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Zoology

A tree with unusual branches

Broad genetic sampling reveals kinship and evolutionary events in the diversification of the rodent family

Eduardo Cesar With its semiaquatic lifestyle, the coypu lives in the state of São Paulo and southwardsEduardo Cesar

Anyone who thinks that rats are nothing more than disgusting creatures with naked tails that prowl sewers has never seen a painted tree rat of the species Callistomys pictus. With a name that means “most beautiful rat” in Latin, the rodent that weighs about half a kilogram (kg) has long, soft fur, white or silver in color, and a black spot that runs down its back. Only a very select group of people has ever seen this animal that lives high in the trees in the cacao-growing region of Ilhéus in southern Bahia State, a restricted distribution that ensures the designation of endangered on the International Union for Conservation of Nature (IUCN) Red List of Threatened Species: zoologists have registered the existence of only 13 specimens. The most recent version of the family tree (phylogeny) belonging to this family of rodents indicated that its closest relative is the coypu (Myocastor coypus), a surprising revelation that further underscores the lack of knowledge about these animals. “The two species are completely different in appearance, habit and geographical distribution,” says zoologist Yuri Leite, a professor at the Federal University of Espírito Santo (UFES) and one of the authors of the article published on the online site of the journal Molecular Biology and Evolution in late December 2016.

Leite, who has spent more than 20 years conducting detective work in an effort to capture rats in the Echimyidae family, or echimyids, to try to understand the relationship between the species, finds kinship between two such different species as the painted tree rat and the coypu astonishing. Even so, it was not news to him since he published the same conclusion in 2014 in the journal Natureza Online, as part of the doctoral dissertation by his student Ana Carolina Loss. At that time, the article’s very title denoted a certain disbelief (“Unexpected phylogenetic relationships of the painted tree rat Callistomys pictus”). “That may have been a sampling bias because we’d had a limited amount of data,” he acknowledges, “but not anymore.” Despite having conducted extensive field work in search of rodents over nearly the entire expanse of Brazil, he himself had never seen a painted tree rat.

The 2014 study involved 14 Echimyidae genera, from which four gene fragments were analyzed.  The most recent study, led by French evolutionist Pierre-Henri Fabre, a professor at the University of Montpellier, encompasses all 26 genera of the family, using genetic material extracted from specimens stored at nine zoos in several countries (among them, a tissue sample from the painted tree rat collection at UFES). Based on this material, more recent sequencing tests have now enabled the construction of phylogenetic trees that take into account 18 different genes, the most complete sampling ever carried out with regard to these animals.

One of the problems of previous family trees is the inclusion of skeletal characteristics that apparently do not reveal the trajectory of evolution in a precise manner. It has always been understood that similarities were a result of kinship, but the principle does not apply to the full anatomy.  Leite refers to the fact that teeth, for example, are quite variable (perhaps as an adaptation to food) and similar among animals that now appear quite far apart in the phylogeny.  The results showed that the arboreal echimyids are to a large extent related and form a branch on the phylogenetic tree. The same applies to terrestrial echimyids, grouped into three subfamilies.   Between six million and 12 million years ago, one of them gave rise to two semifossorial genera (Clyomys and Euryzygomatomys) that spend a considerable amount of time underground.

Another rodent with this lifestyle is the spiny rat Carterodon sulcidens, a rare animal that lives in underground tunnels in the Cerrado savannah of central Brazil.  Despite the advances achieved by the study, its identity continues to be uncertain and it does not appear to be related to the semifossorial echimyids, to which it is very similar. “There is something strange about the molecular evolution of this animal, we cannot even say for sure whether it is an echimyid,” Leite says. “Some analyses place it much closer to the hutias, members of another rodent family endemic to the Caribbean, something really unexpected in morphological and biogeographical terms,” he says. Fabre also points out the speed with which the genetic material undergoes mutations—the rate of molecular evolution—which he finds exceptional, to the point of eluding the analytical methods utilized. “We plan to attempt it again in the future using more genes and genomic data,” he says.

Raquel Moura The painted tree rat is a close relative to the coypuRaquel Moura

Time machine
One contribution of the analysis conducted thus far, in addition to identifying relationships in a more accurate manner than previously possible, was to test hypotheses regarding factors that would have led to the diversification of this family of rodents.  The mechanism most often cited to explain geographic effects on evolution is usually vicariance, where barriers such as mountains or oceans emerge that hinder the movement of organisms and isolate species in subsets, which then go on to evolve separately.  But the recently-published study identifies the most likely event as dispersion—situations in which the movement of animals becomes possible.  It is impossible to go back to the past to be certain about how it happened, but statistical models allow for the determination of relationships between the species, their location and the age of the lineages, and suggest the most likely scenario. “If in one group, all the species appear in the Atlantic Forest, the ancestors must have lived in that forest,” Fabre explains. “But if the closest group to these Atlantic Forest species is Amazonian, there may have been a sort of separation between the Atlantic Forest and the Amazon Forest.” This is a simplification of course.  Based on that, other factors are taken into account to try to differentiate separations and linkages in distant times. “Thanks to geological and dispersion models, we are testing the vicariance and dispersion hypotheses,” the French scientist explains.

A striking example is precisely the improbable pairing between the painted tree rat and the spiny rat. Fabre admits that, despite suggestions in the past that there were similarities between the two species in terms of teeth and the number of chromosomes, it was a surprise to find them together on the tree, strongly supported by statistics. The lineage that gave rise to the two genera is ancient and according to the analyses, would have bifurcated around 10 million years ago, with the uplift of the Andes Mountains and the emergence of large areas of forests, such as the Paraná Basin. “These aquatic incursions may have driven the adaptations that led as much to the arboreal habits as well as to the semiaquatic ones,” Leite suggests.  Climbing trees or swimming are two possible ways to survive under the same conditions.

Alexandra Bezerra/Mpeg The place of the spiny rat in the genealogy is uncertainAlexandra Bezerra/Mpeg

Biogeographical analyses also corroborate previous findings that indicated the important role played by the uplift of the Andes and connections between the Amazon Forest and the Atlantic Forest in the diversification of these animals at different points in the past.  Leite believes that the new phylogenetic tree may be used to raise other ecological or evolutionary questions.  Why did a particular group evolve in the manner observed? What makes the painted tree rat so rare? There is a high degree of endemism in southern Bahia State where they live—with species unique to that zone. “We want to further investigate what occurred as a result of the changes in sea level and forest expansion that enabled diversification of the rodents,” suggests Leite, an expert in finding and capturing even the nearly inaccessible rats that never venture out of the treetops among which they circulate only at night.  He has already described various species of the family.

Fabre, who has dedicated years to the study of these mysterious animals, points to their charm. “We have so little data and yet it is one of the most interesting groups in South America given its diversification from the ecological, morphological and taxonomic standpoints,” he says, underscoring the fact that there are many species left to describe and little is known about those that science has already documented.

Scientific articles
FABRE, P.-H. et al. Mitogenomic phylogeny, diversification, and biogeography of South American spiny rats. Molecular Biology and Evolution. On-line. 25 Dec. 2016.
LOSS, A. C. et al. Unexpected phylogenetic relationships of the painted tree rat Callistomys pictus (Rodentia: Echimyidae). Natureza Online. V. 12, No. 3, p. 132-6. July-September 2014.

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