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Cross-species chromosome painting in Cetartiodactyla: Reconstructing the karyotype evolution in key phylogenetic lineages

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Abstract

Recent molecular and morphological studies place Artiodactyla and Cetacea into the order Cetartiodactyla. Within the Cetartiodactyla such families as Bovidae, Cervidae, and Suidae are well studied by comparative chromosome painting, but many taxa that are crucial for understanding cetartiodactyl phylogeny remain poorly studied. Here we present the genome-wide comparative maps of five cetartiodactyl species obtained by chromosome painting with human and dromedary paint probes from four taxa: Cetacea, Hippopotamidae, Giraffidae, and Moschidae. This is the first molecular cytogenetic report on pilot whale, hippopotamus, okapi, and Siberian musk deer. Our results, when integrated with previously published comparative chromosome maps allow us to reconstruct the evolutionary pathway and rates of chromosomal rearrangements in Cetartiodactyla. We hypothesize that the putative cetartiodactyl ancestral karyotype (CAK) contained 25–26 pairs of autosomes, 2n = 52–54, and that the association of human chromosomes 8/9 could be a cytogenetic signature that unites non-camelid cetartiodactyls. There are no unambiguous cytogenetic landmarks that unite Hippopotamidae and Cetacea. If we superimpose chromosome rearrangements on the supertree generated by Price and colleagues, several homoplasy events are needed to explain cetartiodactyl karyotype evolution. Our results apparently favour a model of non-random breakpoints in chromosome evolution. Cetariodactyl karyotype evolution is characterized by alternating periods of low and fast rates in various lineages. The highest rates are found in Suina (Suidae+Tayasuidae) lineage (1.76 rearrangements per million years (R/My)) and the lowest in Cetaceans (0.07 R/My). Our study demonstrates that the combined use of human and camel paints is highly informative for revealing evolutionary karyotypic rearrangements among cetartiodactyl species.

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Abbreviations

2n:

diploid number of chromosomes

BAC:

bacterial artificial chromosome

BTA:

Bos taurus

CAK:

cetartiodactyl ancestral karyotype

CDR:

Camelus dromedarius

DOP-PCR:

degenerate oligonucleotide primer–polymerase chain reaction

FISH:

fluorescence in-situ hybridization

GCA:

Giraffa camelopardalis

GME:

Globicephala melas

GTG:

banding G banding by trypsin using Giemsa

HAM:

Hippopotamus amphibius

HSA:

Homo sapiens

MMO:

Moschus moschiferus

Mya:

million years ago

OJO:

Okapia johnstoni

PAUP:

phylogenetic analysis using parsimony

PTA:

Pecari tajacu

R/My:

rearrangements per million years

SSC:

Sus scrofa

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Acknowledgements

This study was funded in part by the research grants of the Russian Fund for Basic Research, programs of the Russian Academy of Science MCB, BOE, and Integration program of the Siberian Branch of the Russian Academy of Science (A.S.G.) and a Wellcome Trust grant to M.A.F.-S.

R.S. was partially supported by a grant ‘Mobility of Italian and foreign researchers residing abroad’ from the Italian Ministry of Universities and Research. F.Y. is supported by the Wellcome Trust. We gratefully acknowledge Stephen O’Brien (Laboratory of Genomic Diversity, NCI-Frederick) for providing cell lines of whale and okapi; Marlys Houck and Oliver A. Ryder (Frozen Zoo of San Diego Zoo’s Conservation Research Center, CA) for providing hippo and giraffe cell lines; and Michael Dean, M. Thompson (NCI-Frederick) for help in providing giraffe samples.

R.S. would like to acknowledge Lutz Froenike for discussion and comments on whale phylogenetics.

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Authors and Affiliations

  1. Institute of Cytology and Genetics, Russian Academy of Sciences, Novosibirsk, 630090, Russia

    Anastasia I. Kulemzina, Vladimir A. Trifonov, Polina L. Perelman, Nadezhda V. Rubtsova & Alexander S. Graphodatsky

  2. National Cancer Institute, Frederick, MD, USA

    Polina L. Perelman

  3. Museum National d’Histoire Naturelle, Origine, Structure et Evolution de la Biodiversite, Paris, France

    Vitaly Volobuev

  4. Department of Veterinary Medicine, Cambridge Resource Centre for Comparative Genomics, Cambridge, UK

    Malcolm A. Ferguson-Smith

  5. Department of Evolutionary Biology, University of Florence, Florence, Italy

    Roscoe Stanyon

  6. The Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, UK

    Fengtang Yang

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  1. Anastasia I. Kulemzina
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  2. Vladimir A. Trifonov
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  7. Roscoe Stanyon
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  8. Fengtang Yang
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  9. Alexander S. Graphodatsky
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Correspondence to Vladimir A. Trifonov.

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Responsible Editor: Herbert Macgregor.

Electronic supplementary material

Below is the image is a link to a high resolution version

Supplementary Fig. S1

FISH examples of localization of some human (HSA) and dromedary (CDR) probes onto studied species (JPG 1.29 MB)

Supplementary Fig. S2

FISH of dromedary (CDR) painting probes onto cow (BTA) and pig (SSC), with additional signals revealed (JPG 571 kb)

Supplementary Fig. S3

Supplementary figure S3 Schemes of possible chromosome rearrangements for two conserved associations: CDR 23/21/9/13 and CDR 4/31 (JPG 1.21 MB)

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Kulemzina, A.I., Trifonov, V.A., Perelman, P.L. et al. Cross-species chromosome painting in Cetartiodactyla: Reconstructing the karyotype evolution in key phylogenetic lineages. Chromosome Res 17, 419–436 (2009). https://doi.org/10.1007/s10577-009-9032-3

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