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—Representative individuals showing developmental stages s4–s15 for Talpa occidentalis. All images are shown at the same magnification to indicate relative sizes. Arrow indicates skin fold over base of tail, present in s14 but not s15.
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Moles are the only fertile true hermaphrodites described up to now among mammals. This paper investigates the development and growth of the mole Talpa occidentalis. Fifteen developmental stages (8 prenatal and 7 postnatal) were established and 12 of them, ranging from early gestation to weaning, are described in detail. The growth of moles was show...
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... of stages for mole development.-We established a total of 15 developmental stages, from stage 1 (s1) to stage 15 (s15), comprising the entire development of T. occidentalis (Table 1; Fig. 1). Prenatal development comprises 8 stages (s1- s8) defined according to the criteria proposed by Sterba (1977) for the prenatal development of T. europaea. Description of stages before s4 was not possible due to inadequate sample size. Examination of our data suggests that birth takes place approximately 28 days postcoitus. Because no ...
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... As for fetuses, the exact day age of species, other than a few species of S. murinus, is unknown. Hence, we used the crown-rump length (CRL) and the external characteristics, based on Vogel (1972), Sterba (1977), and Barrionuevo et al. (2004) to infer the rough developmental stage. Based on the study that observed the initial protrusion of the turbinal (Parker 1885), we specified CRL 10 as the early stage. ...
... Based on the study that observed the initial protrusion of the turbinal (Parker 1885), we specified CRL 10 as the early stage. We specified those with approximately CRL 20 as late stage (the gestation length of T. europaea, Crocidura russula, and Sorex etruscus are commonly about 30 days) (Vogel 1972;Barrionuevo et al. 2004). Based on the size of the CRL (approximately CRL 15) and the external characteristics, it was presumed that the turbinals and laminae of the mid stage were more developed than those of the early stage. ...
The phylogenetic relationships of major groups within the Order Eulipotyphla was once highly disputed, but the advent of molecular studies has greatly improved our understanding about the diversification history of talpids, soricids, erinaceids, and solenodontids. Their resolved phylogenetic relationships now allow us to revisit the turbinal and lamina evolution of this group. The inner structure of the nasal cavity of mammals is highly complicated and the homologies of the turbinals among mammalian species are still largely unsettled. In this regard, investigation on fetal anatomy and ontogenetic changes of the nasal capsule allows us to evaluate the homologies of the turbinals and laminae. We observed various fetuses and adults of talpids and soricids using high-resolution diffusible iodine-based contrast-enhanced computed tomography (diceCT) and reviewed previous reports on erinaceids, solenodontids, and other laurasiatherians. Although the turbinal and lamina morphology was previsouly considered to be similar among eulipotyphlans, we found phylogenetic patterns for talpids and soricids. The nasoturbinal of the common ancestor of talpids and soricids was most likely rostrocaudally elongated. The epiturbinal at the ethmoturbinal II disappeared in soricids independently. Finally, we propose two possible scenarios for the maxilloturbinal development: 1) the maxilloturbinal of talpids and soricids became small independently with a limited number of lamellae as a result of convergent evolution, or 2) the common ancestor of talpids and soricids already had a small and simple maxilloturbinal.
... Both sexes are represented in the sample and all individuals are considered fully adult, that is, specimens whose genitalia were well developed and whose weight corresponded to adult specimens. The thresholds used to define adult individuals are 65 g for males and 53 g for females of T. occidentalis (Barrionuevo et al., 2004), 87 g for males and 72 g for females of T. ...
The forelimb is involved in many behaviours including locomotion. Notably, the humero-ulnar articulation, implicated in the elbow joint, is of particular importance for both mobility and stability. Functional constraints, induced in part by environmental plasticity, are thought to drive an important part of the bone shape as bone directly responds and remodels in response to both muscle and external forces. In this context, the study of subterranean moles is of particular interest. These moles occupy a hard and heavy medium in comparison with air or water, requiring a powerful body structure to shear and shift the soil. Their general morphology is therefore adapted to digging and to their subterranean lifestyle. The various morpho-functional patterns, which drive diverse abilities according to the environment, are likely targets of natural selection and it is, therefore, useful to understand the relationships between the bone shape and their function. Here, we quantify, through 3D geometric morphometric methods, the interspecific variability in the morphology of the ulna and humerus of three Talpa species, including the new species Talpa aquitania, to infer their potential consequence in species digging performance. We also quantify shape covariation and morphological integration between the humerus and the ulna to test whether these bones evolve as a uniform functional unit or as more or less independent modules. Our results show that interspecific anatomical differences in the humerus and ulna exist among the three species. Shape changes are mostly located at the level of joints and muscle attachments. As the species tend to live in allopatry and the fossorial lifestyle induces strong ecological constraints, interspecific variations could be explained by the properties of the environment in which they live, such as the compactness of the soil. Our results also show that the humerus and ulna are highly integrated. The covariation between the humerus and ulna in moles is dominated by variation in the attachment areas and particularly of the attachment areas of shoulder muscles concerning the humerus, which affect the mechanical force deployed during locomotion and digging. This study also highlights that in the new species, T. aquitania, variations in anatomical structure (general shape and joints) exist and are related to the locality of collect of the individuals.
... The Iberian mole (Talpa occidentalis) is a soricomorphic mammal in the Talpidae family that feeds on subterranean larvae and worms. It is mainly found in Spain and Portugal and it belongs to the Eulipotyphla order [10]. Eulipotyphla is the third most diverse order of mammals, with more than 450 identified extant species. ...
... Cc- [9][10]17,21,32,38,[40][41] value for the hydrophobic moment (0.148) corresponded to the helix of the common shrew (Solex araneus) Sa-NN35. We next studied the possible influence of the amphipathic properties of the helices and tertiary structures of the putative peptides of the cathelicidins from the Eulipotyphla order in the capacity to interact with biological membranes. ...
... To- 6,[9][10]14,17,20,24,[27][28][31][32][34][35]37 89 (Solex araneus) Sa-NN35. We next studied the possible influence of the amphipathic properties of the helices and tertiary structures of the putative peptides of the cathelicidins from the Eulipotyphla order in the capacity to interact with biological membranes. ...
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.
... Sorex araneus 29 29 Figure 4, listed by day Vogel (1972) Talpa occidentalis 60 1 month of lactation weaning Barrionuevo et al. (2004) ...
Organismal development is defined by progressive transformations that ultimately give rise to distinct tissues and organs. Thus, temporal shifts in ontogeny often reflect key phenotypic differences in phylogeny. Classical theory predicts that interspecific morphological divergence originates towards the end of embryonic or fetal life stages, i.e. the early conservation model. By contrast, the hourglass model predicts interspecific variation early and late in prenatal ontogeny, though with a phylogenetically similar mid-developmental period. This phylotypic period, however, remains challenging to define within large clades such as mammals. Thus, molecular and morphological tests on a mammalian hourglass have not been entirely congruent. Here, we report an hourglass-like pattern for mammalian developmental evolution. By comparing published data on the timing of 74 homologous characters across 51 placental species, we demonstrated that variation in the timing of development decreased late in embryogenesis––when organ formation is highly active. Evolutionary rates of characters related to this timeframe were lowest, coinciding with a phylotypic period that persisted well beyond the pharyngula ‘stage’. The trajectory culminated with elevated variation in a handful of fetal and perinatal characters, yielding an irregular hourglass pattern. Our study invites further quantification of ontogeny across diverse amniotes and thus challenges current ideas on the universality of developmental patterns.
... El tamaño medio de camada es de cuatro crías, aunque puede oscilar entre dos y seis (Blanco, 1998;Román, 2007), siendo estas altriciales (Román, 2007). La emancipación de las crías tiene lugar aproximadamente un mes después de su nacimiento (Barrionuevo et al., 2004a). Además, como característica exclusiva, los topos son los únicos mamíferos hermafroditas fértiles (Barrionuevo et al., 2004b). ...
... En las hembras de topo ibérico, el coeficiente de esfuerzo reproductivo materno, definido como la masa de la descendencia en el destete en relación con la masa de la madre, es inversamente proporcional a la masa materna (Barrionuevo et al., 2004a). Comparados con otros insectívoros soricomorfos de menor masa corporal (musarañas), en los topos dicho coeficiente (2.69) es significativamente más alto que el esperado (1.91), lo que conlleva que su esfuerzo reproductivo sea un 36,4% mayor (Barrionuevo et al., 2004a). ...
... En las hembras de topo ibérico, el coeficiente de esfuerzo reproductivo materno, definido como la masa de la descendencia en el destete en relación con la masa de la madre, es inversamente proporcional a la masa materna (Barrionuevo et al., 2004a). Comparados con otros insectívoros soricomorfos de menor masa corporal (musarañas), en los topos dicho coeficiente (2.69) es significativamente más alto que el esperado (1.91), lo que conlleva que su esfuerzo reproductivo sea un 36,4% mayor (Barrionuevo et al., 2004a). Este dato implica que las hembras de topo presentan una increíble capacidad de alimentación de las crías en comparación con otros insectívoros. ...
... In late April, we collected young moles (age I) and April is considered to be the dispersal season. According to Barrionuevo et al. (2004), regarding mole reproduction in Europe, the mating season is considered to be from late February (when showing maximum sizes of testes) to the late April based on the enlargements of the section profiles of the seminiferous tubules (Figs. 1 and 3). Furthermore, the birthing season is considered to be from late March to the early June based on the collecting dates and the profile changes of the seminiferous tubules in the age I individuals (Table 2, and Figs. 1 and 3). ...
We researched seasonal reproductive activity in the lesser Japanese mole, Mogera imaizumii, by morphometrical and histological methods for male internal genitalia using samples from Kanagawa Pref., central Honshu, Japan. On the basis of the weights of testis and the epididymis, we determined that their weights become higher during February–April. On the other hand, the histological profiles of seminiferous tubules showed variable states annually. In the late winter, a seminiferous tubule profile was mainly occupied with spermatocytes. In addition, in the spring, the profile was also occupied with spermatids increased in the profile. Moreover, from the early summer to the early winter, spermatogonia occupied and this status indicates lower reproductive activity. Accordingly, current results indicated that breeding behavior would be active during the late winter through spring in our research locality.
... Similar to the findings for other mammals (Blasco et al., 2003;Barrionuevo et al., 2004), sexual dimorphism in giant pandas does not contribute to differences in growth during early developmental stages. We did not detect a significant difference in growth between male and female giant panda cubs from 0 to 120 days after birth. ...
Giant panda cubs have a low survival rate during the newborn and early growth stages. However, the growth and developmental parameters of giant panda cubs during the early lactation stage (from birth to 6 months) are not well known. We examined the growth and development of giant panda cubs by the Chapman growth curve model and estimated the heritability of the maximum growth rate at the early lactation stage. We found that 83 giant panda cubs reached their maximum growth rate at approximately 75-120 days after birth. The body weight of cubs at 75 days was 4285.99 g. Furthermore, we estimated that the heritability of the maximum growth rate was moderate (h2 = 0.38). Our study describes the growth and development of giant panda cubs at the early lactation stage and provides valuable growth benchmarks. We anticipate that our results will be a starting point for more detailed research on increasing the survival rate of giant panda cubs. Feeding programs for giant panda cubs need further improvement.
... The European mole Talpa europea and the star-nose mole Candilura cristata have a penile clitoris, which is not trespassed by the urethra, and an ovotestis ( RUBENSTEIN et al., 2003), which are bipolar gonads with the characteristics of testicles and ovaries (BARRIONUEVO et al., 2004). ...
The yellow-toothed cavy (Galea spixii) is a hystricomorph rodent of the Caviidae family. In Brazil, G. spixii are bred in captivity to provide an alternative protein source and to preserve the species. However, there is a lack of data on the animal´s female genital organs. Current research describes the morphology of the species´s adult female genital organs, regardless of the stage of its estrous cycle, and permits basic knowledge on its anatomy that will be a help for future projects in reproduction in captivity. Adult female genital organs of G. spixii comprise two ovaries with follicles at several developmental stages; uterine tubes whose epithelium and muscular layer thickness modify themselves throughout the isthmus, ampulla and infundibulum regions; double uterus and uterine horns with uterine glands that open to a single cervix which is linked to the vagina by the fornix; a variegated vaginal epithelium from different animals; a vulva with a clitoris trespassed by the urethra which features a lack of vaginal vestibule and the presence of a vaginal closure membrane. The morphology of G. spixii female genitalia has interesting characteristics such as the vaginal closure
membrane and a clitoris trespassed by urethra that needs further studies. Other investigations on developmental biology could demonstrate a possible intrauterine masculinization in the G. spixii female.
... Although some studies concentrated on the general reproductive patterns of Eulipotyphla (e.g., Deanesly, 1966;Dryden, 1969;Dryden and Anderson, 1977;Fowler and Racey, 1986;Rissman and Bronson, 1987;Chang et al., 1999;Bedford et al., 2000;Barrionuevo et al., 2004b;Spicer et al., 2009), only little information about their placentation is available. The few studies concerning eulipotyphlan placentation are contradictory in their results. ...
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. J. Morphol., 2014. © 2014 Wiley Periodicals, Inc.
... The skeletal development of Talpa, ranging from chondrogenesis to skeletogenesis, has been extensively investigated (Sterba 1972(Sterba , 1973(Sterba , 1975(Sterba , 1976(Sterba , 1977(Sterba , 1980Sterba and Zelen y 1974;Barrionuevo et al. 2004;Prochel 2006;Prochel et al. 2008). However, none of these studies have addressed the humerus in detail, which is surprising given its derived anatomy in fossorial forms. ...
... In the latter, gestation lasts approximately 22 days (Mock 1982). In Talpa occidentalis, gestation lasts approximately 28 days (Barrionuevo et al. 2004), whereas in Urotrichus talpoides, it is 30 days (Usuki 1968). The gestational age of Talpa specimens was estimated following Jiménez et al. (1988) and Edwards (1937) and Woodman et al. (2003): an, anterior notch; c, capitulum: dma, attachment of deltoid muscle; gt, greater tuberosity; hh, humeral head; le, lateral epicondyle; me, medial epicondyle; o, olecranon fossa; pn, posterior notch; sf, supracondylar foramen; t, trochlea; tt, teres tubercle. ...
... Each scale bars equal 5 mm. Barrionuevo et al. (2004). To282 is an embryo which is 18 days old (s5b, corresponds approximately to ontogenetic stage in Fig. 2C), To317 19 days (s5c, corresponds approximately to Fig. 2D) and To810-2 21-23 days (s7, corresponds in age approximately to the specimen in Fig. 2F). ...
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.
