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Cryptic diversity of Italian bats and the role of the Apennine refugium in the phylogeography of the western Palaearctic
Abstract
The Mediterranean Basin is typified by a high degree of species rarity and endemicity that reflects its position, geomorphology, and history. Although the composition and cryptic variation of the bat faunas from the Iberian and Balkan Peninsulas are relatively well studied, data from the Apennine Peninsula are still incomplete. This is a significant shortfall, given the presumed refugial role of this region in the context of Europe's Pleistocene phylogeography. It was thus our aim to supplement the phylogeographical information from the region, generating mitochondrial sequences and reviewing published data, with a focus on the dispersal and diversification patterns characterizing taxa with different life strategies. Site-specific lineages were ascertained, especially in the genera Myotis and Plecotus and amongst the pipistrelloid bats, representing speciose radiations. It was possible to observe disjunct ranges with patches isolated south of the Alps in several species, corresponding with evolution of elevated genetic distance. The genetic subdivision within the continuous Italian range into northern and southern lineages in several taxa indicated the possible past substructure of the refugium. Several shared lin-eages between the Apennine and Ibero-Maghrebian regions were observed, indicating connectivity between the Adriatic and Atlantic−Mediterranean refuges, and raising questions as to which region these clades originated from and what was the direction of faunal exchange between them. In contrast to Europe's other two main refugia, the Apennine Peninsula is a smaller region with simpler phylogeographical patterns. Nevertheless, our results support the idea that the region generated novel lineages. Whereas diversification in sedentary bats may have been driven through the generation of in situ adaptations, specialization, and niche differentiation, the emergence of species with a tramp strategy could have entailed the utilization of faunal drift and the taxon cycle.
... Palearctic surveys were mainly located in Europe, often focused on vespertilionid bats, and in many cases involved researchers from these countries analyzing species in their own and neighboring countries. Several Palearctic studies examined taxonomic uncertainties or made conservation recommendations, but the overarching focus was testing evolutionary processes such as the effect of Pleistocene climatic oscillations and past refugia (Rossiter et al. 2007;Çoraman et al. 2013;Bogdanowicz et al. 2015). In the Afrotropical and Neotropical regions, the general research focus was different than in the Palearctic. ...
Phylogeography focuses on understanding the mechanisms that have led to the geographic distribution of genetic lineages within species, and studies of mammals have had an important role in its development. Bats are the second most diverse order of mammals; however, they are the subject of fewer phylogeographic studies than less diverse orders of mammals. Herein, we review the global state of phylogeographic bat research. Mitochondrial DNA loci are the most popular molecular markers, and the majority of studies describe geographic patterns of genetic variation. Many phylogeographic surveys were done in the Palearctic (mainly in the family Vespertilionidae), but more species have been studied in the Afrotropics and Neotropics (mainly in Pteropodidae and Phyllostomidae, respectively). Pleistocene climatic change is the main factor that has shaped the genetic diversity of species, but geographical and ecological factors are other important drivers of intraspecific differentiation. More intraspecific phylogeographic studies on bats are needed, but it is also necessary to develop comparative, integrative, and statistical approaches. Bats are excellent models for addressing evolutionary, ecological, and theoretical questions, given their world-wide distribution and their great biological heterogeneity. Annual meetings of the North American Society for Bat Research (NASBR) have contributed to the development of this field of molecular evolution, and we propose some future directions for phylogeographic research on bats.
... In particular, MC and MD have similar foraging behaviour and ecological niches, and outside Italy they can co-occur with the only other European trawling bat Myotis dasycneme (Britton et al., 1997;. This NIGS method was thus applied to investigate the genetic variability of these three co-occurring species that have been only studied in a single phylogenetic case-study in Italy (Bogdanowicz et al., 2015), and for which no NIGS-based works have been carried out so far. ...
In the last century bat populations significantly declined mainly due to habitat fragmentation and degradation. As management-dependent species, bats need appropriate monitoring programs for the implementation of sound conservation strategies. However, bats' small size, high mobility, elusiveness and nocturnal lifestyle make them difficult to survey. Non-Invasive Genetic Sampling (NIGS) may offer safe and cost-effective solutions, but requires well-planned sampling strategies, informative molecular markers and reliable laboratory protocols. Here we developed a NIGS protocol for species and individual identification of three mouse-eared bats, the Geoffroy's bat (Myotis emarginatus), the long-fingered bat (Myotis capaccinii) and the Daubenton's bat (Myotis dauben-tonii). Species identification was accomplished by mitochondrial (mt) DNA sequencing of reference tissue (n=49) and droppings (n=285) from Central-Northern Italy. In addition, we optimized a multiplex panel of seven microsatellites suitable for species and individual identification of the three species from droppings. We obtained a good success with mtDNA sequencing (245/285; 86%) and microsatellite genotyping (129/245; 53%). All microsatellites were successfully amplified with low error rates, and were polymorphic in the three Myotis species, with probabilities of identity 0.001 and observed heterozygosities of Ho=0.48 in M. emarginatus, 0.62 in M. capaccinii and 0.71 in M. daubentonii. Our protocol represents a useful tool for population genetic studies on mouse-eared bats that could likely be extended to other bat species and provide useful information to implement effective conservation plans.
... Molecular studies have also led to the discovery of many cryptic lineages and boosted the number of described bat species. For example, analyses of mitochondrial genes revealed several cryptic species in well-studied areas such as Europe (Kiefer et al. 2002, Ibáñez et al. 2006, Mayer et al. 2007, Bogdanowicz et al. 2015. The use of DNA barcoding (Hebert & Gregory 2005) led to a reevaluation of the number of bat species in the tropics (Francis et al. 2010, Wilson et al. 2014). ...
In this thesis, I investigated the causes and consequences of sociality in the neotropical bat
Molossus molossus. Due to the short availability of the insect patches it forages on and the
energetic costs of flight, this species is at energetic edge every day. Social foraging of group
members, using acoustic information transfer to locate insect patches, was recently proposed
as one reason for sociality of this species. The aim of my thesis was to assess the relationship
between social structure, foraging efficiency and survival using several social groups studied in
the village of Gamboa, Panama. Because species identification in this genus was unreliable, we
first used molecular, morphometric and acoustic data to distinguish M. molossus from the
sympatric species M. coibensis and M. bondae. The social groups of M. molossus typically
formed small harems of ten adults and their offspring. Because members of the same social
group forage together, small group size may result from a trade-off between benefits of patch
detection and costs of conspecific interference. Based on our data collected with automated
monitoring systems, one foraging session of ca. one hour after dusk was energetically sufficient
for individuals to fast until the following dusk period. We found no correlation between group
size and survival which may reflect a similar survival within the natural range of group sizes. The
short female lifespan (median of 1.8 years) that we found is likely a result from life at the
energetic edge due to a highly specialized diet (patches of ephemeral insects).
Insular bat communities are a preeminent conservation taxon due to their ecological role and intriguing and unique species composition. Sicily is the largest island in the Mediterranean. However, research on Sicilian bats is still scattered, with substantial information being overlooked. Here we present a systematic review of all available bibliographic information from 1810 to 2022, including grey literature, archives, and peer-reviewed publications. The analyses of bibliographic sources permitted us to evaluate the status of research on bats using the Bat Research Efficiency (BRE) and Species-Research Effort Allocation (SREA) metrics. A total of 81 documents were obtained. Since 1955, an average of 1.2 contributions have been issued per year. Over half of the documents are in Italian. The studies are primarily conducted in north-western (40%) and south-eastern (28%) Sicily, mainly in the provinces of Palermo and Siracusa. Most of the contributions concern “Species records” (61%) and “Ecology” (21%). There were 28 species reported, but a significant bias exists towards Myotis myotis, Miniopterus schreibersii, Rhinolophus ferrumequinum, Myotis capaccinii, and Rhinolophus euryale. Around 31.5% of the studies focused on threatened species, while 68.5% concentrated on non-threatened species, with an overall preference for cave-dwelling species. Yet, SREA analysis demonstrates a lack of research efforts for all species. We encourage the use of a multidisciplinary approach towards under-studied species while covering geographical gaps and increasing public awareness of the functional role of bats in natural ecosystems.
23 Islands often comprise unique faunal assemblages, particularly when they lie at the boundaries of 24 different bioregions or are located at a great distance from the mainland. Bats are among the few 25 mammals that can regularly be found on islands around the world, yet knowledge of insular bat 26 assemblages is often poor and anecdotal. Here we integrate different approaches to assess the bat 27 assemblage composition on the Mediterranean island of Pantelleria. We found that at least six species 28 occur on the island, including two typically African taxa, thus doubling the numbers known from 29 previous studies. We provide insights into the distribution, biogeography and conservation planning 30 of these bat species, highlighting the importance of studying and conserving insular bat populations. 31 32
Conventional monitoring tools are seldom effective for studying the ecology of rare and elusive mammals. In the present study, we use automated ultrasound detectors to provide information about seasonal activity of the greater noctule bat (Nyctalus lasiopterus), the largest and one of least known European bats. We selected localities within Central Europe with diverse geomorphological contexts, including rivers of different sizes and mountain passes. The study demonstrates the capability of the automatic recording approach to achieve bioacoustic discrimination of this species, but also pointed to the persistent need of integrating results from automatic classification software applications with the feedback from manual approaches. The high throughput capacity of the assay proved to be efficient, and the regular occurrence of the species was identified at two localities. These locations are associated with two known and intensely used migratory corridors of winged animals going through Vltava River valley and Červenohorské Saddle in Jeseníky mountains, as illustrated also by the activity patterns of other migratory species. Together with the occurrence of spring and autumn peaks in activity, these findings are in concordance with the plesiomorphic condition in pipistrelloid bats, showing also migratory behavior, and represent further indirect evidence of migration of the greater noctule. This pattern could be facilitated by the trophic niche of the species, involving predation of migrating songbirds. Differences in phenology of migratory species observed at particular sites likely mirror position of the locality in relation to migration flyways, seasonal and geographic variation in prey availability and energy demands etc. Further application of bioacoustic monitoring and other tools is necessary to obtain detailed information about the range and movement ecology of the species in higher latitudes.
The Myotis nattereri species complex consists of an entangled group of Western Palaearctic bats characterized by fringing hairs
along the rear edge of their uropatagium. Some members are relatively common while others are rare but all forms are
morphologically very similar and their taxonomy is unresolved. Recent studies based on different molecular markers have shown
that several major and unexpected lineages exist within this group of forest-dwelling bats. All the mitochondrial and nuclear markers
tested to date have shown that these major lineages evolved as fully independent and coherent units and therefore each qualifies as
distinct species. In the absence of proper morphological diagnosis, these lineages are informally referred to in the literature under
different names. We explore here the external and craniodental variation of these lineages. Although all morphological
measurements were overlapping between these lineages, we show that lineages can be completely discriminated in a multivariate
morphometric space. Consistent with previous molecular reconstructions, these four major lineages represent two pairs of related species, each represented by a named species (Myotis nattereri s. str. and M. escalerai, respectively) and by unnamed forms
(Myotis sp. A and Myotis sp. B, respectively). Herein we describe formally these two unnamed forms to clarify the taxonomy within
this species complex. This new taxonomic view has important implication for the protection of these species, as three of the four
taxa must now be considered as range-restricted species in need of conservation actions.
Aim
There is an increasing evidence showing that species within various taxonomic groups have reticulate evolutionary histories with several cases of introgression events. Investigating the phylogeography of species complexes can provide insight into these introgressions, and when and where these hybridizations occurred. In this study, we investigate the biogeography of a widely distributed Western Palaearctic bat species complex, namely Myotis nattereri sensu lato. This complex exhibits high genetic diversity and in its western distribution range is composed of deeply diverged genetical lineages. However, little is known about the genetic structure of the eastern populations. We also infer the conservation and taxonomical implications of the identified genetic divergences.
Taxon
Myotis nattereri sensu lato including M. schaubi.
Location
Western Palaearctic.
Methods
We analysed 161 specimens collected from 67 locations and sequenced one mitochondrial and four nuclear DNA markers, and combined these with the available GenBank sequences. We used haplotype networks, PCA, t‐SNE and Bayesian clustering algorithms to investigate the population structure and Bayesian trees to infer the phylogenetic relationship of the lineages.
Results
We identified deeply divergent genetical lineages. In some cases, nuclear and mitochondrial markers were discordant, which we interpret are caused by hybridization between lineages. We identified three such introgression events. These introgressions occurred when spatially separated lineages came into contact after range expansions. Based on the genetic distinction of the identified lineages, we suggest a revision in the taxonomy of this species group with two possible new species: M. hoveli and M. tschuliensis.
Main conclusions
Our findings suggest that the M. nattereri complex has a reticulate evolutionary history with multiple cases of hybridizations between some of the identified lineages.
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.
In contrast to the Eastern Palaearctic region a high degree of cryptic diversity was discovered among temperate bats of the Western Palaearctic region in the last ten years. Climatic oscillations caused severe changes in the distribution of species throughout the Palaearctic region during the Pleistocene. Exploring multiple taxa can help to understand general evolutionary differentiation processes. In the present study genetic variation within and among 94 Mongolian vespertilionid bats of six genera (Hypsugo, Eptesicus, Vespertilio, Myotis, Plecotus, and Nyctalus) was screened by sequencing a 798 bp fragment of the mitochondrial ND1 gene and then subsequently compared with those of Western Palaearctic taxa. This allowed first insights in the differentiation among a wide range of bats across the Palaearctic region. A total of 16 distinct mitochondrial lineages were found in Mongolia. Thirteen lineages differed by at least five percent sequence divergence from Western Palaearctic species. Only three lineages (Eptesicus nilssonii, Vespertilio murinus, and Nyctalus noctula) showed lower divergence values. Our data demonstrate a substantial differentiation between most Western and Eastern Palaearctic vespertilionid bats. Estimations of divergence times showed that most divergence appeared prior to the Pleistocene, but current distributions of bats were most likely shaped by the usage of multiple refugia during glaciations.
Assessing the ecological requirements of species coexisting within a community
is an essential requisite for developing sound conservation action. A particularly interesting
question is what mechanisms govern the stable coexistence of cryptic species within a
community, i.e. species that are almost impossible to distinguish. Resource partitioning
theory predicts that cryptic species, like other sympatric taxa, will occupy distinct ecological
niches. This prediction is widely inferred from eco-morphological studies. A new cryptic
long-eared bat species, Plecotus macrobullaris, has been recently discovered in the complex
of two other species present in the European Alps, with even evidence for a few mixed
colonies. This discovery poses challenges to bat ecologists concerned with planning con-
servation measures beyond roost protection. We therefore tested whether foraging habitat
segregation occurred among the three cryptic Plecotus bat species in Switzerland by ra-
diotracking 24 breeding female bats (8 of each species). We compared habitat features at
locations visited by a bat versus random locations within individual home ranges, applying
mixed effects logistic regression. Distinct, species-specific habitat preferences were revealed.
P. auritus foraged mostly within traditional orchards in roost vicinity, with a marked pref-
erence for habitat heterogeneity. P. austriacus foraged up to 4.7 km from the roost, selecting
mostly fruit tree plantations, hedges and tree lines. P. macrobullaris preferred patchy
deciduous and mixed forests with high vertical heterogeneity in a grassland dominated-
matrix. These species-specific habitat preferences should inform future conservation programmes. They highlight the possible need of distinct conservation measures for species that
look very much alike.
The demographic history of Rhinolophus hipposideros (lesser horseshoe bat) was reconstructed across its European, North African and Middle-Eastern distribution prior to, during and following the most recent glaciations by generating and analysing a multimarker data set. This data set consisted of an X-linked nuclear intron (Bgn; 543 bp), mitochondrial DNA (cytb-tRNA-control region; 1630 bp) and eight variable microsatellite loci for up to 373 individuals from 86 localities. Using this data set of diverse markers, it was possible to determine the species' demography at three temporal stages. Nuclear intron data revealed early colonization into Europe from the east, which pre-dates the Quaternary glaciations. The mtDNA data supported multiple glacial refugia across the Mediterranean, the largest of which were found in the Ibero-Maghreb region and an eastern location (Anatolia/Middle East)-that were used by R. hipposideros during the most recent glacial cycles. Finally, microsatellites provided the most recent information on these species' movements since the Last Glacial Maximum and suggested that lineages that had diverged into glacial refugia, such as in the Ibero-Maghreb region, have remained isolated. These findings should be used to inform future conservation management strategies for R. hipposideros and show the power of using a multimarker data set for phylogeographic studies.
We investigate the contribution of the Iberian bat fauna to the cryptic diversity in Europe using mitochondrial (cytb and ND1) and nuclear (RAG2) DNA sequences. For each of the 28 bat species known for Iberia, samples covering a wide geographic range within Spain were compared to samples from the rest of Europe. In this general screening, almost 20% of the Iberian species showed important mitochondrial discontinuities (K2P distance values > 5%) either within the Iberian or between Iberian and other European samples. Within Eptesicus serotinus and Myotis nattereri, levels of genetic divergence between lineages exceeded 16%, indicating that these taxa represent a complex of several biological species. Other well-differentiated lineages (K2P distances between 5-10%) appeared within Hypsugo savii, Pipistrellus kuhlii and Plecotus auritus, suggesting the existence of further cryptic diversity. Most unsuspected lineages seem restricted to Iberia, although two have crossed the Pyrenees to reach, at least, Switzerland.
Nietoperzowa Cave in southern Poland has more than 30 subfossils of mouse-eared bats of known age (820 ± 25 years BP). If DNA has been preserved in a useable fashion in these fossils, they will provide unique opportunities for studying historic population genetics of these animals. We sequenced the entire cytochrome b gene (1,140 bp) from seven subfossil and 56 contemporary individuals of mouse-eared bats from Europe and the Caucasus Mts. Our phylogenetic estimates, combined with a low level of genetic differentiation (2.7%) suggest that M. myotis and M. oxygnathus recently diverged and are distinct at the subspecies level. We also included a fragment of mitochondrial hypervariable region (292 bp) from contemporary mouse-eared bats in our analyses, and noted that among eight haplogroups recorded in Europe and the Caucasian Mts., haplogroup D (recognized as oxygnathus) probably arose in the Crimean refugium and evolved in a steppe landscape. The Balkan stock (haplogroup F) was also successful and dispersed over extended areas. Individuals possessing this haplogroup can be found from the northern part of Apennine Peninsula to southern Poland. On the other hand, during the last ice age, individuals with haplogroup A (described as myotis) most likely found refugia in Iberia. As the glaciers retreated north, these individuals migrated north of the Alps to central Europe (and then to the Balkans). As this group has much stronger affinities with forests than mouse-eared bats from southern parts of Europe, the dispersal of these individuals would have followed the northern migration of deciduous trees in this area. The Carpathian Basin is an area of mixing for several haplogroups from different refugia, including those in Iberia, Apennine Peninsula, Balkans, and the Crimea. Nuclear RAG2 sequence data revealed reciprocal hybridization events of both historic and recent origins. Our results document for the first time that both taxa were present north of the Carpathian Mts. for at least the past 800 years (ca. 400 generations). These are the first subfossil bats from which DNA has been extracted and sequenced, opening new possibilities for future research. Finally, these data highlight the importance of large phylogeographic surveys even among very common taxa.
The discovery that the most widespread bat in Europe comprises cryptic species, Pipistrellus pipistrellus (Schreber, 1774) (common pipistrelle) and Pipistrellus pygmaeus (Leach, 1825) (soprano pipistrelle), provides a great opportunity to look at the mechanism of species coexistence. Based on eight nuclear microsatellite loci (n = 353), we observed similarities between the species in Poland with respect to heterozygosity, allelic richness, mean relatedness, and inbreeding coefficients. However, pronounced differences in migratory patterns (shown by assignment tests) suggest that P. pygmaeus is the more migratory species. The proportion of bats migrating between colonies differed significantly, with 17.1% and 41.8% individuals of P. pygmaeus and P. pipistrellus, respectively, confidently assigned to colonies of origin. Both species demonstrated a more migratory character in central Europe compared with the populations from the British Isles. Given the cryptic nature of the examined taxa, we also assessed whether they hybridize. Hybridization was confirmed by three methods—one based on genetic distance and two based on Bayesian approaches. The overall hybridization rate, depending on assumed threshold values, ranged from 1.7% to 13.3% for both species. We conclude that the population structuring in these pipistrelles is not homogenous across their range. Moreover, hybridization between them in continental Europe does occur and is not rare.
This paper investigates the distribution of species richness, rarity and endemicity of European land mammals (bats and introduced species excluded). The highest level of species richness was in Central Europe, while Southern areas had the highest rarity and endemicity scores. The distribution of richness was affected by the location of sampling points in islands and peninsulas. After excluding these sampling points, richness continued to decrease Westward suggesting the existence of a large-scale peninsular effect on mammal distribution. These patterns of continental distribution of richness, rarity and endemicity could be the result of the distribution of refuge areas in the southern Mediterranean peninsulas, and the Pleis-tocene advances and retreats of mammals throughout the Western Palearctic. Thus, European mammal distribution can be interpreted on the basis of two different patterns of abundance distribution in which Palearctic species reduce their abundance from central-Europe outwards, while endemic, rare species show a similar depletion in the North. It should be useful to evaluate the role of the different regions in Europe in conserving the demographic interactions between central and peripheral populations of mammal species. Given the restricted distribution and potential small size of population, these endemic species are most likely to be susceptible to anthropogenic environmental degradation.
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.
1. A field experiment was used to test the effectiveness of a synthesized bat call as an acoustic lure to attract bats into mist nets in woodlands in southeast England. The stimulus was modelled on a social call of the rare Bechstein's bat Myotis bechsteinii.
2. In the Test condition, when the synthesized call was played, 23 bats of four species were captured, including six Bechstein's bats. In the Control condition, when no calls were played, only one bat was caught.
3. The bat call synthesizer is an effective tool for increasing capture rates for bats. Used as part of a systematic survey programme, it has the potential to provide the first baseline data on the distribution of bats in British woodlands.
Molecular analysis of diet overcomes the considerable limitations of traditional techniques for identifying prey remains in bat faeces. We collected faeces from individual Mountain Long-eared Bats Plecotus macrobullaris trapped using mist nets during the summers of 2009 and 2010 in the Pyrenees. We analysed their diet using DNA mini-barcodes to identify prey species. In addition, we inferred some basic features of the bat's foraging ecology that had not yet been addressed. P. macrobullaris fed almost exclusively on moths (97.8%). As prey we detected one dipteran genus (Tipulidae) and 29 moth taxa: 28 were identified at species level (23 Noctuidae, 1 Crambidae, 1 Geometridae, 1 Pyralidae, 1 Sphingidae, 1 Tortricidae), and one at genus level (Rhyacia sp., Noctuidae). Known ecological information about the prey species allowed us to determine that bats had foraged at elevations between 1,500 and 2,500 m amsl (above mean sea level), mostly in subalpine meadows, followed by other open habitats such as orophilous grasslands and alpine meadows. No forest prey species were identified in the diet. As 96.4% of identified prey species were tympanate moths and no evidence of gleaning behaviour was revealed, we suggest P. macrobullaris probably forages by aerial hawking using faint echolocation pulses to avoid detection by hearing moths. As we could identify 87.8% of the analysed sequences (64.1% of the MOTUs, Molecular Operational Taxonomic Units) at species level, we conclude that DNA mini-barcodes are a very useful tool to analyse the diet of moth-specialist bats.
Viewed from a geological perspective, present-day animal and plant communities in many parts of the world have a remarkably short history. The environmental revolution at the end of the Pleistocene, a mere 10 000 years ago, triggered major shifts in the ranges of species and hence composition of communities. Present-day communities in the boreal and temperate zones assembled at this time by combining species that survived the northern environment of the Last Cold Stage with those returning from more temperate refugia. Increasing evidence suggests that the well-studied European southern and eastern refugia for thermophilous animal and plant taxa were supplemented by cryptic refugia in northern Europe during the Late Pleistocene. These northern refugia would have been in areas of sheltered topography that provided suitable stable microclimates, and could partially explain the ‘nonanalogue’ mammalian assemblages of the Late Pleistocene. They also have implications for phylogeography and speciation.
The second largest order of mammals, Chiroptera comprises more than one thousand species of bats. Because of their mobility, bats are often the only native mammals on isolated oceanic islands, where more than half of all bat species live. These island bats represent an evolutionarily distinctive and ecologically significant part of the earthâs biological diversity. Island Bats is the first book to focus solely on the evolution, ecology, and conservation of bats living in the worldâs island ecosystems. Among other topics, the contributors to this volume examine how the earthâs history has affected the evolution of island bats, investigate how bat populations are affected by volcanic eruptions and hurricanes, and explore the threat of extinction from human disturbance. Geographically diverse, the volume includes studies of the islands of the Caribbean, the Western Indian Ocean, Micronesia, Indonesia, the Philippines, and New Zealand. With its wealth of information from long-term studies, Island Bats provides timely and valuable information about how this fauna has evolved and how it can be conserved.
We define a genetic species as a group of genetically compatible interbreeding natural populations that is genetically isolated from other such groups. This focus on genetic isolation rather than reproductive isolation distinguishes the Genetic Species Concept from the Biological Species Concept. Recognition of species that are genetically isolated (but not reproductively isolated) results in an enhanced understanding of biodiversity and the nature of speciation as well as speciation-based issues and evolution of mammals. We review criteria and methods for recognizing species of mammals and explore a theoretical scenario, the Bateson-Dobzhansky-Muller (BDM) model, for understanding and predicting genetic diversity and speciation in mammals. If the BDM model is operating in mammals, then genetically defined phylogroups would be predicted to occur within species defined by morphology, and phylogroups experiencing stabilizing selection will evolve genetic isolation without concomitant morphological diversification. Such species will be undetectable using classical skin and skull morphology (Morphological Species Concept). Using cytochrome-b data from sister species of mammals recognized by classical morphological studies, we estimated the number of phylogroups that exist within mammalian species and hypothesize that there will be >2,000 currently unrecognized species of mammals. Such an underestimation significantly affects conclusions on the nature of speciation in mammals, barriers associated with evolution of genetic isolation, estimates of biodiversity, design of conservation initiatives, zoonoses, and so on. A paradigm shift relative to this and other speciation-based issues will be needed. Data that will be effective in detecting these "morphologically cryptic genetic species" are genetic, especially DNA-sequence data. Application of the Genetic Species Concept uses genetic data from mitochondrial and nuclear genomes to identify species and species boundaries, the extent to which the integrity of the gene pool is protected, nature of hybridization (if present), and introgression. Genetic data are unique in understanding species because the use of genetic data 1) can quantify genetic divergence from different aspects of the genome (mitochondrial and nuclear genes, protein coding genes, regulatory genes, mobile DNA, microsatellites, chromosomal rearrangements, heterochromatin, etc.); 2) can provide divergence values that increase with time, providing an estimate of time since divergence; 3) can provide a population genetics perspective; 4) is less subject to convergence and parallelism relative to other sets of characters; 5) can identify monophyly, sister taxa, and presence or absence of introgression; and 6) can accurately identify hybrid individuals (kinship and source of hybrid individuals, F(1)s, backcrosses, direction of hybridization, and in concert with other data identify which hybrids are sterile or fertile). The proposed definition of the Genetic Species Concept is more compatible with a description of biodiversity of mammals than is "reproductively isolated species." Genetic profiles of mammalian species will result in a genetic description of species and mammalian diversity, and such studies are being accelerated by technological advances that reduce cost and increase speed and efficiency of generating genetic data. We propose that this genetic revolution remain museum- and voucher specimen-based and that new names are based on a holotype (including associated tissues) deposited in an accredited museum.
Climate change in the past has led to significant changes in species' distributions. However, how individual species respond to climate change depends largely on their adaptations and environmental tolerances. In the Quaternary, temperate-adapted taxa are in general confined to refugia during glacials while cold-adapted taxa are in refugia during interglacials. In the Northern Hemisphere, evidence appears to be mounting that in addition to traditional southern refugia for temperate species, cryptic refugia existed in the North during glacials. Equivalent cryptic southern refugia, to the south of the more conventional high-latitude polar refugia, exist in montane areas during periods of warm climate, such as the current interglacial. There is also a continental/oceanic longitudinal gradient, which should be included in a more complete consideration of the interaction between species ranges and climates. Overall, it seems clear that there is large variation in both the size of refugia and the duration during which species are confined to them. This has implications for the role of refugia in the evolution of species and their genetic diversity.
The Messinian salinity crisis--the desiccation of the Mediterranean Sea between 5.96 and 5.33 million years (Myr) ago--was one of the most dramatic events on Earth during the Cenozoic era. It resulted from the closure of marine gateways between the Atlantic Ocean and the Mediterranean Sea, the causes of which remain enigmatic. Here we use the age and composition of volcanic rocks to reconstruct the geodynamic evolution of the westernmost Mediterranean from the Middle Miocene epoch to the Pleistocene epoch (about 12.1-0.65 Myr ago). Our data show that a marked shift in the geochemistry of mantle-derived volcanic rocks, reflecting a change from subduction-related to intraplate-type volcanism, occurred between 6.3 and 4.8 Myr ago, largely synchronous with the Messinian salinity crisis. Using a thermomechanical model, we show that westward roll back of subducted Tethys oceanic lithosphere and associated asthenospheric upwelling provides a plausible mechanism for producing the shift in magma chemistry and the necessary uplift (approximately 1 km) along the African and Iberian continental margins to close the Miocene marine gateways, thereby causing the Messinian salinity crisis.
Previous genetic analyses have demonstrated that two phonic types of one of the most common European bats, the Common pipistrelle, belong to distinct species, although they are almost identical morphologically (45 kHz Pipistrellus pipistrellus and 55 kHz Pipistrellus pygmaeus). To reconstruct the history of the species complex and explain the codistribution of both forms in Europe and the Mediterranean, we performed phylogenetic analysis based on a 402-bp portion of the cytochrome b gene. Particular attention was paid to the eastern and southern parts of the range where no data were available. We found further distinctive allopatric haplotypes from Libya and Morocco. The difference of about 6-7% described in the Libyan population suggests the occurrence of a new species in the southern Mediterranean. The species status of Moroccan population is also discussed. The phylogeographic patterns obtained and analysis of fossil records support the hypothesis of expansion of both species into Europe from the Mediterranean region during the Holocene. The allopatric speciation model fits our data best. The paleobiographic scenario envisaged is corroborated also by molecular clock estimations and correlations with Late Neogene environmental changes in the Mediterranean region which ended with the Messinian salinity crisis.
The two sibling bat species Myotis myotis and Myotis blythii occur in sympatry over wide areas of Southern and Central Europe. Morphological, ecological and previous genetic evidence supported the view that the two species constitute two well-differentiated groups, but recent phylogenetic analyses have shown that the two species share some mtDNA haplotypes when they occur in sympatry. In order to see whether some genetic exchange has occurred between the two species, we sequenced a highly variable segment of the mitochondrial control region in both species living in sympatry and in allopatry. We also analysed the nuclear diversity of 160 individuals of both species found in two mixed nursery colonies located north and south of the Alps. MtDNA analysis confirmed that European M. blythii share multiple, identical or very similar haplotypes with M. myotis. Since allopatric Asian M. blythii presents mtDNA sequences that are very divergent from those of the two species found in Europe, we postulate that the mitochondrial genome of the European M. blythii has been replaced by that of M. myotis. The analysis of nuclear diversity shows a strikingly different pattern, as both species are well differentiated within mixed nursery colonies (F(ST) = 0.18). However, a Bayesian analysis of admixture reveals that the hybrids can be frequently observed, as about 25% of sampled M. blythii show introgressed genes of M. myotis origin. In contrast, less than 4% of the M. myotis analysed were classified as non-parental genotypes, revealing an asymmetry in the pattern of hybridization between the two species. These results show that the two species can interbreed and that the hybridization is still ongoing in the areas of sympatry. The persistence of well-differentiated nuclear gene pools, in spite of an apparent replacement of mitochondrial genome in European M. blythii by that of M. myotis, is best explained by a series of introgression events having occurred repeatedly during the recent colonization of Europe by M. blythii from Asia. The sharp contrast obtained from the analysis of mitochondrial and nuclear markers further points to the need to cautiously interpret results based on a single class of genetic markers.
The climatic cycles with subsequent glacial and intergalcial periods have had a great impact on the distribution and evolution of species. Using genetic analytical tools considerably increased our understanding of these processes. In this review I therefore give an overview of the molecular biogeography of Europe. For means of simplification, I distinguish between three major biogeographical entities: (i) "Mediterranean" with Mediterranean differentiation and dispersal centres, (ii) "Continental" with extra-Mediterranean centres and (iii) "Alpine" and/or "Arctic" with recent alpine and/or arctic distribution patterns. These different molecular biogeographical patterns are presented using actual examples.
Many "Mediterranean" species are differentiated into three major European genetic lineages, which are due to glacial isolation in the three major Mediterranean peninsulas. Postglacial expansion in this group of species is mostly influenced by the barriers of the Pyrenees and the Alps with four resulting main patterns of postglacial range expansions. However, some cases are known with less than one genetic lineage per Mediterranean peninsula on the one hand, and others with a considerable genetic substructure within each of the Mediterranean peninsulas, Asia Minor and the Maghreb. These structures within the Mediterranean sub-centres are often rather strong and in several cases even predate the Pleistocene.
For the "Continental" species, it could be shown that the formerly supposed postglacial spread from eastern Palearctic expansion centres is mostly not applicable. Quite the contrary, most of these species apparently had extra-Mediterranean centres of survival in Europe with special importance of the perialpine regions, the Carpathian Basin and parts of the Balkan Peninsula.
In the group of "Alpine" and/or "Arctic" species, several molecular biogeographical patterns have been found, which support and improve the postulates based on distribution patterns and pollen records. Thus, genetic studies support the strong linkage between southwestern Alps and Pyrenees, northeastern Alps and Carpathians as well as southeastern Alps and the Dinaric mountain systems, hereby allowing conclusions on the glacial distribution patterns of these species. Furthermore, genetic analyses of arctic-alpine disjunct species support their broad distribution in the periglacial areas at least during the last glacial period.
The detailed understanding of the different phylogeographical structures is essential for the management of the different evolutionary significant units of species and the conservation of their entire genetic diversity. Furthermore, the distribution of genetic diversity due to biogeographical reasons helps understanding the differing regional vulnerabilities of extant populations.
We announce the release of the fourth version of MEGA software, which expands on the existing facilities for editing DNA sequence data from autosequencers, mining Web-databases, performing automatic and manual sequence alignment, analyzing sequence alignments to estimate evolutionary distances, inferring phylogenetic trees, and testing evolutionary hypotheses. Version 4 includes a unique facility to generate captions, written in figure legend format, in order to provide natural language descriptions of the models and methods used in the analyses. This facility aims to promote a better understanding of the underlying assumptions used in analyses, and of the results generated. Another new feature is the Maximum Composite Likelihood (MCL) method for estimating evolutionary distances between all pairs of sequences simultaneously, with and without incorporating rate variation among sites and substitution pattern heterogeneities among lineages. This MCL method also can be used to estimate transition/transversion bias and nucleotide substitution pattern without knowledge of the phylogenetic tree. This new version is a native 32-bit Windows application with multi-threading and multi-user supports, and it is also available to run in a Linux desktop environment (via the Wine compatibility layer) and on Intel-based Macintosh computers under the Parallels program. The current version of MEGA is available free of charge at (http://www.megasoftware.net).
This is the first book in English reviewing and updating the geology of the whole Apennines, one of the recent most uplifted mountains in the world. The Apennines are the place from which Steno (1669) first stated the principles of geology. The Apennines also represent amongst others, the finding/testing sites of processes and products like volcanic eruptions, earthquakes, olistostromes and mélanges (argille scagliose), salinity crisis, geothermal fluids, thrust-top basins, and turbidites (first represented in a famous Leonardo's painting). As such, the Apennines are a testing and learning ground readily accessible and rich of any type of field data. A growing literature is available most of which is not published in widely available journals.
The objective of the book is to provide a synthesis of current data and ideas on the Apennines, for the most part simply written and suitable for an international audience. However, sufficient details and in-depth analyses of the various complex settings have been presented to make this material useful to professional scholars and to students of senior university courses.
A new method called the neighbor-joining method is proposed for reconstructing phylogenetic trees from evolutionary distance data. The principle of this method is to find pairs of operational taxonomic units (OTUs [= neighbors]) that minimize the total branch length at each stage of clustering of OTUs starting with a starlike tree. The branch lengths as well as the topology of a parsimonious tree can quickly be obtained by using this method. Using computer simulation, we studied the efficiency of this method in obtaining the correct unrooted tree in comparison with that of five other tree-making methods: the unweighted pair group method of analysis, Farris's method, Sattath and Tversky's method, Li's method, and Tateno et al.'s modified Farris method. The new, neighbor-joining method and Sattath and Tversky's method are shown to be generally better than the other methods.
Limited information from existing data sets and the tremendous amount of diversity in number and kind within the chiropteran family Vespertilionidae (about one-third of all bat species) have hampered efforts to provide adequate assessments of long-standing genealogic hypotheses (e.g., monophyly of the family and of the five subfamilies). We generated approximately 2.6 kilobase pairs of mitochondrial DNA (mtDNA) sequence ecompassing three adjacent genes (12S rRNA, tRNAVa1, 16S rRNA) for 120 vespertilionids representing 110 species, 37 of 44 genera, and all subfamilies. We assessed monophyly of Vespertilionidae in initial analyses of 171 taxa including representatives of all bat families (except the monotypic Craseonycteridae), and assessed lower-level relationships by analysis of several truncated taxon sets. Phylogenetic analysis of ribosomal gene sequences provides well-supported resolution for vespertilionid relationships across taxonomic levels. Furthermore, the resolution is not heavily burdened by alignment of ambiguous regions of the ribosomal gene sequences, and topologies and levels of support produced by two phylogenetic methods (Bayesian and Parsimony) agreed markedly. Our analyses suggest relationships that support many parts of the traditional classification but which also support several changes. The majority of these changes also receives support from other data sources, particularly bacular and karyotypic data. We make more than 20 taxonomic conclusions or recommendations and construct a working classification for vespertilionoid bats. Highlights include: Miniopterus (subfamily Miniopterinae) is recognized in its own family, Miniopteridae, as it represents an extremely divergent lineage relative to other vespertilionids, and in some analyses is sister to the molossids and natalids; all other vespertilionids examined form a well-supported clade; two of the traditional subfamilies within Vespertilionidae (sensu stricto) are monophyletic, Murininae and Kerivoulinae; Nyctophilinac has no validity and Vespertilioninae is paraphyletic relative to the position of Myotis; Myotis is sister to a clade containing Kerivoulinae and Murininae and is recognized in its own subfamily, Myotinae; Myotis subgenera Leuconoe, Selysius, and Myotis are polyphyletic, and a subgeneric classification reflecting geography is suggested, broadening subgenus Myotis to include the sampled Old World species, and allocating the sampled New World species to another subgenus (Aeorestes Fitzinger, 1870); Vespertilioninae (excluding Myotis) is monophyletic; Pipistrellus-like bats (i.e., the traditional tribe Vespertilionini) are divided into three tribes (Nycticeiini, Pipistrellini; Vespertilionini); and support for three tribes of Pipistrellus-like bats has several implications at the genus level. Overall, this study offers a robust working hypothesis for vespertilionid relationships and provides a good starting point for new investigations into the evolutionary history of Vespertilionidae.
This revised edition of a book first published in 1973 provides an insight into contemporary biogeography and its historical roots. The concept of biogeography is introduced, followed by a short discussion on biodiversity. Chapter 3 deals with distribution patterns, covering topics such as distribution barriers and endemicity. Next the concepts of community, ecosystem and biome are covered. The origin of diversity through speciation and evolution is then discussed. Chapter 6 reviews the theory of island biogeography outlining, for instance, its potential applicability to reserve design. The next chapter looks at past patterns of organism distribution, followed by a review of present day patterns. After a brief review of techniques for interpreting the past (eg phylogenetic cladistics), the effects of glaciation on biogeography are explored. The final chapter looks to the future by analysing the present and probable future influence (eg climatic deterioration) of humans on biogeography. -S.R.Harris
The term ‘refugia’ was originally used to describe the restricted full-glacial locations of modern mid- and high-latitude taxa, especially trees and shrubs. We discuss the extension of this original use to other situations, including its widening to encompass ‘interglacial refugia’. Recent genetic work with modern populations suggests that, at the glacial–interglacial transition, those taxa that did vastly increase their ranges and abundances did so from a small subset of their full-glacial populations. We suggest that ‘bottleneck’ might be a more appropriate term to use for temporarily reduced populations, to indicate continuity of the populations, and that individualistic response of taxa to climate change appears to extend to intra-specific levels. The extent to which expanded populations contribute to long-term genetic pools remains uncertain.
Undisturbed ant faunas of islands in the Moluccas-Melanesian arc are for the most part "saturated," that is, approach a size that is correlated closely with the landmass of the island but only weakly with its geographic location (figure 1). In the Ponerinae and Cerapachyinae combined the saturation level can be expressed approximately as F=3A0.6, where F is the number of species in the fauna and A the area of the island in square miles. Interspecific competition, involving some degree of colonial warfare, plays a major role in the determination of the saturation curve. It deploys the distribution of some ant species into mosaic patterns and increases the diversification of local faunas. Perhaps because of the complex nature of the Melanesian fauna, differences between local faunas appear that give the subjective impression of randomness. Despite the action of species exclusion, the size of local faunas occurring within a set sample area increases with the total size of the island (figure 2). Water gaps br...
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.
The large Myotis complex in continental Europe, Asia Minor, and Transcaucasia comprises two sibling bat species, the greater mouse-eared bat, Myotis myotis, and the lesser mouse-eared bat, Myotis blythii, also referred to as Myotis oxygnathus. Here, we investigate the phylogeography of these bats using two mitochondrial markers: the second hypervariable domain of the control region (HVII) and a fragment of the cytochrome b gene (cyt b). The HVII haplotypes formed six distinct haplogroups associated with different geographical regions. Most of the European HVII haplotypes were exclusive to M.?myotis, whereas the majority of HVII haplotypes found in Asia Minor were exclusive to M. blythii/M. oxygnathus. The phylogenetic reconstruction based on the concatenated cyt b and HVII fragments recovered two major lineages. The first lineage comprised samples from Europe (western lineage), and the second lineage included samples from Asia Minor, Transcaucasia, Crimea, Western Ukraine, Thrace, the Balkans, and Eastern Europe (eastern lineage). The mitochondrial lineage of M. blythii, reported from Kyrgyzstan, was not present in Asia Minor and Transcaucasia. Therefore, we consider the possibility that the M. blythii/M. oxygnathus found in Europe, Asia Minor, and Transcaucasia are not recent descendants of the Central Asian M. blythii. Instead, we suggest that M. blythii/M.?oxygnathus and M. myotis diverged through allopatric speciation in Asia Minor and Europe, and that they are represented by the eastern and western mitochondrial lineages. We also examine an alternative hypothesis: that the large Myotis complex consists of more than two species that diverged independently in Asia Minor and Europe through ecological speciation.
The role of glacial refugia in the biogeographical patterns in the Western Palaearctic region has been widely discussed, but many questions remain unresolved. We examined the biogeography, genetic diversity, spatial distribution and evolutionary history of the Myotis nattereri bat species complex to investigate the presence of multiple refugia and the persistence of Quaternary differentiation between and within Mediterranean refugia in a flying mammal.
Western Palaearctic region (central and southern Europe and north-western Maghreb).
We analysed three mitochondrial fragments (cytochrome b, NADH dehydrogenase subunit 1 and the control region; 1570 bp) from 136 individuals of the M. nattereri complex sampled from 87 different localities using a range of phylogenetic techniques. Divergences among clades were also dated using a Bayesian coalescence approach.
Phylogenetic analyses identified four main lineages, coincident with the four cryptic species recently described. Each species is further subdivided into well-supported lineages with evident geographical structure. Estimates of genetic diversity and polymorphism were very high for the majority of subclades, with the exception of M. nattereri s.s.
The M. nattereri bat complex comprises four species whose distributions in the Western Palaearctic correspond to four main glacial refugia (Iberia, Italy, Balkans and Morocco). These species are the result of long-term isolation (remarkable in a flying mammal) over several glacial cycles. The Balkan species expanded into central Europe in a rapid recolonization process. Both the Iberian and Italian peninsulas show a clear pattern of refugia-within-refugia in their genetic structuring, with a deeply differentiated southern Italian clade. Morocco shows two markedly differentiated lineages, probably separated by the Atlas Mountains. The legacy of Pleistocene cycles is evident in both the speciation and the intraspecific diversification events.
Aim The Mediterranean Basin is a centre of radiation for numerous species groups. To increase our understanding of the mechanisms underlying speciation and radiation events in this region, we assessed the phenotypic variability within the Pipistrellus pipistrellus–pygmaeus–hanaki species complex. Although bats form the second largest mammalian order, studies of insular evolution in this group are scarce. We approached this problem from a microevolutionary perspective and tested for the recurrence of the insular syndrome.
Aim We investigate the population genetic structure of the Maghrebian bat, Myotis punicus , between the mainland and islands to assess the island colonization pattern and current gene flow between nearby islands and within the mainland.
Location North Africa and the Mediterranean islands of Corsica and Sardinia.
Methods We sequenced part of the control region ( HVII ) of 79 bats across 11 colonies. The phylogeographical pattern was assessed by analysing molecular diversity indices, examining differentiation among populations and estimating divergence time. In addition, we genotyped 182 bats across 10 colonies at seven microsatellite loci. We used analysis of molecular variance and a Bayesian approach to infer nuclear population structure. Finally, we estimated sex‐specific dispersal between Corsica and Sardinia.
Results Mitochondrial analyses indicated that colonies between Corsica, Sardinia and North Africa are highly differentiated. Within islands there was no difference between colonies, while at the continental level Moroccan and Tunisian populations were highly differentiated. Analyses with seven microsatellite loci showed a similar pattern. The sole difference was the lack of nuclear differentiation between populations in North Africa, suggesting a male‐biased dispersal over the continental area. The divergence time of Sardinian and Corsican populations was estimated to date back to the early and mid‐Pleistocene.
Main conclusions Island colonization by the Maghrebian bats seems to have occurred in a stepping‐stone manner and certainly pre‐dated human colonization. Currently, open water seems to prevent exchange of bats between the two islands, despite their ability to fly and the narrowness of the strait of Bonifacio. Corsican and Sardinian populations are thus currently isolated from any continental gene pool and must therefore be considered as different evolutionarily significant units (ESU).
The phylogenetic relationships within the genus Plecotus were assessed using molecular as well as morphological methods. With only three species missing, our study is based on an almost comprehensive taxonomic sampling. The genetic analysis comprised 151 individuals from throughout the range. Sequences of two mitochondrial sections, parts of the 16S rRNA gene (16S) and of the control region (CR) were analysed. The morphological analysis of cranial and external characters comprised 697 individuals, including 10 holotypes and one lectotype. Data from 15 craniometric characters of 442 specimens were used in the multivariate analyses. The molecular data identified nine primary clades representing 11 species, 10 of which could be assigned to described taxa, whereas one was described as a new species, Plecotus strelkovi Spitzenberger sp. nov. The tree based on 16S revealed two major lineages, one consisting of only one primary clade restricted to the Mediterranean, the other consisting of eight primary clades representing Eurasian taxa. The morphological analysis revealed five additional species, two of them not described. Together with the recently described P. taivanus, P. sardus and P. balensis, which were not included in our analysis, the genus Plecotus comprises at least 19 more or less cryptic species. Phylogenetic and phenetic analyses resulted in similar but not completely concordant arrangements of the species. The proposed classification relies mainly on the tree based on 16S sequences. The current distribution indicates that 16 species can be linked to arboreal refugia, three to eremial refugia. We assume that speciation within the gleaning, rather slow flying long-eared bats is due to a multitude of disruption and isolation processes within a formerly continuous range of the broad-leaved Arcto-Tertiary forest in which Plecotus probably originated. An exact calibrated molecular dating of the splits is not possible. The Early Oligocene age of the presumed ancestor of the Plecotini and a correlation of the molecular diversifications with palaeogeographic reconstructions suggest that the divergence of the two major lineages may have occurred already during the Middle Miocene, 14.5 Mya.
The species problem is the long-standing failure of biologists to agree on how we should identify species and how we should define the word ‘species’. The innumerable attacks on the problem have turned the often-repeated question ‘what are species?’ into a philosophical conundrum. Today, the preferred form of attack is the well-crafted argument, and debaters seem to have stopped inquiring about what new information is needed to solve the problem. However, our knowledge is not complete and we have overlooked something. The species problem can be overcome if we understand our own role, as conflicted investigators, in causing the problem.
Here, we present a study of the Pipistrellus pipistrellus species complex, a highly diversified bat group with a radiation centre in the Mediterranean biodiversity hotspot. The study sample comprised 583 animals from 118 localities representatively covering the bats' range in the western Palearctic. We used fast-evolving markers (the mitochondrial D-loop sequence and 11 nuclear microsatellites) to describe the phylogeography, demography and population structure of this model taxon and address details of its diversification. The overall pattern within this group includes a mosaic of phylogenetically basal, often morphologically distant, relatively small and mostly allopatric demes in the Mediterranean Basin, as well as two sympatric sibling species in the large continental part of the range. The southern populations exhibit constant size, whereas northern populations show a demographic trend of growth associated with range expansion during the Pleistocene climate oscillations. There is evidence of isolation by distance and female philopatry in P. pipistrellus sensu stricto. Although the northern populations are reproductively isolated, we detected introgression events among several Mediterranean lineages. This pattern implies incomplete establishment of reproductive isolating mechanisms in these populations as well as the existence of a past reinforcement stage in the continental siblings. The occurrence of reticulations in the radiation centre among morphologically and ecologically derived relict demes suggests that adaptive unequal gene exchange within hybridizing populations could play a role in speciation and adaptive radiation within this group.
A new method called the neighbor-joining method is proposed for reconstructing phylogenetic trees from evolutionary distance data. The principle of this method is to find pairs of operational taxonomic units (OTUs [= neighbors]) that minimize the total branch length at each stage of clustering of OTUs starting with a starlike tree. The branch lengths as well as the topology of a parsimonious tree can quickly be obtained by using this method. Using computer simulation, we studied the efficiency of this method in obtaining the correct unrooted tree in comparison with that of five other tree-making methods: the unweighted pair group method of analysis, Farris's method, Sattath and Tversky's method, Li's method, and Tateno et al.'s modified Farris method. The new, neighbor-joining method and Sattath and Tversky's method are shown to be generally better than the other methods.
European hedgehogs, Erinaceus europaeus and E. concolor, are among the many European plant and animal taxa that have been subjected to cyclical restriction to glacial refugia and interglacial expansion. An analysis of 95 mitotypes, comprising partial cytochrome b and control region sequences, shows deep divergence between the two hedgehog species. Three europaeus and two concolor clades are clearly identified and are consistent with previously identified refugia for Europe: the Iberian peninsula, Italy, and the Balkans. The degree of mitochondrial divergence among these clades suggests pre-Pleistocene separation of the refugial populations. In contrast, analysis of two nuclear introns clearly separates the two concolor clades, as in the mitochondrial data, but cannot discriminate the three europaeus clades. This discrepancy between nuclear and mitochondrial data is attributed to historical differences in the refugial population size of europaeus and concolor. The geographical distribution of mitotypes is analysed using nested clade analysis. This method, by including unobserved ('missing') mitotypes, can identify mitotype groupings that remain undetected in conventional analyses. However, the application of nested clade analysis to the study of refugial populations may be hampered by such factors as the loss of haplotypes from the refugial areas by repeated contractions of the population and the recent time scale of colonization relative to mutation rate.
Long-eared bats of the genus Plecotus are widespread and common over most of the western Palaearctic. Based on recent molecular evidence, they proved to represent a complex of several cryptic species, with three new species being described from Europe in 2002. Evolutionary relationships among the different lineages are still fragmentary because of the limited geographic coverage of previous studies. Here we analyze Plecotus mitochondrial DNA sequences from the entire Mediterranean region and Atlantic Islands. Phylogenetic reconstructions group these western Palaearctic Plecotus into two major clades which split at least 5 Myr ago and that are each subdivided into further subgroups. An 'auritus group' includes the traditional P. auritus species and its sister taxon P. macrobullaris (=P. alpinus) plus related specimens from the Middle East. P. auritus and P. macrobullaris have broadly overlapping distributions in Europe, although the latter is apparently more restricted to mountain ranges. The other major clade, the 'austriacus group,' includes the European species P. austriacus and at least two other related taxa from North Africa (including P. teneriffae from the Canary Islands), the Balkans and Anatolia (P. kolombatovici). The sister species of this 'austriacus group' is P. balensis, an Ethiopian endemic. Phylogenetic reconstructions further suggest that P. austriacus reached Madeira during its relatively recent westward expansion through Europe, while the Canary Islands were colonized by a North African ancestor. Although colonization of the two groups of Atlantic Islands by Plecotus bats followed very distinct routes, neither involved lineages from the 'auritus group.' Furthermore, the Strait of Gibraltar perfectly segregates the distinct lineages, which confirms its key role as a geographic barrier. This study also stresses the biogeographical importance of the Mediterranean region, and particularly of North Africa, in understanding the evolution of the western Palaearctic biotas.
In order to contribute to the debate about southern glacial refugia used by temperate species and more northern refugia used by boreal or cold-temperate species, we examined the phylogeography of a widespread snake species (Vipera berus) inhabiting Europe up to the Arctic Circle. The analysis of the mitochondrial DNA (mtDNA) sequence variation in 1043 bp of the cytochrome b gene and in 918 bp of the noncoding control region was performed with phylogenetic approaches. Our results suggest that both the duplicated control region and cytochrome b evolve at a similar rate in this species. Phylogenetic analysis showed that V. berus is divided into three major mitochondrial lineages, probably resulting from an Italian, a Balkan and a Northern (from France to Russia) refugial area in Eastern Europe, near the Carpathian Mountains. In addition, the Northern clade presents an important substructure, suggesting two sequential colonization events in Europe. First, the continent was colonized from the three main refugial areas mentioned above during the Lower-Mid Pleistocene. Second, recolonization of most of Europe most likely originated from several refugia located outside of the Mediterranean peninsulas (Carpathian region, east of the Carpathians, France and possibly Hungary) during the Mid-Late Pleistocene, while populations within the Italian and Balkan Peninsulas fluctuated only slightly in distribution range, with larger lowland populations during glacial times and with refugial mountain populations during interglacials, as in the present time. The phylogeographical structure revealed in our study suggests complex recolonization dynamics of the European continent by V. berus, characterized by latitudinal as well as altitudinal range shifts, driven by both climatic changes and competition with related species.
After volcanic explosions or tidal waves had defaunated several islands near New Guinea, bird species number rapidly returned to equilibrium on coral islets and rapidly returned to quasi-steady-state values limited by regrowth of vegetation in lowland forest of larger islands. However, reequilibration in montane forest has been limited by slow dispersal of the birds. Colonists have been drawn disproportionately from r-selected "supertramrip" species, which maintain much higher population densities than do K-selected faunas, perhaps due to selection for resource overexploitation by the latter.
Models for the development of species distribution in Europe typically invoke restriction in three temperate Mediterranean refugia during glaciations, from where recolonization of central and northern Europe occurred. The brown bear, Ursus arctos, is one of the taxa from which this model is derived. Sequence data generated from brown bear fossils show a complex phylogeographical history for western European populations. Long-term isolation in separate refugia is not required to explain our data when considering the palaeontological distribution of brown bears. We propose continuous gene flow across southern Europe, from which brown bear populations expanded after the last glaciation.
Sicily) collected the material
- B C La )
la), B. C ˇ. B., and P. H. (Sicily) collected the material;
Guidelines for bat monitoring: methods for the study and conservation of bats in Italy Ministero dell'Ambiente, Istituto Nazionale per la Fauna Selvatica The for-aging ecology of the mountain long-eared bat Plecotus macrobullaris revealed with DNA mini-barcodes
- P H P Agnelli
- A Martinoli
- Russo E D Patriarca
- D Scaravelli
- P Genovesi
P. H. wrote the paper and all authors contribut-ed to the final version of the manuscript. REFERENCES Agnelli P, Martinoli A, Patriarca E, Russo D, Scaravelli D, Genovesi P. 2004. Guidelines for bat monitoring: methods for the study and conservation of bats in Italy. Quaderni di Conservazione della Natura. 19 bis. Rome and Ozzano dell'Emilia, Bologna, Italy: Ministero dell'Ambiente, Istituto Nazionale per la Fauna Selvatica. Alberdi A, Garin I, Aizpurua O, Aihartza J. 2012. The for-aging ecology of the mountain long-eared bat Plecotus macrobullaris revealed with DNA mini-barcodes. PLoS ONE 7: e35692.
Phylogeography: the history and formation of species Speciation in mammals and the genetic species concept
- Jc Avise
Avise JC. 2000. Phylogeography: the history and formation of species. Cambridge, MA: Harvard University Press. Baker RJ, Bradley RD. 2006. Speciation in mammals and the genetic species concept. Journal of Mammalogy 87: 643– 662.
The Mediterranean region: biological diversity through time and space
- J Blondel
- J Aronson
- J-Y Bodiou
- G Boeuf
Blondel J, Aronson J, Bodiou J-Y, Boeuf G. 2010. The Mediterranean region: biological diversity through time and space.
Oxford: Oxford University Press.
Cryptic diversity in Mongolian vespertilionid bats (Vespertilionidae, Chiroptera, Mammalia). Results of the Mongolian-German biological expeditions since
- T Datzmann
- D Dolch
- N Batsaikhan
- A M Kiefer
- U Zophel
- M Stubbe
- Mayer
Datzmann T, Dolch D, Batsaikhan N, Kiefer A, Helbig-Bonitz M, Zophel U, Stubbe M, Mayer F. 2012. Cryptic diversity in Mongolian vespertilionid bats (Vespertilionidae, Chiroptera, Mammalia). Results of the Mongolian-German biological expeditions since 1962, No. 299. Acta Chiropterologica 14: 243–264.