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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.

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.

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 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.

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.

Pelvic morphology in mammals is shaped by several factors, including the functional commitment with parturition. Due to this, some mammalian clades, like primates, show a detectable evolutionary relationship between the magnitude of pelvic sexual dimorphism and cranial morphology of neonates. However, this correlation is less understood within the most diversified mammalian order, Rodentia. The present study aims to describe the general patterns of sexual dimorphism in pelvic shape among Neotropical spiny rats (Echimyidae), assessing its hypothesized coevolution with cranial morphology. We investigated the main sources of sexual variation in pelvic shape among 12 echimyid taxa using linear morphometry and subsequently tested the phylogenetically controlled correlation between male and female pelvic morphologies and craniometric variation. Results reveal that pelvic sexual dimorphism is concentrated in the pubis, with females showing a shorter and thicker pubic symphysis and a thinner cranial pubic ramus than males, a pattern already reported in other mammals and evidently related to obstetric demands. An evolutionary association was found between the intensity of pelvic femininization, the increase in pelvic sexual dimorphism, and the acquisition of relatively large crania and relatively inflated braincases; all of these traits are notably developed in the semi-fossorial broad-headed spiny rat, Clyomys laticeps . We argue that selection on the pelvis of female spiny rats, associated with their cranial morphologies and constraints linked to locomotory specializations, probably resulted in a correlated selective response in the pelvis of males. Our findings suggest that the magnitude of pelvic sexual dimorphism in echimyids is likely associated with obstetric demands imposed by cranial morphology.

Locomotion, as a fundamental function in mammals directly associated with the use of ecological resources, is expected to have anatomical structures functionally committed that evolved under intense selective pressure, possibly carrying specializations for different locomotor habits. Among caviomorph rodents, the family Echimyidae stands out for having the greatest species richness, with relatively well-resolved phylogenetic relationships, wide variation in body mass, and remarkable diversity of locomotor habits, including arboreal, scansorial, semi-aquatic, semifossorial, and terrestrial forms. Thus, Echimyidae constitutes a promising model for understanding how phylogenetic, allometric, and ecological factors affect the evolution of postcranial structures directly linked to locomotor function. We investigated the influence of these three factors on scapular and humeral morphological variation in 38 echimyid species using two-dimensional geometric morphometry and phylogenetically informed comparative methods. Scapular and humeral shape variation had a low correlation with body mass and structure size, conveying a small or negligible allometric effect. Conversely, a significant moderate to strong phylogenetic signal was detected in both structures, suggesting that an important part of their morphometric variation results from shared evolutionary history. Notably, morphological variation of the scapula was extensively structured by phylogeny, without the marked influence of locomotor habits, suggesting that its shape may be a suitable taxonomic marker. Finally, locomotor habits were important in structuring the morphological variation of the humerus. Our results suggest that the morphologies of the scapula and humerus, despite being anatomically and functionally interconnected, were differentially shaped by ecological factors associated with locomotor habits.

The evolution of subterranean and fossorial rodents has been linked to the Neogene climatic shift to xeric conditions leading to open vegetation, like prairies and grasslands; most modern subterranean rodents occur in arid and open areas. Among South American spiny rats (family Echimyidae), the subfamily Euryzygomatomyinae includes both fossorial ( Clyomys and Euryzygomatomys ) and ambulatorial ( Trinomys ) genera, some of them endemic to open vegetated areas and other ones restricted to forested regions. The closely related genus Carterodon is also a fossorial rodent endemic to open vegetated areas. If the open environments constitute a determinant factor triggering the evolution of fossoriality in these spiny rats, it is expected that the fossorial lineages evolving since the Miocene in open environments ( Carterodon sulcidens and Clyomys laticeps ) show morphologies more specialized for digging than those currently restricted to Atlantic Forest habitats ( Euryzygomatomys spinosus ). Moreover, it is likely that Trinomys species specialized for xeric environments ( T. albispinus and T. yonenagae ) show incipient adaptations for fossoriality. The appendicular skeleton of three fossorial and five ambulatorial echimyid species were morphometrically analyzed with multivariate statistical approaches in order to test these presuppositions. The analyses showed that the appendicular morphology of T. yonenagae and T. albispinus , in comparison with the Atlantic Forest Trinomys species, and of C. sulcidens and C. laticeps in relation to E. spinosus are more adapted to scratch-digging activities, corroborating the hypothesis that open environments favor the evolution of fossoriality in spiny rats.

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.

Complex cross-talk occurs between gastrointestinal nematodes and gut symbiotic microbiota, with consequences for animal metabolism. To investigate the connection between methane production and endoparasites, this study evaluated the effect of mixed infection with Haemonchus contortus and Trichostrongylus colubriformis on methanogenic and methanotrophic community in rumen microbiota of lambs using shotgun metagenomic and real-time quantitative PCR (qPCR). The rumen content was collected from six Santa Inês lambs, (7 months old) before and after 42 days infection by esophageal tube. The metagenomic analysis showed that the infection affected the microbial community structure leading to decreased abundance of methanotrophs bacteria, i.e. α-proteobacteria and β-proteobacteria, anaerobic methanotrophic archaea (ANME), protozoa, sulfate-reducing bacteria, syntrophic bacteria with methanogens, geobacter, and genes related to pyruvate, fatty acid, nitrogen, and sulfur metabolisms, ribulose monophosphate cycle, and Entner–Doudoroff Pathway. Additionally, the abundance of methanogenic archaea and the mcrA gene did not change. The co-occurrence networks enabled us to identify the interactions between each taxon in microbial communities and to determine the reshaping of rumen microbiome associations by gastrointestinal nematode infection. Besides, the correlation between ANMEs was lower in the animal’s postinfection. Our findings suggest that gastrointestinal parasites potentially lead to decreased methanotrophic metabolism-related microorganisms and genes.