William Corrêa Tavares

New species of Cerradomys from coastal sandy plains of southeastern Brazil (Cricetidae: Sigmodontinae)

Abstract A new species of Cerradomys is described from the sandy plains of the northeastern littoral of Rio de Janeiro State and the southern littoral of Espírito Santo State, southeastern Brazil. Morphological and karyological characters were used to distinguish the new taxon from the 3 closest related species: C. subflavus, C. vivoi, and C. langguthi. Skull differences include the relatively larger general size, pronounced crests, broader rostrum, broader lacrimals, and wider sphenopalatine vacuities. Canonical variate analyses based on craniometric data showed that the new species has little overlap with C. subflavus, C. vivoi, and C. langguthi in multivariate space. The pelage of the new species has a unique, sparser, and thinner aspect. The diploid number of 54 chromosomes and the autosomal fundamental number of 66 arms (the highest among the 3 related species), added to the morphology of both sexual chromosomes, are diagnostic for the new species. The new taxon is restricted to a particular section of the Brazilian littoral covered by a mosaic of open vegetation locally named restingas, where it is one of the most abundant terrestrial mammals. In the restingas of this region this species is associated more with shrub patches than more forested physiognomies, being captured both on ground and on tree branches, especially of Clusia trees, suggesting a degree of arboreality. The recognition of this species adds further biogeographic uniqueness to the restingas of the northeastern littoral of Rio de Janeiro and southern littoral of Espírito Santo.

Phylogenetic and size constrains on cranial ontogenetic allometry of spiny rats (Echimyidae, Rodentia).

Analysis of ontogenetic development is crucial for understanding the emergence of phenotypic discrepancies between animal taxa. The study of allometric trajectories within a phylogenetic context is a feasible approach to assess the morphological change across different evolutionary lineages. Here, we report the disparity of multivariate ontogenetic allometry in the Echimyidae, a taxonomically diverse rodent family, as well as the effects of size on the evolution of skull ontogeny. The ontogenetic trajectories of 15 echimyid operational taxonomic unities (12 genera plus one genus with three species) belonging to all subfamilies and major clades, when plotted in allometric space, revealed strong and significant phylogenetic signals. Allometric trajectories were found to be constrained by phylogenetic ancestry, with changes approximately adjusting to a Brownian motion model of evolution. Moreover, the occupation of allometric space by echimyid taxa was significantly correlated with adult size rather than with shape, suggesting that the variation in adult size might result in critically intrinsic and structural constraints on allometric coefficients. These findings disagreed with the hypothesis that allometric disparities might be mainly adaptive with undetectable phylogenetic signals.

Plio-Pleistocene history of the endangered spiny rat Trinomys eliasi (Echimyidae) from Rio de Janeiro, Brazil

Trinomys eliasi is an endangered species of spiny rat endemic to a small area in the lowlands of Rio de Janeiro state (Brazil). Limited data on its biology and variation are available for designing conservation policies. Here, we provide data on genetic variation of T. eliasi, elucidating aspects of its evolutionary differentiation based on analysis of cytochrome b DNA. Our findings showed that T. eliasi diverged from its sister species T. paratus in the early Pleistocene or late Pliocene (∼2.5 million years ago [mya]). Two T. eliasi mitochondrial lineages diverged in the early Pleistocene (∼2.1 mya) and are currently separated by a large river and Holocene areas previously occupied by a vast Pleistocene internal sea, which may have operated as a historical barrier between populations. The haplotypes of the southern lineage diverged relatively late in the Pleistocene (∼0.6 mya), and diversity of this lineage is not equally distributed across the landscape, but rather, it appears to be concentrated in the rainiest areas, which contain major forest remnants. This region should be considered a priority for conservation. In the northern extreme of Rio de Janeiro state, we found an isolated, highly divergent T. eliasi lineage, which deserves further investigation. This work highlights the need for fine-scale studies of genetic variation in endangered species for the preservation of their evolutionary diversity.

Systematics and Acceleration of Cranial Evolution in Cerradomys (Rodentia, Cricetidae, Sigmodontinae) of Quaternary Sandy Plains in Southeastern Brazil

The genus Cerradomys, comprising eight species, is distributed mainly in transitional, dry, open and inland South American biomes like Caatinga, Cerrado, and Chaco. However, Cerradomys goytaca is restricted to very harsh ecosystems along the Quaternary coast sandy plains (restingas) of the Rio de Janeiro and Espírito Santo states, in southeastern Brazil. Cytochrome b and IRBP DNA data were used for elucidating the phylogenetic relationships of Cerradomys and estimating the time of divergence of different evolutionary lineages, while morphometric analyses were carried out for analyzing the rate of phenotypic evolution. Our findings showed that the first speciation events occurred in the Pliocene and early Pleistocene, leading to the C. marinhus, C. maracajuensis, and C. scotti distributed in central and western Brazil while species from eastern Brazil (C. langguthi, C. vivoi, C. subflavus, and C. goytaca) originated in the middle to late Pleistocene. Cerradomys goytaca populations diverged from inland C. subflavus ca. 0.29 MYBP with an accelerated rate of phenotypic evolution resulting in unique craniometric attributes, likely due to the strong selective pressures imposed by harsh habitats.

Disease-associated mitochondrial mutations and the evolution of primate mitogenomes

Several human diseases have been associated with mutations in mitochondrial genes comprising a set of confirmed and reported mutations according to the MITOMAP database. An analysis of complete mitogenomes across 139 primate species showed that most confirmed disease-associated mutations occurred in aligned codon positions and gene regions under strong purifying selection resulting in a strong evolutionary conservation. Only two confirmed variants (7.1%), coding for the same amino acids accounting for severe human diseases, were identified without apparent pathogenicity in non-human primates, like the closely related Bornean orangutan. Conversely, reported disease-associated mutations were not especially concentrated in conserved codon positions, and a large fraction of them occurred in highly variable ones. Additionally, 88 (45.8%) of reported mutations showed similar variants in several non-human primates and some of them have been present in extinct species of the genus Homo. Considering that recurrent mutations leading to persistent variants throughout the evolutionary diversification of primates are less likely to be severely damaging to fitness, we suggest that these 88 mutations are less likely to be pathogenic. Conversely, 69 (35.9%) of reported disease-associated mutations occurred in extremely conserved aligned codon positions which makes them more likely to damage the primate mitochondrial physiology.

Cellular Scaling Rules for the Brains of Marsupials: Not as “Primitive” as Expected

In the effort to understand the evolution of mammalian brains, we have found that common relationships between brain structure mass and numbers of nonneuronal (glial and vascular) cells apply across eutherian mammals, but brain structure mass scales differently with numbers of neurons across structures and across primate and nonprimate clades. This suggests that the ancestral scaling rules for mammalian brains are those shared by extant nonprimate eutherians - but do these scaling relationships apply to marsupials, a sister group to eutherians that diverged early in mammalian evolution? Here we examine the cellular composition of the brains of 10 species of marsupials. We show that brain structure mass scales with numbers of nonneuronal cells, and numbers of cerebellar neurons scale with numbers of cerebral cortical neurons, comparable to what we have found in eutherians. These shared scaling relationships are therefore indicative of mechanisms that have been conserved since the first therians. In contrast, while marsupials share with nonprimate eutherians the scaling of cerebral cortex mass with number of neurons, their cerebella have more neurons than nonprimate eutherian cerebella of a similar mass, and their rest of brain has fewer neurons than eutherian structures of a similar mass. Moreover, Australasian marsupials exhibit ratios of neurons in the cerebral cortex and cerebellum over the rest of the brain, comparable to artiodactyls and primates. Our results suggest that Australasian marsupials have diverged from the ancestral Theria neuronal scaling rules, and support the suggestion that the scaling of average neuronal cell size with increasing numbers of neurons varies in evolution independently of the allocation of neurons across structures.

Changes in selection intensity on the mitogenome of subterranean and fossorial rodents respective to aboveground species

Several rodent lineages independently acquired the ability to dig complex networks of tunnels where fossorial and subterranean species spend part or their whole life, respectively. Their underground lifestyles imposed harsh physiological demands, presumably triggering strong selective pressures on genes involved in energy metabolism like those coding for mitochondrial proteins. Moreover, underground lifestyles must have increased inbreeding and susceptibility to population bottlenecks as well as restricted migration, leading to small effective population size (Ne) that, in turn, must have reduced the effectiveness of selection. These stringent environmental conditions and small Ne might be still operating as antagonist factors of selection efficacy in these rodents. In this report, we tested, in a phylogenetic framework, how the intensity of selection on protein-coding mitochondrial genes (mt-genes) fluctuated along the evolution of fossorial and subterranean rodents respective to aboveground lineages. Our findings showed significant selection relaxation in most mt-genes of subterranean hystricomorphs (African mole-rats, tuco-tucos, and coruro), while only in three mt-genes of fossorial hystricomorphs (degus, red vizcacha rat, and fossorial spiny rats) selection efficacy was strongly reduced, probably due to demographic constraints. Conversely, selection intensification was found to have occurred in three mt-genes in fossorial sciuromorphs (ground squirrels, chipmunks, marmot, and allies). Our findings indicated that evolution of mitogenomes in fossorial and, mainly, in subterranean rodents was a complex output of a balance between intense ecological and physiological pressures, together with demographic constraints leading to genetic drift that, in turn, might have resulted in relaxed selection in hystricomorphs.

Changes in Ontogenetic Allometry and their Role in the Emergence of Cranial Morphology in Fossorial Spiny Rats (Echimyidae, Hystricomorpha, Rodentia)

All evolutionary modifications of morphology in adult animals presuppose occurrence of changes in developmental programming. While some developmental changes affect rates of trait growth during the entire ontogeny, other developmental changes modify timing and growth rates during limited stages, usually in early development. Identifying which kind of these alterations are more frequent during evolution is crucial for understanding processes influencing the emergence of phenotypic diversity and specializations. Here, we used an allometric approach to assess the relative impact of these two kinds of ontogenetic alterations in the emergence of specialized skull morphology in fossorial spiny rats, comparing them with closely related, more generalist, terrestrial species. Univariate and multivariate analyses of adult shape consistently showed that fossorial spiny rats remarkably differed from terrestrial species, mainly by showing shorter and lower rostrum and more expanded auditory bullae, a set of traits usually considered specializations for life underground. Slopes and elevations of allometric trajectories of cranial traits were estimated for each species and compared with Analysis of Covariance, Likelihood-ratio tests, and Analysis of Variance based on Burnaby-corrected data. These tests showed that changes in allometric elevations were more recurrent during evolution and more congruent with the change in adult morphology than change in allometric slopes. These findings indicated that developmental changes modifying timing and growth rates during limited stages of early development were more frequent than alterations of trait covariation patterns along the entire ontogeny. This kind of developmental change accounts for a large effect on diversification of adult morphology and emergence of burrowing specializations in spiny rats.

The human retinoblastoma susceptibility gene (RB1): an evolutionary story in primates

The tumor suppressor gene RB1 (Human Retinoblastoma Susceptibility Gene) plays a prominent role in normal development, gene transcription, DNA replication, repair, and mitosis. Its complete biallelic dysfunction in retinoblasts is the main cause of retinoblastoma in the human. Although this gene has been evolutionary conserved, comparisons between the reference and human RB1 coding region with its counterparts in 19 non-human primates showed 359 sites where nucleotide replacements took place during the radiation of these species. These resulted in missense substitutions in 97 codons, 91 of which by amino acids with radically different physicochemical properties. Several in frame deletions and two insertions were also observed in the N-terminal region of the pRB protein where the highest number of amino acid substitutions and radical amino changes were found. Fifty-six codons were inferred to be under negative selection and five under positive selection. Differences in codon usage showed evident phylogenetic signals, with hominids generally presenting higher indices of codon bias than other catarrhines. The lineage leading to platyrrhines and, within platyrrhines, the lineage leading to Saimiri boliviensis showed a high rate of nucleotide substitutions and amino acids. Finally, several RB1 alterations associated to retinoblastoma in the human were present in several non-human primates without an apparent pathological effect.