Talpa Occidentalis Research Articles

Multiple Lineages of Hantaviruses Harbored by the Iberian Mole (Talpa occidentalis) in Spain.

The recent detection of both Nova virus (NVAV) and Bruges virus (BRGV) in European moles (Talpa europaea) in Belgium and Germany prompted a search for related hantaviruses in the Iberian mole (Talpa occidentalis). RNAlater®-preserved lung tissue from 106 Iberian moles, collected during January 2011 to June 2014 in Asturias, Spain, were analyzed for hantavirus RNA by nested/hemi-nested RT-PCR. Pairwise alignment and comparison of partial L-segment sequences, detected in 11 Iberian moles from four parishes, indicated the circulation of genetically distinct hantaviruses. Phylogenetic analyses, using maximum-likelihood and Bayesian methods, demonstrated three distinct hantaviruses in Iberian moles: NVAV, BRGV, and a new hantavirus, designated Asturias virus (ASTV). Of the cDNA from seven infected moles processed for next generation sequencing using Illumina HiSeq1500, one produced viable contigs, spanning the S, M and L segments of ASTV. The original view that each hantavirus species is harbored by a single small-mammal host species is now known to be invalid. Host-switching or cross-species transmission events, as well as reassortment, have shaped the complex evolutionary history and phylogeography of hantaviruses such that some hantavirus species are hosted by multiple reservoir species, and conversely, some host species harbor more than one hantavirus species.

Winter conditions, not resource availability alone, may drive reversible seasonal skull size changes in moles

Seasonal changes in the environment can lead to astonishing adaptations. A few small mammals with exceptionally high metabolisms have evolved a particularly extreme strategy: they shrink before winter and regrow in spring, including changes of greater than 20% in skull and brain size. Whether this process is an adaptation to seasonal climates, resource availability or both remains unclear. We show that European moles (Talpa europaea) also decrease skull size in winter. As resources for closely related Iberian moles (Talpa occidentalis) are lowest in summer, we predicted they should shift the timing of size changes. Instead, they do not change size at all. We conclude that in moles, seasonal decrease and regrowth of skull size is an adaptation to winter climate and not to a changing resource landscape alone. We not only describe this phenomenon in yet another taxon, but take an important step towards a better understanding of this enigmatic cycle.

Antimicrobial Activity of Cathelicidin-Derived Peptide from the Iberian Mole Talpa occidentalis

The immune systems of all vertebrates contain cathelicidins, a family of antimicrobial peptides. Cathelicidins are a type of innate immune effector that have a number of biological functions, including a well-known direct antibacterial action and immunomodulatory function. In search of new templates for antimicrobial peptide discovery, we have identified and characterized the cathelicidin of the small mammal Talpa occidentalis. We describe the heterogeneity of cathelicidin in the order Eulipotyphla in relation to the Iberian mole and predict its antibacterial activity using bioinformatics tools. In an effort to correlate these findings, we derived the putative active peptide and performed in vitro hemolysis and antimicrobial activity assays, confirming that Iberian mole cathelicidins are antimicrobial. Our results showed that the Iberian mole putative peptide, named To-KL37 (KLFGKVGNLLQKGWQKIKNIGRRIKDFFRNIRPMQEA) has antibacterial and antifungal activity. Understanding the antimicrobial defense of insectivores may help scientists prevent the spread of pathogens to humans. We hope that this study can also provide new, effective antibacterial peptides for future drug development.

Cell adhesion and immune response, two main functions altered in the transcriptome of seasonally regressed testes of two mammalian species.

In species with seasonal breeding, male specimens undergo substantial testicular regression during the nonbreeding period of the year. However, the molecular mechanisms that control this biological process are largely unknown. Here, we report a transcriptomic analysis on the Iberian mole, Talpa occidentalis, in which the desquamation of live, nonapoptotic germ cells is the major cellular event responsible for testis regression. By comparing testes at different reproductive states (active, regressing, and inactive), we demonstrate that the molecular pathways controlling the cell adhesion function in the seminiferous epithelium, such as the MAPK, ERK, and TGF-β signaling, are altered during the regression process. In addition, inactive testes display a global upregulation of genes associated with immune response, indicating a selective loss of the "immune privilege" that normally operates in sexually active testes. Interspecies comparative analyses using analogous data from the Mediterranean pine vole, a rodent species where testis regression is controlled by halting meiosis entry, revealed a common gene expression signature in the regressed testes of these two evolutionary distant species. Our study advances in the knowledge of the molecular mechanisms associated to gonadal seasonal breeding, highlighting the existence of a conserved transcriptional program of testis involution across mammalian clades.

Variations in the abundance of the Iberian mole (Talpa occidentalis) in a habitat and climatic gradient in central Spain

Variations in the abundance of the Iberian mole (Talpa occidentalis) in a habitat and climatic gradient in central Spain

Comparative Neurology of Circadian Photoreception: The Retinohypothalamic Tract (RHT) in Sighted and Naturally Blind Mammals.

The mammalian eye contains two systems for light perception: an image detecting system constituted primarily of the classical photoreceptors, rods and cones, and a non-image forming system (NIF) constituted of a small group of intrinsically photosensitive retinal ganglion cells driven by melanopsin (mRGCs). The mRGCs receive input from the outer retina and NIF mediates light entrainment of circadian rhythms, masking behavior, light induced inhibition of nocturnal melatonin secretion, pupillary reflex (PLR), and affect the sleep/wake cycle. This review focuses on the mammalian NIF and its anatomy in the eye as well as its neuronal projection to the brain. This pathway is known as the retinohypothalamic tract (RHT). The development and functions of the NIF as well as the knowledge gained from studying gene modified mice is highlighted. Furthermore, the similarities of the NIF between sighted (nocturnal and diurnal rodent species, monkeys, humans) and naturally blind mammals (blind mole rats Spalax ehrenbergi and the Iberian mole, Talpa occidentalis) are discussed in relation to a changing world where increasing exposure to artificial light at night (ALAN) is becoming a challenge for humans and animals in the modern society.

First spermatological data on the digenean genus Ityogonimus derived from the description of sperm characters of Ityogonimus ocreatus (Brachylaimidae: Ityogoniminae)

The present study describes the ultrastructural organization of the spermatozoa of the brachylaimid digenean Ityogonimus ocreatus (Ityogoniminae) by means of transmission electron microscopy (TEM). Live digeneans were collected from the digestive tract of an Iberian mole Talpa occidentalis (Eulipotyphla, Talpidae) captured accidentally during a vole pest control campaign in Priesca (Asturias, Spain). The TEM study reveals that the I. ocreatus sperm are filiform, tapered at both extremities, and have two 9+'1' trepaxonematan axonemes, external ornamentation of the plasma membrane associated with cortical microtubules, spine-like bodies, two bundles of parallel cortical microtubules and one mitochondrion overlapping the anterior part of the nucleus. The external ornamentation of the plasma membrane is located in the posterior part of the anterior region. The maximum number of parallel cortical microtubules (45) is located in the anterior part of the sperm cells. Our results are compared with the available data on the family Brachylaimidae, especially on the other Ityogoniminae studied to date (Scaphiostomum palaearcticum).

Erratum to “Palaeoecological context for the extinction of the Neanderthals: A small mammal study of Stratigraphic Unit V of the El Salt site, Alcoi, eastern Spain” [Palaeogeography, Palaeoclimatology, Palaeoecology 530 (2019) 163–175

Abstract El Salt is an important reference site for understanding the extinction of Neanderthal populations in the eastern Iberian Peninsula during MIS 3. In this paper, we describe the small mammal assemblage from Stratigraphic Unit V, the youngest unit with evidence of human presence, based on nearly 1300 specimens. A total of seven rodents (Microtus arvalis, Microtus duodecimcostatus, Microtus cabrerae, Sciurus vulgaris, Arvicola sapidus, Eliomys quercinus and Apodemus sylvaticus), three insectivores (Talpa occidentalis, Crocidura sp., Sorex sp.) and one lagomorph (Oryctolagus cf. cuniculus) were identified. Palaeocological analyses point to drier conditions in this part of the stratigraphic sequence, supporting the hypothesis that an aridification scenario may have played a role in the extinction of the Neanderthal groups inhabiting this region of the Iberian Peninsula.

Intersexuality in female moles

Developmental Biology Female moles are intersexual and develop masculinizing ovotestes, a distinctive trait among mammals. Real et al. investigated the origin of this trait by sequencing the Iberian mole genome and applying comparative strategies that integrate transcriptomic, epigenetic, and chromatin interaction data. They identified mole-specific genomic rearrangements that alter the three-dimensional regulatory landscape of the androgen-converting gene CYP17A1 and the pro-testicular factor gene FGF9 , both of which show distinct expression patterns in mole gonads. The use of transgenic mice confirms the capability of these factors to increase circulating testosterone levels and to induce gonadal masculinization. This study highlights how integrative approaches can reveal the phenotypic impact of genomic variation. Science , this issue p. [208][1] [1]: /lookup/doi/10.1126/science.aaz2582

The mole genome reveals regulatory rearrangements associated with adaptive intersexuality.

Linking genomic variation to phenotypical traits remains a major challenge in evolutionary genetics. In this study, we use phylogenomic strategies to investigate a distinctive trait among mammals: the development of masculinizing ovotestes in female moles. By combining a chromosome-scale genome assembly of the Iberian mole, Talpa occidentalis, with transcriptomic, epigenetic, and chromatin interaction datasets, we identify rearrangements altering the regulatory landscape of genes with distinct gonadal expression patterns. These include a tandem triplication involving CYP17A1, a gene controlling androgen synthesis, and an intrachromosomal inversion involving the pro-testicular growth factor gene FGF9, which is heterochronically expressed in mole ovotestes. Transgenic mice with a knock-in mole CYP17A1 enhancer or overexpressing FGF9 showed phenotypes recapitulating mole sexual features. Our results highlight how integrative genomic approaches can reveal the phenotypic impact of noncoding sequence changes.

Ultrastructure and cytochemistry of intrauterine embryonic and larval stages of Ityogonimus lorum (Digenea: Brachylaimidae) involving transitory development of ciliated miracidia

Results of the present study provide ultrastructural evidence that miracidial morphogenesis is fully completed within the intrauterine eggs while in the most posterior uterine regions of Ityogonimus lorum, a digenean parasite of an Iberian mole, Talpa occidentalis (Eulipotyphla, Talpidae). Using transmission electron microscopy (TEM), the ultrastructural characteristics of diverse cell types and their organelles of these developing embryos and fully formed miracidia within the eggshell were examined. The eggshell and embryonic envelopes are similar to those described previously by many authors for other digeneans. However, the developing miracidia are unique among previously described digeneans in possessing transitory cilia during larvigenesis, but completely lacking cilia in fully formed miracidium larvae. The evidence for completion of miracidial maturation in intrauterine eggs is based on the presence of the following structures: (1) transitional stage of ciliated differentiating miracidial epithelium; (2) apical and lateral glands, characteristic for digenean miracidia; and (3) fully developed germinative cells grouped together in the germinative sac localized in the posterior region of the miracidium. The protonephridial system with its characteristic flame cells and the nervous system with diverse types of neurons and nerve centers, which are characteristic for other digenean species reported until now, are absent from all these developmental stages of I. lorum. Based on these observations, we hypothesize that the life cycle of I. lorum is entirely terrestrial, involving passive transmission by ingestion of eggs containing unciliated miracidia to the first intermediate host.

Mercury, Lead and Cadmium Concentrations in Talpa occidentalis and in Their Digeneans of the Genus Ityogonimus.

Many parasites living in aquatic ecosystems are useful indicators of environmental health. On the other hand, information is scarcer with respect to the use of helminth parasites of vertebrates living in terrestrial ecosystems as monitoring tools for toxic element environmental pollution. The present study evaluates the suitability of the model Talpa occidentalis/Ityogonimus spp. as a bioindicator system for mercury (Hg), lead (Pb) and cadmium (Cd) contamination in agricultural soils from Asturias (Spain). Kidney and liver samples collected from T. occidentalis specimens (n=36) and Ityogonimus spp. samples collected from 14 infected hosts were analyzed by ICP-MS. The highest mean levels of Hg and Pb were found in Ityogonimus individuals (20.9 and 12.4µgg-1 wet weight, respectively). Considering renal and hepatic concentrations in T. occidentalis, bioaccumulation factors of Ityogonimus for Hg were 83.7 and 58.6, respectively, whereas concerning Pb bioaccumulation factors were 38.2 and 82.9, respectively. No bioaccumulation was detected in Ityogonimus in the case of Cd. More studies involving digenean parasites of small mammals are needed, especially when biomonitoring environmental toxic element pollution in terrestrial ecosystems. The present results support the above-mentioned model as a suitable biomonitoring system to evaluate environmental Hg and Pb contamination in terrestrial non-urban Iberian habitats. Similar models involving other species (Talpa spp./Ityogonimus spp.) might be used in a much wider geographical range.

Palaeoecological context for the extinction of the Neanderthals: A small mammal study of Stratigraphic Unit V of the El Salt site, Alcoi, eastern Spain

El Salt is emerging as a reference site for the study of the extinction of Neanderthal populations in the Eastern Iberian Peninsula during MIS 3. The small vertebrate assemblage analysed in this work is framed within this general objective and comes from Stratigraphic Unit V, the most recent unit with human presence. Nearly 1300 small mammal remains have been studied in order to reconstruct the palaeoecological conditions of this debated period. A total of seven rodents (Microtus arvalis, Microtus duodecimcostatus, Microtus cabrerae, Sciurus vulgaris, Arvicola sapidus, Eliomys quercinus and Apodemus sylvaticus), three insectivores (Talpa occidentalis, Crocidura sp., Sorex sp.) and one lagomorph (Oryctolagus cf. cuniculus) were identified. Palaeocological analyse points to drier conditions in the upper part (Unit V) of the stratigraphic sequence, supporting the hypothesis that an aridification scenario may have played a role in the disappearance of the Neanderthal groups inhabiting this region of the Iberian Peninsula.

First finding of Ityogonimus lorum and I. ocreatus co-infection in the Iberian mole, Talpa occidentalis.

The Ityogonimus lorum-I. ocreatus co-infection is reported for the first time in the Iberian mole Talpa occidentalis in Asturias (NW Spain). Both Ityogonimus species are stenoxenous helminths of insectivores of the genus Talpa and they have often been found parasitizing the Iberian mole and also the European mole T. europaea, but a mixed infection had not been previously reported. The present study also highlights the main differential morphometric characteristics between I. lorum and I. ocreatus such as the body length, the ventral sucker diameter, the ratio between suckers and the distance between suckers.

Complete mitochondrial genome of the Iberian Mole Talpa occidentalis (Talpidae, Insectivora) and comparison with Talpa europaea.

The complete mitogenome of Talpa occidentalis, the Iberian mole, was sequenced using a combination of the Illumina and Sanger methods. The 16,962bp genome obtained contains 13 protein-coding genes, 22 transfer RNAs, 2 ribosomal RNAs, and a control region. Thirty-seven identical repetitions of a 10-nucleotide (CACACGTACG) repeat element were identified in the non-coding control region (D-loop). The number, order, and orientation of the mitochondrial genes are the same as in T. europaea, the only mitogenome published so far for this genus. These two mitogenomes differ only at the repeat element included in the control region. The phylogeny obtained for the Talpidae species using the protein-coding genes of these mitogenomes agrees with the current classification of this family.

Hox gene expression in the specialized limbs of the Iberian mole (Talpa occidentalis).

Fossorial talpid moles use their limbs predominantly for digging, which explains their highly specialized anatomy. The humerus is particularly short and dorsoventrally rotated, with broadened distal and proximal parts where muscles attach and which facilitate powerful abductive movements. The radius and ulna are exceptionally robust and short. The ulna has an expanded olecranon process. The femur is generalized, but the fused tibia-fibula complex is short and robust. To understand the developmental bases of these specializations, we studied expression patterns of four 5' Hox genes in the fossorial Iberian mole (Talpa occidentalis). These genes are known to play major roles in patterning the developing limb skeleton in the mouse, with which comparisons were made (Mus musculus, C57BL/6Jico strain). We find that HoxA9 expression is spatially expanded in the developing stylopodial area in the mole forelimb, compared to the less specialized mouse forelimb and mole hind limb. HoxD9 expression does not extend into the thoracic body wall in the mole forelimb in contrast to the mouse, and is also reduced in the presumptive zeugopodium in mole forelimb, compared to mouse. Expression of HoxD11 is upregulated in the mole in the postaxial area of the hind limb zeugopod, compared to the mouse. On the other hand, HoxD13 is downregulated in the postaxial zeugopodial area in the forelimb of the mole, compared to the mouse. The differences in the expression patterns of these 5' Hox genes between Talpa and Mus are an indication of the developmental changes going hand in hand with anatomical digging adaptations in the mole adult.

The placentation of eulipotyphla-reconstructing a morphotype of the Mammalian placenta.

Placentation determines the developmental status of the neonate, which can be considered as the most vulnerable stage in the mammalian life cycle. In this respect, the different evolutionary and ecological adaptations of marsupial and placental mammals have most likely been associated with the different reproductive strategies of the two therian clades. The morphotypes of marsupial and placental neonates, as well as the placental stem species pattern of Marsupialia, have already been reconstructed. To contribute to a better understanding of the evolution of Placentalia, a histological and ultrastructural investigation of the placenta in three representatives of Eulipotyphla, that is, core insectivores, has been carried out in this study. We studied the Musk shrew (Suncus murinus), the four-toed hedgehog (Atelerix albiventris), and the Iberian mole (Talpa occidentalis). As a result, a eulipotyphlan placental morphotype consisting of a compact and invasive placenta was reconstructed. This supports the widely accepted hypothesis that the stem lineage of Placentalia is characterized by an invasive, either endothelio- or hemochorial placenta. Evolutionary transformations toward a diffuse, noninvasive placenta occurred in the stem lineages of lower primates and cetartiodactyles and were associated with prolonged gestation and the production of few and highly precocial neonates. Compared to the choriovitelline placenta of Marsupialia, the chorioallantoic placenta of Placentalia allows for a more intimate contact and is associated with more advanced neonates.

Genetic Diversity of Talpa Europaea and Nova Hanta Virus (NVAV) in France.

Nova hantavirus (NVAV) was first identified in a single European mole (Talpa europaea), captured in Hungary. Analysis of lung tissues from 94 moles captured in France revealed NVAV in 50%. Based on the genetic diversity of the cytochrome b mtDNA, moles collected in Poitiers and Bordeaux were more closely related to the Iberian mole (T. occidentalis), a species previously assumed to be restricted to the Iberian Peninsula. Several hypotheses are discussed to explain these observations: 1) presence of hitherto unnoticed T. occidentalis in southwestern France; 2) existence of an ancient mitochondrial introgression phenomenon between the two Talpa species, producing a particular phenotype in some hybrids; 3) existence of a hybrid zone between the two species; and 4) existence of a new Talpa species. NVAV was not detected in the southwestern moles, which begs the question of the potential presence of a particular Hantavirus sp. in this population and/or in the Iberian moles.

Scaling of species distribution models across spatial resolutions and extents along a biogeographic gradient. The case of the Iberian mole Talpa occidentalis

Scaling is a key process in modelling approaches since it allows for translating information from one scale to another. However, the success of this procedure may depend on ‘source’ and ‘target’ scales, but also on the biogeographic/ecological context of the study area. We aimed to quantify the performance and success of scaling species distribution model (SDM) predictions across spatial resolution and extent along a biogeographic gradient using the Iberian mole as study case. We ran separate MaxEnt models at two extents (national and regional) using independent datasets (species locations and environmental predictors) collected at 10 km and 50 m resolutions respectively. Model performance and success of scaling SDMs were quantified on the basis of accuracy measures and spatial predictions. Complementarily, we calculated marginality and tolerance as indicators of habitat availability and niche truncation along the biogeographic gradient. Model performance increased with resolution and extent, as well as from north to south (mainly for high resolution models). When regional models were validated at different scales, their performance reduced severely, particularly in the case of coarse resolution models (some of them performed worse than random). However, when the 10 km‐national model was downscaled within regions, it performed better (AUCtest: 0.82, 0.85 and 0.55 respectively for Galicia, Madrid and Granada) than models specifically calibrated within each region at 10 km (0.47, 0.65, 0.44). Indeed, it also had a better accuracy when projected at 50 m (0.77, 0.91, 0.79) than models fitted at that resolution (0.62, 0.83, 0.96) in two of the three cases. The success of scaling model predictions decreased along the biogeographic gradient, being these differences associated to niche truncation. Models representing non‐truncated niches were more successfully scaled across resolutions and extents (particularly in areas not offering all possible habitats for species), which has important implications for SDM applications.

Identification of Live Germ-Cell Desquamation as a Major Mechanism of Seasonal Testis Regression in Mammals: A Study in the Iberian Mole (Talpa occidentalis)1

In males of seasonally breeding species, testes undergo a severe involution at the end of the breeding season, with a major volume decrease due to massive germ-cell depletion associated with photoperiod-dependent reduced levels of testosterone and gonadotropins. Although it has been repeatedly suggested that apoptosis is the principal effector of testicular regression in vertebrates, recent studies do not support this hypothesis in some mammals. The purpose of our work is to discover alternative mechanisms of testis regression in these species. In this paper, we have performed a morphological, hormonal, ultrastructural, molecular, and functional study of the mechanism of testicular regression and the role that cell junctions play in the cell-content dynamics of the testis of the Iberian mole, Talpa occidentalis, throughout the seasonal breeding cycle. Desquamation of live, nonapoptotic germ cells has been identified here as a new mechanism for seasonal testis involution in mammals, indicating that testis regression is regulated by modulating the expression and distribution of the cell-adhesion molecules in the seminiferous epithelium. During this process, which is mediated by low intratesticular testosterone levels, Sertoli cells lose their nursing and supporting function, as well as the impermeability of the blood-testis barrier. Our results contradict the current paradigm that apoptosis is the major testis regression effector in vertebrates, as it is clearly not true in all mammals. The new testis regression mechanism described here for the mole could then be generalized to other mammalian species. Available data from some previously studied mammals should be reevaluated.