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Systematics and taxonomy of Pipistrellus kuhlii (Kuhl, 1817) in Central Europe and the Balkans

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Abstract

We examined selected external characteristics and measurements of Pipistrellus k. kuhlii and P. k. lepidus representatives from the Balkans and Central Europe, whose ranges have rapidly expanded over the past few decades. We also sequenced and analysed two mitochondrial (16S and COI genes) and one nuclear (RAG2) markers of these two bat morphotypes to determine haplotype diversity and distribution patterns with a wider geographic perspective. We found that bats of the two taxa differed markedly with regard to the overall body coloration, size (P. k. lepidus is larger than P. k. kuhlii), extent and shape of the pale wing margin, and penis coloration, a finding which seems to be of diagnostic value, similarly to other Pipistrellus species. No polymorphism in RAG2 marker was found, but in both mtDNA markers we detected different haplotypes characteristic for both taxa, corresponding to morphological and morphometric patterns established in this study. Our genetic analysis results confirmed a clear division into two phylogenetic lineages and may indicate their allopatric speciation and a very recent simultaneous expansion to the Balkans and Central Europe from the Mediterranean region (P. kuhlii/deserti) and south-west Asia across eastern Europe (P. k. lepidus). We also show that P. k. lepidus distribution is wider than previously reported, and that the ranges of P. k. lepidus and P. k. kuhlii have already contacted in Central Europe.

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... Populations of P. kuhlii from the south and west of Europe and north of Africa (hereafter P. kuhlii), and from the east of Europe and the Middle East (hereafter Pipistrellus lepidus) may be treated as distinct phylogeographic and morphological species of allopatric origin (Mayer et al. 2007, Dietz & Kiefer 2016, Sachanowicz et al. 2017. In recent decades, both species have spread northwards, P. kuhlii from the Balkans and P. lepidus from Russia and Ukraine, and their ranges have become parapatric in parts of Central Europe, where both co-occur locally (Strelkov et al. 1985, Strelkov & Iljin 1990, Sachanowicz et al. 2006, 2017, Danko 2007. ...
... Populations of P. kuhlii from the south and west of Europe and north of Africa (hereafter P. kuhlii), and from the east of Europe and the Middle East (hereafter Pipistrellus lepidus) may be treated as distinct phylogeographic and morphological species of allopatric origin (Mayer et al. 2007, Dietz & Kiefer 2016, Sachanowicz et al. 2017. In recent decades, both species have spread northwards, P. kuhlii from the Balkans and P. lepidus from Russia and Ukraine, and their ranges have become parapatric in parts of Central Europe, where both co-occur locally (Strelkov et al. 1985, Strelkov & Iljin 1990, Sachanowicz et al. 2006, 2017, Danko 2007. Adaptation to urban areas, prevalent in Europe, appears to be one of the main factors enabling their expansion, which has similarly been observed in other synanthropic bat species, such as Hypsugo savii (Uhrin et al. 2016), and some bird species, such as Streptopelia decaocto (Kasparek 1996). ...
... In a previous study we showed that European P. lepidus and P. kuhlii differ not only in genetics, but also in their morphology and morphometry (Sachanowicz et al. 2017). The aim of the present study was to test whether P. lepidus and P. kuhlii also differ in their songflight call structure and parameters, which would support the species status of P. lepidus. ...
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We analysed and compared the structure and parameters of the songflight calls of expansive Pipistrellus kuhlii and Pipistrellus lepidus, that recently colonized Central Europe from the south and east, respectively. Bat calls were recorded mainly in urban areas of Central Europe and the Balkans, including a narrow zone of these species' recent parapatric or sympatric occurrence (around the Carpathians and the eastern part of the Pannonian Basin). The newly described songflight calls of P. lepidus consist of more elements (median 6), are longer (mean 56.4 ms) and of a higher frequency of maximum energy (mean 25.7 kHz) than those of P. kuhlii (median 3, mean 41.0 ms and mean 14.0 kHz, respectively). This finding provides new evidence that P. lepidus represents a different species, in accordance with results from previous genetic and morphological studies. Reported differences in songflight calls permit the acoustic discrimination of P. kuhlii and P. lepidus, which is not possible based on overlapping parameters of their echolocation calls. Our findings enable distributional and ecological studies of these two species, based on acoustic methods, in the context of their rapid European expansion and the local co-occurrence.
... Colonization of the northern regions by populations from two separate segments of the distribution range, i.e. central Europe from the Mediterranean and eastern Europe from the Ponto-Caspian region, respectively, suggested already by Strelkov et al. (1985), was later supported in a study with the use of genetic markers by Sachanowicz et al. (2017). The latter authors further revealed that the two genetic lineages, corresponding roughly to the Mediterranean and Ponto-Caspian origins, respectively, have different phenotypes and thus should be treated as separate (probably subspecific) forms, tentatively referred to as Pipistrellus kuhlii kuhlii and P. k. lepidus Blyth, 1845. ...
... The latter authors further revealed that the two genetic lineages, corresponding roughly to the Mediterranean and Ponto-Caspian origins, respectively, have different phenotypes and thus should be treated as separate (probably subspecific) forms, tentatively referred to as Pipistrellus kuhlii kuhlii and P. k. lepidus Blyth, 1845. These two forms, originally allopatric outside of the Mediterranean, have probably came into secondary contact just recently in eastern Slovakia (Sachanowicz et al. 2017). ...
... When examining bats for identification, we used a combination of quantitative and qualitative criteria given by Dietz et al. (2009). Further, we inspected the state of characters distinguishing two subspecific forms Pipistrellus kuhlii kuhlii and P. k. lepidus sensu Sachanowicz et al. (2017). ...
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Based on 25 records (both published and new) we summarize the recent distribution of Pipistrellus kuhlii in the Czech Republic and discuss possible colonization routes. The species colonized a major part of the Czech Republic during 14 years since its first record in 2007. Based on locations and chronology of the records it seems that the eastern part of the Czech Republic (Moravia) was colonized from the south along the Dyje and Morava rivers, while in Bohemia, two possible routes may have existed: one from the south along the Vltava river from the Danube valley, and another from the east or south-east along the valley of the Svitava and Orlice rivers. Given the fact that already in 2018 the presence of P. kuhlii was confirmed in Saxony, which predated the species confirmation in the north-western and central parts of Bohemia, we do not exclude possible existence of a third colonization route along the Labe river from the north-west (Germany). All the records come from human settlements, typically cities or towns, and dates of the records suggests the year-round occurrence. At least four records (including two roosts of maternity colonies), all from Moravia, proved reproduction of this bat in the country. All examined individuals displayed pelage and skin colouration patterns typical for P. kuhlii kuhlii.
... Within this range, the P. kuhlii species group includes several morphological and genetic forms the taxonomic status of which is still subject to debate (e.g. Benda et al. 2015;Andriollo et al. 2015;Sachanowicz et al. 2017). In Europe, two forms have been clearly described P. k. kuhlii and P. k. lepidus (Sachanowicz et al. 2017). ...
... Benda et al. 2015;Andriollo et al. 2015;Sachanowicz et al. 2017). In Europe, two forms have been clearly described P. k. kuhlii and P. k. lepidus (Sachanowicz et al. 2017). The first resides throughout the Mediterranean basin, while the second is found chiefly in Eastern Europe and SE Asia. ...
... The first resides throughout the Mediterranean basin, while the second is found chiefly in Eastern Europe and SE Asia. According to Sachanowicz et al. (2017) both of these forms are undergoing range expansion in opposite directions with P. k. kuhlii moving from the Mediterranean to the northeast, while P. k. lepidus is expanding from Central Asia towards the northwest. These two subspecies are sympatric and their current ranges overlap in eastern Slovakia and Hungary (Sachanowicz et al. 2017). ...
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Urbanization is one of the main drivers of ecological change in the modern world. In most cases, species diversity in urban landscapes is lower than in natural ones; however, some groups of animals are able to exploit and benefit from urban habitat. Pipistrellus kuhlii s.l. is (P. k. lepidus according to recent taxonomic review), a common European urban bat, whose range has expanded on a wide scale in the last 40 years. Thought to originate in Central Asia, this species has extended its range throughout Eastern and Central and Europe (a distance of more than 2,500 km) in part by using human settlements as a habitat. This study examines the ecological features of P. k. lepidus in wintertime in the Eastern part of Ukraine, where this species has been living for 20 years. Thirty-nine winter records of P. k. lepidus (1,301 individuals totally) were selected from the database of the Bat Rehabilitation Center of Feldman Ecopark, 19 of which were groups from 2 to 641 individuals. Pipistrellus k. lepidus was found in various types of structures, but most often in administrative buildings (school buildings - 69%). Records were usually obtained during renovation works (85%), and the roosting sites were cavities between the wooden planks of window frames and a wall (75%). The records were obtained in 26 settlements, from a village (0,293 km2 and 252 people) to the biggest cities in the country (Kharkiv and Odessa). The sex ratio in winter aggregation in adults varied from 47% to 61% of females and for this-year individuals from 48% to 58%, respectively. The body mass at the end of the hibernation period (February/March) decreases for 17–20% compared to the beginning of the period (December). Adult females have bigger body size (body mass and forearm length) (p-value < 0.05). Our results showed that P. k. lepidus is capable of forming homogeneous, sedentary populations in all types of settlements in Ukraine for these twenty years. However, this choice of habitat means that the species faces a high mortality risk from humans during building renovation and insulation works or pest control actions.
... To evaluate the risk to bats from trace metal pollution it is necessary to find a species that lives in urban and industrial areas, is sedentary and has a small daily home range. Among European bats the most urban-associated species is Kuhl's pipistrelle (Pipistrellus kuhlii) (Ancillotto et al., 2016;Maxinová et al., 2016)a small vespertilionid that became common or even mass species in human settlements of Eastern and Central Europe in the last 20-30 years (Sachanowicz et al., 2009;Sachanowicz et al., 2017;Kravchenko et al., 2017;Hukov et al., 2020). It is a sedentary species (Kravchenko et al., 2017;Hukov et al., 2020) with a small home range, which hunts for insects in urban or suburban areas with high degree of artificial illumination (Maxinová et al., 2016). ...
... kuhlii) is a small-sized Eurasian sedentary bat, strongly associated with urban, rural and industrial environments, whose populations live residentially for many years in one location (Ancillotto et al., 2015;Dietz and Kiefer, 2014;Maxinová et al., 2016;Hukov et al., 2020). In Europe this species is presented by two taxa differentiated by morphological, genetical and acoustical features (Sachanowicz et al. 2017;Hukov et al., 2020;Piskorski and Sachanowicz 2021), the western -P. kuhlii kuhlii and the eastern one P. kuhlii lepidus. ...
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Bats are an endangered group of mammals that are very sensitive to environmental stresses. One of such stress factor is trace metals pollution which threatens populations of insectivorous bats due to their top position in the food webs and exceptionally long life span. In our research Pipistrellus kuhlii was tested as a promising indicator species (urban-dwelling, sedentary, with limited daily home-range) for trace metal exposure of bats. We measured concentrations of Pb, Cu, Zn and Cd in internal and external tissues of bats from the industrial city Mariupol and the village Karlovka, Ukraine, to answer the following questions: (1) Do metal concentrations in soil samples differ between urban and rural areas, and between populations of P. kuhlii from those areas? (2) Does metal contamination differ between individuals of different sexes and ages? (3) Whether fur and/or wing membrane, the two tissues that can be collected from live bats, can be used as proxies of metal contamination in internal tissues (liver, kidney, lung, forearm bones) of P. kuhlii? Metal concentrations in soil samples were significantly higher in the city. Bats from the city accumulated significantly more Cd, Pb and Zn in external tissues than those from the rural area. Females accumulated more Cd than males, and this-year-born did not differ significantly from adult individuals. We did not find, however, significant positive correlations between metal concentrations in external and internal tissues, indicating that external tissues cannot serve as an indicator of the metal contamination of internal tissues in P. kuhlii.
... Останні відповідають «первинному» ареалу форми lepidus, яку ці дослідники запропонували відновити у статусі виду, як Pipistrellus lepidus Blyth, 1845. Віднесення білосмугих нетопирів до форми lepidus припускається і для Польщі (Popczyk et al. 2008) та Румунії (Barti 2010), а останнім часом і для всього регіону Східної Європи (Sachanowicz et al. 2017). Належність популяцій з України до форми lepidus очевидна і приймається в частині публікацій (напр.: Sachanowicz et al. ...
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General issues of "taxonomic monitoring" of the mammal fauna of Ukraine are considered, including current changes and clarifications on the species composition of fauna, taxonomic ranks of species and superspecies groups, and current scientific and vernacular (Ukrainian) names. Analytical references and comments on the ranks and names of 24 taxa or taxonomic groups are presented, including 6 on Glires non-Muroidae, 7 on Muroidae, 5 on Chiroptera, 2 on Carnivora, and 4 on Ungulata. Most of the changes concern taxa ranks (especially genus / subgenus or family / subfamily) and, to a lesser extent, scientific and Ukrainian names. All changes are analysed as an update to the checklist approved by the Ukrainian Theriological Society (UTS) and published in 2012 in the Proceedings of the NMNH. In particular, this publication recognises the species status and correct use of scientific species names of Spalax graecus, Spalax arenarius, Apodemus (Sylvaemus) tauricus, and Myotis aurascens, as well as the Ukrainian vernacular names “hipsuh” (for Hypsugo) and “saiga” (for Saiga), scientific generic names Myodes (Ukr. “norytsia”) and Alexandromys (Ukr. “shaparka”), the family rank of long-winged bats (Miniopteridae), and the scientific name Cricetulus migratorius for the grey hamster as valid. The following provisions are adopted based on recent publications and trends in the development of classifications: 1) a new understanding of the volume and species name of Spermophilus planicola (little souslik) and Pipistrellus lepidus (Kuhl's pipistrelle); confirmation of the family status of birch mice, but with a new scientific name Sminthidae; correctness of scientific names Neogale vison (American mink) and Ovis gmelini (mouflon); 2) clarification of the Ukrainian vernacular name “molossovi” for Molossidae; 3) the genus coypu (Myocastor) is considered within the family of spiny rats (Echimyidae), whereas genera of voles (Microtus), red-backed voles (Myodes) and water voles (Arvicola) within the family of hamsters (Cricetidae); 4) lowering the ranks of several taxa, in particular Arvicolidae to subfamily Arvicolinae (within the family Cricetidae), Allactagidae to subfamily Allactaginae (within the family Dipodidae), Terricola to subgenus within the genus Microtus (s. l.), Bison to subgenus within the genus Bos (hence the bison is Bos bonasus), 5) the genus Sylvaemus is preserved at the same rank as the genus Apodemus. Trends in further changes of checklists and the need to align them with basic checklists and to adapt "thematic" lists, such as "red lists" for national or regional levels, game fauna lists, species lists in annexes to various international agreements (e.g. CITES, Bern Convention, EUROBATs, etc.) are considered.
... Çoraman et al. (2013) studied the genetic relationships between Anatolian and European populations of several species of bats, including P. kuhlii, and found genetically distinct populations and suggested that some of the bats may represent biologically distinct taxa. Sachanowicz et al. (2017) also compared populations of P. k. kuhlii and P. k. lepidus from the Balkans and Central Europe. Based on morphological and genetic markers, they found two phylogenetic lineages. ...
Chapter
This comprehensive species-specific chapter covers all aspects of the mammalian biology, including paleontology, physiology, genetics, reproduction and development, ecology, habitat, diet, mortality, and behavior. The economic significance and management of mammals and future challenges for research and conservation are addressed as well. The chapter includes a distribution map, a photograph of the animal, and a list of key literature.
... Despite the spotlight recently put on the Kuhl's pipistrelle (Smirnov and Vekhnik, 2011;Godlevs'ka, 2015;Shpak and Larchenko, 2016;Ancillotto et al., 2016;Sachnowicz et al., 2017), the parasitic fauna and pathogens associated with the species are considered in scattered fragmentary communications from various (primarily, African, Asian, and South European) parts of the range. As for Russia, five or six species of ectoparasites were described earlier. ...
Article
Here we report the results of our own survey and literary published data on the ectoparasite fauna and pathogens of the alien bat species, the Kuhl's pipistrelle Pipistrellus kuhlii (Kuhl, 1817) (Chiroptera: Ves-pertilionidae). This bat is a host of 36 species of parasitic mites, ticks and insects (including accidental findings) and 13 species of pathogens (protozoa, bacteria, viruses). The flea Ischnopsyllus variabilis is recorded on this host for the first time. We have found that outside of the host ancestral range, the core of the bat parasite fauna is significantly different due to the loss of host species-specific ectoparasites. Particularly, in Rus-sia, only 6 species of parasitic arthropods have been recorded for Kuhl's pipistrelle and all of them are host genus-specific. At the same time, the features of ecology and occasional finds of extrinsic parasites allow to suggest that P. kuhlii has wide contacts with animals which are the reservoirs of zoonotic infections, that in combination with the fact of isolation of several pathogens from this species (including two coronaviruses) points to a possible medical importance of Kuhl's pipistrelle.
... Due to similarities in echolocation characteristics (Zsebok et al. 2012), we cannot fully disclose the possibility of our recordings belonging to P. kuhlii, or its subspecies, P. kuhlii lepidus. This species has not been observed in Finland previously, but both P. kuhlii and P. kuhlii lepidus has shown considerable range expansion during the last decades (Ancillotto et al. 2016;Sachanowicz et al. , 2017. The probability of either of these taxa occurring in Finland is still small, but the observed range shifts call for increased vigilance in identification procedures. ...
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Highly mobile species are considered to be the first to respond to climate change by transforming their ranges of distribution. There is evidence suggesting that Pipistrellus nathusii , a species capable of long-distance migration, is expanding both its reproduction and overwintering ranges to the North. We recorded the echolocation calls of bats at 16 sites in South-Western Finland on two consecutive winters, and detected calls of P. nathusii at one of the sites throughout the second winter. To our knowledge, this is the northernmost record of an overwintering P. nathusii , and contributes to evidence that the species is already responding to climate change.
... deserti" morphotype, seems to share a common nuclear genepool. Our P. kuhlii samples showed a haplotype previously recorded in Morocco (Veith et al., 2011), Italy (Locatelli et al., 2016, and Albania (Sachanowicz et al., 2017), and thus belongs to the mitochondrial eastern lineage of Andriollo et al. (2015) and, more specifically, to the sub-cluster of P. cf. deserti haplotypes. ...
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In the Mediterranean region, cryptic diversity of bats is common. As distinct genetic lineages should be managed independently for conservation, insight into bat phylogeography is important. The Maltese islands are located in the centre of the Mediterranean between North Africa and Sicily and are densely populated. At present, it is thought that at least seven species of bats are native, but phylogeographic affiliations remain largely unexplored. Therefore, we sequenced a ca. 540 bp fragment of the mitochondrial 16S rRNA gene from 23 bats, which were captured during the citizen-science project Akustika. We found two morphologically cryptic lineages common in North Africa, Plecotus gaisleri and a mainly North-African lineage of Hypsugo savii (named Hypsugo cf. darwinii in some recent studies). We also recorded two Pipistrellus species. The P. kuhlii haplotype belonged to a lineage present in North-Africa and across the Mediterranean. Within P. pipistrellus we found two novel haplotypes that clustered within a North-African clade, well distinguished from the European haplotypes. Our results highlight the historic connection between the bat fauna of the Maltese Islands and North Africa. Malta is one of the few regions in the European Union where P. gaisleri and the North-African clades of P. pipistrellus and H. savii occur. Hence, Malta has an exceptionally high responsibility for the conservation of these taxa in Europe.
... Nejnovější poznatky o taxonomii netopýra vroubeného tuto skutečnost rovněž podporují. Netopýři vroubení z Polska náležejí populacím geneticky odlišným od středomořských (nominotypických) populací P. kuhlii, které se rozšířily do západní části střední Evropy včetně ČR, a před-stavují odlišný taxon, P. k. lepidus (sachanoWicz et al. 2017). ...
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The Kuhl’s pipistrelle ( Pipistrellus kuhlii ) was recorded in Bohemia for the first time. An adult female was found in a house in the Hradec Králové town during reconstruction on 18 January 2016. The bat was transported to a wildlife rescue station in Jaroměř and kept until April, then it was released in good condition.
... На сьогодні фактично все Полісся і Лісостеп відносяться до зони поширення тільки P. pygmaeus (прилеглі райони Росії -те саме: Крускоп, 2007). У групі білосмугих нетопирів назріває ситуація, яка подібна до пари Eptesicus serotinus-lobatus: їх тепер поділяють на два аловиди -західний Pipistrellus kuhlii та поширений в Україні й прилеглих країнах P. lepidus (Sachanowicz et al., 2017). ...
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Summaries of taxonomic revisions, analysis of identification criteria, spatial and eco-morphological differentiation of close pairs of species are summed up. Five superspecies are considered: Myotis “myotis”, Myotis “mystacinus”, Plecotus “auritus”, Pipistrellus “pipistrellus”, Eptesicus “serotinus” and other problematic pairs. The distribution of species by the forearm length as the key ecomorphological character (EMC) is analyzed. It is shown that stable groups are formed from species with a wide distribution of EMC without their overlapping. However, the superspecies, which include siblings and generally close species, are characterized by considerable spatial differentiation (allopatry). All pairs of close species are characterized by one of four statuses: 1) they are alopatric (e.g. the group Eptesicus "serotinus" and partly Myotis "mystacinus"), 2) they are marginal sympatric (M. "myotis"), 3) primary alopatry is excited by the expansion of one species into the range of another one (Plecotus "auritus"), 4) sympatry is unnatural and is determined by the synanthropy of one of them (Pipistrellus "pipistrellus").
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For four decades, there have been changes in the ranges of many bat species in Europe, particularly shifts in their northern limits. This phenomenon is more spectacular for migratory species than sedentary ones, especially for representatives of the genera Pipistrellus and Hypsugo. Kuhl's pipistrelle Pipistrellus kuhlii (Kuhl, 1817) is the one of western Palaearctic bat species with conspicuous range expansion in the last three decades, the species has rapidly expanded and colonised new territories both northwards and westwards. In Central Europe, two genetic lineages occur that are also quite different morphologically: P. kuhlii kuhlii (hereaf-ter P. kuhlii) and P. kuhlii lepidus (hereafter P. lepidus). The contact zone between these two lineages passes through Hungary and Slovakia, although the real range of distinct lineages and/or morphotypes are still unclear. The first records of P. kuhlii from Poland (probably belonging to P. lepidus) come from Warszawa, central Poland (2004) and Zawiercie, southern Poland (2005): both specimens were males, found in December in buildings. Since then, there have been further reports of the presence of this species in Poland-occurring mostly in large cities along the valleys of large rivers such as the Wisła and Bug, from both periods of activity and hibernation. In subsequent years in Poland the occurrence of only P. lepidus has been confirmed, while P. kuhlii has been recorded from southern locations in the Carpathian Mountains in Slovakia. This paper describes the first record of this species from Poland, further indicating the existence of a maternity colony. In mid-July of 2020, a non-volant juvenile male was found in Kraków, Krowodrza district (50°04'11.7" N, 19°54'55.9" E). Initially poorly visible diagnostic features have become unambiguous with development and similar to those in P. kuhlii: narrow pale wing margin and orange penis colouration. After about two months in captivity , a mature individual capable of flying was released at the site where it was found. The presence of a maternity colony indicates that this species (i) has been part of the Polish fauna for several years, and (ii) its range in Poland possibly expands much further north.
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Cabo Verde Archipelago presents one of the largest knowledge gaps in the distribution and taxonomy of bats in the world. Old works indicated that there are five species classified as European taxa. We have conducted an integrative taxonomy to revise the systematic position and distribution of Cabo Verdean bats with molecular, morphological, and ecological data, to test their native or exotic origin, and infer possible colonization patterns based on fieldwork and museum samples. Results showed that Cabo Verde Hypsugo is closely related to those from the Canary Islands, in which the taxonomic status is under debate, presenting unique mitochondrial and nuclear haplotypes. We also expanded the distribution of Taphozous nudiventris for Fogo Island through pellets and acoustic identification, showed unique haplotypes for this species, and that Miniopterus schreibersii shared a haplotype with European, North African, and Western Asian specimens. The morphological and acoustic identification of Cabo Verdean specimens was challenging because of the lack of modern morphological descriptions and similarity of echolocation calls within the same genus. More studies are definitely needed to access the systematic of bat species in the archipelago, but this work is the first step for the establishment of conservation actions of the probable only native Cabo Verdean mammals.
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The Kuhl’s pipistrelle (Pipistrellus kuhlii) is a Western Palaearctic species of bat that exhibits several deeply divergent mitochondrial lineages across its range. These lineages could represent cryptic species or merely ancient polymorphism, but no nuclear markers have been studied so far to properly assess the taxonomic status of these lineages. We examined here two lineages occurring in Western Europe, and used both mitochondrial and nuclear markers to measure degrees of genetic isolation between bats carrying them. The sampling focused on an area of strict lineage sympatry in Switzerland but also included bats from further south, in North Africa. All individuals were barcoded for the COI gene to identify their mitochondrial lineages and five highly polymorphic microsatellite loci were used to cluster them according to their nuclear genotypes. Despite this low number of nuclear markers, all North African nuclear genotypes were grouped in a highly distinct subpopulation when compared with European samples sharing the same mitochondrial barcodes. The reverse situation prevailed in Switzerland where bats carrying distinct barcodes had similar nuclear genotypes. There was a weak east/west nuclear structure of populations, but this was independent of mitochondrial lineages as bats carrying either variant were completely admixed. Thus, the divergent mitochondrial barcodes present in Western Europe do not represent cryptic species, but are part of a single biological species. We argue that these distinct barcodes evolved in allopatry and came recently into secondary contact in an area of admixture north of the Alps. Historical records from this area and molecular dating support such a recent bipolar spatial expansion. These results also highlight the need for using appropriate markers before claiming the existence of cryptic species based on highly divergent barcodes.
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Pipistrellus deserti is a small, pale-coloured bat occurring in the most arid parts of the Sahara, in Morocco, Algeria, Libya, Egypt, and the Sudan, and marginally also in sub-Saharan Africa. Although most authors consider P. deserti as a full species, others regard it as a subspecies, or even as a junior synonym of Pipistrellus kuhlii. We analysed the topotype material of P. deserti from Libya using both morphologic and molecular characters, and compared them with samples from other Saharan countries and with P. kuhlii from around the Mediterranean. The Libyan samples of deserti are morphologically very similar to other populations from arid parts of North Africa (Morocco, Algeria, Egypt, Sudan), but differ markedly in the size of most skull dimensions when compared to P. kuhlii sampled in more mesic areas. However, phylogenetic reconstructions indicate that mitochondrial haplotypes of typical P. deserti from Libya and those from Morocco do not form a monophyletic group but are fully embedded within the larger radiation of P. kuhlii from Africa and Europe, rendering this species paraphyletic. Limited nuclear information (five microsatellite loci) also failed to provide evidence of significant differences between the two morphotypes, as pipistrelles are instead grouped by geographic origin. Altogether, these genetic data suggest that the morphological uniqueness of P. deserti may result from recent adaptations to arid habitats, rather than reflect a long independent evolutionary history. In the absence of more compelling evidence of barriers to gene flow, we therefore suggest Pipistrellus deserti to be considered a junior synonym of Vespertilio kuhlii (=P. kuhlii).
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A comprehensive, but simple-to-use software package for executing a range of standard numerical analysis and operations used in quantitative paleontology has been developed. The program, called PAST (PAleontological STatistics), runs on standard Windows computers and is available free of charge. PAST integrates spreadsheettype data entry with univariate and multivariate statistics, curve fitting, time-series analysis, data plotting, and simple phylogenetic analysis. Many of the functions are specific to paleontology and ecology, and these functions are not found in standard, more extensive, statistical packages. PAST also includes fourteen case studies (data files and exercises) illustrating use of the program for paleontological problems, making it a complete educational package for courses in quantitative methods.
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We announce the release of an advanced version of the Molecular Evolutionary Genetics Analysis (MEGA) software, which currently contains facilities for building sequence alignments, inferring phylogenetic histories, and conducting molecular evolutionary analysis. In version 6.0, MEGA now enables the inference of timetrees, as it implements our RelTime method for estimating divergence times for all branching points in a phylogeny. A new Timetree Wizard in MEGA6 facilitates this timetree inference by providing a graphical user interface (GUI) to specify the phylogeny and calibration constraints step-by-step. This version also contains enhanced algorithms to search for the optimal trees under evolutionary criteria and implements a more advanced memory management that can double the size of sequence data sets to which MEGA can be applied. Both GUI and command-line versions of MEGA6 can be downloaded from www.megasoftware.net free of charge.
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New distributional data was reported for 16 bat species in Bulgaria. Six new species were discovered for the fauna from the Sarnena Sredna Gora Mountain, two from the Sakar Mountain, four from the Upper Thracian Valley. Three species were newly discovered for the biogeographic sub-region of the Upper Thracian Valley located in the Middle Bulgarian biogeographic region.
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Islands are biodiversity hotspots, often containing numerous endemic species. This makes them also hotspots for conservation. Within the Mediterranean region, Sardinia is known for its comparatively high degree of endemism, including cryptic diversity. In this paper we aim to elucidate the variability of pipistrelles (Pipistrellus and Hypsugo) on Sardinia. More specifically, we ask which species occur on Sardinia and we describe the geographic affiliations of these evolutionary lineages. We sequenced ca. 560 bp of the 16S rRNA gene from 36 pipistrelle specimens representing 17 localities from all major parts of Sardinia. For comparison we added samples from the entire Mediterranean region as well as sequences stored at GenBank. We constructed Bayesian phylogenetic trees and minimum spanning networks to identify which species occur on Sardinia and to infer their genetic affiliation to lineages occurring throughout the Mediterranean and the Canary Islands. We identified five pipistrelle lineages on Sardinia: Pipistrellus pipistrellus (haplolineage II), P. pygmaeus, P. kuhlii/desertii, Hypsugo savii s.str. and H. cf. darwinii. Colonization of Sardinia occurred at different times from different geographical sources, namely Europe and Africa. Some lineages may have invaded Sardinia recently. The Sardinian H. cf. darwinii may be endemic to the island. Our results highlight the importance of Sardinia as a major Mediterranean hotspot for bat biodiversity. The island harbours a pipistrelle diversity that is higher than that on any other Mediterranean island. Lying geographically at the interface between Europe and Africa, Sardinia combines elements from both continents.
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Nowadays, molecular techniques are widespread tools for the identification of biological entities. However, until very few years ago, their application to taxonomy provoked intense debates between traditional and molecular taxonomists. To prevent every kind of disagreement, it is essential to standardize taxonomic definitions. Along these lines, we introduced the concept of Integrated Operational Taxonomic Unit (IOTU). IOTUs come from the concept of Operational Taxonomic Unit (OTU) and paralleled the Molecular Operational Taxonomic Unit (MOTU). The latter is largely used as a standard in many molecular-based works (even if not always explicitly formalized). However, while MOTUs are assigned solely on molecular variation criteria, IOTUs are identified from patterns of molecular variation that are supported by at least one more taxonomic characteristic. We tested the use of IOTUs on the widest DNA barcoding dataset of Italian echolocating bats species ever assembled (i.e. 31 species, 209 samples). We identified 31 molecular entities, 26 of which corresponded to the morphologically assigned species, two MOTUs and three IOTUs. Interestingly, we found three IOTUs in Myotis nattereri, one of which is a newly described lineage found only in central and southern Italy. In addition, we found a level of molecular variability within four vespertilionid species deserving further analyses. According to our scheme two of them (i.e. M.bechsteinii and Plecotus auritus) should be ranked as unconfirmed candidate species (UCS). From a systematic point of view, IOTUs are more informative than the general concept of OTUs and the more recent MOTUs. According to information content, IOTUs are closer to species, although it is important to underline that IOTUs are not species. Overall, the use of a more precise panel of taxonomic entities increases the clarity in the systematic field and has the potential to fill the gaps between modern and traditional taxonomy.
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A new statistical method for estimating divergence dates of species from DNA sequence data by a molecular clock approach is developed. This method takes into account effectively the information contained in a set of DNA sequence data. The molecular clock of mitochondrial DNA (mtDNA) was calibrated by setting the date of divergence between primates and ungulates at the Cretaceous-Tertiary boundary (65 million years ago), when the extinction of dinosaurs occurred. A generalized leastsquares method was applied in fitting a model to mtDNA sequence data, and the clock gave dates of 92.311.7, 13.31.5, 10.91.2, 3.70.6, and 2.70.6 million years ago (where the second of each pair of numbers is the standard deviation) for the separation of mouse, gibbon, orangutan, gorilla, and chimpanzee, respectively, from the line leading to humans. Although there is some uncertainty in the clock, this dating may pose a problem for the widely believed hypothesis that the bipedal creatureAustralopithecus afarensis, which lived some 3.7 million years ago at Laetoli in Tanzania and at Hadar in Ethiopia, was ancestral to man and evolved after the human-ape splitting. Another likelier possibility is that mtDNA was transferred through hybridization between a proto-human and a protochimpanzee after the former had developed bipedalism.
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The program MRBAYES performs Bayesian inference of phylogeny using a variant of Markov chain Monte Carlo. Availability: MRBAYES, including the source code, documentation, sample data files, and an executable, is available at http://brahms.biology.rochester.edu/software.html. Contact: johnh{at}brahms.biology.rochester.edu
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Although several decades of study have revealed the ubiquity of variation of evolutionary rates among sites, reliable methods for studying rate variation were not developed until very recently. Early methods fit theoretical distributions to the numbers of changes at sites inferred by parsimony and substantially underestimate the rate variation. Recent analyses show that failure to account for rate variation can have drastic effects, leading to biased dating of speciation events, biased estimation of the transition:transversion rate ratio, and incorrect reconstruction of phylogenies.
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The lack of obvious morphological differences between species impedes the identification of species in many groups of organisms. Meanwhile, DNA-based approaches are increasingly used to survey biological diversity. In this study we show that sequencing the mitochondrial protein-coding gene NADH dehydrogenase, subunit 1 (nd1) from 534 bats of the Western Palaearctic region corroborates the promise of DNA barcodes in two major respects. First, species described with classical taxonomic tools can be genetically identified with only a few exceptions. Second, substantial sequence divergence suggests an unexpected high number of undiscovered species.
Article
Sequences of the DNA barcode region of the cytochrome oxidase subunit I gene were obtained from 38 species of northeastern Palaearctic bats to assess patterns of genetic diversity. These results confirmed earlier findings of deep phylogeographic splits in four pairs of vicariant species (Myotis daubentonii/petax, M. nattereri/bombinus, Plecotus auritus/ognevi and Miniopterus schreibersii/fuliginosus) and suggested previously unreported splits within Eptesicus nilssoni and Myotis aurascens. DNA barcodes support all taxa raised to species rank in the past 25 years and suggest that an additional species - Myotis sibiricus - should be separated from Myotis brandtii. Major phylogeographic splits occur between European and Asian populations of Myotis aurascens, Rhinolophus ferrumequinum and Myotis frater; smaller scale splits are observed between insular and mainland populations in the Far East (M. frater, Myotis ikonnikovi and Murina ussuriensis) and also between southeastern Europe and Ciscaucasia (Myotis daubentonii, Plecotus auritus, and Pipistrellus pipistrellus). One confirmed case of sequence sharing was observed in our dataset - Eptesicus nilssoni/serotinus. This study corroborates the utility of DNA barcodes as a taxonomic assessment tool for bats.
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Identification of intraspecific conservation units and incorporating the distribution of genetic diversity into management plans are crucial requirements for assessing effective protection strategies. This study investigates the phylogeographic structures of 33 bat species present in the Near East in order to evaluate the conservation implications of their intraspecific genetic diversity both at regional and large-scale levels. To compare Anatolian populations with the European ones, we utilized two commonly used mitochondrial markers, Cytb and ND1, and analysed them together with the available sequences from GenBank. The management requirements of the identified clades and their taxonomical relations were evaluated by analysing their distributions and the levels of their genetic differentiations. In 12 species and the large Myotis complex, we identified a total of 15 genetically distinct populations found in the Near East, some of which might represent biologically distinct taxa. Comparing the phylogeographic patterns of different taxa indicates that three regions, the Balkans, the Caucasus, and the southern Anatolia, harbour genetically divergent populations and should have higher priority in conservation practices. Considering that Turkey has one of the richest bat fauna in the Mediterranean region and the Anatolian populations of various species are genetically distinct, protecting populations in Turkey is critically important for preserving the genetic diversity of the bats in the Western Palaearctic. Both regional and large-scale conservation strategies, which incorporate the distribution of genetic diversity, should be assessed and further ecological studies are needed to clarify the taxonomic relations of the identified clades.
Article
Evolution of three Canary Island Vespertilionid bat species, Pipistrellus kuhlii, Pipistrellus maderensis, and Hypsugo savii was studied by comparison of approximately 1 kbp of mtDNA (from cytochrome b and 16S rRNA genes) between islands. mtDNA reveals that both P. kuhlii and P. maderensis exist in sympatry on Tenerife (and possibly other islands). Their morphological similarity explains why their co-occurrence had not been detected previously. Levels of sequence divergence are quite low within P. maderensis. Haplotypes were either identical or separated by </=2 mutational steps on two of the islands (La Gomera and El Hierro). However there is sufficient between-island divergence between haplotypes from Tenerife, La Palma, and La Gomera/El Hierro to suggest that they could represent three evolutionary significant units (ESU). H. savii has an overlapping island distribution but a contrasting phylogeographical pattern. Most significantly, sequence divergence is greatest between La Gomera and El Hierro (>/=12 mutational steps) indicating colonization of the latter from the former sometime during the last approximately 1.2 Ma, with low subsequent gene flow. Unlike P. maderensis the El Hierro population alone appears to represent an ESU. The H. savii haplotypes detected in Gran Canaria and Tenerife are identical or separated by 1 mutational step.
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