgeon; Joseph Gaspard; Alicia Hahn; Mark McDonough; Isabel Garcia-Treviño; Jordan Gentry; Rob L. Coke; Jan E. Janecka; Ryan J. Harrigan; Jen Tinsman; Thomas B. Smith; Erez Lieberman Aiden; and Olga Dudchenko. 2023. "Chromosome-length genome assemblies and cytogenomic analyses of pangolins reveal remarkable chromosome counts and plasticity." Chromosome Research , (13). doi:10.1007/s10577-023-09722-y.