Tracing genome evolution: from ancestral karyotypes to current genomes in three mammalian clades

Mammals show a wide range of chromosomic diversity. Their karyotypes range from 2n=6/7 in the Indian muntjac (Ruminantia) to 2n=102 in the Viscacha rat (Rodentia). Although the mammalian genome size is round 3.5 Gb, the mammalian average chromosome size is highly variable, including species with a high number of small chromosomes such as cattle (a ruminant with 2n=60 and an average chromosome size of 87 Mb), and species with a low number of big chromosomes such as Tasmanian devil (a marsupial with 2n=14 and an average chromosome size of 440 Mb). Identifying and timing when and where gross genomic rearrangements occurred during evolution will help to explain changes in genome structure with functional consequences that might eventually lead to speciation. Here we used DESCHRAMBLER to reconstruct eight ancestral genomes from three different lineages: Ruminantia, Marsupialia and Afrotheria. We classified the rearrangement events occurring in each lineage and identified the Evolutionary Breakpoints Regions (EBRs) and Homologous Synteny Blocks (HSBs). Cattle and African elephant showed the same number of well-defined EBRs, 32, while Tasmanian devil only showed 19. Marsupial and ruminant genomes are characterised by inversions, while interchromosomal rearrangements are also important in the oldest ancestor of ruminants and are the main rearrangement force in the afrotherians. These EBRs are located in gene-rich regions of the genome, and in ruminants and afrotherians, they are also located in regions with a high density of transposable elements (TEs). Moreover, we identified signatures of convergent evolution in mammals with an extreme range of both, diploid numbers and chromosome sizes, using representative species of the three lineages and searching for positive selection in their orthologous genes. We found that some genes under convergent evolution and positive selection were related to processes such as chromatin structure or DNA repair, such as MSH6 or RNF123, that, at the same time, are related to causes and consequences of chromosome rearrangements (CRs). Overall, our results significantly expand knowledge of genome evolution and will facilitate greater understanding of the role of CRs in mammalian evolution.