Marsupial Chromosome Evolution

Abstract

Marsupial chromosomes were among the first mammalian chromosomes to be studied in the early twentieth century and have since been extensively characterised by multiple approaches. With relatively few and large chromosomes, marsupials have proven to be ideal subjects for studying how chromosomes have changed during marsupial evolution from a predicted ancestral marsupial karyotype consisting of just seven pairs of chromosomes. In this article, the current understanding of marsupial chromosome evolution is reviewed and the way two families of marsupials with different rates of chromosome evolution help to decipher the mechanisms involved in chromosome evolution is discussed. The family Dasyuridae is characterised by remarkable chromosome stability, whereas the family Macropodidae has experienced extensive chromosome shuffling. Comparisons of the differences in chromosome features between these two families may hold the key to understanding the role of chromosome rearrangements in speciation.

Key Concepts

  • Marsupials have large, relatively conserved karyotypes, making it possible to track the evolution of their chromosomes.
  • Chromosome numbers in marsupials range from 2n = 10 to 2n = 32.
  • Different marsupial karyotypes have evolved from a predicted ancestral marsupial with seven pairs of chromosomes (2n = 14).
  • All the members of the Dasyuridae family karyotyped to date have a 2n = 14 karyoytpe similar to that of the predicted ancestral marsupial.
  • Dasyurids have a unique telomere length dimorphism not found in any other species.
  • The family Macropodidae has a lot of karyotype diversity with chromosome numbers ranging from 2n = 10 to 2n = 24, evolving from a 2n = 22 ancestral macropod.
  • The Y chromosome of marsupials has been termed ‘minimal mammalian Y’.
  • X chromosomes in marsupials have experienced substantial rearrangement between species.

Keywords: marsupial; mammal; karyotype; comparative genomics; comparative cytogenetics; sex chromosomes; genome evolution; chromosome rearrangement

Figure 1. Arrangement of conserved chromosome segments (C1–C19) in different marsupials. All members of the family Dasyuridae have 2n = 14 karyotypes, with an arrangement of conserved segments similar to the Tasmanian devil and 2n = 14 marsupial ancestor. Examples of different chromosome arrangements observed in the family Macropodidae are shown, with the unadorned rock‐wallaby having a similar arrangement to the 2n = 22 macropod ancestor. Mya, millions of years ago.
Figure 2. The telomere length dimorphism on Tasmanian devil chromosomes. The intensity of the telomere signal (red) varies between chromosome homologues. Strong red signals correspond to long telomeres, whereas weaker signals correspond to short telomeres.
Figure 3. Chromosome rearrangements including fissions, inversions, fissions and centromere repositioning, resulting in a 2n = 22 macropod ancestor from a 2n = 14 marsupial ancestor.
Figure 4. Comparison of gene order between the X chromosomes of human, Tasmanian devil, Brazilian opossum and tammar wallaby. The yellow region of the human X chromosome is located on the autosomes in marsupials (not shown). The position of the noncoding RNA (RSX) involved in X chromosome inactivation is indicated on opossum X chromosome (its position is unknown on other marsupial X chromosomes). Each line indicates where a gene is located. Two lines ending at the same position indicate that the genes map to a similar position on the chromosome.
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Further Reading

Deakin JE (2012) Marsupial genome sequences: providing insight into evolution and disease. Scientifica 2012: 543176.

Deakin JE (2017) Implications of monotreme and marsupial chromosome evolution on sex determination and differentiation. General and Comparative Endocrinology 244: 130–138.

Deakin JE (2018) Chromosome evolution in marsupials. Genes 9: 72.

Deakin JE, Koina E, Waters PD, et al. (2008) Physical map of two tammar wallaby chromosomes: a strategy for mapping in non‐model mammals. Chromosome Research 16: 1159–1175.

Graves JA (2015) Weird mammals provide insights into the evolution of mammalian sex chromosomes and dosage compensation. Journal of Genetics 94: 567–574.

Graves JAM (2018) Weird animals, sex, and genome evolution. Annual Review of Animal Biosciences 6: 1–22.

Ingles ED and Deakin JE (2016) Telomere, species differences, and unusual telomeres in vertebrates: presenting challenges and opportunities to understand telomere dynamics. AIMS Genetics 3: 1–24.

Potter S and Deakin JE (2018) Cytogenetics: an important inclusion in the conservation genetics toolbox. Pacific Conservation Biology 24: 280–288.

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Deakin, Janine E(May 2019) Marsupial Chromosome Evolution. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028284]