Early skeletal development in Talpa europaea, the common European mole

An ontogenetic series of 22 cleared and double-stained prenatal specimens was used to study the sequence of ossification of selected postcranial skeletal elements of Talpa europaea. Results were compared with nine other therian mammals, with Alligator, Chelydra, and Lacerta as outgroups. Using the event-pairing method, shifts in the onset of ossification in T. europaea, Sus, and Homo were identified. In T. europaea, the ossification of the cervical vertebrae starts before the metatarsals. In Homo and Sus, the tarsals ossify before the pubic bone. These shifts in the sequence of ossification are unique among the mammals examined, whereas many other changes, characterising monophyletic groups and/or evolving convergently, were also identified. Particular attention was given to some peculiar calcified elements of the hand in T. europaea, which were identified as accessory ;sesamoid bones', and do not display a chondrified precursor. They start to calcify before all others of the hand and later fuse. They appear in all fingers and function as reinforcement for the distal phalanges, most likely as an adaptation for burrowing. The development of the sesamoid bones was examined using histological sections and macerated adults.     

Apical protuberances of supporting cells in the regio olfactoria of the mole,Talpa europaea,Linnaeus, 1758 (Insectivora,Talpidae)

Summary The regio olfactoria of the mole, Talpa europaea, was studied by scanning and transmission electron microscopy. Peculiar structural differentiations, i.e. ovoid-shaped, balloon-like protuberances were found on the surface of the supporting cells. The apical portion of these protuberances contained finely dispersed granular material, whereas in their central part vesicular extensions of the smooth endoplasmic reticulum were observed.     

The pineal gland of the mole (Talpa europaea L.)

Summary The ultrastructure of the mole pinealocytes, a mammal which lives practically in complete darkness, has been examined and compared with that of other mammals. Mitochondria, ribosomes, smooth and granular endoplasmic reticulum, lysosomes and lipid incluclusions are present in the perikaryon. The presence of a paracrystalline structure of a possibly proteinaceous nature in some cisterns of the granular endoplasmic reticulum and between the two layers of the nuclear membrane, is characteristic of the mole pinealocyte. The Golgi complex produces clear vesicles of 500–1500 Å in diameter. Occasionally, some dense core secretory vesicles were observed in the perikaryon and in the ending of cell processes. Their presumed origin from the Golgi complex could not yet be demonstrated. A large number of ciliary derivatives (9+0 pattern) are also present in the mole pinealocyte.

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Résumé Les pinéalocytes (au sens strict: Wolfe, 1965) de l'épiphyse de la Taupe (animal vivant pratiquement toujours dans une complète obscurité) examinés au microscope électronique, ont été comparés à ceux d'autres Mammifères. Dans le périkaryon des mitochondries, des ribosomes, du réticulum endoplasmique lisse et granulaire et quelques lysosomes et inclusions lipidiques sont présents. La présence à l'intérieur de certaines cavités du réticulum endoplasmique granulaire et parfois entre les deux feuillets de l'enveloppe nucléaire, de structures paracristallines (de nature protéique ?) est caractéristique des pinéalocytes de cet animal. L'appareil de Golgi sécréte des vésicules claires de 500 à 1500 Å de diamètre. Quelques très rares grains de sécrétion, dont l'origine golgienne n'a pas encore été démontré, ont été observé dans le périkaryon et à l'extrémité de certains prolongements. Un grand nombre de structures ciliaires (9+0 paires de tubules) ont également été observés dans les pinéalocytes.

     

The pineal gland of the mole (Talpa europaea L.)

Summary The pineal gland of the mole, a mammal which lives in permanent darkness, has been studied using fluorescence histochemistry. An extensive catecholaminergic innervation is demonstrated. A yellow formaldehyde-induced fluorescence, characteristic of indoleamines, was not observed. If formaldehyde vapour treatment was omitted in the procedure, numerous cells containing yellow-orange autofluorescent material could be shown. The nature and possible function of this material is discussed.This paper is dedicated in great admiration and appreciation to Prof. Dr. W. Bargmann on the occasion of his 70th birthday.     

Tracing the evolutionary history of the mole,Talpa europaea,through mitochondrial DNA phylogeography and species distribution modelling

Our understanding of the effect of Pleistocene climatic changes on the biodiversity of European mammals mostly comes from phylogeographical studies of non‐subterranean mammals, whereas the influence of glaciation cycles on subterranean mammals has received little attention. The lack of data raises the question of how and to what extent the current amount and distribution of genetic variation in subterranean mammals is the result of Pleistocene range contractions/expansions. The common mole (Talpa europaea) is a strictly subterranean mammal, widespread across Europe, and represents one of the best candidates for studying the influence of Quaternary climatic oscillation on subterranean mammals. Cytochrome b sequences, as obtained from a sampling covering the majority of the distribution area, were used to evaluate whether Pleistocene climate change influenced the evolution of T. europaea and left a trace in the genetic diversity comparable to that observed in non‐subterranean small mammals. Subsequently, we investigated the occurrence of glacial refugia by comparing the results of phylogeographical analysis with species distribution modelling. We found three differentiated mitochondrial DNA lineages: two restricted to Spain and Italy and a third that was widespread across Europe. Phylogenetic inferences and the molecular clock suggest that the Spanish moles represent a highly divergent and ancient lineage, highlighting for the first time the paraphyly of T. europaea. Furthermore, our analyses suggest that the genetic break between the Italian and the European lineages predates the last glacial phase. Historical demography and spatial principal component analysis further suggest that the Last Glacial Maximum left a signature both in the Italian and in the European lineages. Genetic data combined with species distribution models support the presence of at least three putative glacial refugia in southern Europe (France, Balkan Peninsula and Black Sea) during thelast glacial maximum that likely contributed to post‐glacial recolonization of Europe. By contrast, the Italian lineage remained trapped in the Italian peninsula and, according to the pattern observed in other subterranean mammals, did not contribute to the recolonization of northern latitudes. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 495–512.     

The central visual pathways and their functional significance in the mole(Talpa europaea)

Anatomical studies on the visual system of the mole (Talpa europaea) using degeneration techniques, show that the distribution of optic fibres is reduced compared with hedgehog and other mammals. In five of the six moles studied, degeneration after eye removal was found in only the pretectal region and the ventral lateral geniculate body. A behavioural study shows that moles can respond to some visual stimuli and learn a light-dark discrimination.     

Factors affecting the distribution of the mole (Talpa europaea) in Snowdonia (North Wales)

Moles are widespread in the uplands of Snowdonia, North Wales, and their distribution has been studied in relation to soil physical and chemical characteristics. Moles are significantly associated with freely drained mineral soils of pH greater than about 4.0. They are not present in soils with a very stony matrix which would preclude the construction of an effective tunnel system. Data are presented showing that moles are associated with sites showing a high return of sheep dung and the reason for this may be an increase in arthropod populations associated with decaying dung. The sites sampled which were not selected with this study in mind show that no factors other than soil characteristics need be invoked to explain the present distribution of moles.     

Size matters: mole (Talpa europaea) hills and nest-site selection of the ant Formica exsecta

Moles are fossorial mammals that can act both as zoogeomorphic agents and species diversity drivers. These popular animals regularly push heaps of earth from their subterranean tunnel systems to the surface. Thereby they rearrange and improve the local microtopography for ant nesting. Here we use a strongly molehill (Talpa europaea) mediated nest system of the unicolonial wood ant Formica (Coptoformica) exsecta to test for ecological factors influencing nest-site selection at the microhabitat scale. Our results show that the size of molehills plays an important role in the multifactorial process of the ant’s nest-site choice with solar insolation as a paramount factor. The ants clearly favored larger and better sun-exposed molehills, suggesting that the coaction of a zoogeomorphic modified microrelief and solar insolation can drive the spatial colonization of F. exsecta.     

Seasonal changes in the fine structure of the accessory sex gland in the mole (Talpa europaea)

The mole has a single pair of accessory sex organs with features of both the prostate and the seminal vesicle, for which the term prostate gland is not appropriate. Seasonal changes occuring in this gland were related to four periods: a) the quiescence period, b) the maturation period, c) the active period and d) the involution period. During the quiescence period the cuboidal epithelial cells display a quasi-embryonic fine structure and are sparse in cytoplasmic organelles, but rich in glycogen and lipopigment. With the onset of sexual activity glycogen and lipopigment disappear and the rough endoplasmic reticulum as well as the Golgi apparatus begin to proliferate. The fully active gland is lined by a low epithelium with parallel stacks of rough endoplasmic reticulum, a large Golgi apparatus and several lysosomes and secretory granules. In the involution period the gland collapses and the epithelial cells are eliminated by hetero- and autophagic processes. During this period a great number of presumably endocrine cells were observed. The results were compared with findings in experimental studies and those on postnatal development of accessory sex glands in laboratory animals.     

Zoo-FISH in the European mole (Talpa europaea) detects all ancestral Boreo-Eutherian human homologous chromosome associations

Zoo-FISH with human whole-chromosome paint probes delineated syntenic association of human homologous chromosome segments 3-21, 14-15, 16-19, 4-8, 7-16 and 12-22 (twice) in the European mole (Talpa europaea, Talpidae, Eulipotyphla, Mammalia). These segment associations represent shared ancestral Boreo-Eutherian traits, half of which were previously not described for Eulipotyphla. The karyotype of the European mole acquired a minimum of 19 translocations and six inversions compared to the presumed Boreo-Eutherian ancestor.     

Vacuolated pinealocytes in the hedgehog (Erinaceus europaeus L.) and the mole (Talpa europaea L.)

Special cells in the hedgehog and mole pineal gland which are characterized by an enormous single vacuole were studied. The presence of secretory granules (in the hedgehog) and of paracrystalline structures (in the mole) in the cytoplasm of these cells indicates that they are pinealocytes.     

Evolution of crystallins: expression of lens-specific proteins in the blind mammals mole (Talpa europaea) and mole rat (Spalax ehrenbergi)

The mole (Talpa europaea; Insectivora) and the mole rat (Spalax ehrenbergi; Rodentia) both have degenerated eyes as a convergent adaptation to subterranean life. The rudimentary eye lenses of these blind mammals no longer function in a visual process. The crystallin genes, which display a lens-specific expression pattern, were studied in these blind mammals and in related species with normal eyes by hybridizing their genomic DNAs with probes obtained from cDNA clones for alpha A-, alpha B-, and beta Bp-crystallins from calf and gamma 3- crystallin from the rat. For all crystallin genes examined, the hybridization signals of mole and mole rat genomic DNA were comparable, respectively, with those of shrew and of rat and mouse, normal-vision representatives of the orders Insectivora and Rodentia. The expression of the crystallins at the protein level was tested by using antiserum specific for alpha-crystallin in immunofluorescence reactions on lens sections of mole and mole rat eyes and by using antisera against the beta- and gamma-crystallins on sections of the mole eye. All antisera gave positive fluorescence reactions exclusively with lens tissue of these blind mammals, indicating that the crystallins are still normally expressed despite the fact that these lenses have had no function in a visual process in these mammals for at least many million years. These findings apparently imply that some unknown selective advantage has conserved the crystallin genes and their expression after the loss of normal function of the lenses.