Phylogeographical structure in the subterranean tuco-tuco Ctenomys talarum (Rodentia: Ctenomyidae): contrasting the demographic consequences of regional and habitat-specific histories

In this work we examined the phylogeography of the South American subterranean herbivorous rodent Ctenomys talarum (Talas tuco-tuco) using mitochondrial DNA (mtDNA) control region (D-loop) sequences, and we assessed the geographical genetic structure of this species in comparison with that of subterranean Ctenomys australis, which we have shown previously to be parapatric to C. talarum and to also live in a coastal sand dune habitat. A significant apportionment of the genetic variance among regional groups indicated that putative geographical barriers, such as rivers, substantially affected the pattern of genetic structure in C. talarum. Furthermore, genetic differentiation is consistent with a simple model of isolation by distance, possibly evidencing equilibrium between gene flow and local genetic drift. In contrast, C. australis showed limited hierarchical partitioning of genetic variation and departed from an isolation-by-distance pattern. Mismatch distributions and tests of neutrality suggest contrasting histories of these two species: C. talarum appears to be characterized by demographic stability and no significant departures from neutrality, whereas C. australis has undergone a recent demographic expansion and/or departures from strict neutrality in its mtDNA.     

Energy and distribution in subterranean rodents: sympatry between two species of the genus Ctenomys

The low basal metabolic rate (BMR) observed in subterranean rodents, compared to that of surface-dwelling species of comparable size, has been proposed to be an adaptation to underground life. Two main hypotheses have been proposed to explain this finding, the cost of burrowing and the thermal stress. The former states that the low BMR is due to the high cost of extending the tunnel system whereas the other relates it to the possibility of overheating in burrows where evaporative and convective heat exchange are restricted. Additionally, both hypotheses related the energetics of subterranean rodent with spatial distribution. The genus Ctenomys is an excellent model to evaluate the cost of burrowing or thermal stress, since they are widely distributed, with members differing markedly in body mass. The aim of this study was to assess digging and basal energetics in two Ctenomys species that live in sympatry in a coastal grassland, but differ in their microspatial distribution by soil preference. We used the obtained energetic data to test both energy-distribution hypotheses. We measured BMR and digging metabolic rate (DMR) through open flow respirometry in two species exposed to soft and hard soils. In brief, DMR in Ctenomys talarum (100-170 g), as in Ctenomys australis (250-600 g), was unaffected by soil hardness. Within thermoneutral zone of each species, DMR/RMR quotient was lower in the smaller species. Our data did not support the thermal stress hypothesis, but the cost of burrowing hypothesis was not rejected. Other alternative hypotheses are proposed to explain the distribution of C. talarum and C. australis.     

Size, shape and structural versatility of the skull of the subterranean rodent Ctenomys (Rodentia, Caviomorpha): functional and morphological analysis

Morphological analysis of the skull of the subterranean rodent Ctenomys , a highly speciose genus which uses both claws and teeth when digging, shows that for a broad range of species size, scaling was associated with both variation and maintenance of shape. Our results show that the angle of incisor procumbency (AIP), a character largely viewed as an adaptation to digging with teeth, is highly variable. We found a non-significant relationship between AIP and basicranial axis (basioccipital + basisphenoid) length, a measure of overall skull size. Accordingly, both small and large Ctenomys species possess either high or low AIP. A significant relationship between AIP and diastema length, given the rostral allometry seen in Ctenomys , suggests that hypermorphosis to a certain extent influences AIP. However, the roots of the incisor are lateral to those of the cheek teeth and their position may thus shift freely. This observation supports the notion that skull structural design, and to a certain extent rostral allometry, underlies variation in AIP. On the other hand, the positive allometry of incisor width and thickness indicates that, in larger species, proportionately powerful incisors are able to resist greater bending forces. We found that the out-lever arm of the jaw adductor muscles scales with positive allometry against basicranial axis length. However, we found an isometric relationship between in- and out-lever arms. In this case, conservation of skull proportions, regardless of variation in size, is a feature possibly related to the maintenance of an effective tooth digging capability. Functional and ecological data are discussed when assessing the implications of size and shape variation in the skull of Ctenomys .  © 2003 The Linnean Society of London. Biological Journal of the Linnean Society , 2003, 78 , 85−96.     

New Karyotypes and Some Considerations about the Chromosomal Diversification of Ctenomys minutus (Rodentia: Ctenomyidae) on the Coastal Plain of the Brazilian State of Rio Grande do Sul

The dominant mammals occupying the subterranean niche in South America are rodents of the genus Ctenomys, which form a large group of 56 species with chromosome numbers ranging from 2n= 10 to 70. In southern Brazil, Ctenomys minutus is the species with the widest geographic distribution, inhabiting sandy fields and dunes extending from Jaguaruna beach in the state of Santa Catarina to the town of São José do Norte in the state of Rio Grande do Sul. Eleven karyotypes (2n= 42; 2n= 46a; 2n= 46b; 2n= 47a; 2n= 47b; 2n= 48a; 2n= 48b; 2n= 49a; 2n= 49b; 2n= 50a and 2n= 50b) were described for this species and zones of hybridization are also known. A sample of 51 C. minutus specimens was collected from five sampling sites about 20 km apart along the coastal plain of Rio Grande do Sul between the municipalities of Tavares (31°23′S 51°09′W) and São José do Norte (31°52′S 51°54′W). We were able to extend the known geographic distribution of C. minutus by 90 km, from Tavares southwards to São José do Norte. During our study we found five karyotypes (2n= 46b, 47b, 48b, 49b and 50b), four of which (2n= 47b, 48b, 49b and 50b) have not previously been described for this species.     

Postnatal ontogeny of limb proportions and functional indices in the subterranean rodent Ctenomys talarum (Rodentia: Ctenomyidae)

Burrow construction in the subterranean Ctenomys talarum (Rodentia: Ctenomyidae) primarily occurs by scratch‐digging. In this study, we compared the limbs of an ontogenetic series of C. talarum to identify variation in bony elements related to fossorial habits using a morphometrical and biomechanical approach. Diameters and functional lengths of long bones were measured and 10 functional indices were constructed. We found that limb proportions of C. talarum undergo significant changes throughout postnatal ontogeny, and no significant differences between sexes were observed. Five of six forelimb indices and two of four hindlimb indices showed differences between ages. According to discriminant analysis, the indices that contributed most to discrimination among age groups were robustness of the humerus and ulna, relative epicondylar width, crural and brachial indices, and index of fossorial ability (IFA). Particularly, pups could be differentiated from juveniles and adults by more robust humeri and ulnae, wider epicondyles, longer middle limb elements, and a proportionally shorter olecranon. Greater robustness indicated a possible compensation for lower bone stiffness while wider epicondyles may be associated to improved effective forces in those muscles that originate onto them, compensating the lower muscular development. The gradual increase in the IFA suggested a gradual enhancement in the scratch‐digging performance due to an improvement in the mechanical advantage of forearm extensors. Middle limb indices were higher in pups than in juveniles–adults, reflecting relatively more gracile limbs in their middle segments, which is in accordance with their incipient fossorial ability. In sum, our results show that in C. talarum some scratch‐digging adaptations are already present during early postnatal ontogeny, which suggests that they are prenatally shaped, and other traits develop progressively. The role of early digging behavior as a factor influencing on morphology development is discussed. J. Morphol. 275:902–913, 2014. © 2014 Wiley Periodicals, Inc.     

Early evolutionary differentiation of morphological variation in the mandible of South American caviomorph rodents (Rodentia, Caviomorpha)

Caviomorphs are a clade of South American rodents recorded at least since the early Oligocene (> 31.5 Ma) that exhibit ample eco-morphological variation. It has been proposed that phylogenetic structure is more important than ecological factors for understanding mandibular shape variation in this clade. This was interpreted as a result of the long-standing evolutionary history of caviomorphs and the early divergence of major lineages. In this work, we test this hypothesis through the analysis of morphological variation in the mandible of living and extinct species and compare this information with that obtained through comparative phylogenetic analyses. Our results support the hypothesis of early origin of mandibular variation; moreover, they suggest the conservation of early differentiated morphologies, which could indicate the existence of constrained evolutionary diversification.     

Effects of Acute and Chronic Exposure to Predatory Cues on Spatial Learning Capabilities in the Subterranean Rodent Ctenomys talarum (Rodentia: Ctenomyidae)

Spatial learning, the cognitive ability that allows animals to efficiently locate food, partners or avoid predators, can be affected by various factors such as stress. Stressors represent a threat to the animal's homeostasis and trigger a set of physiological and behavioral changes known as stress response. The herbivorous rodent Ctenomys talarum (tuco‐tuco) inhabits underground complex gallery systems. Dispersal as well as food collection occurs on the surface, where they are exposed to terrestrial and aerial predators. We evaluated the effect of a natural stress factor, predation, on spatial learning of C. talarum. Additionally, we collected data on neutrophil/lymphocyte ratio, hematocrit, blood glucose, and plasma cortisol to assess physiological levels of stress. The acute exposure to direct cues indicating the presence of a predator (immobilization + cat urine) increased the time needed to reach the goal in a longitudinal labyrinth. The number of errors also increased albeit the difference was only marginally significant. The chronic exposure to predator cues (immobilization, cat urine, and cat fur) presented in an unpredictable order significantly increased both time and errors committed by tuco‐tucos during learning trials in the labyrinth. Results show the strong impact of predatory stress on the spatial abilities of C. talarum, a key cognitive process involved in most of their vital activities. They also highlight the importance of investigating wild species as regards the development of antipredatory defensive behaviors that contribute both to the avoidance of deleterious consequences of a direct attack and the influence on food search and mate localization performance.     

Evolutionary transformation of the subcutaneous muscle in rodents of Ctenohystrica (Rodentia: Diatomyidae,Ctenodactylidae, and Hystricognathi)

The present study examined the subcutaneous muscle (m. cutaneus trunci) in a relict species Laonastes aenigmamus (Diatomyidae) and in two ctenodactylids (Ctenodactylidae: Ctenodactylus gundi and Pectinator spekei), which are closely related to Laonastes according to current phylogenetic hypotheses. The comparative morphological analysis also included four representatives of Hystricognathi: Echimys sp., Proechimys sp., Cercomys cunicularis, and Hystrix indica. Laonastes and ctenodactylids have a number of common ancestral traits in the morphology of m. cutaneus trunci. This suggests that they are probably related to the ancestral forms of Ctenohystrica. However, the structural similarity of the subcutaneous muscle in Diatomyidae and Ctenodactylidae is based not only on plesiomorphic (presence of the medial head of m. cutaneus trunci), but also on an apomorphic (the development of the thoracoabdominal portion) feature which is common to both branches of Ctenohystrica (Ctenodactiloidea and Hystricognathi). The results of the comparative analysis suggest a new scenario for the evolutionary transformations of m. cutaneus trunci within the clade Ctenohystrica. This scenario differs from earlier suggestions and proposes initial differentiation of the subcutaneous muscle and possibly its secondary simplification, but on a new basis. On this new basis a further secondary increase in complexity of subcutaneous muscle appears possible in response to various adaptations in hystricognaths.     

Phylogenetic analysis of G-banded karyotypes among the South American subterranean rodents of the genus Ctenomys (Caviomorpha: Octodontidae), with special reference to chromosomal evolution and speciation

The chromosomes of subterranean rodents of the South American genus Ctenomys are highly variable with diploid numbers ranging from 10 to 70. The phylogenetic relationships of this group have been analysed cladistically using G-banded karyotypes as have the chromosomal rearrangements involved in its karyotypic differentiation. One group, called the 'Corrientes group', has very variable chromosomes but low allozymic and morphological differentiation among its members. This group has been analysed with respect to chromosomal speciation. Using a member of another subfamily (Octodontomys gliroides) as an outgroup, the results indicate that karyotypes with low diploid and fundamental numbers are plesiomorphic. The range of diploid numbers studied here is between 22 and 70, while the fundamental numbers are between 40 and 86. It was found that the main chromosomal rearrangement that transforms karyotypes towards higher diploid and fundamental numbers is the acquisition of new chromosomal material via unknown mechanisms, followed by pericentric inversions that generate new chromosomal arms, centric fusions and centric fissions. In spite of their low differentiation regarding allozymic and morphological features, it was found that the karyomorphs of the Corrientes group have enough chromosomal differentiation to consider them as distinct species. Beside the range of diploid and fundamental numbers of this group (42–70 and 80–84 respectively), their pairwise chromosomal differences are high. The most closely related of them differ in one nonhomologous arm, one Robertsonian change and a whole chromosome duplication. The most differentiated taxa differ in 20 arms with lack of homology, 12 Robertsonian changes (one with monobrachial homology), six pericentric inversions and the above mentioned probable arm duplication. For these reasons, it is probable that some kind of chromosomal speciation has occurred in the Corrientes group.     

Evolution of host use in fruit flies of the genus Blepharoneura (Diptera: Tephritidae): cryptic species on sexually dimorphic host plants

Blepharoneura , a neotropical genus of tephritid fruit flies, includes newly discovered morphologically cryptic species that are highly host specific. Several species of fly, each specific to a different host tissue can infest a single species of sexually dimorphic host. Using allozyme electrophoresis, we analysed morphologically similar populations of flies reared from various tissues of five species of host plant representing three subtribes of the Cucurbitaceae. In Venezuela, we found three sympatric species of Blepharoneura feeding on Gurania spinulosa Cogn. (one species on male flowers, another on female flowers, and a third on seeds). In Costa Rica, we found four non-interbreeding populations of Blepharoneura feeding on G. costaricensis Cogn. : two sympatric 'lowland' populations (one feeding on male flowers and another on female flowers) and two sympatric 'highland' populations (also specific to flowers of different sexes). Phylogenetic analyses revealed a species-rich clade of specialists associated with flowers of the Guraniinae, and a species-poor clade of generalists associated with seeds of the Guraniinae. Specialization on male vs. female flowers appears to have occurred repeatedly. Patterns of laryal dispersal may underlie differehces in diversification of seed vs. flower clades: larvae that feed on seeds are dispersed by bats; larvae feeding on flowers are not dispersed.     

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.     

Dispersal and diversification: macroevolutionary implications of the MacArthur–Wilson model, illustrated by Simulium (Inseliellum) Rubstov (Diptera: Simuliidae)

Aim Provide an empirical test of the ‘radiation zone’ hypothesis of the MacArthur–Wilson theory of island biogeography using the taxon‐pulse hypothesis of Erwin and Brooks Parsimony Analysis (BPA) on Simulium (Inseliellum) Rubstov. Location Micronesia, Cook Islands, Austral Islands, Society Islands, Marquesas Islands, Fiji and New Caledonia. Methods Primary and secondary BPA of the phylogeny of Inseliellum. Results Primary BPA showed that 15% of the taxon area cladogram contained area reticulations. Secondary BPA (invoking the area duplication convention) generated a clear sequence of dispersal for Inseliellum. The sequence follows a Micronesia – Cook Islands – Marquesas Islands – Society Islands dispersal, with a separate dispersal from the Cook Islands to the Austral Islands less than 1 Ma. A radiation in the island of Tahiti (Society Islands) produced numerous dispersals from Tahiti to other islands within the Society Islands system. Islands close to Tahiti (source island) have been colonized from Tahiti more often than islands far from Tahiti, but a higher proportion of those species colonizing distant islands have become distinct species. Main conclusions The dispersal sequence of Inseliellum exhibits both old to young island dispersal and young to old island dispersal. This is due to habitat availability on each island. Inseliellum is a model system in exemplifying the ‘radiation zone’ hypothesis of MacArthur and Wilson. As well, islands close to the source are colonized more often that those far from the source, but colonization of islands far away from the source results in a higher proportion of speciation events than for islands close to the source. The diversification of Inseliellum corresponds to a taxon‐pulse radiation, with a centre of diversification on Tahiti resulting from its large area and abundant freshwater habitats. This study illustrates the utility of BPA in identifying complex scenarios that can be used to test theories about the complementary roles of ecology and phylogeny in historical biogeography.     

Age of association between the nurse shark, Ginglymostoma cirratum, and tapeworms of the genus Pedibothrium (Tetraphyllidea: Onehobothriidae): implications from geography

The first records of the tapeworm genus Pedibothrium from nurse sharks (Ginglymostoma cirratum) in the eastern Pacific and eastern Atlantic Oceans provide new insights on the age of the association between these tapeworms and this host. Four individuals of G. cirratum examined from the southern tip of the Baja Peninsula, Mexico, were found to host P. manteri and P. brevispine. Tapeworm specimens discovered in the collection of J. Cadenet, taken from G. cirratum off Goree near Dakar, Senegal in 1947, were of P. globicephalum and P. manteri. These tapeworm faunas are consistent with those found previously in small and large nurse sharks, respectively, in the western Atlantic Ocean. The distributional data, combined with the non-vagile habits of the nurse shark, indicate this host-parasite association dates from the most recent completion of the Panamanian Isthmus, approximately 2 Mya. This suggests that P. manteri and R brevispine have remained unchanged for at least 2 Myr. The data from the eastern Atlantic Ocean are less informative. The amphi-Atlantic distribution of P. manteri and P. globicephalum in G. cirratum may have resulted from vicariant events associated with the formation of the Atlantic Ocean. However, fossils of at least two extinct species of Ginglymostoma are also known from both sides of the Atlantic Ocean. Short of parallel evolution of three different species of Ginglymostoma on either side of the Atlantic Ocean, these data séem more consistent with dispersal as an explanation for this disjunction and are thus of limited utility for extending the age of this host-parasite association at this time. Analysis of the degree of genetic divergence among individuals of G. cirratum and among individuals of the broadly distributed species of Pedibothrium from all three localities would be extremely interesting.     

Introgressive hybridization between two species of waterstriders (Hemiptera: Gerridae: Limnoporus): geographical structure and temporal change of a hybrid zone

Where the distribution ranges of the waterstriders Limnoporus notabilis and L. dissortis meet in western Canada, extensive hybridization and introgression occurs. Multivariate ordination analyses of genetic and morphometric data by principal component analysis revealed that a single axis separating the two parent species could account for nearly all the variation in both data sets. Maps of principal component scores for both data sets revealed geographical patterns of variation reflecting specific topographic features in the region. Comparisons of morphometric data from some of the samples collected in the 1980s and from the same sites revisited in the 1990s revealed substantial changes. An ‘island’ of dissortis‐like populations inside the range of L. notabilis in interior British Columbia expanded, and a marked local protrusion of notabilis‐like phenotypes into the range of L. dissortis on the east slope of the Rocky Mountains diminished during the decade between collections. We conclude that introgressive hybridization between these two species of waterstriders is a spatially complex and highly dynamic process.     

Unravelling the distinctive craniomandibular morphology of the Plio-Pleistocene Eumysops in the evolutionary setting of South American octodontoid rodents (Hystricomorpha)

Echimyidae is a species-rich clade of Neotropical rodents, which diversified in association with forested biomes. Since the late Miocene, a few lineages from southern South America have been adapted to open environments. Eumysops is one of these southern echimyids, and its peculiar craniomandibular morphology has been assumed to be a result of adaptation to open environments. We performed a geometric morphometric analysis of craniomandibular shape variation to explore whether, as suspected, Eumysops is divergent from other echimyids and octodontoids. In addition, we explored whether deterministic factors driven by different ecological dimensions can explain the diversification of shape among octodontoids. We found that craniomandibular shape variation in octodontoids was related to ecological variables. Comparing competing evolutionary models suggested that the input of selective factors play a key role in octodontoid craniomandibular shape diversification; habitat and habits were found to be the most influential factors. In the analysed morphospaces, Eumysops was located distant from other echimyids due to its distinctive traits, especially wide and posteriorly displaced orbits, and related low craniomandibular joint. Divergent orbits and resulting wider panoramic vision support the interpretation of Eumysops as an open-habitat specialist echimyid. But what is more relevant, is that Eumysops occupied a sector of the octodontoid cranial morphospace not filled by living representatives; this highlights the contribution of fossils in providing key information on the specialization boundaries explored by a clade throughout its history.     

Geographical variation in the cranial measurements of the midday jird Meriones meridianus (Rodentia: Muridae) and its taxonomic implications

Cranial variation was studied across the geographical range of the Meriones meridianus species complex using 665 specimens from 112 localities. Morphometric results were compared with previously published data on genetic variation. Unsupervised model‐based clustering analysis implemented in Mclust software was employed to identify the number and content of morphological clusters. Three clearly defined morphological groups corresponding to mtDNA clades were found. The results of the morphometric analysis are consistent with the hypothesis that these 3 groups should be treated as distinct species; specifically, M. psammophilus Milne‐Edwards, 1871, M. penicilliger Heptner, 1933 and M. meridianus Pallas, 1773. M. psammophilus inhabits the Mongolian–Chinese part of the superspecies range, except for the Mongolian Dzungaria region, which is inhabited by M. meridianus. The range of the latter species extends westwards to north‐west Kazakhstan and Kalmykia. M. penicilliger inhabits the southern part of the superspecies range from Tian Shan to Turkmenistan. M. dahli is craniometrically similar to M. meridianus; hence, its species status remains questionable.     

Distribution patterns of the small mammals (Insectivora and Rodentia) in a transitional zone between the Eurosiberian and the Mediterranean regions

To determine, by means of quantitative analyses, the distribution patterns of the insectivores and rodents in Catalonia using physiographical regions as Operative Geographical Units (OGUs). Catalonia (north‐eastern Iberian Peninsula). Based on the presence/absence of twenty‐five small mammals in thirteen physiographical regions, which were used as OGUs, the following aspects were studied: (a) identification of biotic boundaries; (b) determination of chorological association of species; (c) climatic characterization of the biotic regions and the chorotypes. Groups of biotic regions and species were established, and their statistical significance was tested. The possible effect of several climatic factors on these groupings was studied using discriminant analyses. A significant biotic boundary was found to separate the central and eastern Pyrenees from the remaining physiographical regions. The climatic variables that defined this boundary were related to the severity and the availability of environmental energy. Four chorotypes were identified. One chorotype was constituted by Pyrenean or Pre‐Pyrenean species, an association determined by their mid‐European requirements; another chorotype was formed by Eurosiberian species, but showed a variable degree of tolerance to Mediterranean conditions; a third chorotype included species with a wide distribution that are Mediterranean, anthropic, generalist or have very specific habitats; and finally the fourth chorotype was constituted by a strictly Mediterranean species. The climatic factors that accounted for the distribution of these chorotypes were the mean July temperature and the mean annual precipitation. We conclude that the axial zone of the Pyrenees, except the coastal portion, determines two biotic regions in Catalonia. As for the classification of species, using quantitative techniques for the first time, we offer a new biogeographicalal configuration for the small mammals in this temperate‐Mediterranean transition.