Evolution and biogeography of talpid moles from continental East Asia and the Japanese islands inferred from mitochondrial and nuclear gene sequences

We sequenced the cytochrome b gene from two little-studied mammal species from the highlands of Southwest China, the long-tailed mole Scaptonyx fusicaudus and the gracile shrew-like mole Uropsilus gracilis. This data was used to examine the phylogenetic relationships among 19 talpid species within the family Talpidae (Mammalia: Eulipotyphla). Cytochrome b gene trees supported a basal placement of shrew-like moles (Uropsilus) within the Talpidae, and suggested that fossorial specializations arose twice during talpid evolution. To assess the evolutionary relationships of moles endemic to this region, we additionally sequenced the 12S rRNA gene and the nuclear recombination-activating gene-1 from eight and ten East Asian taxa, respectively. Analyses of these single and concatenated data sets suggested that East Asian shrew moles diverged prior to the evolution of fossorial Eurasian moles. However, we were unable to determine whether semi-fossorial shrew moles are monophyletic. In contrast, fossorial Eurasian genera (Talpa, Mogera and Euroscaptor) were consistently found to form a monophyletic clade, with Mogera and Euroscaptor representing sister taxa. Furthermore, this fossorial clade grouped with the semi-aquatic Desmana, although with fairly low (35-62%) bootstrap support. Mogera imaizumii was found to be more closely related to M. wogura than to M. tokudae. This implies that the ancestors of these three species entered Japan from the Asian continent in this order via a series of migration events, suggesting that the Japanese Islands have played an important role in preserving mole lineages from ancient to recent times.     

A comprehensive morphological analysis of talpid moles (Mammalia) phylogenetic relationships

Some talpid moles show one of the most specialized suites of morphological characters seen among small mammals. Fossorial and more generalized shrew‐looking moles inhabit both North America and Eurasia but these land masses share none of the same genera. One of the central questions of mole evolution has been that of how many times specialized fossorial habits evolved. We investigated the origin of mole characters with a maximum parsimony analysis of 157 characters, mostly craniodental and postcranial, of representatives of all 17 living mole genera and three shrews and one hedgehog as outgroups. The result was one most‐parsimonious tree and its most novel aspect was the position of a Japanese shrew mole clade (Urotrichus, Dymecodon), which branched off after Uropsilus and was not closely related to the American shrew mole (Neurotrichus). The desmans (Galemys and Desmana) were the next clade in the tree, followed by Neurotrichus. We confirmed the monophyly of the Eurasian fossorial mole clade Talpini (Euroscaptor, Parascaptor, Mogera, Scaptochirus and Talpa). Condylura, the star‐nosed mole from North America, was sister group to a clade consisting of the Talpini plus Scaptonyx and the Scalopini (Scalopus, Scapanus, Parascalops, and Scapanulus). Based on our results and on the assumption that moles originated in Eurasia, it is most parsimonious to infer one migration from Eurasia to North America and two back‐migrations to Eurasia. It is ambiguous if Talpini and Scalopini evolved their full fossorial habits independently or not. © The Willi Hennig Society 2006.     

Humerus development in moles (Talpidae,Mammalia)

The humerus of fossorial moles has a highly derived anatomy, reflecting the ecological specialization of these animals for digging. It is short and broad, with enlarged muscle attachment sites and pronounced articulations compared to non‐fossorial sister taxa and other mammals. Both condyles are rotated in opposite directions, resulting in a torsion which is unique among eutherian mammals. The development of this exceptional bone was studied in embryonic stages of the fossorial Iberian mole (Talpa occidentalis) from mesenchymal condensation to incipient ossification based on histological serial sections using 3D reconstruction methods. For comparison, embryonic stages of the semi‐fossorial Japanese shrew mole (Urotrichus talpoides) as well as a sister taxon of moles, the terrestrial North American least shrew (Cryptotis parva), were studied. Results show that the humerus of Talpa already shows its derived anatomy with broadened muscle attachment sites and distinct articulations at early cartilaginous stages, when ossification has just started in the mid‐diaphyseal region. The torsion takes place simultaneously with the medial rotation of the forelimbs. The supracondylar foramen is closed in all studied Talpa embryos, but patent in Cryptotis and Urotrichus. This is an example of developmental penetrance, suggesting that variation of adult elements can be found at early stages as well.     

The evolution of female mole ovotestes evidences high plasticity of mammalian gonad development

Previous studies of the reproductive biology and genetics of European moles (Talpa spp.) showed that all females of these species have ovotestes (gonads with testicular and ovarian tissue) instead of normal ovaries, a unique specialization among mammals. Females are fertile as their ovarian tissue is fully functional. Testicular tissue is abnormal and sterile, but produces high levels of testosterone. This phenomenon also characterizes other talpid species from Europe and North America. To study the origin of this singular reproductive specialization, we examined the gonads of several female specimens belonging to two critical taxa. Although large Japanese moles (Mogera wogura) posses ovotestes, greater Japanese shrew moles (Urotrichus talpoides) are characterized by normal ovaries. The results fit parsimoniously with a recent phylogenetic study that places Urotrichus relatively basal in the talpid tree and separate from the American shrew mole. Parsimony reconstruction on alternative phylogenetic hypotheses clearly indicates that reversal(s) must have occurred and suggests that a relatively simple genetic mechanism must be associated with the evolution of female hermaphroditism in moles.     

Shape variation in the mole dentary (Talpidae: Mammalia)

The clade Talpidae consists of specialized fossorial forms, shrew‐like moles and semi‐aquatic desmans. As with all higher jawed vertebrates, different functional, phylogenetic and developmental constraints act on different parts of dentary influencing its shape. In order to determine whether morphological variation in the dentary was unified or dispersed into an integrated complex of structural–functional components, a morphometric analysis of the mole dentary was undertaken. The dentary was subdivided into component parts – horizonal ramus; coronoid, condylar, angular processes of the ascending ramus – and outline‐based geometric morphometric methods used to quantify, compare and contrast modes of shape variation within the clade. These were successful in revealing subtle differences and aspects of shape important in distinguishing between mole genera. Closer examination of shape variation within the two fully fossorial mole clades (Talpini and Scalopini) revealed several similarities in ascending ramus shapes between genera from each clade. For example, the broad, truncated appearance of the coronoid process in the talpine genera Talpa and Parascalops was shared with the scalopine genus Scapanus. Also, the more slender, hook‐shaped coronoid process of Euroscaptor and Parascaptor (Talpini) closely resembles that of Scalopus (Scalopini). Interestingly, subspecies (one from each clade) more closely resembled genera other than their own in coronoid process shape. Important distinctions in horizontal ramus shape were found to exist between the two clades, such as the extent of curvature of the ventral margin and relative depth of the horizontal ramus. Results show shape variation in this region is correlated with dental formulae and the relative sizes of the teeth. The taxonomically important dentition differences characteristic of mammals are also reflected in the horizontal ramus results. Moreover, these results suggest size may be affecting shape and the extent of variation in, for example, the coronoid and condylar processes between the semi‐aquatic moles Desmana and Galemys. It is likely that the effects of morphological integration seen at this level of analysis – covariation between shapes of dentary components – may exist because interacting traits are evolving together. Horizontal ramus and coronoid process shape, for example, are similar across Scapanus and Parascalops, but both these shapes have diverged in Scalopus. © 2008 Trustees of the Natural History Museum (London). Journal compilation © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 153 , 187–211.     

Evolution of the middle ear apparatus in Talpid moles

The middle ear structures of eight species of mole in the family Talpidae (Mammalia: Eulipotyphla) were studied under light and electron microscopy. Neurotrichus, Parascalops, and Condylura have a simple middle ear cavity with a loose ectotympanic bone, ossicles of a "microtype" morphology, and they retain a small tensor tympani muscle. These characteristics are ancestral for talpid moles. Talpa, Scalopus, Scapanus, and Parascaptor species, on the other hand, have a looser articulation between malleus and ectotympanic bone and a reduced or absent orbicular apophysis. These species lack a tensor tympani muscle, possess complete bullae, and extensions of the middle ear cavity pneumatize the surrounding basicranial bones. The two middle ear cavities communicate in Talpa, Scapanus, and Parascaptor species. Parascaptor has a hypertrophied malleus, a feature shared with Scaptochirus but not found in any other talpid genus. Differences in middle ear morphology within members of the Talpidae are correlated with lifestyle. The species with middle ears closer to the ancestral type spend more time above ground, where they will be exposed to high-frequency sound: their middle ears appear suited for transmission of high frequencies. The species with derived middle ear morphologies are more exclusively subterranean. Some of the derived features of their middle ears potentially improve low-frequency hearing, while others may reduce the transmission of bone-conducted noise. By contrast, the unusual middle ear apparatus of Parascaptor, which exhibits striking similarities to that of golden moles, probably augments seismic sensitivity by inertial bone conduction.     

Systematics and macroevolution of extant and fossil scalopine moles (Mammalia,Talpidae)

Scalopini is one of the two fully fossorial mole tribes in the family Talpidae, with remarkable adaptations to subterranean lifestyles. Most living Scalopini species are distributed in North America while a sole species occurs in China. On the other hand, scalopine fossils are found in both Eurasia and North America from upper Oligocene strata onwards, implying a complex biogeographical history. The systematic relationships of both extant and fossil Scalopini across North America and Eurasia are revised by conducting phylogenetic analyses using a comprehensive morphological character matrix together with 2D geometric–morphometric analyses of the humeral shape, with a specific emphasis on Mioscalops, a genus commonly found in North America and formerly known as Scalopoides. Our phylogenetic analyses support the monophyly of the tribe Scalopini as well as a proposed two‐subtribe‐division scenario of Scalopini (i.e. Scalopina and Parascalopina), although Proscapanus could not be assigned to either subgenus. Our geometric–morphometric analyses indicate that the European Mioscalops from southern Germany should be allocated to Leptoscaptor, which in turn implies that Mioscalops may be endemic to North America and never arrived in Europe. Examination of biogeographical patterns does not unambiguously determine the geographical origin of Scalopini. Nevertheless, it does support multiple transcontinental colonization events across Asia, Europe and North America. Scapanulus oweni, distributed in central China, is the only remaining representative of one of those out‐of‐North‐America migrations, whereas scalopine moles are common in North America nowadays with up to five species.     

Skeletal adaptations and phylogeny of the oldest mole Eotalpa (Talpidae,Lipotyphla, Mammalia) from the UK Eocene: the beginning of fossoriality in moles

The oldest talpid, Eotalpa, was previously known only from isolated cheek teeth from the European late Middle Eocene to earliest Oligocene. Screenwashing of Late Eocene sediments of the Hampshire Basin, UK, has yielded cranial and postcranial elements: maxilla, dentary, ulna, metacarpals, distal tibia, astragalus, calcaneum, metatarsals and phalanges. In addition to M_1–2 myotodonty, typical talpid features are as follows: ulna with long medially curved olecranon and deep abductor fossa and astragalar body with lateral process. However, Eotalpa retains certain soricid‐like primitive states (M¹ preparacrista, P⁴ with prominent mesiolingual protocone lobe, strongly angled astragalar neck and calcaneum with no space for a cuboid medial process) not found in modern talpids. Eotalpa is more derived than the most primitive living talpid Uropsilus in having lost the M^1–2 talon shelf, developed a convex radial facet on the ulna, an incipient proximal olecranon crest, relatively shorter metapodials and depressed manual unguals. Its astragalus with medial trochlear ridge taller than the lateral one and massive medial plantar process is typical of the Lipotyphla. Eotalpa lacks synostosis of tibia and fibula, found in other Talpidae, Soricidae and Erinaceidae, suggesting that synostosis in these groups has been independently acquired. Cladistic analysis places Eotalpa as stem member of the Talpidae and shows that much homoplasy arose during the early evolution of the family. Ground dwelling in Eotalpa is indicated by the following: astragalus with a medially dipping head, curved in a single plane; calcaneum with distal peroneal process and strongly overlapping ectal and sustentacular facets; and matching sized ectal and sustentacular facets on calcaneum and astragalus. These features would have restricted ankle mobility. Ungual and metatarsal shape and ulnar structure suggest a primitive stage in fossorial evolution and argue against a semiaquatic precursor stage in talpid fossoriality. Shrew‐moles may represent a reversal to surface foraging rather than an intermediate stage in fossoriality.     

Environmental control on the biogeographical distribution of Desmanella (Soricomorpha,Mammalia) in the Miocene of the Iberian Peninsula

Abstract: This paper reports the first record of Desmanella (Mammalia, Soricomorpha) from the Granada Basin in southern Iberian Peninsula, which represents its south‐westernmost occurrence in all Eurasia. It is a controversial taxon whose systematic assignment has been discussed for a long time. This genus belongs to the family Talpidae, a group of insectivores that include extant moles, shrew moles and desmans. Desmanella was very abundant in the late Miocene and early Pliocene of Eurasia, including several basins of northern Iberian Peninsula, but it has not been found until now in southern Iberia. Previous studies have shown that the faunal record and the climatic conditions during the Neogene in the Granada Basin were different from other areas of the Iberian Peninsula. The particular distribution of Desmanella supports the hypothesis that specific climatic features (wetter than neighbouring areas) prevailed in the Granada Basin during the late Turolian (late Miocene).     

Fasting metabolism and thermoregulatory competence of the star-nosed mole, Condylura cristata (Talpidae: Condylurinae).

Metabolic and body temperature (Tb) responses of star-nosed moles (Condylura cristata) exposed to air temperatures ranging from 0 to 33 degrees C were investigated. The thermoneutral zone of this semi-aquatic mole extended from 24.5 to 33 degrees C, over which its basal rate of metabolism averaged 2.25 ml O2 g-1 h-1 (45.16 J g-1 h-1). This rate of metabolism is higher than predicted for terrestrial forms, and substantially higher than for other moles examined to date. Minimum thermal conductance was nearly identical to that predicted for similar-sized eutherians and may represent a compromise between the need to dissipate heat while digging and foraging in subterranean burrows, and the need to conserve heat and avoid hypothermia during exposure to cold. C. cristata precisely regulated Tb (mean +/- SE = 37.7 +/- 0.05 degrees C) over the entire range of test temperatures. Over three separate 24-h periods, Tb of a radio-implanted mole varied from 36.6 to 38.8 degrees C, and generally tracked level of activity. No obvious circadian variation in Tb and activity was apparent, although cyclic 2-4 h intervals of activity punctuated by periods of inactivity lasting 3-5 h were routinely observed. We suggest that the elevated basal metabolic rate and relatively high Tb of star-nosed moles may reflect the semi-aquatic habits of this unique talpid.     

Cortical-organization in moles: evidence of new areas and a specialized S2

The somatosensory cortex of several mole species (family Talpidae), with different peripheral sensory adaptations, was investigated and compared to determine common and specialized features of cortical organization. Previously unidentified medial representations of the trunk and limbs were found in all species, indicating that S1 in moles occupies a medial to lateral strip of cortex as in most other mammals. This finding suggests a large lateral forelimb representation, previously attributed to S1, is actually part of S2. In the face representation, evidence was found for three representations of the unusual nose of the star-nosed mole (Condylura cristata). Each of these areas was divided into a series of modules (visible in cytochrome oxidase processed tissue) representing individual nasal appendages on the star. In the closely related but less specialized eastern mole (Scalopus aquaticus) and coast mole (Scapanus orarius), only two nose representations were identified in an area of cortex with a more uniform histological appearance. The results indicate that moles have enlarged somatosensory representations of the glabrous nose as compared to shrews and rats that instead have large vibrissal representations. In addition moles have a very large and specialized representation of the digging forepaw in S2. Since this part of S2 projects directly to the cervical spinal cord, the specialization may provide adaptive sensorimotor functions related to digging.     

Functional and systematic implications of the ear in golden moles (Chrysochloridae)

Golden moles (Chrysochloridae) are fossorial mammals known to have unusual mallei. The aim of this study was to describe and quantify aspects of the auditory morphology of golden moles in order to determine their systematic and functional implications. Observations were made on skeletal material as well as histological sections. The results of this study do not support the separation of the genus Calcochloris from Amblysomus . It was found that the morphology shared by all the studied genera is indicative of specialization for hearing low frequency sound. The tympanic membrane to stapes footplate ratios, ossicular lever arm ratios and incudomallear joint morphology suggest low frequency specializations in genera with small mallear heads and high frequency specializations in genera with large mallear heads. However, the size and degree of trabeculation of the tympanic cavity are not consistent with this result. It is proposed that all golden moles are low frequency hearers with differences in their range of sensitivity according to how much time they spend foraging above ground.     

Cortical organization in moles: evidence of new areas and a specialized S2

The somatosensory cortex of several mole species (family Talpidae), with different peripheral sensory adaptations, was investigated and compared to determine common and specialized features of cortical organization. Previously unidentified medial representations of the trunk and limbs were found in all species, indicating that S1 in moles occupies a medial to lateral strip of cortex as in most other mammals. This finding suggests a large lateral forelimb representation, previously attributed to S1, is actually part of S2. In the face representation, evidence was found for three representations of the unusual nose of the star-nosed mole ( Condylura cristata ). Each of these areas was divided into a series of modules (visible in cytochrome oxidase processed tissue) representing individual nasal appendages on the star. In the closely related but less specialized eastern mole ( Scalopus aquaticus ) and coast mole ( Scapanus orarius ), only two nose representations were identified in an area of cortex with a more uniform histological appearance. The results indicate that moles have enlarged somatosensory representations of the glabrous nose as compared to shrews and rats that instead have large vibrissal representations. In addition moles have a very large and specialized representation of the digging forepaw in S2. Since this part of S2 projects directly to the cervical spinal cord, the specialization may provide adaptive sensorimotor functions related to digging.     

New causal animal for the growth of <Emphasis Type="Italic">Hebeloma radicosum</Emphasis> (Agaricales): shrew, <Emphasis Type="Italic">Sorex</Emphasis> sp. (Mammalia,Insectivora)

Hebeloma radicosum fructification occurred in 2003 in Hokkaido where Talpidae moles, known causal animals for H. radicosum growth, are not distributed. An excavation carried out in 2005 revealed a mass of deserted latrines and a collapsed nest in the soil. The latrines, being full of deteriorating ectomycorrhizas, were considered to have borne that fungal growth. The responsible animal was identified as a shrew (Sorex) species by the characteristics of hairs remaining in the soil. Thus, in addition to the moles (Insectivora, Talpidae) and the wood mouse (Rodentia, Muridae; in Europe), a shrew species (Insectivora, Soricidae) is found to cause H. radicosum growth.     

Shared ancestry between a newfound mole-borne hantavirus and hantaviruses harbored by cricetid rodents

Discovery of genetically distinct hantaviruses in multiple species of shrews (order Soricomorpha, family Soricidae) and moles (family Talpidae) contests the conventional view that rodents (order Rodentia, families Muridae and Cricetidae) are the principal reservoir hosts and suggests that the evolutionary history of hantaviruses is far more complex than previously hypothesized. We now report on Rockport virus (RKPV), a hantavirus identified in archival tissues of the eastern mole (Scalopus aquaticus) collected in Rockport, TX, in 1986. Pairwise comparison of the full-length S, M, and L genomic segments indicated moderately low sequence similarity between RKPV and other soricomorph-borne hantaviruses. Phylogenetic analyses, using maximum-likelihood and Bayesian methods, showed that RKPV shared a most recent common ancestor with cricetid-rodent-borne hantaviruses. Distributed widely across the eastern United States, the fossorial eastern mole is sympatric and syntopic with cricetid rodents known to harbor hantaviruses, raising the possibility of host-switching events in the distant past. Our findings warrant more-detailed investigations on the dynamics of spillover and cross-species transmission of present-day hantaviruses within communities of rodents and moles.     

鼹科长吻鼩鼹和库氏长吻鼹的首次转录组分析

现生的鼹科动物分布于欧亚大陆和北美大陆,包括54种已知物种。鼹科动物有丰富的生态类型,是研究适应性进化的较好模型。本研究通过二代测序的方法分别获得了长吻鼩鼹和库氏长吻鼹两个物种心脏和肺脏以及脾脏和肺脏的转录组数据。这两个物种分别代表了分布于中国西南部、缅甸北部的没有特化的原始类群鼩鼹亚科以及高度适应地下生活的鼹亚科鼹族。我们首次报道了库氏长吻鼹在中国的分布。通过从头拼接,分别获得长吻鼩鼹和库氏长吻鼹197 092个和225 956个转录本,以及125 427个和94 023个unigene。通过与GenBank中的基因组注释文件比对,得到鼹科物种同源基因家族8 376个,及鼹科鼩鼱科同源基因家族8 114个。差异表达基因中各组织的高表达基因中均找到10个以上组织特异性基因。然而BUSCO分析确定完整单拷贝基因在两个物种中分别为43.0%和56.6%,提示死后mRNA迅速降解并影响转录组拼接。比较两个物种肺部基因的表达差异发现库氏长吻鼹335个相对高表达的基因,其中包括HMGB1、HSPD1、SF3B1、COL3A1、SUMO1和JUNB等,有报道上述基因可能与低氧或高海拔适应有关。     

Circumventing the polydactyly 'constraint': the mole's 'thumb'

Talpid moles across all northern continents exhibit a remarkably large, sickle-like radial sesamoid bone anterior to their five digits, always coupled with a smaller tibial sesamoid bone. A possible developmental mechanism behind this phenomenon was revealed using molecular markers during limb development in the Iberian mole (Talpa occidentalis) and a shrew (Cryptotis parva), as shrews represent the closest relatives of moles but do not show these conspicuous elements. The mole's radial sesamoid develops later than true digits, as shown by Sox9, and extends into the digit area, developing in relation to an Msx2-domain at the anterior border of the digital plate. Fgf8 expression, marking the apical ectodermal ridge, is comparable in both species. Developmental peculiarities facilitated the inclusion of the mole's radial sesamoid into the digit series; talpid moles circumvent the almost universal pentadactyly constraint by recruiting wrist sesamoids into their digital region using a novel developmental pathway and timing.     

Evolutionary Insights from a Genetically Divergent Hantavirus Harbored by the European Common Mole (Talpa europaea)

Background

The discovery of genetically distinct hantaviruses in shrews (Order Soricomorpha, Family Soricidae) from widely separated geographic regions challenges the hypothesis that rodents (Order Rodentia, Family Muridae and Cricetidae) are the primordial reservoir hosts of hantaviruses and also predicts that other soricomorphs harbor hantaviruses. Recently, novel hantavirus genomes have been detected in moles of the Family Talpidae, including the Japanese shrew mole (Urotrichus talpoides) and American shrew mole (Neurotrichus gibbsii). We present new insights into the evolutionary history of hantaviruses gained from a highly divergent hantavirus, designated Nova virus (NVAV), identified in the European common mole (Talpa europaea) captured in Hungary.

Methodology/Principal Findings

Pair-wise alignment and comparison of the full-length S- and L-genomic segments indicated moderately low sequence similarity of 54–65% and 46–63% at the nucleotide and amino acid levels, respectively, between NVAV and representative rodent- and soricid-borne hantaviruses. Despite the high degree of sequence divergence, the predicted secondary structure of the NVAV nucleocapsid protein exhibited the characteristic coiled-coil domains at the amino-terminal end, and the L-segment motifs, typically found in hantaviruses, were well conserved. Phylogenetic analyses, using maximum-likelihood and Bayesian methods, showed that NVAV formed a distinct clade that was evolutionarily distant from all other hantaviruses.

Conclusions

Newly identified hantaviruses harbored by shrews and moles support long-standing virus-host relationships and suggest that ancestral soricomorphs, rather than rodents, may have been the early or original mammalian hosts.     

A composite species-level phylogeny of the 'Insectivora' (Mammalia: Order Lipotyphla Haeckel, 1866)

The first MRP (matrix representation with parsimony) supertree phylogeny of the Lipotyphla is presented, covering all the families that were considered to make up the traditional mammalian order Insectivora. The phylogeny does not examine relationships within the shrew subfamily Crocidurinae, but all other taxa are considered at the species level, drawing upon 41 years of systematic literature and combining information from 47 published sources. The MRP technique is also critically discussed. This study will be of use to comparative biology studies of the Lipotyphla (or of mammals as a whole) and is a rigorous review of past systematic work, as well as clearly demonstrating our current level of knowledge. The supertree clearly details a strong imbalance in phylogenetic understanding across the taxon: a great deal is known about the hedgehogs and gymnures (Erinaceidae), the New World moles (Talpidae), Palaearctic species of Sorex (subgenus Sorex ) and the relationships between genera of red-toothed shrews (Soricinae). The supertree, however, clearly shows areas where our knowledge is conflicting or non-existent, and these gaps do not always correspond to obscure species: nothing is known about the systematics of Old World mole genera. Also very little is known about golden moles (Chrysochloridae) and the shrew-tenrec genus Microgale , some of the most threatened mammals on Earth.