Evolution and Characteristics of the Opossum Genome


The opossum genome sequence furnishes a critical comparator for examining the evolutionary histories of vertebrate genomes in general, and provides the most appropriate outgroup sequence for establishing the relative antiquity or novelty of genetic features among the major lineages of eutherian (‘placental’) mammals. Comparative analyses using the opossum genome have already provided a wealth of evidence regarding the importance of noncoding elements in the evolution of mammalian genomes, the role of transposable elements in driving genomic innovation, and the relationships between recombination rate, nucleotide composition, and the genomic distributions of repetitive elements. This article summarizes key features of the opossum genome and discusses their implications for better understanding the varied processes that contribute to genome evolution and how changes in structural organization, complexity, and molecular functions of mammalian (and other) genomes can lead to differences in gene regulation, expression, and action among and within species.

Key concepts:

  • Because the pace of evolutionary change varies for different classes of genomic elements, the power of comparative genomic analysis is dependent on the availability of genomic data from organisms occupying key phylogenetic positions that enable comparisons of both slow and fast evolving genomic features.

  • Metatherian (marsupial) and eutherian (placental) mammals are each other's closest relatives. During divergence from their common ancestor they evolved distinctive morphologic, physiologic, and genetic variations on the elemental mammalian patterns. These distinctions hold great potential for examining relationships between the molecular structures of mammalian genomes and the functional attributes of their components.

  • Representing the Metatheria, the opossum genome furnishes a crucial reference for examining the evolutionary histories of vertebrate genomes in general, and provides the most appropriate outgroup sequence for establishing ancestral versus derived polarity for genomic and genetic features among the major lineages of eutherian mammals.

  • The opossum genome sequence has provided new evidence regarding the importance of noncoding elements in the evolution of mammalian genomes, the role of transposable elements in driving genomic innovation, and the relationships between recombination rate, nucleotide composition, and the genomic distributions of repetitive elements.

  • The opossum genome is comprised of eight very large autosomes and a sex chromosome (X or Y), and exhibits extremely low levels of meiotic recombination relative to other mammalian genomes examined.

  • The opossum genome exhibits the lowest levels of G and C nucleotides known among sequenced amniotes.

  • At least 52% of the opossum genome is composed of interspersed repeat family elements—the highest level known from sequenced amniotes.

  • Low recombination rate may contribute to the unusual nucleotide composition and the high levels of interspersed repeat elements in the opossum genome.

  • The protein‐coding gene complement of the opossum genome is very similar to that of eutherian mammals and other vertebrates.

  • Conserved noncoding genomic elements (CNEs) show high levels of novelty between opossum and eutherian genomes and strong lineage specificity among eutherian clades. This finding strengthens the idea that in mammalian evolution alterations in the repertoires of noncoding elements that regulate protein‐coding gene function may be more important than changes in the structures or numbers of protein‐coding genes.

  • The opossum genome has provided new evidence regarding the structure of the ancestral eutherian karyotype and the evolution of genomic imprinting. It also furnishes new tools to study the evolution and function of the mammalian immune system and the phenomenon of X‐chromosome inactivation.

Keywords: comparative genomics; marsupials; genome evolution; recombination; phylogeny

Figure 1.

Phylogenetic relationships and approximate divergence dates for mammalian clades discussed in this article. Species in bold type: high‐coverage genome sequence assembly available. Species in nonbold type: low‐coverage genome sequence assembly available or in progress. Species in parenthesis: no genome sequence assembly available. Blue‐filled circle: most recent therian ancestor. Red‐filled circle: most recent boreoeutherian ancestor. Divergence dates are point estimates based on data from multiple sources (see Samollow, for details).

Figure 2.

Monodelphis domestica. (a) Adult female. (b) Female with a litter of 10 pups. The newborns are approximately 36 h post‐partum age. Note that M. domestica does not possess a pouch. (c) Detail of litter seen in panel (b). (d) Newborn, less than 12 h post‐partum age. Scale is 1 mm between marks. Photos: Larry Wadsworth, TAMU Media Resources. Reproduced with permission from Samollow . Permission given from Cold Spring Harbor Press.

Figure 3.

The chromosomes of Monodelphis domestica. Main panel (a) ideograms of M. domestica autosomes 1–8 and X‐ and Y sex chromosomes, based on patterns modified from Pathak et al. (used by kind permission of Springer Science and Business Media). Orientation: p arm at top; q arm at bottom; centromere position indicated by constriction. Chromosome sizes are estimated total lengths (see Table ). Inset (b) inverted DAPI‐banded (similar to G‐banded) mid‐metaphase chromosomes from a female M. domestica peripheral lymphocyte (photograph courtesy of Matthew Breen).



Behringer RR, Eakin GS and Renfree MB (2006) Mammalian diversity: gametes, embryos and reproduction. Reproduction, Fertility and Development 18: 99–107.

Belov K, Deakin JE, Papenfuss AT et al. (2006) Reconstructing an ancestral mammalian immune supercomplex from a marsupial major histocompatibility complex. PLoS Biology 4: e46doi: 10.1371/journal.pbio.0040046.

Belov K, Sanderson CE, Deakin JE et al. (2007) Characterization of the opossum immune genome provides insights into the evolution of the mammalian immune system. Genome Research 17: 982–991.

Bennett JH, Hayman DL and Hope RM (1986) Novel sex differences in linkage values and meiotic chromosome behaviour in a marsupial. Nature 323: 59–60.

Cooper DW, Johnston PG, Watson JM and Graves JAM (1993) X‐inactivation in marsupials and monotremes. Seminars in Developmental Biology 4: 117–128.

Davidow LS, Breen M, Duke SE et al. (2007) The search for a marsupial XIC reveals a break with vertebrate synteny. Chromosome Research 15: 137–146.

Dermitzakis ET, Reymond A and Antonarakis SE (2005) Conserved non‐genic sequences – an unexpected feature of mammalian genomes. Nature Reviews. Genetics 6: 151–157.

Duret L, Chureau C, Samain S, Weissenbach J and Avner P (2006a) The Xist RNA gene evolved in eutherians by pseudogenization of a protein‐coding gene. Science 312: 1653–1655.

Duret L, Eyre‐Walker A and Galtier N (2006b) A new perspective on isochore evolution. Gene 385: 71–74.

Galtier N, Piganeau G, Mouchiroud D and Duret L (2001) GC‐content evolution in mammalian genomes: the biased gene conversion hypothesis. Genetics 159: 907–911.

Gentles AJ, Wakefield MJ, Kohany O et al. (2007) Evolutionary dynamics of transposable elements in the short‐tailed opossum Monodelphis domestica. Genome Research 17: 992–1004.

Goodstadt L, Heger A, Webber C and Ponting CP (2007) An analysis of the gene complement of a marsupial, Monodelphis domestica: evolution of lineage‐specific genes and giant chromosomes. Genome Research 17: 969–981.

Graves JA and Westerman M (2002) Marsupial genetics and genomics. Trends in Genetics 18: 517–521.

Gregory TR (2009) Animal Genome Size Database. http://www.genomesize.com/.

Gu W, Ray DA, Walker JA et al. (2007) SINEs, evolution and genome structure in the opossum. Gene 396: 46–58.

Hillier LW, Miller W, Birney E et al. (2004) Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432: 695–716.

Hogstrand K and Bohme J (1999) Gene conversion of major histocompatibility complex genes is associated with CpG‐rich regions. Immunogenetics 49: 446–455.

Hore TA, Koina E, Wakefield MJ and Marshall Graves JA (2007a) The region homologous to the X‐chromosome inactivation centre has been disrupted in marsupial and monotreme mammals. Chromosome Research 15: 147–161.

Hore TA, Rapkins RW and Graves A (2007b) Construction and evolution of imprinted loci in mammals. Trends in Genetics 23: 440–448.

Kamal M, Xie X and Lander ES (2006) A large family of ancient repeat elements in the human genome is under strong selection. Proceedings of the National Academy of Sciences of the USA 103: 2740–2745.

Kemkemer C, Kohn M, Cooper DN et al. (2009) Gene synteny comparisons between different vertebrates provide new insights into breakage and fusion events during mammalian karyotype evolution. BMC Evolutionary Biology 9: 84.

Kemkemer C, Kohn M, Kehrer‐Sawatzki H et al. (2006) Reconstruction of the ancestral ferungulate karyotype by electronic chromosome painting (E‐painting). Chromosome Research 14: 899–907.

Koina E, Chaumeil J, Greaves IK, Tremethick DJ and Graves JA (2009) Specific patterns of histone marks accompany X chromosome inactivation in a marsupial. Chromosome Research 17: 115–126.

Lewis A and Reik W (2006) How imprinting centres work. Cytogenetic and Genome Research 113: 81–89.

Lindblad‐Toh K, Wade CM, Mikkelsen TS et al. (2005) Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438: 803–819.

McEwen GK, Woolfe A, Goode D et al. (2006) Ancient duplicated conserved noncoding elements in vertebrates: a genomic and functional analysis. Genome Research 16: 451–465.

Metcalfe CJ, Eldridge MD and Johnston PG (2007) Mapping the distribution of the telomeric sequence (T2AG3)n in the Macropodoidea (Marsupialia) by fluorescence in situ hybridization. II. The ancestral 2n=22 macropodid karyotype. Cytogenetic and Genome Research 116: 212–217.

Mikkelsen TS, Wakefield MJ, Aken B et al. (2007) Genome of the marsupial Monodelphis domestica reveals innovation in non‐coding sequences. Nature 447: 167–177.

Muotri AR, Marchetto MC, Coufal NG and Gage FH (2007) The necessary junk: new functions for transposable elements. Human Molecular Genetics 16(Spec No. 2): R159–R167.

Murphy SK and Jirtle RL (2003) Imprinting evolution and the price of silence. BioEssays 25: 577–588.

Murphy WJ, Larkin DM, Everts‐van der Wind A et al. (2005) Dynamics of mammalian chromosome evolution inferred from multispecies comparative maps. Science 309: 613–617.

Pathak S, Ronne M, Brown NM, Furlong CL and VandeBerg JL (1993) A high‐resolution banding pattern idiogram of Monodelphis domestica chromosomes (Marsupialia, Mammalia). Cytogenetics and Cell Genetics 63: 181–184.

Rapkins RW, Hore T, Smithwick M et al. (2006) Recent assembly of an imprinted domain from non‐imprinted components. PLoS Genetics 2: e182 doi:110.1371/journal.pgen.0020182.

Rens W, O'Brien PC, Fairclough H et al. (2003) Reversal and convergence in marsupial chromosome evolution. Cytogenetic and Genome Research 102: 282–290.

Rens W, O'Brien PC, Yang F et al. (2001) Karyotype relationships between distantly related marsupials from South America and Australia. Chromosome Research 9: 301–308.

Rettenberger G, Klett C, Zechner U et al. (1995) ZOO‐FISH analysis: cat and human karyotypes closely resemble the putative ancestral mammalian karyotype. Chromosome Research 3: 479–486.

Rofe R and Hayman D (1985) G‐banding evidence for a conserved complement in the Marsupialia. Cytogenetics and Cell Genetics 39: 40–50.

Samollow PB (2006) Status and applications of genomic resources for the gray, short‐tailed opossum, Monodelphis domestica, an American marsupial model for comparative biology. Australian Journal of Zoology 54: 173–196.

Samollow PB (2008) The opossum genome: insights and opportunities from an alternative mammal. Genome Research 18: 1199–1215.

Samollow PB, Gouin N, Miethke P et al. (2007) A microsatellite‐based, physically anchored linkage map for the gray, short‐tailed opossum (Monodelphis domestica). Chromosome Research 15: 269–281.

Scherthan H, Cremer T, Arnason U et al. (1994) Comparative chromosome painting discloses homologous segments in distantly related mammals. Nature Genetics 6: 342–347.

Selwood L and Johnson MH (2006) Trophoblast and hypoblast in the monotreme, marsupial and eutherian mammal: evolution and origins. BioEssays 28: 128–145.

Shevchenko AI, Zakharova IS, Elisaphenko EA et al. (2007) Genes flanking Xist in mouse and human are separated on the X chromosome in American marsupials. Chromosome Research 15: 127–136.

Shifman S, Bell JT, Copley RR et al. (2006) A high‐resolution single nucleotide polymorphism genetic map of the mouse genome. PLoS Biology 4: e395 doi: 310.1371/journal.pbio.0040395.

Siepel A, Bejerano G, Pedersen JS et al. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Research 15: 1034–1050.

Tyndale‐Biscoe H (2005) Life of Marsupials. Collingwood: CSIRO Publishing.

VandeBerg JL (1999) The laboratory opossum (Monodelphis domestica). In: Poole T and English P (eds) UFAW Handbook on the Management of Laboratory Animals, 7th edn, vol. 1: Terrestrial Vertebrates, pp. 193–209. Oxford, UK: Blackwell Science Ltd.

VandeBerg JL and Robinson ES (1997) The laboratory opossum (Monodelphis domestica) in laboratory research. ILAR Journal 38: 4–12.

Warren WC, Hillier LW, Marshall Graves JA et al. (2008) Genome analysis of the platypus reveals unique signatures of evolution. Nature 453: 175–183.

Wong ES, Young LJ, Papenfuss AT and Belov K (2006) In silico identification of opossum cytokine genes suggests the complexity of the marsupial immune system rivals that of eutherian mammals. Immunome Research 2: 4 doi: 10.1186/1745‐7580‐1182‐1184.

Wutz A and Gribnau J (2007) X inactivation Xplained. Current Opinion in Genetics & Development 17: 387–393.

Zenger KR, McKenzie LM and Cooper DW (2002) The first comprehensive genetic linkage map of a marsupial: the tammar wallaby (Macropus eugenii). Genetics 162: 321–330.

Further Reading

Belle EM, Duret L, Galtier N and Eyre‐Walker A (2004) The decline of isochores in mammals: an assessment of the GC content variation along the mammalian phylogeny. Journal of Molecular Evolution 58: 653–660.

Ferreri GC, Liscinsky DM, Mack JA, Eldridge MDB and O'Neill RJ (2006) Retention of latent centromeres in the mammalian genome. Journal of Heredity 96: 217–224.

Ferreri GC, Marzelli M, Rens W and O'Neill RJ (2004) A centromere‐specific retroviral element associated with breaks of synteny in macropodine marsupials. Cytogenetic and Genome Research 107: 115–118.

Gu J and Li WH (2006) Are GC‐rich isochores vanishing in mammals? Gene 385: 50–56.

Heard E and Disteche CM (2006) Dosage compensation in mammals: fine‐tuning the expression of the X chromosome. Genes and Development 20: 1848–1867.

Hedges SB and Kumar S (2009) The Timetree of Life. Oxford: The Oxford University Press.

Ideraabdullah FY, Vigneau S and Bartolomei MS (2008) Genomic imprinting mechanisms in mammals. Mutation Research 647: 77–85.

King DC, Taylor J, Zhang Y et al. (2007) Finding cis‐regulatory elements using comparative genomics: some lessons from ENCODE data. Genome Research 17: 775–786.

Renfree MB (2006) Society for Reproductive Biology Founders' Lecture 2006 – life in the pouch: womb with a view. Reproduction, Fertility and Development 18: 721–734.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Samollow, Paul B(Dec 2009) Evolution and Characteristics of the Opossum Genome. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021781]