Some 40 million years ago in South America, following the arrival of the common ancestor of caviomorph rodents from the Old World, big changes were afoot.
Specifically, the caviomorph colonists were beginning to give rise to an extant evolutionary progeny of nearly 250 species and 13 families of endemic South American rodents, which show notable diversity in morphology, ecology, and life history (think New World porcupines, chinchillas, and guinea pigs). Interestingly, caviomorphs are also the bearers of notable genomic changes (i.e., evolution of genome size and structure; like the number, form, and arrangement of chromosomes). Functional numbers of chromosomes vary widely from 10-118; moreover, the most extreme instances of genomic evolution in caviomorphs tend to be found in clades with highest diversification rates. That pattern (correlated rates of speciation and genomic evolution) is not uncommon in mammals, and its presence in caviomorphs reiterates persistent holes in our understanding of the links between genomic evolution, speciation, and molecular adaptation.
Present (and prominent) within this milieu of caviomorph chromosomal combinatorics is a species named Tympanoctomys barrerae, or the red vizcacha rat (Figure 1). Red vizcacha rats are small rodents (if you’re a North American desert dweller, think kangaroo rat size) that inhabit the high-latitude, cis-Andean deserts of western Argentina, where they eke out a living largely on low-hanging saltbush fruits. Amazingly, the cells of T. berrarae host nuclear genomes that are more than double the size of an average mammal, and nearly three times that of the human genome. This mass of DNA is packaged into a whopping 102 chromosomes that, while failing to comprise the largest known mammalian karyotype (an honor that belongs to the Bolivian bamboo rat), are still double that of most of its closest living relatives. Possession of the largest known mammalian genome is plenty sufficient for status as an ‘evolutionary curiosity’; however, there are still major questions related to how and why the red vizcacha rat’s genome became so large.
“Evolutionary relationships, chromosome number (2n), and genome size in picograms (C-value) of vizcacha rats and other members of the family Octodontidae (left). Red vizcacha rat T. barrerae in El Nihuil, Mendoza, Argentina (photo credit: Fernanda Cuevas).” Caption from Evans et al. 2017.
In a new paper in Genome Biology and Evolution, Ben Evans, Nate Upham, and colleagues bring whole-genome and whole-transcriptome data to bear on those questions. Their analysis compares and contrasts genomic properties of T. barrerae with those of one of its closest relatives, the mountain vizcacha rat (Octomys mimax). Geologically speaking, these 2 lineages are relatively recently diverged (earliest Pliocene), but the genome of the red vizcacha rat is still twice as large and comprised of nearly double the number of chromosomes. It is worth noting that new specimens of T. barrerae were collected specifically for this work, hard-fought during recent expeditions to the Argentinian high desert. (That part of the study is nicely chronicled here, allowing lots of room for vicarious experience!).
Evans et al. use a variety of tests to understand whether red vizcacha rat genome expansion might be the result of whole genome duplication (polyploidy is extremely rare in vertebrates), but also if accumulation of repetitive elements may have played a role. As an experimental control in the test for polyploidy, the authors subjected genomes of 2 African clawed frogs (Xenopus; 1 of which is a confirmed tetraploid) to the same battery of tests.
The preponderance of their results reject polyploidization in T. barrerae, instead suggesting significant accumulation of repetitive regions as the cause for genome expansion. Interestingly, however, only a few of the repetitive elements BLAST to regions of known biological function in related rodent species. The rest either find their match in regions of unknown function (satellite or micro satellite DNA) or simply lack a clear match at all. According to the authors, their results “support that 1) [the genome of T. barrerae] evolved by expansion of a diverse mosaic of repetitive sequences, and 2) the genomic distribution of these elements is not uniform.”
Still an open question is whether these repetitive genomic elements serve actual biological function(s), and whether those functions were involved in the speciation process. One hypothesis is that the repetitive regions (which make up a whopping 1/2 of the genome of T. barrerae) are somehow involved in adaptation to desert environments and processing of desert food sources. T. barrerae inhabits regions of high-latitude South America that, due to a sizable Andean rain shadow, receive among the lowest rainfall of anywhere in the New World. The species has also evolved an ability to survive on diets made up largely of saltbush fruits. Continuing to pinpoint the causes and consequences of genome expansion in T. berrarae will likely teach us much more about genome evolution, adaptation, and diversification and their links in endemic South American rodents.