Abstract

BackgroundThe increasing number of assembled mammalian genomes makes it possible to compare genome organisation across mammalian lineages and reconstruct chromosomes of the ancestral marsupial and therian (marsupial and eutherian) mammals. However, the reconstruction of ancestral genomes requires genome assemblies to be anchored to chromosomes. The recently sequenced tammar wallaby (Macropus eugenii) genome was assembled into over 300,000 contigs. We previously devised an efficient strategy for mapping large evolutionarily conserved blocks in non-model mammals, and applied this to determine the arrangement of conserved blocks on all wallaby chromosomes, thereby permitting comparative maps to be constructed and resolve the long debated issue between a 2n = 14 and 2n = 22 ancestral marsupial karyotype.ResultsWe identified large blocks of genes conserved between human and opossum, and mapped genes corresponding to the ends of these blocks by fluorescence in situ hybridization (FISH). A total of 242 genes was assigned to wallaby chromosomes in the present study, bringing the total number of genes mapped to 554 and making it the most densely cytogenetically mapped marsupial genome. We used these gene assignments to construct comparative maps between wallaby and opossum, which uncovered many intrachromosomal rearrangements, particularly for genes found on wallaby chromosomes X and 3. Expanding comparisons to include chicken and human permitted the putative ancestral marsupial (2n = 14) and therian mammal (2n = 19) karyotypes to be reconstructed.ConclusionsOur physical mapping data for the tammar wallaby has uncovered the events shaping marsupial genomes and enabled us to predict the ancestral marsupial karyotype, supporting a 2n = 14 ancestor. Futhermore, our predicted therian ancestral karyotype has helped to understand the evolution of the ancestral eutherian genome.

Highlights

  • The increasing number of assembled mammalian genomes makes it possible to compare genome organisation across mammalian lineages and reconstruct chromosomes of the ancestral marsupial and therian mammals

  • Our analysis enabled us to reconstruct the karyotype of the marsupial ancestor, and provided insight into the genome organisation of the therian ancestor

  • The debate over the whether the ancestral marsupial karyotype was 2n = 14 or 2n = 22 has persisted for many years because data were not available to compare the marsupial chromosome arrangement with that observed in representatives of other lineages

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Summary

Introduction

The increasing number of assembled mammalian genomes makes it possible to compare genome organisation across mammalian lineages and reconstruct chromosomes of the ancestral marsupial and therian (marsupial and eutherian) mammals. Metatherians (marsupials) are a diverse group of mammals found in the Americas and Australasia They diverged from eutherian (“placental”) mammals approximately 143178 million years ago (MYA) [1,2] and possess many unique biological features that have intrigued biologists since these animals were first described. Studies of marsupial chromosome number, morphology and G-banding revealed an astonishing level of conservation across the entire infraclass of Metatheria This was supported by cross-species chromosome painting, which demonstrated that all karyotypic variation amongst marsupials could be attributed to the arrangement of just 19 conserved segments [6]

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