Chromosome Numbers in Mammals

Abstract

180 million years of mammalian radiation have shaped the genomes of approximately 4600 extant species and are witnessed by karyotypic diversity in extant species. Knowledge of chromosome numbers and morphology among mammalian species arrived during the period of classical cytogenetics in the 1960s and provided a first glimpse of the extent of karyotype reorganisation among various mammalian species. Further technical advances like banding techniques and the subsequent arrival of molecular tools like chromosome sorting, painting and deoxyribonucleic acid (DNA) probes of different complexity led to improved molecular tools that allowed the visualisation of homology at the DNA level directly on chromosomes leading to modern phylogenomics. This article will provide an overview of what is known about mammalian karyotypic diversity and the research in mechanisms of chromosome rearrangements that shaped the present‐day karyotypes, with a special emphasis on muntjac chromosome evolution.

Key Concepts:

  • The chromosome number and morphology is a species‐specific feature.

  • Most diploid chromosome numbers of mammals lie within the range of 36–60.

  • Comparative cytogenomics suggests a 2n=44 karyotype for the mammalian ancestor.

  • Comparative cytogenetic comparisons are only informative among species that display a similarly low rates of karyotypic change.

  • Despite a wide range of chromosome numbers and morphologies there is remarkable conservation of the coding part of mammalian genomes.

  • Chromosome rearrangements fixed during mammalian evolution are witness of benign karyotypic change.

  • Polymorphisms in heterochromatin and copy number variation of repetitive DNA sequences are the source of significant karyotype and genome size variations in mammals and beyond.

  • Cervidae evolution is associated with a rapid karyotypic turnover leading to chromosome numbers from 2n=6 to 2n=80.

  • The extant muntjac karyotype displays the remnants of numerous chromosomal tandem fusions, an evolutionary rare aberration type.

  • Illegitimate recombination events among telomeric and centromeric repetitive sequences in combination with a prevalence of inbreeding can be considered as driving force of muntjac karyotype evolution.

Keywords: karyotype evolution; chromosome number; rearrangements; mammals; muntjac; comparative cytogenetics; phylogenomics; genome evolution; Zoo‐FISH

Figure 1.

Outline of global chromosome rearrangements that are involved in alterations of chromosome number and morphology of a species' karyotype. (a) Robertsonian fusion (centric fusion or translocation) involves two breaks (red arrows) in the centromeric regions and the subsequent joining of the two chromosomes, which reduces chromosome number. Chromosome fission – a break (green arrow) at a centromeric region splits a chromosome into two. This increases chromosome number and requires maintenance of centromere activity after break repair in both chromosomes. Both rearrangements leave the number of major chromosome arms (NF) unaffected. (b) Reciprocal translocation – one break each in two unrelated chromosomes (red arrows) leads to exchange of nonhomologous segments between the two (black arrow). This may alter arm length and banding patterns. (c) Inversion – two breaks (red wavy lines) within a chromosome and reversal of a chromosome segment alter the orientation of markers in the former. This may involve segments on chromosome arms (paracentric; black arrow) or segments that include a centromere (pericentric; red arrow). The type of pericentromeric inversion depicted leads to a change in NF. (d) Tandem fusion – two chromosome breaks (red arrows), one near a distal telomere and one near the centromere of a second chromosome, lead to a head‐to‐tail fusion between the two chromosomes and inactivation of the broken centromere, thereby reducing the NF and elongating the new chromosome arm. Other, not depicted rearrangements involve duplication, insertion and deletion of chromosome segments, terminal deletion requiring healing of the dsDNA break by telomerase.

Figure 2.

Distribution of diploid chromosome numbers (only even numbers shown) among eutherian mammals. It is an extended version of a figure published by Matthey and includes the more recently karyotyped species with extreme chromosome numbers like Indian, Black or Gongshan muntjac at the lower end and the South American rodents Ichthyomys pittieri and Tympanoctomys barrerae with the highest numbers (see Table ).

Figure 3.

(a) 4′,6‐Diamidino‐2‐phenylindole(DAPI)‐banded, colour‐inverted metaphase chromosomes (2n=46) of a male Chinese muntjac (M. reevesi). (b) DAPI‐banded metaphase chromosomes of a male Indian muntjac. The huge chromosome 1 is metacentric, chromosome 2 is subacrocentric and the Y1 (3) acrocentric. The X chromosome is a translocation of the actual X (which represents the short arm) on to an autosomal long arm (by some authors referred to as X+3). The Xp is separated from the q arm by the largest known mammalian centromere (curly bracket), which contains a compound kinetochore. The autosomal homologue of Xq is referred to as Y1 (or 3) and the actual Y as Y2 (or Y). (c) FISH with a fusion sequence product (red) highlights satellite sequences in the pericentric region (arrow heads) and at the ancestral fusion points within chromosome arms (blue). DAPI‐banded colour‐inverted chromosomes 1 and 2 are shown below. The arrow heads mark the centromeric region.

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Further Reading

Chowdhary BP, Raudsepp T, Frönicke L and Scherthan H (1998) Emerging patterns of comparative genome organization in some mammalian species as revealed by Zoo‐FISH. Genome Research 8: 577–589.

Hartmann N and Scherthan H (2005) Characterization of the telomere complex, TERF1 and TERF2 genes in muntjac species with fusion karyotypes. Experimental Cell Research 306: 64–74.

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Murphy WJ, Stanyon R and O'Brien SJ (2001) Evolution of mammalian genome organization inferred from comparative gene mapping. Genome Biology 2 reviews0005.1–reviews0005.8. (http://genomebiology.com/2001/2/6/reviews/0005)

Pardo‐Manuel de Villena P and Sapienza C (2001) Recombination is proportional to the number of chromosome arms in mammals. Mammalian Genome 12: 318–322.

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Scherthan, Harry(Oct 2012) Chromosome Numbers in Mammals. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0005799.pub3]