Evolution of the Largest Mammalian Genome

Abstract

The genome of the red vizcacha rat (Rodentia, Octodontidae, Tympanoctomys barrerae) is the largest of all mammals, and about double the size of their close relative, the mountain vizcacha rat Octomys mimax, even though the lineages that gave rise to these species diverged from each other only about 5 Ma. The mechanism for this rapid genome expansion is controversial, and hypothesized to be a consequence of whole genome duplication or accumulation of repetitive elements. To test these alternative but nonexclusive hypotheses, we gathered and evaluated evidence from whole transcriptome and whole genome sequences of T. barrerae and O. mimax. We recovered support for genome expansion due to accumulation of a diverse assemblage of repetitive elements, which represent about one half and one fifth of the genomes of T. barrerae and O. mimax, respectively, but we found no strong signal of whole genome duplication. In both species, repetitive sequences were rare in transcribed regions as compared with the rest of the genome, and mostly had no close match to annotated repetitive sequences from other rodents. These findings raise new questions about the genomic dynamics of these repetitive elements, their connection to widespread chromosomal fissions that occurred in the T. barrerae ancestor, and their fitness effects-including during the evolution of hypersaline dietary tolerance in T. barrerae.

Keywords: Caviomorpha; Octodontidae; Rodentia; mammals; repetitive DNA; whole genome duplication.

Fig. 1.

—Evolutionary relationships, somatic chromosome number (2n), and genome size in picograms (C-value) of vizcacha rats and other members of the family Octodontidae (left) based on the analysis of Upham and Patterson (2015) and data from Gallardo et al. (2003). Scale bar is in millions of years; dark branches on phylogeny subtend focal species in this study, with the presumed timing of genome expansion indicated with a red branch. According to Upham and Patterson (2015), the divergence of vizcacha rats from other members of the family Octodontidae has a 95% confidence interval (CI) of 7.4–10.5 Ma, divergences of the Octomys from other vizcacha rats has a 95% CI of 3.9–7.3 Ma, and divergence of Pipanacoctomys from Tympanoctomys has a 95% CI of 1.8–4.3 Ma. Not depicted in this phylogeny are the Tympanoctomys species T. loschalchalerosorum and T. kirchnerorum. Some researchers have included P. aureus as a member of Tympanoctomys (Diaz et al. 2015), but we opt to maintain this separate genus to reflect their molecular divergence. Depicted on the right is the red vizcacha rat T. barrerae in El Nihuil, Mendoza, Argentina (photo credit: Fernanda Cuevas).

Fig. 2.

—Occurrence of 35-mers in trimmed and filtered WGS data from O. mimax (left) and T. barrerae (right). The occurrence of 35-mers that were observed only once is not shown; the sum of occurrences of 35-mers that were observed >100 is represented by a bar on the right side of each graph (which were 5.7 million and 35.7 million occurrences for O. mimax and T. barrerae, respectively).

Fig. 3.

—Length and coverage of high abundance k-mer contigs in O. mimax (left) and T. barrerae (right). In both plots, gray dots indicate contigs with length >200 that match mitochondrial DNA of T. barrerae GenBank accession number HM544132.1.