Geographic variation and evolutionary relationships among broad-clawed shrews of the Cryptotis goldmani-group (Mammalia, Insectivora, Soricidae) / Neal Woodman, Robert M. Timm.

n.s. no.91(1999)

Intraspecific and interspecific variation in the Cryptotis nigrescens species complex of small-eared shrews (Insectivora, Soricidae) : with the description of a new species from Colombia / Neal Woodman, Robert M. Timm.

n.s. no.74(1993)

Phylogeographical footprints of the Strait of Gibraltar and Quaternary climatic fluctuations in the western Mediterranean: a case study with the greater white-toothed shrew, Crocidura russula (Mammalia: Soricidae).

We used mitochondrial cyt b sequences to investigate the phylogenetic relationships of Crocidura russula (sensu lato) populations across the Strait of Gibraltar, western Europe, Maghreb, and the Mediterranean and Atlantic islands. This revealed very low genetic divergence between European and Moroccan populations. The application of a molecular clock previously calibrated for shrews suggested that the separation of European from Moroccan lineages occurred less than 60 000 bp, which is at least 5 million years (Myr) after the reopening of the Strait of Gibraltar. This means that an overwater dispersal event was responsible for the observed phylogeographical structure. In contrast, genetic analyses revealed that Moroccan populations were highly distinct from Tunisian ones. According to the molecular clock, these populations separated about 2.2 million years ago (Ma), a time marked by sharp alternations of dry and humid climates in the Maghreb. The populations of the Mediterranean islands Ibiza, Pantelleria, and Sardinia were founded from Tunisian populations by overwater dispersal. In conclusion, overwater dispersal across the Strait of Gibraltar, probably assisted by humans, is possible for small terrestrial vertebrates. Moreover, as in Europe, Quaternary climatic fluctuations had a major effect on the phylogeographical structure of the Maghreb biota.

Secondary contact zones and hybridizations: the case of the lesser white-toothed shrew (Crocidura suaveolens group, Soricidae)

In the present study, we analyzed 58 samples of the lesser white-toothed shrew group (Crocidura suaveolens) from eastern Europe and Turkey, where, according to previous publications, three different mitochondrial and nuclear lineages are present. We sequenced 799 bp of the nuclear BRCA1 gene and 400 bp of the mitochondrial cytochrome b gene to: (1) determine a potential contact zone between the lineages; (2) detect hybridizations and introgressions between them; and (3) comment on the level of reproductive isolation of the different lineages. We revealed two zones of hybridization in Turkey, of which the first occurred west of the Bosphorus Straits (three hybrids) and the second in Anatolia (twelve hybrids). In the latter, the nuclear markers revealed a large zone of hybridization, of approximately 600 km. It also revealed that hybrids of first, second, and later generations are present within the populations, and therefore that the reproductive isolation between the different lineages is weak.

Ecologie d'une population de Crocidura russula en milieu rural montagnard (Insectivora, Soricidae)

Crocidura russula is restricted to the vicinity of human dwellings in the northern parts of its range and in the mountain regions of Central and Western Europe. In order to better understand the causes of such a distribution, a population was studied in a rural mountain habitat (750 m above sea level), where the species was found almost exclusively in the neighbourhood of human dwellings. The study was conducted on a 2000 m2 area, over a period of 20 months, by live-trapping and radioactive tracking. The abundance, the local distribution and the behaviour of the shrews vary greatly throughout the year. In summer, they chiefly inhabit areas with a dense herbaceous cover or shruby vegetation; they are mainly active at ground level, in the litter. In autumn, changes in the environmental conditions (lowering of temperatures, subsidence of the herbaceous vegetation, presence of snow) create important energetic problems. At that time, the shrews gradually become more active around and inside compost-heaps and buildings. The microclimate of such environments is mild and prey are numerous. The winter population is reduced (reaching its lowest level in late winter) and consists only of shrews frequenting these sites. The observed spatial distribution is the result of the energetic dependence of the wintering shrews on human dwellings and their surroundings. This dependence is probably related to the physiological characteristics of the species. In the prospected region, Crocidura russula is the only shrew which regularly takes advantage of man-made habitats; the maintenance of the species in the rural mountain enviroment is probably favoured by the social organization of the populations in winter. The other native Soricids are observed only occasionaly int he neighbourhood of human dwellings.

Biogeographic origin and radiation of the Old World crocidurine shrews (Mammalia: Soricidae) inferred from mitochondrial and nuclear genes.

The crocidurine shrews include the most speciose genus of mammals, Crocidura. The origin and evolution of their radiation is, however, poorly understood because of very scant fossil records and a rather conservative external morphology between species. Here, we use an alignment of 3560 base pairs of mitochondrial and nuclear DNA to generate a phylogenetic hypothesis for the evolution of Old World shrews of the subfamily Crocidurinae. These molecular data confirm the monophyly of the speciose African and Eurasian Crocidura, which also includes the fossorial, monotypic genus Diplomesodon. The phylogenetic reconstructions give further credit to a paraphyletic position of Suncus shrews, which are placed into at least two independent clades (one in Africa and sister to Sylvisorex and one in Eurasia), at the base of the Crocidura radiation. Therefore, we recommend restricting the genus Suncus to the Palaearctic and Oriental taxa, and to consider all the African Suncus as Sylvisorex. Using molecular dating and biogeographic reconstruction analyses, we suggest a Palaearctic-Oriental origin for Crocidura dating back to the Upper Miocene (6.8 million years ago) and several subsequent colonisations of the Afrotropical region by independent lineages of Crocidura.

Kälteresistenz und reversible Hypothermie der Etrskerspitzmaus (Suncus etruscus, Soricidae, Insectivora)

On a testé la sensibilité présumée aux basses températures de Suncus etruscus, le plus petit mammifère connu. Nourri à profusion, cette espèce a supporté des températures inférieures à 0° C. L'activité de l'animal (=absence du nid) à une température ambiante de 0-10° C s'élève en moyenne de 303min/24 h contre 358 min24 h à des températures de 15°-20° C. Si on retire toute nourriture à la musaraigne étrusque, celle-ci entre en hypothermie réversible et léthargique, de laquelle elle sort de temps en temps à la recherche de nourriture. En léthargie, la température corporelle est d'environ 2° C au dessus de la température ambiante. Avec 1 1/2 à 2 g de nourriture par jour et à la température ambiante de 16° à 18° C, les phases de léthargie durent de 1 1/2 à 2 h avec un maximum de 7 1/2h. En 24 h, un animal insuffisamment nourri montrait une activité totale de 205 min seulement. Pendant 696 min l'animal a dormi en conservant sa température "normale", et pendant 539 min il était en léthargie. L'hypothermie réversible chez un représentant des Soricidae s'explique probablement par une insuffisance de son métabolisme par rapport à sa taille minuscule. Comme les espèces du genre Sorex de taille voisine n'ont pas la possibilité d'entrer en léthargie réversible, cette adaptation particulière peut être considérée comme un indice d'un métabolisme relativement bas chez les Crocidurinae

Rythme journalier d'activité chez quelques Crocidurinae africains et européens (Soricidae, Insectivora)

Le rythme journalier de l'activité a été étudié en captivité, à 25° C, chez 7 espèces de Crocidurinae africaines (Sylvisorex megalura, Crocidura bottegi, C. jouvenetae, C. poensis, C. wimmeri, C. flavescens, C. giffardi), pesant entre 4 et 100 g. Ces observations sont comparées à des données choisies obtenues à 5° C et 20° C chez deux espèces européennes (Suncus etruscus et Crocidura russula). 1. L'activité journalière totale n'est pas liée de façon nette au poids corporel au sein des espèces étudiées. 2. Les espèces tropicales sont caractérisées par une activité presque exclusivement nocturne (4 à 30min/h de nuit contre 0 à 2 min/f de jour). Durant le repos diurne, C. jouvenetae présente régulièrement des torpeurs spontanées. 3. Les espèces européennes ont comparativement une activité diurne importante. En été, à température élevée, l'activité présente cependant également un rythme journalier marqué à prédominance nocturne; ce rythme s'atténue progressivement lorsque la température s'abaisse, essentiellement par la diminution de l'activité nocturne. Une faible activité diurne semble caractériser les Crocidurinae. Cette particularité est discutée à la lumière de données physiologiques et paléozoogéographiques.

Etude de la torpeur chez Suncus etruscus (Savi, 1822) (Soricidae, Insectivora) en captivité

Some aspects of torpor have been studied among captive Suncus etruscus by recording the nest temperature. Torpors show a circadian pattern and occur spontaneously or can be induced by food shortage. Body temperature can be controlled during torpor, remaining relatively high at low ambiant temperatures. At 20° C, spontaneous torpors seem to be less deep than induced tropors, but both show similar patterns at 5-8 ° C. Spontaneous torpors begin between 01°° and 06°°, whereas the onset of diet induced torpors seems to depend also on food exhausting. The rates of activity (A) and of torpor (T) show under constant conditions a daily variability. Increase of T is linked with a decrease of A and the relationship could agree with A(%) = Ao( 1-T/100), where Ao is daily rate of activity when T = 0. Occurence of torpor among other Soricidae, possible occurence among free living Suncus etruscus and energy saving are discussed

Détermination spécifique d'individus vivants des deux espèces jumelles Sorex araneus et S. coronatus, par deux techniques biochimiques (Insectivora, Soricidae)

As the morphological determination of living individuals of the two sibling species S. araneus and S. coronatus is not possible, we have tested two biochemical methods to determine these shrews in ecological studies. After producing specific antibodies by rabbits, we performed an immunological test on 25 individuals. With this first method, a correct determination was achieved in 76% of the cases only. The second method proved very successful: a polyacrylamide gel electrophoresis showed a systematic difference for albumin (73 individuals analyzed). According to our experience, the necessary blood sampling (10-20 μl) seems harmless for the shrews

Habitat, morphology and karyotype of the Saharan shrew Crocidura tarfayaensis (Mammalia : Soricidae)

The Saharan shrew Crocidura tarfayaensis Vesmanis and Vesmanis, 1980, has a limited disribution along the Atlantic coast of Sahara, south of Agadir (Morocco) through Western Sahara into Mauritania and is only known from few captures and some owl pellets. Here we report field data from the successful trapping of five specimens of C. tarfayaensis in the Guelmim region. The habitat was characterized by sand dunes along a river, with dense shrubberies of Tamarix sp., the huge grass Erianthus ravennae (Poaceae) and flat bushes of Atriplex glauca var. ifniensis (Chenopodiaceae). Morphological discrimination with C. whitakeri were examined. The chromosomes of C. tarfayaensis revealed a karyotype of 2n = 36, similar to that of the Canary shrew C. canariensis and the Sicilian shrew C. sicula. In conclusion, C. tarfayaensis seems to be a descendant of the presumed continental ancestor of the two island species.

Hierarchical analyses of genetic differentiation in a hybrid zone of Sorex araneus (Insectivora : Soricidae)

Microsatellites are used to unravel the fine-scale genetic structure of a hybrid zone between chromosome races Valais and Cordon of the common shrew (Sorex araneus) located in the French Alps. A total of 269 individuals collected between 1992 and 1995 was typed for seven microsatellite loci. A modified version of the classical multiple correspondence analysis is carried out. This analysis clearly shows the dichotomy between the two races. Several approaches are used to study genetic structuring. Gene flow is clearly reduced between these chromosome races and is estimated at one migrant every two generations using X-statistics and one migrant per generation using F-statistics. Hierarchical F- and R-statistics are compared and their efficiency to detect inter- and intraracial patterns of divergence is discussed. Within-race genetic structuring is significant, but remains weak. F-ST displays similar values on both sides of the hybrid zone, although no environmental barriers are found on the Cordon side, whereas the Valais side is divided by several mountain rivers. We introduce the exact G-test to microsatellite data which proved to be a powerful test to detect genetic differentiation within as well as among races. The genetic background of karyotypic hybrids was compared with the genetic background of pure parental forms using a CRT-MCA. Our results indicate that, without knowledge of the karyotypes, we would not have been able to distinguish these hybrids from karyotypically pure samples.

Molecular phylogenetics of shrews (Mammalia: Soricidae) reveal timing of transcontinental colonizations.

We sequenced 2167 base pairs (bp) of mitochondrial DNA cytochrome b and 16S, and 1390 bp of nuclear genes BRCA1 and ApoB in shrews taxa (Eulipotyphla, family Soricidae). The aim was to study the relationships at higher taxonomic levels within this family, and in particular the position of difficult clades such as Anourosorex and Myosorex. The data confirmed two monophyletic subfamilies, Soricinae and Crocidurinae. In the former, the tribes Anourosoricini, Blarinini, Nectogalini, Notiosoricini, and Soricini were supported. The latter was formed by the tribes Myosoricini and Crocidurini. The genus Suncus appeared to be paraphyletic and included Sylvisorex. We further suggest a biogeographical hypothesis, which shows that North America was colonized by three independent lineages of Soricinae during middle Miocene. Our hypothesis is congruent with the first fossil records for these taxa. Using molecular dating, the first exchanges between Africa and Eurasia occurred during the middle Miocene. The last one took place in the Late Miocene, with the dispersion of the genus Crocidura through the old world.

Phylogeny of shrews (Soricidae) : taxonomic and biogeographic implications

Résumé Les Soricidae sont l'une des plus grandes familles de mammifères avec plus de 300 espèces décrites. Elle a été récemment divisée en trois sous-familles, les Soricidae, qui sont distribuées dans la région Holarctique, les Crocidurinae en Afrique et en Eurasie, et les Myosoricinae en Afrique. La diversité spécifique de cette famille a conduit à des interprétations taxonomiques multiples, qui sont à l'origine de polémiques entre spécialistes, et même les premiers résultats moléculaires ont été fortement contradictoires. Le but de cette thèse est donc d'appliquer des meilleures techniques sur des échantillons mieux ciblés, afin de résoudre les contradictions taxonomiques et comprendre l'histoire de cette famille. Par le biais de marqueurs génétiques mitochondriaux et nucléaires, j'ai étudié: (i) Les relations taxonomiques à différent niveaux hiérarchiques au sein des Soricidae, c'est-à dire, entre les sous-familles, tribus, et genres, ainsi qu'au sein de deux complexes d'espèces largement distribués, et d'une espèce européenne, le but étant d'établir la congruence entre les données génétiques et les interprétations morphologiques classiques. (ii) Les relations biogéographiques, soit l'origine potentielle des différentes sous-familles, tribus, et genres, le nombre d'échanges intercontinentaux, ainsi que la structure phylogéographique à un niveau (péri)-spécifique, afin d'établir l'histoire de la diversification de cette famille. Les analyses combinées d'ADN mitochondrial et nucléaire ont montré un rapport clair entre les taxa à un niveau taxonomique élevé, mettant en évidence les rapports entre les sous-familles, les tribus, et les genres. Bien que Myosorex constitue un groupe monophylétique distinct, sa définition en tant que sous-famille séparée ne peut pas être reconnue. Ainsi, nous proposons d'attribuer un niveau de tribu pour ce clade (inclus dans les Crocidurinae). Nous avons également montré l'inclusion du genre Anourosorex dans les Soricinae et non en position basale dans les Soricidae. Au sein des Crocidurinae, Suncus s'est révélé être paraphylétique, et le genre Diplomesodon devrait être considéré d'un point de vue génétique comme invalide, puisque il se trouve au sein du clade du genre Crocidura. À un niveau taxonomique plus bas, nous avons montré la monophylie de deux complexes d'espèces largement distribués, le groupe de C. suaveolens et de C. olivieri. Néanmoins à l'intérieur de ceux-ci, des différences majeures avec la classification morphologique se sont révélées. Par exemples, C. sibirica n'est pas une espèce valide, les analyses de phylogénie moléculaire ne montrant pas de variations génétiques entre celle-ci et un échantillon de la localité type de C. suaveolens. D'un point de vue biogéographique, les fluctuations climatiques et les activités tectoniques des 20 derniers millions d'années ont fortement influencé la diversité actuelle des Soricidae. À un niveau taxonomique élevé, l'apparition de connexions de terre temporaires entre le Vieux et le Nouveau Monde au Miocène moyen ont mené à plusieurs colonisations indépendantes de l'Amérique par les Soricinae. Celles-ci ónt conduit à une diversification d'une tribu (Notiosoricini), ainsi que de genres (par ex: Cryptotis, Blarina) et d'un sous-genre (Otisorex) endémique au Néarctique. Dans le Vieux Monde, les barrières entre l'Afrique et Eurasie étaient plus perméables, menant à plusieurs échanges bidirectionnels de Crocidurinae. La diversification des clades principaux s'est produite au Miocène, certains clades étant endémiques d'Afrique ou d'Eurasie, tandis que d'autres se sont diversifiés à travers le Vieux Monde. À un niveau spécifique ou péri-spécifique, la fluctuation climatique du Pliocène et les glaciations du Pléistocène ont fortement divisé les populations dans tout le Paléarctique, menant à des entités génétiques distinctes. En Europe, les populations du groupe de C. suaveolens ont été divisées en une lignée Sud-Ouest et une Sud-Est, alors qu'au Proche-Orient et au Moyen-Orient, la diversité de clades est plus importante. En conclusion, mes études ont révélé que du Miocène à nos jours, la diversification des Soricidae a été provoquée par la colonisation de nouveaux habitats (dispersion), ainsi que par l'isolement des populations par diverses barrières (vicariance). Abstract The Soricidae is one of the largest mammalian families with more than 300 species described. It has been recently divided into three subfamilies, the Soricinae, which are distributed in the Holartic region, the Crocidurinae in Africa and Eurasia, and the Myosoricinae in Africa. The specific diversity of this family have led to multiple systematic interpretations and controversies between authors. Fortunately, today, cytotaxonomic, allozymic and molecular studies have permitted to clarify some uncertainties. Nevertheless, the Soricidae remains still poorly known. In this thesis, we aim at understanding with the use of mitochondrial and nuclear markers: (i) the taxonomic relationships at different hierarchical levels within Soricidae, i.e., between the subfamilies, tribes, and genera, as well as within two largely distributed species complexes, and within a European species, the goal being to establish congruence between the genetic data and traditional morphological interpretations; (ii) the biogeographic relationships, especially the potential origin of the different subfamilies, tribes, and genera, the number of transcontinental exchanges, as well as the phylogeographic structure at a (peri)-specific level, in order to establish the history of the genetic diversification of this family. The combined analyses of mitochondrial and nuclear DNA highlight for the first time a clear relationship between taxa at a high taxonomical level, permitting to distinguish the relationships between subfamilies, tribes, and genera. Although Myosorex formed a distinct monophyletic group, its definition as a distinct sub-family cannot be advocated. Thus, we propose to attribute a tribe level for this Glade (included within the Crocidurinae). Additionally, this combination of genes pleads in favour of the inclusion of the genus Anourosorex within the Soricinae and not in a basal position within the Soricidae. Within the Crocidurinae, Suncus appeared to be paraphyletic, and Diplomesodon should be considered from a genetic point of view as invalid, and is presently considered as Crocidura. At a lower taxonomic level, we showed the monophyly of two widely distributed species complexes, the C. suaveolens group and the C. olivieri group. Nevertheless within those, we showed major differences compared to morphological classification. For examples, C. sibirica revealed to not be a valid species, the molecular phylogenetic analyses failed to evidence genetical variations between it and samples of the type locality of C. suaveolens. In a biogeographic point of view, the climatic fluctuations and the tectonic plate activities of the last 20 Myr have strongly influenced the actual diversity of the family. At a high taxonomic level, the successive land bridge connections between the Old and the New World, which occurred during the Middle Miocene, have led to several independent colonisations of America by Soricinae, and a subsequent diversification of endemic Nearctic's tribe (Notiosoricini), genera (e.g. Cryptotis, Blaring) and sub-genus (Otisorex) within the Soricinae. Within the Old World, the barriers between Africa and Eurasia were more permeable, leading to several bidirectional exchanges within the Crocidurinae. The diversification of major clades occurred through the Miocene, some clades being endemic to Africa or Eurasia, whereas others diversified through the Old World. At a species level or a peri-specific level, the Pliocene climatic fluctuation and the Pleistocene glaciations have strongly divided the populations throughout the Palaearctic, leading to well defined genetic entities. In Europe, populations of the C. suaveolens group were split in a classical south-western and south-eastern lineage. In contrast, the Near East and the Middle East reveal many differentiated clades. In conclusion, our studies revealed that, from the Miocene to present, the diversification and speciation events within the Soricidae were caused by natural colonisation of new habitats (dispersion) and isolation of populations by various barriers (vicariance).

Energy requirements during reproduction and reproductive effort in shrews (Soricidae)

The energy requirements of reproducing and non-reproducing females of three species of Crocidura (C. russula, C. viaria, C. olivieri), and two species of Sorex (S. coronatus, S. minutus) were measured. Members of these two genera show different rates of metabolism and reproductive strategies (extreme altriciality and larger litter size in Sorex). During pregnancy, the daily energy intake (on either an absolute or a mass-specific basis) remained close to the non-reproductive value in all species. The absolute energy intake increased strongly after parturition and was influenced by the litter size. Peak energy intake of lactating females was extremely high, typically between 100% and 200% above the non-reproductive requirements in the Crocidura and about 300% above the non-reproductive intake in the Sorex. The mass-specific daily energy intake was reduced during lactation in the three smaller species but not in C. viaria and C. olivieri. This decrease probably involves the different thermoregulatory abilities and/or basal rate of metabolism of the pups. Average reproductive effort was about 50%, in the Crocidura species and above 150% in the Sorex species. The higher effort in the latter is partly due to a larger litter size. But in addition, extreme altriciality in the Sorex leads to an earlier increase in the energy requirements and thus is an energetically more expensive reproductive mode. The present results support the hypothesis that a higher basal rate of metabolism is associated with a higher reproductive effort in shrews.