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

Marlys L Houck; Klaus-Peter Koepfli; Taylor Hains; Ruqayya Khan; Suellen J Charter; Julie A Fronczek; Ann C Misuraca; Sergei Kliver; Polina L Perelman; Violetta 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; Olga Dudchenko

doi:10.1007/s10577-023-09722-y

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

Chromosome Res. 2023 Apr 12;31(2):13. doi: 10.1007/s10577-023-09722-y.

Authors

Marlys L Houck¹, Klaus-Peter Koepfli^{2

3

4}, Taylor Hains⁵, Ruqayya Khan⁶, Suellen J Charter⁷, Julie A Fronczek⁷, Ann C Misuraca⁷, Sergei Kliver⁸, Polina L Perelman⁹, Violetta Beklemisheva⁹, Alexander Graphodatsky⁹, Shu-Jin Luo¹⁰, Stephen J O'Brien^{11

12}, Norman T-L Lim¹³, Jason S C Chin¹⁴, Vanessa Guerra^{15

16}, Gaik Tamazian¹⁷, Arina Omer⁶, David Weisz⁶, Kenneth Kaemmerer¹⁸, Ginger Sturgeon¹⁸, Joseph Gaspard¹⁸, Alicia Hahn¹⁸, Mark McDonough¹⁸, Isabel Garcia-Treviño¹⁹, Jordan Gentry¹⁹, Rob L Coke¹⁹, Jan E Janecka²⁰, Ryan J Harrigan²¹, Jen Tinsman²¹, Thomas B Smith^{21

22}, Erez Lieberman Aiden^{6

23

24

25}, Olga Dudchenko^{26

27}

Affiliations

¹ Conservation Science and Wildlife Health, San Diego Zoo Wildlife Alliance, Escondido, CA, 92027, USA. mhouck@sdzwa.org.
² Smithsonian-Mason School of Conservation, George Mason University, Front Royal, VA, 22630, USA. kkoepfli@gmu.edu.
³ Center for Species Survival, Smithsonian's National Zoo and Conservation Biology Institute, Front Royal, VA, 22630, USA. kkoepfli@gmu.edu.
⁴ Computer Technologies Laboratory, ITMO University, 197101, St. Petersburg, Russia. kkoepfli@gmu.edu.
⁵ Committee On Evolutionary Biology, University of Chicago, Chicago, IL, 60637, USA.
⁶ The Center for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA.
⁷ Conservation Science and Wildlife Health, San Diego Zoo Wildlife Alliance, Escondido, CA, 92027, USA.
⁸ Center for Evolutionary Hologenomics, The Globe Institute, The University of Copenhagen, 5A, Oester Farimagsgade, 1353, Copenhagen, Denmark.
⁹ Department of the Diversity and Evolution of Genomes, Institute of Molecular and Cellular Biology SB RAS, 630090, Novosibirsk, Russia.
¹⁰ The State Key Laboratory of Protein and Plant Gene Research, Peking-Tsinghua Center for Life Sciences (CLS), School of Life Sciences, Peking University, Beijing, 100871, China.
¹¹ Laboratory of Genomic Diversity, Computer Technologies Laboratory, ITMO University, 197101, St. Petersburg, Russia.
¹² Guy Harvey Oceanographic Center, Halmos College of Arts and Sciences, Nova Southeastern University, Fort Lauderdale, FL, 33004, USA.
¹³ Natural Sciences and Science Education, National Institute of Education, Nanyang Technological University, Singapore, 637616, Singapore.
¹⁴ Taipei Zoo, No. 30 Sec. 2 Xinguang Rd., Taipei, 11656, Taiwan.
¹⁵ Department of Biological Sciences, Simon Fraser University, Burnaby, BC, Canada.
¹⁶ Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA.
¹⁷ Centre for Computational Biology, Peter the Great Saint Petersburg Polytechnic University, St. Petersburg, 195251, Russia.
¹⁸ Pittsburgh Zoo & Aquarium, PA, 15206, Pittsburgh, USA.
¹⁹ Center for Conservation and Research, San Antonio Zoo, San Antonio, TX, 78212, USA.
²⁰ Department of Biological Sciences, Bayer School of Natural and Environmental Sciences, Duquesne University, Pittsburgh, PA, 15282, USA.
²¹ Center for Tropical Research, Institute of the Environment and Sustainability, University of California, Los Angeles, CA, 90095, USA.
²² Department of Ecology and Evolutionary Biology, University of California, Los Angeles, CA, 90095, USA.
²³ Departments of Computer Science and Computational and Applied Mathematics, Rice University, Houston, TX, 77030, USA.
²⁴ Center for Theoretical and Biological Physics, Rice University, Houston, TX, 77030, USA.
²⁵ Broad Institute of Harvard and Massachusetts Institute of Technology (MIT), Cambridge, MA, 02139, USA.
²⁶ The Center for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX, 77030, USA. Olga.Dudchenko@bcm.edu.
²⁷ Center for Theoretical and Biological Physics, Rice University, Houston, TX, 77030, USA. Olga.Dudchenko@bcm.edu.

PMID: 37043058
DOI: 10.1007/s10577-023-09722-y

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.

Keywords: Phataginus tricuspis; Pholidota; chromosome number; genome assembly; karyotype.

Publication types

Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural

MeSH terms

Animals
Chromosomes / genetics
Female
Genome
Male
Mammals* / genetics
Pangolins* / genetics

Abstract

Publication types

MeSH terms

Grants and funding