Evolution and Characteristics of the Opossum Genome

Abstract

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).

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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]