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.     

Evolutionary diversification of spiny rats (genus Trinomys, Rodentia: Echimyidae) in the Atlantic Forest of Brazil

Phylogenetic and phylogeographic relationships within and among species of the Atlantic Forest spiny rat Trinomys (family Echimyidae) were examined using cytochrome b sequence data. Levels of sequence divergence among species of Trinomys are as high as those found among taxa of echimyids that are recognized as different genera. Trinomys contains three distinct monophyletic clades that show a striking concordance with vegetational distribution. Haplotypes of clade 1 are distributed along the coastal margins of southeastern Brazil, following the moist tropical forest. Members of clade 2 are found in the semi-deciduous tropical forest. T. albispinus represents clade 3 and is found in a more xeric vegetation. Estimates of divergence times separating the three clades are very deep and range from 1.6 to 7.4 millions of years, predating the climatic fluctuations of the Pleistocene. Therefore, the proposed Late Pleistocene refugia in the Atlantic Forest cannot account for the divergence of the clades of Trinomys , but most likely shaped the modern distribution of species. The current taxonomy of this group does not reflect the diversity and phylogenetic relationships of the named species. However, morphological characters are congruent with the phylogeny uncovered by the molecular data. An extensive taxonomic rearrangement is suggested, reflecting phylogenetic relationships of monophyletic entities within the genus Trinomys , degree of sequence differences, and morphological diagnosability.     

Ecomorphological diversification among South American spiny rats (Rodentia; Echimyidae): a phylogenetic and chronological approach

The phylogeny of South American spiny rats (Rodentia; Echimyidae) was studied using the exon 28 of the von Willebrand Factor nuclear gene (vWF). Sequences were analysed separately and in combination with a mitochondrial dataset (cyt b, 12S and 16S rRNAs) used in previous publications. The basal polytomy of echimyids was partially resolved and unexpected intergeneric clades were recovered. Thus, the intimate nested position of Myocastor within echimyids is evidenced. A well-supported clade is identified, including all the arboreal genera, and a group formed by Myocastor, Thrichomys, and Proechimys+Hoplomys. The clustering of Euryzygomatomys+Clyomys with Trinomys is also suggested. On the opposite, the phylogenetic position of Capromys as well as the relationships among arboreal genera remain unclear. Molecular divergence times were estimated using a Bayesian relaxed molecular clock and suggest a Middle Miocene origin for most of modern genera. The ecomorphological diversification of echimyids is discussed in the light of these new results and past environmental modifications in South America.     

Evolutionary integration and morphological diversification in complex morphological structures: mandible shape divergence in spiny rats (Rodentia, Echimyidae)

The rodent mandible has become a paradigm for studies on the development and evolution of complex morphological structures. We use a combination of geometric and multivariate morphometric methods in order to assess the correspondence between integration patterns and a priori biological models in the context of evolutionary shape divergence in the mandible of rodents of the family Echimyidae. The correlation of shape distances among operational taxonomic units (individuals, species, genera) in separate morphogenetic components allowed the construction of integration matrices among mandible components for data sets corresponding to varying levels of genetic divergence (intergeneric, interspecific, and intrapopulational). The integration matrices were associated with a priori biological (developmental, genetical, modular) models, and the maximum integration axes (singular warps) were compared with realized axes of maximum interspecific variation (relative warps). The integration pattern and intensity were not stable in data sets with different levels of genetic divergence, and the varying functional demands during the ecological radiation in the family were probably responsible for the differences in observed integration patterns. Developmental and genetic models were significantly associated with the interspecific integration patterns observed, suggesting a role for neutral evolution during the evolutionary divergence of mandible shape. However, directional and stabilizing selection were not discarded as processes responsible for the generation of interspecific integration. The choreography of the morphogenetic components in the mandible is highly flexible and the integrated groups of components can be reorganized depending on functional demands during evolutionary shape changes.     

Morphological evolution in the mandible of spiny rats, genus Trinomys (Rodentia: Echimyidae)

The development and evolution of the rodent mandible have been studied in depth in recent years. The mandible is a complex structure because it consists of six morphogenetic components formed by different condensations of mesenchymal cells. Using recent techniques for the geometric analysis of shape, we have combined developmental information with a powerful quantification of shape variation and an independent estimate of phylogeny (molecular data) to assess the evolutionary patterns of shape change in mandibles of the rodent genus Trinomys . In general, the major trends in shape variation did not agree with the expected phylogenetic pattern. However, for small-scale morphological differences, one species ( T. yonenagae ) was responsible for the lack of association between morphology and molecular divergence. This species is genetically similar to but morphologically different from other Trinomys . The coronoid process was considered to be the most conservative morphogenetic component in the mandible.     

Chromosome differentiation of spiny rats of the genus Proechimys (Rodentia, Echimyidae)]

Karyological analysis of spiny rats of the genus Proechimys revealed four chromosome forms: 2n = 30; 2n = 29; 2n = 28; 2n = 24. 30-chromosome spiny rats are characterized by unique karyotype constitution. 27-chromosome spiny rats from the territory near Iquitos differ from the same of Pucalpa (Ucayali Department) by Y-chromosome structure and banding of long arms with two pairs of autosomes. 24-chromosome rats from the regions mentioned above do not differ in G-banded chromosomes. Diploid chromosome set equal to 29, has a family originated from the parents which had 2n = 30 and 2n = 28 under the laboratory conditions. The absence of clear morphological differentiation, similarity of constituent parts of the karyotype and hybridization possibility point to relatively recent origination of the chromosome forms under study.     

Evolution of South American spiny rats (Rodentia,Echimyidae): the star-phylogeny hypothesis revisited

We analyzed the phylogenetic relationships of echimyid genera based on sequences of the cytochrome b, 12S, and 16S mitochondrial genes. Our results corroborate the monophyly of Octodontoidea and the rapid diversification of echimyid rodents as previously proposed. The analyses indicate that the family Echimyidae, including Myocastor to the exclusion of Capromys, is paraphyletic, since Capromys and Myocastor are well-supported sister-taxa. We therefore suggest the inclusion of both Capromys and Myocastor in the family Echimyidae. Five other suprageneric clades are well supported: Dactylomys+Kannabateomys, Euryzygomatomys+Clyomys, Proechimys+Hoplomys, Mesomys+Lonchothrix, and Makalata+(Echimys+Phyllomys). Trinomys and Thrichomys have no clear close relatives, and Isothrix emerged as sister to Mesomys+Lonchothrix, but with no support. We suggest that most of the cladogenesis leading to the extant echimyid genera probably occurred during the Late Miocene, about eight million years ago.     

Comparative cytogenetics of spiny rats of the genus Proechimys (Rodentia, Echimyidae) from the Amazon region

We made a comparative analysis of the cytogenetics of spiny rat species of the genus Proechimys collected from several sites of the Madeira River basin (Amazonas State, Brazil) and Jari River valley (Pará State, Brazil). Individuals were assigned to three groups based on diploid and fundamental numbers: 2n = 28, FN = 46 (P. cuvieri and P. gr. longicaudatus); 2n = 38, FN = 52 (Proechimys gr. guyannensis), and 2n = 40, FN = 54 (P. gardneri). The nucleolar organizer region (NOR) was interstitial on the long arm of one submetacentric pair, as seen in all species of Proechimys analyzed thus far. However, its position in the karyotype was variable. A duplication of the NOR in one of the homologues was detected in P. gr. longicaudatus from the Aripuan? basin along the mid Madeira. The C-band pattern varied between species and, together with the NOR, allowed the identification of two evolutionary units in P. gr. longicaudatus in the region of the mid Madeira River (cytotypes A and B). The morphology and banding of the sex chromosomes were species specific. A range extension is suggested for the geographic distribution of P. gardneri and P. gr. longicaudatus. Moreover, we suggest that species of Proechimys with 2n = 38 chromosomes are restricted to east of the Negro River and north of the Amazon River. We also revised the published chromosome data available for Proechimys.     

Karyologic evidence of diversification of the genus Thrichomys (Rodentia,Echimyidae)

Karyologic analysis of Thrichomys specimens from different Brazilian localities, in Pantanal, Cerrado and Caatinga biomes, shows different chromosome complements. The 2n = 34, FN = 64 karyotype is found in Mato Grosso do Sul state; the 2n = 30, FN = 54 karyotype in Bahia, Pernambuco, Piauí and Ceará states; the 2n = 30, FN = 56 karyotype in Goiás and Tocantins states, the 2n = 28, FN = 50 karyotype in Minas Gerais state, the 2n = 28, FN = 52 and 2n = 26, FN = 48 karyotypes in Bahia state. Comparisons of G-band patterns allowed the identification of homologies shared by all karyotypes and show that the two karyotypes with the lowest diploid number (2n = 26 and 2n = 28) belong to two different evolutionary lineages. The most proper names for each karyomorphic population are: Thrichomys pachyurus for 2n = 34; Thrichomys apereoides apereoides for 2n = 28, FN = 50; Thrichomys apereoides laurentius for 2n = 30, FN = 54 and Thrichomys inermis for 2n = 26. Two karyotypes (2n = 28, FN = 52 and 2n = 30, FN = 56) could not be attributed to any subspecies. These different karyomorphotypes are allopatric and/or parapatric.     

Differences in ingestive balance of two populations of neotropical Thrichomys apereoides (Rodentia, Echimyidae)

Thrichomys apereoides is widely distributed in the Caatinga, a semi-arid region in Brazil, but is presumed to lack capabilities for water conservation. In the present study, we compared two populations of adult individuals living under different precipitation conditions (700 and 450 mm year(-1)). Animals from the less dry area were twice as heavy as those from the drier locality. Under ad libitum water regimen, there were differences between populations in relative food intake as well as in water intake and urine concentration, but not in normalized body mass water intake. Under short-term water deprivation, both populations presented similar body mass loss. Whereas individuals from the more arid locality maintained food consumption, urine volume and urine osmolality, Thrichomys from the less dry locality reduced food consumption and urine volume. The occurrence of anuria in 75% of animals from this population indicates that the limits of their ability to deal with water shortage had been reached. The morphological and physiological difference and the non-allometric similarities found between the two populations of T. apereoides fulfill the criteria for physiological adaptations to differences in annual rainfall. Our data challenge the hypothesis that the irregularity of annual rainfall in the Caatinga precludes the evolution of adaptations to this semi-arid climate.     

Variation in the skull morphometry of four taxonomic units of Thrichomys (Rodentia: Echimyidae), from different Neotropical biomes

The echimyid rodents of the genus Thrichomys vary considerably in their behavior and feeding ecology, reflecting their occurrence in environments as different as the Caatinga, Cerrado, Pantanal, and Chaco biomes. While the genus was originally classified as monospecific, a number of Thrichomys species have been recognized in recent decades, based on morphometric, cytogenetic, and molecular analyses. While Thrichomys is well studied, the variation found in its cranial morphology is poorly understood, given the taxonomic and ecological complexities of the genus. Using a geometric morphometric approach, we characterized the differences found in the cranial morphology of four Thrichomys taxonomic units, including three established species, Thrichomys apereoides, Thrichomys fosteri, and Thrichomys laurentius, and one operational taxonomic unit (OTU), Thrichomys aff. laurentius. No significant differences were found among these units in cranium size, but significant variation was found in skull shape. The Procrustes distances provided a quantification of the differences in the shape of the skull, with the largest distances being found between T. aff. laurentius and T. fosteri in the dorsal view, and between T. aff. laurentius and T. apereoides in the ventral view. A Discriminant Function Analysis (DFA) with cross-validation determined that the pairings with the highest correct classification were T. aff. laurentius vs. T. apereoides and T. aff. laurentius vs. T. fosteri, in both views. The principal variation in skull shape was found in the posterior region and the zygomatic arch, which may be related to differences in diet.     

Tooth morphology of Echimyidae (Rodentia,Caviomorpha): homology assessments,fossils, and evolution

Echimyidae constitute the most important radiation of caviomorph rodents in the Neotropical region, represented by 20 extant genera and several extinct species. Both in extant and fossil forms, this diversity is reflected by a significant morphological variation found in crown structures of the cheek teeth. Different hypotheses of primary homology have been proposed for these structures, which, in turn, support diverse dental evolutionary hypotheses. In this contribution we inspect the main structures (cusps and lophids) of the lower deciduous teeth and molars in extinct and extant Echimyidae, and establish their topological correspondences. Comparisons with cusps and lophids of Erethizontidae are emphasized. We explore the testing of alternative primary hypotheses of lophid correspondences in a cladistic context. Following a ‘dynamic’ approach, we select the hypothesis of primary homology, which produced the more parsimonious results, and evaluate the evolutionary transformations of the dental characters analysed. In this context, the phylogenetic relationships of living Myocastor coypus (Molina, 1782) with the extinct Tramyocastor and Paramyocastor are tested. Our results indicate that pentalophodonty is the derived condition for the lower molars in Echimyidae, that trilophodonty evolved independently at least three times during the evolutionary history of these rodents, and that tetralophodonty represents the plesiomorphic condition. This study shows that dental evolution in echimyids can be better understood when occlusal structures are expressed as reliably comparable characters, and when fossils are taken into account. © 2012 The Linnean Society of London, Zoological Journal of the Linnean Society, 2012, 164 , 451–480.     

Ecological and evolutionary factors in the morphological diversification of South American spiny rats

Understanding the processes underlying morphological diversification is a central goal in ecology and evolutionary biology and requires the integration of information about phylogenetic divergence and ecological niche diversity. In the present study, we use geometric morphometrics and comparative methods to investigate morphological diversification in Neotropical spiny rats of the family Echimyidae. Morphological diversification is studied as shape variation in the skull, comprising a structure composed of four distinct units: vault, base, orognathofacial complex, and mandible. We demonstrate association among patterns of variation in shape in different cranial units, levels of phylogenetic divergence, and ecological niche diversification. At the lower level of phylogenetic divergence, there is significant and positive concordance between patterns of phylogenetic divergence and cranial shape variation in all cranial units. This concordance may be attributable to the phylogenetic and shape distances being calculated between species that occupy the same niche. At higher phylogenetic levels of divergence and with ecological niche diversity, there is significant concordance between shape variation in all four cranial units and the ecological niches. In particular, the orognathofacial complex revealed the most significant association between shape variation and ecological niche diversity. This association may be explained by the great functional importance of the orognathofacial complex.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 646–660.     

Molecular and karyologic variation in the genus Isothrix (Rodentia, Echimyidae)

Phylogenetic relationships among available samples of the genus Isothrix using mitocondrial gene cytochrome b were carried out and a new karyotype of Isothrix specimens referred to Isothrix negrensis from the mid course of Rio Negro, in the Brazilian Amazon, was described. Molecular, karyological and morphological data of Isothrix negrensis was compared to that of I. bistriata and I. pagurus. Cytochrome b DNA sequence analyses clearly separate I. negrensis from I. bistriata and genetic distances estimates between then are greater than between species of the related genus Mesomys. The median-joining analysis postulated the presence of two median vectors between I. bistriata haplotypes from adjacent localities, suggesting that genetic isolation between them is unrelated to geographic distance. These results confirm previous molecular differences suggesting that I.bistriata is a composite of several taxa. The karyotype of Isothrix negrensis also differs from those reported for I. bistriata and I. pagurus. In relation to the external morphology I. negrensis differs from I. bistriata by the overall darker dorsal coloration, head darker than dorsum, presence of a longitudinal line of blackish hairs in the proximal part of the tail extending until near to its base, dorsal surface of hind feet covered with yellowish hairs and stripe of light hairs in the head reduced to a small patch.     

Bots (Diptera: Oestridae) infesting a neotropical forest rodent, Proechimys semispinosus (Rodentia: Echimyidae), in Panama

Botfly larvae (Cuterebra sp.) infesting spiny rats (Proechimys semispinosus) in 8 small islands in the Panama Canal were studied. Rats were live trapped monthly on each island from January 1991 through February 2000 and visually examined for the presence of bots. Overall, bot prevalence was 4.6% and differed statistically among island rat populations. Rats were simultaneously infested by as many as 4 bots. Overall bot intensity was 1.3 bots per infested rat and did not differ among islands. Mean bot density across all islands was 0.0111 and was greater during the dry seasons than during the rainy seasons, but it did not differ among islands. Bots were found during all the 12 calendar months, suggesting a multivoltine reproductive schedule. Although bot activity varied seasonally, there was little synchrony of bot activity among islands. Bot density was related negatively to rainfall but was not related to host density, suggesting that drier ambient conditions may promote reproduction by adult bot flies in this system.     

Molecular systematics,taxonomy and biogeography of the genus Cavia (Rodentia: Caviidae)

Phylogenetic analyses were conducted on cytochrome b sequence data of the most geographically and taxonomically broad sampling of Cavia taxa to date. Primary objectives included providing the first extensive molecular phylogenetic framework for the genus, testing the taxonomic and systematic hypotheses of previous authors and providing insight into the evolutionary and biogeographic history of the genus. Support was found for the morphologically defined species C. aperea, C. tschudii, C. magna and C. fulgida and the taxonomic placement of taxa previously subject to conflicting taxonomic opinions (e.g. C. nana, C. anolaimae and C. guianae) was further resolved. Additionally, we elevate the Ecuadorian C. a. patzelti to species status, restrict the distributional limits and suggest taxonomic affiliations of some C. tschudii subspecies, and provide strong evidence for the geographic origin of guinea pig domestication. Finally, we provide an estimated evolutionary timeline for the genus Cavia, which appears to extend well into the late Miocene.