Evolution Of Rodents Research Articles

First virtual endocast description of an early Miocene representative of Pan-Octodontoidea (Caviomorpha, Hystricognathi) and considerations on the early encephalic evolution in South American rodents

AbstractThe study of the cranial endocast provides valuable information to understand the behavior of an organism because it coordinates sensory information and motor functions. In this work, we describe for the first time the anatomy of the encephalon of an early Miocene pan-octodontoid caviomorph rodent (Prospaniomys priscus Ameghino, 1902) found in the Argentinean Patagonia, based on a virtual 3D endocast. This fossil rodent has an endocast morphology here considered ancestral for Pan-Octodontoidea and other South American caviomorph lineages, i.e., an encephalon with anteroposteriorly aligned elements, mesencephalon dorsally exposed, well-developed vermis of the cerebellum, and rhombic cerebral hemispheres with well-developed temporal lobes. Prospaniomys Ameghino, 1902 also has relatively small olfactory bulbs, large paraflocculi of the cerebellum, and low endocranial volume and degree of neocorticalization. Its encephalization quotient is low compared with Paleogene North American and European noncaviomorph rodents, but slightly higher than in several late early and late Miocene caviomorphs. Paleoneurological anatomical information supports the hypothesis that Prospaniomys was a generalist caviomorph rodent with terrestrial habits and enhanced low-frequency auditory specializations. The scarce paleoneurological information indicates that several endocast characters in caviomorph rodents could change with ecological pressures. This work sheds light on the anatomy and evolution of several paleoneurological aspects of this particular group of South American rodents.

Endemic rodents of Hispaniola: biogeography and extinction timing during the Holocene

Hispaniola is the second-largest island in the West Indies bioregion and along with Cuba is considered the cradle of Greater Antillean rodent evolution and diversification. While the fossil record in Hispaniola includes ten extinct species of late Quaternary rodents, only a single species, the Hispaniola hutia (Plagiodontia aedium), is extant on the island. Changes in climate and anthropogenic effects have been suggested as drivers for these extinctions, but there are few radiometric dates associated with these fossils which limits our understanding of the timing of rodent extinctions on Hispaniola relative to shifts in Holocene climate and major events in human settlement and colonization. We report nine new AMS radiocarbon dates for six endemic rodents of Hispaniola that, when coupled with previously reported dates, provide last occurrence records for eight of the ten extinct rodent species there. Results show that Hispaniola rodent extinction occurred in a series of episodes, with more than half (63.6%) surviving into the late Holocene (4200 cal BP to present), postdating the initial arrival of Ceramic Age Indigenous groups, with extinction likely only after European colonization. This pattern in Hispaniola is consistent with what recent studies have found on the timing of extinction of other terrestrial vertebrates in the West Indies. Results from analysis of stable isotopes of fossil bone suggest that the extinction of endemic rodents from Hispaniola largely also postdate habitat changes following the onset of drier conditions in the late Holocene, suggesting that while climate may have shaped the geographic distribution of species, it probably played a minimal direct role in their extinctions on Hispaniola.

Frontoparietal connectivity as a product of convergent evolution in rodents and primates: functional connectivity topologies in grey squirrels, rats, and marmosets

Robust frontoparietal connectivity is a defining feature of primate cortical organization. Whether mammals outside the primate order, such as rodents, possess similar frontoparietal functional connectivity organization is a controversial topic. Previous work has primarily focused on comparing mice and rats to primates. However, as these rodents are nocturnal and terrestrial, they rely much less on visual input than primates. Here, we investigated the functional cortical organization of grey squirrels which are diurnal and arboreal, thereby better resembling primate ecology. We used ultra-high field resting-state fMRI data to compute and compare the functional connectivity patterns of frontal regions in grey squirrels (Sciurus carolinensis), rats (Rattus norvegicus), and marmosets (Callithrix jacchus). We utilized a fingerprinting analysis to compare interareal patterns of functional connectivity from seeds across frontal cortex in all three species. The results show that grey squirrels, but not rats, possess a frontoparietal connectivity organization that resembles the connectivity pattern of marmoset lateral prefrontal cortical areas. Since grey squirrels and marmosets have acquired an arboreal way of life but show no common arboreal ancestor, the expansion of the visual system and the formation of a frontoparietal connectivity architecture might reflect convergent evolution driven by similar ecological niches in primates and tree squirrels.

Multivariate analyses of skull morphology inform the taxonomy and evolution of geomyoid rodents.

Morphological analyses are critical to quantify phenotypic variation, identify taxa, inform phylogenetic relationships, and shed light on evolutionary patterns. This work is particularly important in groups that display great morphological disparity. Such is the case in geomyoid rodents, a group that includes 2 of the most species-rich families of rodents in North America: the Geomyidae (pocket gophers) and the Heteromyidae (kangaroo rats, pocket mice, and their relatives). We assessed variation in skull morphology (including both shape and size) among geomyoids to test the hypothesis that there are statistically significant differences in skull measurements at the family, genus, and species levels. Our sample includes 886 specimens representing all geomyoid genera and 39 species. We used the geometric mean to compare size across taxa. We used 14 measurements of the cranium and lower jaw normalized for size to compare shape among and within taxa. Our results show that skull measurements enable the distinction of geomyoids at the family, genus, and species levels. There is a larger amount of size variation within Geomyidae than within Heteromyidae. Our phylomorphospace analysis shows that the skull shape of the common ancestor of all geomyoids was more similar to the common ancestor of heteromyids than that of geomyids. Geomyid skulls display negative allometry whereas heteromyid skulls display positive allometry. Within heteromyids, dipodomyines, and non-dipodomyines show significantly different allometric patterns. Future analyses including fossils will be necessary to test our evolutionary hypotheses.

The genes from the pseudoautosomal region 1 (PAR1) of the mammalian sex chromosomes: Synteny, phylogeny and selection

Sex chromosomes recombine restrictly in their homologous area, the pseudoautosomal region (PAR), represented by PAR1 and PAR2, which behave like an autosome in both pairing and recombination. The PAR1, common to most of the eutherian mammals, is located at the terminus of the sex chromosomes short arm and exhibit recombination rates ~20 times higher than the autosomes. Here, we assessed the interspecific evolutionary genomic dynamics of 15 genes of the PAR1 across 41 mammalian genera (representing six orders). The strong negative selection detected in most of the assessed groups reinforces the presence of evolutionary constraints, imposed by the important function of the PAR1 genes. Indeed, mutations in these genes are associated with various diseases in humans, including stature problems (Klinefelter Syndrome), leukemia and mental diseases. Yet, a few genes exhibiting positive selection (ω-value >1) were depicted in Rodentia (ASMT and ZBED1) and Primates (CRLF2 and CSF2RA). Rodents have the smallest described PAR1, while that of simian primates/humans underwent a 3 to 5 fold size reduction. The assessment of the PAR1 genes synteny revealed differences among the mammalian species, especially in the Rodentia order where chromosomic translocations from the sex chromosomes to the autosomes were observed. Such syntenic changes may be an evidence of the rapid evolution in rodents, as previous referred in other papers, also depicted by their increased branch lengths in the phylogenetic analyses. Concluding, we suggest that genome migration is an important factor influencing the evolution of mammals and may result in changes of the selective pressures operating on the genome.

Skull morphological evolution in Malagasy endemic Nesomyinae rodents.

Madagascar is a large island to the south-east of Africa and in many ways continental in size and ecological complexity. Here we aim to define how skull morphology of an endemic and monophyletic clade of rodents (sub-family Nesomyinae), that show considerable morphological variation, have evolved and how their disparity is characterized in context of the geographical and ecological complexity of the island. We performed a two-dimensional geometric morphometric analysis on 370 dorsal and 399 ventral skull images of 19 species (comprising all nine extant endemic genera) and tested the influence of three ecological parameters (climate, locomotor habitat and nychthemeral cycle) in a phylogenetic context on size and shape. The results indicate that skull shape appears to importantly reflect phylogeny, whereas skull size does not carry a significant phylogenetic signal. Skull shape is significantly influenced by climate while, skull size is not impacted by any of the ecological factors tested, which is controversial to expectations in an insular context. In conclusion, Nesomyinae must have evolved under unusual types of local constraints, preventing this radiation from demonstrating strong ecological release.

Look at those feet! Early evolution of rodents and lagomorphs

Look at those feet! Early evolution of rodents and lagomorphs

Secondary loss of miR-3607 reduced cortical progenitor amplification during rodent evolution.

The evolutionary expansion and folding of the mammalian cerebral cortex resulted from amplification of progenitor cells during embryonic development. This process was reversed in the rodent lineage after splitting from primates, leading to smaller and smooth brains. Genetic mechanisms underlying this secondary loss in rodent evolution remain unknown. We show that microRNA miR-3607 is expressed embryonically in the large cortex of primates and ferret, distant from the primate-rodent lineage, but not in mouse. Experimental expression of miR-3607 in embryonic mouse cortex led to increased Wnt/β-catenin signaling, amplification of radial glia cells (RGCs), and expansion of the ventricular zone (VZ), via blocking the β-catenin inhibitor APC (adenomatous polyposis coli). Accordingly, loss of endogenous miR-3607 in ferret reduced RGC proliferation, while overexpression in human cerebral organoids promoted VZ expansion. Our results identify a gene selected for secondary loss during mammalian evolution to limit RGC amplification and, potentially, cortex size in rodents.

Dispersal and early evolution of the first modern cricetid rodents in Western Europe: new data from the Vallès-Penedès Basin (Catalonia)

Modern cricetids originated in Asia and dispersed into Western Europe by the end of the early Miocene, where they quickly became major components of the rodent faunas. Here we review the early Miocene rodent record of the genera Democricetodon Fahlbusch, 1964 and Megacricetodon Fahlbusch, 1964 in the Vallès-Penedès Basin (Catalonia, Spain). Democricetodon is represented by four species in the studied sites (D. hispanicus Freudenthal, 1967, D. cf. decipiens (Freudenthal & Daams, 1988), D. gracilis Fahlbusch, 1964 and a large-sized undetermined species) and Megacricetodon by one (M. primitivus (Freudenthal, 1963)). The cricetid succession bears several similarities with that of the nearby Calatayud-Montalbán Basin (East-Central Spain) to the point that the same detailed local biostratigraphy could be extended to the Catalan basin. The rare presence of certain Democricetodon species (D. gracilis) and other small mammal taxa also reveal affinities with regions beyond the Iberian Peninsula and indicate that the Vallès-Penedès Basin was more humid and forested than inland Iberian basins during the early Miocene.

Tempo and Mode: Evidence on a Protracted Split From a Dense Fossil Record

Fossil records generally inform paleobiologists about extinct taxa and rates of evolution measured at the scale of millions of years. Good records that are densely sampled through time can reveal species level details such as longevity in local sections. Yet fossil data normally do not address details of lineage microevolution because the density through time of lineage sampling is insufficient to perceive patterns at a precision finer than 106 years in most cases. This study concerns details of a splitting event in the evolution of murine rodents, an event for which multiple fossil samples dated to a precision of 105 years fortuitously document the tempo and mode of origin of sister species, the stems of two extant tribes of mice. Evolution of early Murinae in the northern part of the biogeographically restricted Indian subcontinent between 11.6 and 10.5 Ma involved cladogenesis of two crown taxa, the extant tribes Murini and Arvicanthini. Large samples of fossil rodent teeth document their divergence from a common morphological pool. Definitive basal Murini and Arvicanthini at 10.5 Ma are similar in size and differ by subtle features of the dentition. Those features occur sporadically in the common pool of older fossil teeth at 11.2, 11.4, and 11.6 Ma as inconsistent polymorphisms. Interpreted as a single lineage in the 11.6–11.2 Ma interval, variability of this abundant murine incorporated the roots of the two crown tribes. The pattern through time suggests morphological stasis for several hundred thousand years prior to splitting. This special case informs us on one example of evolution and shows that the tempo of splitting evolution in some cases may be measured in hundreds of thousands of years, followed by stasis once daughter species have differentiated morphologically.

Adaptive evolution of β-globin gene in subterranean in South America octodontid rodents.

The convergent evolution of subterranean rodents is an excellent model to study how natural selection operates and the genetic bases of these adaptations, but the study on the different taxa has been very uneven and still insufficient. In the octodontoid caviomorph rodent superfamily there are two independent lineages where they have recently evolved into totally underground lifestyles: the genera Ctenomys (tuco-tucos) and Spalacopus (coruro). The underground habitat is characterized by an hypoxic and hypercapnic atmosphere, thus gas exchange is one of the most important challenges for these animals. The invasion of the underground niche could have modified the selective regimes of proteins involved in the respiration and transport of O2 of these rodents, positively selecting mutations of higher affinity for O2. Here we examine the sequence variation in the beta globin gene in these two lineages, within a robust phylogenetic context. Using different approaches (classical and Bayesian maximum likelihood (PAML/Datamonkey) and alternatives methods (TreeSAAP)) we found at least three sites with evidence of positive selection in underground lineages, especially the basal branch that leads to the Octodontidae family and the branch that leads to the coruro, suggesting some adaptive changes to the underground life. We also found a convergence with another underground rodent, which cannot be identified by the above methods.

Noncoding RNA, Intragenomic Conflict, and Rodent SRY Evolution

The sex-determining gene SRY has undergone rapid evolution in rodents. Curiously, a new study by Miyawaki et al. reveals that a recently evolved SRY gene sequence antagonizes SRY protein stability, necessitating splicing of a novel intron. Other data suggest that this troublesome gene region has noncoding RNA functions, possibly related to conflict between sex chromosomes.

Tandem Fusions in Evolution of Ethiopian Endemic Rodents

The species number has been strikingly increasing in recent current works on Ethiopian endemic rodents, which to a great extent is due to genomic studies including the karyotype discoveries. Here, the diploid number 2N = 52 is defined anew for the genus Stenocephalemys, endemic to the Ethiopian Highlands, where four karyotypes with 2N values of 54, 50 and 46 were so far described for four taxa. The new karyotype (S. “pseudogriseicauda”) combines into a nearly full series with other 2Ns (except the not yet found 2N = 48) within the genus and shows one interspecific chromosome rearrangement associated with the tandem fusion, in the direction 2N = 54 to 2N = 52. Together with the earlier detection of tandem fusions between karyotypes with 2N = 46 (S. albipes) and 2N = 54 (S. albocaudatus, S. griseicauda), this rodent taxonomic group presents an interesting case for the phenomenon of karyotypic orthoselection in an intrageneric phyletic line via the reoccurence of such characteristic chromosomal rearrangements as tandem fusions.

Battle of the Sex Chromosomes: Competition between X and Y Chromosome-Encoded Proteins for Partner Interaction and Chromatin Occupancy Drives Multicopy Gene Expression and Evolution in Muroid Rodents.

Transmission distorters (TDs) are genetic elements that favor their own transmission to the detriments of others. Slx/Slxl1 (Sycp3-like-X-linked and Slx-like1) and Sly (Sycp3-like-Y-linked) are TDs, which have been coamplified on the X and Y chromosomes of Mus species. They are involved in an intragenomic conflict in which each favors its own transmission, resulting in sex ratio distortion of the progeny when Slx/Slxl1 versus Sly copy number is unbalanced. They are specifically expressed in male postmeiotic gametes (spermatids) and have opposite effects on gene expression: Sly knockdown leads to the upregulation of hundreds of spermatid-expressed genes, whereas Slx/Slxl1-deficiency downregulates them. When both Slx/Slxl1 and Sly are knocked down, sex ratio distortion and gene deregulation are corrected. Slx/Slxl1 and Sly are, therefore, in competition but the molecular mechanism remains unknown. By comparing their chromatin-binding profiles and protein partners, we show that SLX/SLXL1 and SLY proteins compete for interaction with H3K4me3-reader SSTY1 (Spermiogenesis-specific-transcript-on-the-Y1) at the promoter of thousands of genes to drive their expression, and that the opposite effect they have on gene expression is mediated by different abilities to recruit SMRT/N-Cor transcriptional complex. Their target genes are predominantly spermatid-specific multicopy genes encoded by the sex chromosomes and the autosomal Speer/Takusan. Many of them have coamplified with not only Slx/Slxl1/Sly but also Ssty during muroid rodent evolution. Overall, we identify Ssty as a key element of the X versus Y intragenomic conflict, which may have influenced gene content and hybrid sterility beyond Mus lineage since Ssty amplification on the Y predated that of Slx/Slxl1/Sly.

A new late Miocene Anomalomys species from western Ukraine with implications for the diversity and evolution of anomalomyid rodents in Eastern Europe

ABSTRACT Anomalomyid rodents first appeared in the fossil record of Europe in the early Miocene being represented by three small-sized species of the genus Anomalomys (A. aliveriensis, A. minor, and A. minutus). During the middle and late Miocene, they were replaced by larger forms (A. gaudryi, A. rudabanyensis, A. gaillardi) with a simpler tooth morphology pattern. Here we describe a new medium-sized species of Anomalomys – A. grytsivensis sp. n. – from the early late Miocene locality Grytsiv in western Ukraine. The exceptional large sample size (ca. 500 specimens including maxillae and mandibles with dentition, isolated teeth) are confined to early Vallesian, MN9. The new species is characterised by the presence of brachio-hypselodont molars, separation of the anteroconid from the protoconid and mesoconid on m1 and m2, as well as the connection of mesoconid and protoconid to the hypoconid. Anomalomys grytsivensis sp. n. demonstrates a variable set of morphotypes and can be regarded as a transitional form between Anomalomys and Prospalax. Fossorial activity could be inherent to Anomalomys (as for Spalax), however it hardly played an important role in the life of these rodents because of their small and narrow incisors which could only occasionally be used as a digging tool.

Rodent Suborders

Abstract For two hundred years the status of rodent suborders has been unstable. What are the natural groupings of extant rodent families? The formal recognition of rodent suborders has remained challenging and consensus has been elusive. Classically conceived rodent suborders are widely viewed as artificial, but no universally accepted classification has emerged to reflect the major features of rodent evolution. Over the last two decades molecular studies have established that extant rodents comprise three monophyletic clades. We review the molecular basis for these groups and recognize them as taxonomic units: Suborder Ctenohystrica Huchon et al., 2000, Suborder Supramyomorpha D’Elía et al., 2019, and a group of families clustered with Sciuridae. The latter differs from Sciuromorpha as traditionally conceived because the suborder includes Aplodontiidae but excludes Castoridae. We review morphological character complexes that are distributed broadly within these three clades, name the third group Eusciurida, new suborder, and find this three-fold division of extant Rodentia to reflect well the major features of rodent phylogeny. That some morphological features do not characterize all families within suborders, or are not unique to individual suborders, indicates major parallel innovations and reversals in rodent evolution. These incongruent morphologies invite future study.

Shape Feature Extraction Methods of Rodents in the Field Based on Machine Vision

In order to obtain the shape features of rodents from the field, a feature extraction scheme based on machine vision was proposed. We design an experimental device with a camera. The camera placed on the top of the device to get the rodent image. After thresholding rodent image based on the global value, we get the binary image, and then the morphological erosion and dilation operation are used to denoise, and the contour are detected by the 8 adjacent pixels of a point. Chain code analysis method is used to track the contour. Multi-contour tracking extraction method is used to remove the non-rodent region. Based on the shape of the rodent tail that is slenderer than the body, we split the rodent’s tail from the body on the precise contour image. The length of the tail, the length of the body, the height of the body, the proportions of the tail and the body are extract based on contour analysis. Experiments show that this method can extract shape features of rodents accurately. It can provide basic data for analyzing the life habits and population evolution of field rodents.

Correlation of Pliocene and Pleistocene fossil assemblages from the central and eastern United States: toward a continental rodent biochronology

ABSTRACT The ubiquitous presence and rapid evolution of rodents lend this group to the development of a correlational scheme for United States Cenozoic continental fossil deposits, equivalent to the later Cenozoic section of European MN zones. Expanding on earlier work in the Meade Basin of southwestern Kansas and Florida, Pliocene and Pleistocene mammal assemblages from the northern and southern Great Plains and the eastern United States are correlated based on rodent biostratigraphy. Eleven rodent zones (RZs) are constructed for the last 5 million years based on a new database including all rodent species assemblages during the study period. In addition to the 11 refined RZs that aid in temporal sequencing of unknown rodent assemblages, three broader biozones are recognised, including an early period characterised by the Promimomys immigration event and Hemphillian holdovers, a longer, relatively warm Pliocene to early Pleistocene period dominated by primitive cricetids and archaic arvicolids, and a final zone spanning the last two million years defined by the immigration and radiation of hypselodont Microtus and large, dentally advanced species of the cotton rat, Sigmodon. Modern rodent communities are established in the later part of Biozone 3, between about 0.6–0.3 Ma.

Convergent reduction of V1R genes in subterranean rodents

BackgroundVomeronasal type 1 receptor genes (V1Rs) are expected to detect intraspecific pheromones. It is believed that rodents rely heavily on pheromonal communication mediated by V1Rs, but pheromonal signals are thought to be confined in subterranean rodents that live in underground burrows. Thus, subterranean rodents may show a contrasting mode of V1R evolution compared with their superterranean relatives.ResultsWe examined the V1R evolution in subterranean rodents by analyzing currently available genomes of 24 rodents, including 19 superterranean and 5 subterranean species from three independent lineages. We identified a lower number of putatively functional V1R genes in each subterranean rodent (a range of 22–40) compared with superterranean species (a range of 63–221). After correcting phylogenetic inertia, the positive correlation remains significant between the small V1R repertoire size and the subterranean lifestyle. To test whether V1Rs have been relaxed from functional constraints in subterranean rodents, we sequenced 22 intact V1Rs in 29 individuals of one subterranean rodent (Spalax galili) from two soil populations, which have been proposed to undergo incipient speciation. We found 12 of the 22 V1Rs to show significant genetic differentiations between the two natural populations, indicative of diversifying selection.ConclusionOur study demonstrates convergent reduction of V1Rs in subterranean rodents from three independent lineages. Meanwhile, it is noteworthy that most V1Rs in the two Spalax populations are under diversifying selection rather than relaxed selection, suggesting that functional constraints on these genes may have retained in some subterranean species.

Dental Variation in a Collection of Lemmiscus curtatus from the Northern Plains of Southern Saskatchewan: Implications for Morphological Evolution

We provide the first documentation of morphological variation in the lower first molar (m1) of Lemmiscus curtatus from southern Canada. A total of 370 specimens were obtained from owl pellets taken from 4 localities in southern Saskatchewan. The 4 most common morphotypes are, in order of descending relative abundance, molars with 5 closed triangles and a well-developed but widely open sixth triangle, molars with 5 closed triangles and a sixth triangle that is pinched at the confluence of the anterior cap, molars with 5 closed triangles and incipient closure of the sixth triangle from the anterior cap, and specimens with 6 closed triangles. As is true of other modern populations of L. curtatus, the samples from Saskatchewan include no morphotypes with only 4 closed triangles. This collection is notable for the relatively high proportion of specimens with pinched, incipient, or full closure of a sixth triangle on the m1, and it also highlights the complex dynamics of dental evolution in arvicoline rodents.