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Cryptic diversity of Italian bats and the role of the Apennine refugium in the phylogeography of the western Palaearctic
Abstract
Keywords: Chiroptera; cryptic taxa; glacial refugium; mtDNA; species diversity.
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 lineages 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. © 2015 The Linnean Society of London
... In contrast to the lack of apparent geographical morphological differentiation and ecological plasticity, several divergent lineages of the mitochondrial genome were found in different regions of the Palearctic (Mayer and Helversen 2001;Ibáñez et al. 2006;Mayer et al. 2007;García-Mudarra et al. 2009;Veith et al. 2011;Galimberti et al. 2012;Çoraman et al. 2013;Bogdanowicz et al. 2015;Batsleer et al. 2019;Mi̇fsud and Vella 2019;Borloti et al. 2020;Dolch et al. 2021). All studies had a regional focus in respect of the large Palearctic distribution of this species. ...
... Therefore, the larger extent and distribution of these lineages remained unclear, including larger geographic gaps of knowledge. So far, three mitochondrial lineages had been detected: A lineage from South-Western Europe (Pestano et al. 2003;Ibáñez et al. 2006;García-Mudarra et al. 2009;Veith et al. 2011), a wide-spread lineage ranging from Macaronesia to Italy (Pestano et al. 2003;Ibáñez et al. 2006;Mayer et al. 2007;García-Mudarra et al. 2009;Veith et al. 2011;Bogdanowicz et al. 2015;Batsleer et al. 2019;Mi̇fsud and Vella 2019;Borloti et al. 2020), and a South-Eastern European and Middle Eastern lineage (Ibáñez et al. 2006;Mayer et al. 2007;Çoraman et al. 2013;Mi̇fsud and Vella 2019;Dolch et al. 2021). ...
... Uncorrected p-distances were chosen as a measure of genetic distance and to allow continuity with previous studies (e.g., Mayer et al. 2007;Çoraman et al. 2013;Bogdanowicz et al. 2015;Mi̇fsud and Vella 2019). To obtain reliable results, we manually reduced each alignment by excluding sequences that (1) did not overlap with the majority or (2) were of lesser quality. ...
Today’s biodiversity was strongly impacted by glacial cycles during the Pleistocene. They generated species diversity and population structuring, which can easily remain undetected, if populations differentiation is not accompanied by divergence in external morphological traits. This phenomenon, described as cryptic diversity, has been intensively researched in bats, which are known to harbour cryptic phylogenetic lineages. Many studies however have a regional focus or suffer from geographical gaps. Widely understudied areas include Central and Western Asia, although they connect the western and eastern Palearctic fauna. These areas are characterized by topographic heterogeneity and therefore high ecosystem diversity. In this study we investigated the phylogeography of the Savii’s pipistrelle (Hypsugo savii), a bat species assumed to be widely distributed across the Palaearctic. We compiled published sequences from four mitochondrial genes (ND1, CytB, COI and 16 S), added new sequences especially from the Asian part of the distribution range and performed phylogenetic and phylogeographic analyses. They indicate that H. savii is a taxonomic unit with extensive cryptic diversity, comprising at least four major mitochondrial lineages with allopatric or parapatric distribution ranges. Divergence time dating reveals the impact of Pleistocene glaciations on shaping highly structured populations of a highly mobile mammal across the Palearctic. Our study also revealed several zones of secondary contact among populations where hybridization and gene flow likely occur. This study highlights the necessity for studying biodiversity in Western and Central Asia in order to understand biogeographic patterns, evolutionary processes and conservation needs in the area that connects eastern and western Palearctic faunas.
... Hence, under the taxonomic view adopted here, M. punicus Felten, 1977 is a biologically independent species that is endemic to North Africa, Corsica, Sardinia, and the Maltese archipelago (see Fig. 1). There is no subspecies described, but some insular populations are slightly larger than Map template: © Getty Images/iStockphoto (Bogdanowicz et al. 2015) is not depicted here, as it might represent a stray individual away from the permanent breeding range of the species. (Map template: © Getty Images/iStockphoto) continental ones and may warrant further taxonomic scrutiny Evin et al. 2008). ...
... However, a single female caught in June 2007 near the entrance of a collapsed tunnel in Catania was biopsied and released. This individual was sequenced for a mitochondrial gene (available in the GenBank under the accession number KJ948264), which proved to be closely related to M. punicus (Bogdanowicz et al. 2015). As no other recent or paleontological evidence exist for Maghrebian mouse-eared bats in Sicily, this single bat either might represent a stray individual from adjacent populations living in Sardinia or Tunisia or, less likely, might be a sign of a recent and overlooked colonization event of Sicily by M. punicus. ...
... The morphological distinction of M. punicus from the other two sibling species in this group is, however, very difficult due to the broad morphometric overlap of characters but is possible based on an analysis of skull shape (Evin et al. 2008) (Fig. 3). Genetic markers, such as mitochondrial and nuclear genes, discriminate M. punicus from any other species of Myotis (Bogdanowicz et al. 2015;Castella et al. 2000;) and thus provide the most Table 1 External measurements (expressed in mm) of adult M. punicus from both sexes issued from Corsica. (2004) reliable method of identification when the origin of the sample is unknown. ...
... However, multivariate morphological analyses of the skull variability of all larger forms of mouse-eared bats (Benda and Horácek 1995a;Evin et al. 2008), as well as multiple genetic markers , showed that the Maghrebian mouse-eared bats differ in shape and are phylogenetically divergent from all other taxa in this group. Hence, under the taxonomic view adopted here, M. punicus Felten, 1977 is a biologically independent species that is endemic to North Africa, Corsica, Sardinia, and the Maltese archipelago (see © Getty Images/iStockphoto (Bogdanowicz et al. 2015) is not depicted here, as it might represent a stray individual away from the permanent breeding range of the species Fig. 1). There is no subspecies described, but some insular populations are slightly larger than continental ones and may warrant further taxonomic scrutiny Evin et al. 2008). ...
... However, a single female caught in June 2007 near the entrance of a collapsed tunnel in Catania was biopsied and released. This individual was sequenced for a mitochondrial gene (available in the GenBank under the accession number KJ948264), which proved to be closely related to M. punicus (Bogdanowicz et al. 2015). As no other recent or paleontological evidence exist for Maghrebian mouse-eared bats in Sicily, this single bat either might represent a stray individual from adjacent populations living in Sardinia or Tunisia or, less likely, might be a sign of a recent and overlooked colonization event of Sicily by M. punicus. ...
... The morphological distinction of M. punicus from the other two sibling species in this group is, however, very difficult due to the broad morphometric overlap of characters but is possible based on an analysis of skull shape (Evin et al. 2008) (Fig. 3). Genetic markers, such as mitochondrial and nuclear genes, discriminate M. punicus from any other species of Myotis (Bogdanowicz et al. 2015;Castella et al. 2000;) and thus provide the most reliable method of identification when the origin of the sample is unknown. Otherwise, as the Maghrebian mouse-eared bat is the only species of large Myotis in its range (see above), geographic origin allows its specific assignation. ...
... One of the latest published research on bats from Malta has confirmed through acoustic and morphological analyses the presence of six resident bat species (Mifsud & Vella, 2018) representing species within genera which showed signs of cryptic diversity when studied across the Western Palaearctic using molecular techniques (Ibáñez et al., 2006;Spitzenberger et al., 2006;Mayer et al., 2007;García-Mudarra et al., 2009;Bogdanowicz et al., 2015). Previous acoustic surveys of bats from Malta revealed sensory divergence for the species Pipistrellus pipistrellus and Rhinolophus hipposideros when compared to their mainland conspecifics (Mifsud & Vella 2018), and therefore the addition of molecular data to the morphological and acoustic data available would further uncover the evolutionary significance of bat populations present in the Maltese Islands. ...
... The haplotype diversity (π) for the Maltese and Italian H. savii population was 0.7714 and 0.2714, respectively. The 21 individuals of H. savii from Malta and Gozo were sampled from 5 locations being 8 -36 km apart, while samples from Italy were collected from 8 sampling areas separated by c. 27 -300 km (Bogdanowicz et al., 2015). ...
... The sequences from this study represent the first COI sequences of P. pipistrellus SW mitochondrial lineage. The ND1 dataset including sequences from Malta and those analysed by Bogdanowicz et al. (2015) recovered the same phylogenetic tree topology with a main continental lineage, P. pipistrellus s.str., a Moroccan lineage and a central Mediterranean lineage which includes samples from south Italy and Malta (Figure 3). The Maltese haplogroup had a p-distance of 3.1 ± 0.5, 2.7 ± 0.5, 1.5 ± 0.4% to the continental, Moroccan and Italian lineages, respectively. ...
This work presents the first genetic species identification and phylogenetic analyses of all six bat species known to inhabit the Maltese archipelago. The results provide a DNA-based reference library of 12S rRNA, 16S rRNA, COI, Cytb and ND1 mitochondrial sequences for Maltese bat species. Phylogenetic analyses revealed that the Maltese bat populations do not harbour cryptic diversity. Analyses of genetic diversity for Maltese bat species showed contrasting matrilineal diversity between species, Hypsugo savii exhibited the highest haplotype diversity (Hd = 0.802), while Rhinolophus hipposideros showed no haplotype diversity and Plecotus gaisleri exhibited low values for haplotype diversity (Hd = 0.091). Comparative phylogeographical analyses of mtDNA gene datasets from this study with sequences of conspecific bat populations outside of Malta indicate that mitochondrial haplotypes of Pipistrellus pipistrellus and Rhinolophus hipposideros are unique to the Maltese Islands. Hypsugo savii, Pipistrellus kuhlii, Myotis punicus and Plecotus gaisleri shared the most common mitochondrial haplotype with surrounding geographical areas, including the Ibero-Maghreb region, the Apennine Peninsula and Sicily. The observed genetic diversity and phylogenetic relationships are discussed in the context of the species' biology and long-term conservation planning of Maltese bat populations.
... It was officially described only in 2019 ) as a sister species of M. nattereri (García-Mudarra et al. 2009;Salicini et al. 2011). The presence of a differentiated mtDNA lineage in the southern half of the Italian Peninsula, which is still in need of a taxonomical appraisal, indicates that further complexity may be present within this species (Bogdanowicz et al. 2015). ...
... Based on three mtDNA markers (cytochrome b, NADH dehydrogenase subunit 1 [ND1], and control region), Salicini et al. (2013) identified four main clades, two within the Italian Peninsula, the central-northern and southern clades, the latter of which was further divided into three distinct lineages, and two across France and the Iberian Peninsula, one restricted to the Eastern Pyrenees and the second widely distributed from Central and Northern Iberia to France. Bogdanowicz et al. (2015), based on ND1 sequences alone, identified only two main clades, splitting Southern Italy from the rest of Italy and the Iberian Peninsula. Similarly, Çoraman et al. (2019) also identified two main clades across the range of M. crypticus based on ND1 sequences, separating samples from Southern Italy from the rest of the range, including Slovenia. ...
... A very shallow mitochondrial genetic diversity between distant populations (e.g. Belgium, Germany and Greece) was also observed by Bogdanowicz et al. (2015), who analysed another mitochondrial marker (ND1) in a small number of specimens of Geoffroy's bat. This spatial genetic pattern indicates at least one postglacial population expansion, during which some refugial haplotype variants have been maintained, but simultaneously, new haplotypes have also evolved and increased in frequency due to genetic drift and serial founder events during range expansion. ...
... The number of mitochondrial haplotypes, as well as haplotype and nucleotide diversity generally decreased from south to north, which also seems to be the case in other bat species (Ruedi and Castella 2003;Juste et al. 2004;Bogdanowicz et al. 2015). Surprisingly, however, haplotype and nucleotide diversity were highest in the 'Luxembourg' pre-defined group, as a result of a low number of haplotypes with similar frequencies (see Avise 2000). ...
In the European Union, all bat species are strictly protected and member states must ensure their conservation. However, if populations are genetically structured, conservation units that correspond to whole countries may be too large, putting small populations with specific conservation requirements at risk. Geoffroy's bat (Myotis emarginatus) has undergone well-documented declines at its northwestern European range edge between the 1960 and 1990s and is considered to be negatively affected by habitat fragmentation. Here we analysed the species' genetic population structure and diversity to identify subpopula-tions with reduced genetic diversity and to scientifically inform conservation management. We generated 811 microsatellite-based genetic profiles obtained from 42 European nursery colonies and analysed a total of 932 sequences of the hypervariable region II of the mitochondrial control region sampled from across Europe. While two geographically widespread genetic populations were inferred to be present in northwestern Europe, both nuclear and mitochondrial genetic diversity were lowest in the areas that had experienced a decline during the last century. A microsatellite-based analysis of demographic history did not permit, however, to unequivocally link that reduced genetic diversity to the population contraction event. Given the large geographic extent of the genetic populations, preserving the connectivity of mating sites requires concerted conservation efforts across multiple political jurisdictions. Genetic monitoring ought to be done on a regular basis to ensure that large-scale connectivity is maintained and further loss of genetic diversity is prevented.
... The number of bats described has been increasing dramatically since the beginning of the 20th century because of advances in DNA sequencing. Spectacular levels of cryptic diversity have been frequently reported in Europe [7][8][9][10][11][12][13]. ...
... However, some permeability occurs in a very low proportion of the haplotypes from Iberia that clustered within the Moroccan lineages [13]. Instead, Hypsugo individuals from Italian peninsula could have reached the north of Africa using Sicily as stepping-stone, as suggested by ND1 mtDNA data [10] and then the Canary and Cabo Verde islands. As, unfortunately, we could not include Italian specimens in our mtDNA analyses, neither Canarian nor Italian specimens in our nDNA analyses, it was impossible to choose one between the two alternative scenarios. ...
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.
... The Apennine Peninsula is an interesting biogeographical region and a significant source of diversity for numerous European animal and plant species (Bartolini et al., 2014;Dapporto et al., 2014;Bogdanowicz et al., 2015;Piotti et al., 2017;Vitecek et al., 2017). This area in the Mediterranean region is a biodiversity hotspot and is important for understanding the phylogeography of numerous species (Blondel et al., 2000;Hewitt, 2000;Schmitt, 2007). ...
... The Apennines were a Pleistocene refugium for many animal and plant species, thus being an important region for the distribution and population structure of, for example, European insects, mammals and vascular plants. This biogeographical pattern is also imprinted in their genetic architecture, as reflected, for example, by the presence of private haplotypes (Hewitt, 1996(Hewitt, , 2000Petit et al., 2002;Hewitt, 2004;Schmitt, 2007;Ruedi et al., 2008;Grassi et al., 2009;Pilot et al., 2010;Bogdanowicz et al., 2015). ...
The Apennine Mountains in Italy are an important biogeographical region and of particular interest in phylogeographical research, because they have been a refugium during Pleistocene glaciation events for numerous European species. We performed a genetic study on the Eurasian bark beetle Pityogenes chalcographus (Linnaeus, 1760), focusing on two Apennine (Italian) and two Central European (Austrian) locations to assess the influence of the Apennines in the evolutionary history of the beetle, particularly during the Pleistocene. We analysed a part of the mitochondrial COI gene and a set of 5470 informative genome-wide markers to understand its biogeography. We found 75 distinct mitochondrial haplotypes, which are structured in three main clades. In general, the Apennine locations harbour a higher number of mitochondrial clades than Central European sites, with one specific clade exclusively detected in the Apennines. Analysis of our genome-wide, multi-locus dataset reveals a clustering of P. chalcographus by geography, with Italian individuals clearly separated from Austrian samples. Our data highlight the significance of the Apennines for the genetic diversity of P. chalcographus and support the hypothesis that this area was an important refugium during unfavourable conditions in the Pleistocene. We discuss additional life-history traits and processes that shaped the evolution of this widespread beetle.
... For the exclusion of M. ghardalamensis and for the morphological and morphometric features that allow the distinction between M. blythii and M. myotis, see above and Table 4. Additional comparisons were done with M. punicus, recently added to the Sicilian bat fauna (Bogdanowicz et al., 2015;, although it seems to be based on a single female specimen (Bogdanowicz, in litteris). This species was originally described as a subspecies of M. blythii, for the greater width of M2 compared to European M. blythii populations (Felten, in Felten et al., 1977). ...
... In the cold periods of the late Pleistocene, and particularly during the LGM, central-southern Italy and Liguria hosted many species which are now largely distributed in central and northern Europe (including R. hipposideros, M. myotis, P. auritus), and that have returned to these lands only in the Lateglacial or in the Holocene (Bogdanowicz et al., 2015;Ruedi et al., 2008;Salari, 2010;Kotsakis, 2011, 2017). Thus, the occurrence of fossil remains of the greater mouse-eared bat and the brown long-eared bat in the LGM at the Grotta dei Pipistrelli show that Sicily played a role of refuge area in the late Pleistocene for these species currently distributed also in central and northern Europe. ...
Bat remains are useful for palaeoecological reconstructions, they provide independent information on palaeoenvironment and are good indicators for hypogean microclimates. Nine taxa of Chiroptera divided into three families (Rhinolophidae, Vespertilionidae and Miniopteridae) and four genera (Rhinolophus, Myotis, Plecotus and Miniopterus) were discovered in three fossil assemblages from Grotta dei Pipistrelli, in Sicily, a key region for an understanding of Quaternary climates and environments. Bat remains were deposited during three distinct timespans: one Late Pleistocene, MIS 2, around the Last Glacial Maximum, and two Holocene, both referable to the Atlantic chronozone. The presence of yearlings, adult and old individuals suggests hibernating colonies, but the cave was also utilized as a nursery. The diversity of taxa indicates a composite landscape with prevailing vegetation cover and relatively warm climatic conditions. The percentage variations of the frequencies of the recognized taxa suggest a progressive increase of open spaces in the middle Holocene.
Keywords: Chiroptera; Late Pleistocene; Holocene; Central Mediterranean Islands; Taphonomy; Palaeoenvironment -
Les restes de chauves-souris sont utiles pour les reconstructions paléoécologiques, ils fournissent des informations indépendantes sur le paléoenvironnement et ils sont de bons indicateurs pour les microclimats hypogés. Neuf taxons de Chiroptera divisés en trois familles (Rhinolophidae, Vespertilionidae et Miniopteridae) et quatre genres (Rhinolophus, Myotis, Plecotus et Miniopterus) ont été découverts dans trois assemblages fossiles de Grotta dei Pipistrelli, en Sicile, région clé pour la compréhension des climats et des environnements du Quaternaire. Les restes de chauves-souris ont été déposés pendant trois périodes distinctes: une du Pléistocène supérieur, MIS 2, autour du dernier maximum glaciaire, et deux de l’Holocène, tous le deux référant à la chronozone Atlantique. La présence d’individus jeunes, adultes et âgés suggère des colonies en hibernation, mais la grotte a également été utilisée pour la reproduction. La diversité des taxons indique un paysage composite avec une couverture végétale dominante et des conditions climatiques relativement chaudes. Les variations en pourcentage des fréquences des taxons reconnus suggèrent une augmentation progressive des espaces ouverts dans l’Holocène moyen.
Mots clés: Chiroptera; Pléistocène supérieur; Holocène; Iles de la Méditerranée centrale; Taphonomie; Paléoenvironnement
... For the exclusion of M. ghardalamensis and for the morphological and morphometric features that allow the distinction between M. blythii and M. myotis, see above and Table 4. Additional comparisons were done with M. punicus, recently added to the Sicilian bat fauna (Bogdanowicz et al., 2015;, although it seems to be based on a single female specimen (Bogdanowicz, in litteris). This species was originally described as a subspecies of M. blythii, for the greater width of M2 compared to European M. blythii populations (Felten, in Felten et al., 1977). ...
... In the cold periods of the late Pleistocene, and particularly during the LGM, central-southern Italy and Liguria hosted many species which are now largely distributed in central and northern Europe (including R. hipposideros, M. myotis, P. auritus), and that have returned to these lands only in the Lateglacial or in the Holocene (Bogdanowicz et al., 2015;Ruedi et al., 2008;Salari, 2010;Kotsakis, 2011, 2017). Thus, the occurrence of fossil remains of the greater mouse-eared bat and the brown long-eared bat in the LGM at the Grotta dei Pipistrelli show that Sicily played a role of refuge area in the late Pleistocene for these species currently distributed also in central and northern Europe. ...
Bat remains are useful for palaeoecological reconstructions, they provide independent information on palaeoenvironment and are good indicators for hypogean microclimates. Nine taxa of Chiroptera divided into three families (Rhinolophidae, Vespertilionidae and Miniopteridae) and four genera (Rhinolophus, Myotis, Plecotus and Miniopterus) were discovered in three fossil assemblages from the Grotta dei Pipistrelli, in Sicily, a key region for an understanding of Quaternary climates and environments. Bat remains were deposited during three distinct timespans: one late Pleistocene, MIS 2, around the Last Glacial Maximum, and two Holocene, both referable to the Atlantic chronozone. The presence of yearlings, adult and old individuals suggests hibernating colonies, but the cave was also utilized as a nursery. The diversity of taxa indicates a composite landscape with prevailing vegetation cover and relatively warm climatic conditions. The percentage variations of the frequencies of the recognized taxa suggest a progressive increase of open spaces in the middle Holocene.
... 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 [2][3][4][5][6]. The use of DNA barcoding [7] led to a reevaluation of the number of bat species in the tropics [8][9][10]. ...
... Proper species identification is the important basis for any work with wild animals and thus distinguishing a focal species within a local species complex may only be possible using a multi-method approach. (3), sex (4), mass of the bat in g (5), forearm length in mm (6), total area in mm 2 (7), total wing length in mm (8), arm wing area in mm 2 (9), arm wing length in mm (10), hand wing area in mm 2 (11), hand wing length in mm (12), circularity (13), tip area ratio (14), tip length ratio (15), tip shape index (16), aspect ratio (17) (2), type of echolocation call (approach calls or search calls (3), subtype of call, either SI or SII for "search call" (4), start frequency of the pulse in kHz (5), end frequency of the pulse in kHz (6), bandwidth of the pulse in kHz (7), duration of the pulse in ms (8) and pulse interval in ms (9). The tree was created using the HKY+I substitution model and PAUP Ã . ...
A fundamental condition for any work with free-ranging animals is correct species identification. However, in case of bats, information on local species assemblies is frequently limited especially in regions with high biodiversity such as the Neotropics. The bat genus Molossus is a typical example of this, with morphologically similar species often occurring in sympatry. We used a multi-method approach based on molecular, morphometric and acoustic information collected from 962 individuals of Molossus bondae, M. coibensis, and M. molossus captured in Panama. We distinguished M. bondae based on size and pelage coloration. We identified two robust species clusters composed of M. molossus and M. coibensis based on 18 microsatellite markers but also on a more stringently determined set of four markers. Phylogenetic reconstructions using the mitochondrial gene co1 (DNA barcode) were used to diagnose these microsatellite clusters as M. molossus and M. coibensis. To differentiate species, morphological information was only reliable when forearm length and body mass were combined in a linear discriminant function (95.9% correctly identified individuals). When looking in more detail at M. molossus and M. coibensis, only four out of 13 wing parameters were informative for species differentiation, with M. coibensis showing lower values for hand wing area and hand wing length and higher values for wing loading. Acoustic recordings after release required categorization of calls into types, yielding only two informative subsets: approach calls and two-toned search calls. Our data emphasizes the importance of combining morphological traits and independent genetic data to inform the best choice and combination of discriminatory information used in the field. Because parameters can vary geographically, the multi-method approach may need to be adjusted to local species assemblies and populations to be entirely informative.
... European populations of P. gaisleri, restricted to Malta and Pantelleria, are likewise endangered and declining under the pressure of human action, especially wildfires and residential and commercial development (Russo and Cistrone 2023b). Myotis punicus is now assessed as Vulnerable in Europe (Russo and Cistrone 2023c): its situation in the nearby Sicily, where the species was only recently reported (Bogdanowicz et al. 2015), is practically unknown, while in Malta, over half of the population disappeared in the 1980s-1990s and would now be stable at 400-450 bats (Borg 2002; Russo and Cistrone 2023c). Rhinolophus hipposideros on Pantelleria is relatively widespread yet with low densities and highly threatened by the renovation of traditional buildings ('dammusi') where small nursery colonies can be found (Fichera et al. 2022). ...
With their unique ecosystems and evolutionary dynamics, small islands offer fascinating contexts to explore animal diversity. Island bats are key players in maintaining ecological balance. However, their populations are threatened worldwide, necessitating comprehensive research and conservation strategies. Pantelleria, a small Mediterranean island and a biogeographic crossroad between Europe and Africa, offers an excellent model to exemplify the challenges to bat conservation in such geographic contexts. We tested three hypotheses: (1) bats would show weak preference patterns for landscape composition due to the island's heterogeneous landscapes, (2) farmland (especially vineyards) would strongly affect bat activity, and (3) distance from water sources would highly influence bat richness and activity. We surveyed bats acoustically using Audiomoth recorders covering most of the island's surface. We recorded seven bat species, including endangered Plecotus gaisleri, Myotis punicus and Rhinolophus mehelyi. Bats showed weak preferences for specific landscape composition, but the dominant species (Pipistrellus kuhlii) decreased its activity for increasing portions of vineyards within the landscape. Moreover, distance to water critically influenced bat richness and activity. Agricultural expansion, pesticide use and human activities pose significant threats to bats on Pantelleria. We advocate for sustainable farming practices and careful water resource management to safeguard bat habitats and mitigate these threats. Conservation should target vineyards, a key economic resource to produce world‐renowned wine ‘Passito di Pantelleria’ by reducing pesticide use and adopting organic management. Water might be supplemented in critical dry habitats. We urge the preservation of bat diversity to support ecosystem health and resilience on small islands like Pantelleria.
... Research highlights the importance of considering broader scales to account for the effects of roads and other landscape variables (Medinas et al., 2019). Water availability during summer droughts and bats multiple-habitat foraging strategies further validate this buffer size (Amorim et al., 2018;Bogdanowicz et al., 2015). Collectively, these findings validate the selection of the 5000-m buffer, demonstrating that this scale effectively encompasses the key landscape features necessary for assessing bat foraging behaviours. ...
Bats provide important ecosystem services, particularly in agriculture, yet integrating bat management into conservation plans remains challenging. Some landscape features considerably influence bat presence, diversity, and ecosystem service provision. Understanding the relationship between landscape structure, composition, pest suppression, and ecosystem services is crucial. We modelled areas where bats most effectively suppress pine processionary moths (Thaumetopoea pityocampa), considering landscape characteristics to predict ecosystem services and optimise pest suppression in Serra da Estrela, Portugal. Faecal samples collected during fieldwork were analysed for pine processionary moth presence in bat diets. Lasso regression assessed spatial landscape variables to create an "optimal landscape" for predation. Landscape structure and composition influenced pest suppression differently, with the greatest impact within a 5000-m buffer. "Riparian edge" and "tree cover density" were key habitat structure variables supporting bat navigation and access to hunting areas, while "other forest" and "vineyard/orchard" areas were important composition variables. Optimising landscape composition involves incorporating diverse forest within agroforestry systems to enhance pest suppression by creating habitats reflecting bats' foraging preferences. We recommend strategies focusing on riparian edge conservation, selective canopy reduction, and promoting diverse forest compositions. These strategies aim to create mosaic landscapes balancing land uses, fostering optimal conditions for bat foraging. Our study shows edges provide the highest rates of bats-pine processionary moth interactions. However, caution is needed to avoid excessive fragmentation, which may reduce habitat suitability and increase pest presence before effective bat predation. A balanced approach, focusing on edge creation without over-fragmenting the landscape, is key to promoting sustainable pest management.
... However, populations in Western Europe were part of a single biological species. Based on mitochondrial markers and literature survey, Bogdanowicz et al. (2015), studied the genetics linkage of Italian and non-Italian conspecifics species of bats, among them, P. kuhlii. They tested the refugia-withinrefugia scenario which may have generated novel lineages of bats. ...
... As part of taxonomic methodologies, molecular studies have revealed an unexpectedly high diversity of cryptic lineages among bats worldwide, including Europe (Bogdanowicz et al., 2015;Mayer and von Helversen, 2001). Our study highlighted the importance of taxonomic research in identifying new cryptic species, which were previously thought to be the same. ...
Bat conservation is one of the top global concerns for research today; however, conservation efforts may still be limited and impotent due to inadequacy and scarcity of data. Hence, identifying research trends, threatening factors, species status, and geographical priorities is an essential tool for future conservation attempts. Here we conduct a comprehensive systematic review to identify current research priorities, trends, general patterns and gaps regarding Mediterranean bat researches. A total of 97 studies were found in the years spanning between 2000 and 2021. There were 18 studies with sufficient data for qualitative statistical analysis to investigate the impact of habitats and land managements on bat activity and species richness. A yearly average of 4.6 articles were published, with a slight increase post-2010. Out of 61 identified species, 21% of species are threatened. Approximately, 65 % of studies were conducted in the Mediterranean European region, primarily in Spain (29 %), Italy (15.5 %), and Portugal (10.3 %), primarily focusing on forest habitats (38%). We found that Mediterranean bat species received uneven research efforts, with only 15% of research allocated to threatened bats. Around half of the studies focused on the following bat species; Pipistrellus pipistrellus, Pipistrellus kuhlii, Miniopterus schreibersii, Rhinolophus hipposideros, Pipistrellus pygmaeus, Myotis myotis, and Rhinolophus ferrumequinum. Our statistical analysis revealed that riparian areas had higher bat activity than forest and agriculture areas. Bat population responded positively to forest management and organic agriculture practices. To reduce future research misalignment between current local research status and future global conservation priorities, we strongly advocate for urgent and additional collaborative efforts to target under-researched species and areas. Finally, our review will hopefully provide a general overview and an objective synthesis on the current status of bats in the Mediterranean and serve as a baseline for further effective research.
... One of the challenges in current taxonomy is delimiting cryptic species, which, if left unidentified, may cause inaccurate estimates of species richness (over-or underestimating, or misidentifications) [definitions of what constitutes a cryptic species have been broadly discussed in previous studies (Bickford et al., 2007;Struck et al., 2018)]. With the increasing use of molecular approaches in recent decades, increasing numbers of cryptic species are being distinguished (i.e., Kingston et al., 2001;Jones and Barlow, 2004;Stuart et al., 2006;Sedlock and Weyandt, 2009;Salicini et al., 2011;Bogdanowicz et al., 2015;Tu et al., 2017). However, many such studies make little effort to measure phenotypic disparity in a species and thus empirically differentiate inter-and intra-specific variation. ...
Systematics and taxonomy are the backbone of all components of biology and ecology, yet cryptic species present a major challenge for accurate species identification. This is especially problematic as they represent a substantial portion of undiscovered biodiversity, and have implications for not only species conservation, but even assaying potential risk of zoonotic spillover. Here, we use integrative approaches to delineate potential cryptic species in horseshoe bats (Rhinolophidae), evaluate the phenotypic disparities between cryptic species, and identify key traits for their identification. We tested the use of multispecies coalescent models (MSC) using Bayesian Phylogenetic and Phylogeography (BPP) and found that BPP was useful in delineating potential cryptic species, and consistent with acoustic traits. Our results show that around 40% of Asian rhinolophid species are potentially cryptic and have not been formally described. In order to avoid potential misidentification and allow species to be accurately identified, we identified quantitative noseleaf sella and acoustic characters as the most informative traits in delineating between potential cryptic species in Rhinolophidae. This highlights the physical differences between cryptic species that are apparent in noseleaf traits which often only qualitatively described but rarely measured. Each part of the noseleaf including the sella, lateral lappets, and lancet furrows, play roles in focusing acoustic beams and thus, provide useful characteristics to identify cryptic Rhinolophus species. Finally, species delimitation for cryptic species cannot rely on genetic data alone, but such data should be complemented by other evidence, including phenotypic, acoustic data, and geographic distributions to ensure accurate species identification and delineation.
... For this reason, in most countries, permits are needed for bat capture and handling. Capture is necessary to obtain the bat's DNA, normally from skin tissue sampling, and identify confidently cryptic species (e.g., [58,59]. Bat capture and field identification require well-trained personnel, which limits the involvement of volunteers, rangers, and other non-specialised staff. ...
Simple Summary
Bioindicators are organisms that react to the quality or characteristics of the environment and their changes. They are vitally important to track environmental alterations and take action to mitigate them. As choosing the right bioindicators has important policy implications, it is crucial to select them to tackle clear goals rather than selling specific organisms as bioindicators for other reasons, such as for improving their public profile and encourage species conservation. Bats are a species-rich mammal group that provide key services such as pest suppression, pollination of plants of economic importance or seed dispersal. Bats show clear reactions to environmental alterations and as such have been proposed as potentially useful bioindicators. Based on the relatively limited number of studies available, bats are likely excellent indicators in habitats such as rivers, forests, and urban sites. However, more testing across broad geographic areas is needed, and establishing research networks is fundamental to reach this goal. Some limitations to using bats as bioindicators exist, such as difficulties in separating cryptic species and identifying bats in flight from their calls. It is often also problematic to establish the environmental factors that influence the distribution and behaviour of bats.
Abstract
Bats show responses to anthropogenic stressors linked to changes in other ecosystem components such as insects, and as K-selected mammals, exhibit fast population declines. This speciose, widespread mammal group shows an impressive trophic diversity and provides key ecosystem services. For these and other reasons, bats might act as suitable bioindicators in many environmental contexts. However, few studies have explicitly tested this potential, and in some cases, stating that bats are useful bioindicators more closely resembles a slogan to support conservation than a well-grounded piece of scientific evidence. Here, we review the available information and highlight the limitations that arise in using bats as bioindicators. Based on the limited number of studies available, the use of bats as bioindicators is highly promising and warrants further investigation in specific contexts such as river quality, urbanisation, farming practices, forestry, bioaccumulation, and climate change. Whether bats may also serve as surrogate taxa remains a controversial yet highly interesting matter. Some limitations to using bats as bioindicators include taxonomical issues, sampling problems, difficulties in associating responses with specific stressors, and geographically biased or delayed responses. Overall, we urge the scientific community to test bat responses to specific stressors in selected ecosystem types and develop research networks to explore the geographic consistency of such responses. The high cost of sampling equipment (ultrasound detectors) is being greatly reduced by technological advances, and the legal obligation to monitor bat populations already existing in many countries such as those in the EU offers an important opportunity to accomplish two objectives (conservation and bioindication) with one action.
... Although samples from northern Africa were not available in Viglino (2012) and, thus, further investigations are to be made, this hypothesis is likely to be true considering the high levels of predicted suitability displayed by our LGM projections in northern Tunisia and Algeria, which suggests the association of a strong refugium with the region. Such connectivity between Italy and the Ibero-Maghrebian region has been detected for several bat species (Bogdanowicz et al. 2015). The Iberian peninsula is entirely covered by the 'h5' Voronoi polygon, which is present in central and southern Italy too. ...
In this contribution, we aim at determining the role of climate in shaping the current and historical (Last Glacial Maximum and Middle Holocene) distributions of two parapatric bat species (Myotis daubentonii and Myotis capaccinii) in Europe, using ensemble Habitat Suitability Modelling (HSM). Model projection to current climatic conditions predicted distributions largely coherent with the ones observed for the two species in the study area. Temperature- and precipitation-linked variables well accounted for the observed parapatry of the two target species. Moreover, areas of co-occurrence turned out to be those where the main ecological needs concerning the most important range-limiting variables are met for both species. Model projections to past scenarios allowed us to hypothesize the effects of climatic oscillations over the distribution of the two species during the Late Pleistocene and Holocene. Extreme range contractions during the Last Glacial Maximum and the subsequent expansions during Middle Holocene were predicted, consistently with general patterns of post-glacial recolonization routes of many temperate bat species in Europe. Our findings are largely coherent with recent phylogeographic studies investigating the two target species, thus corroborating the validity of potential distribution scenarios obtained from the models and, more importantly, confirming the great influence that glacial cycles had in shaping the biogeography of the European fauna.
... However, populations in Western Europe were part of a single biological species. Based on mitochondrial markers and literature survey, Bogdanowicz et al. (2015), studied the genetics linkage of Italian and non-Italian conspecifics species of bats, among them, P. kuhlii. They tested the refugia-withinrefugia scenario which may have generated novel lineages of bats. ...
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.
... Този резултат за българските екземпляри на M. davidii носещи mystacinus филопатрично поведение характерно само за женските индивиди. При този тип поведение женските индивиди остават верни на мястото където са се родили и не се отдалечават от него(Kunz 1982, Kerth & Petit 2005, Hulva et al. 2010, Bogdanowicz et al. 2015. Филопатричното поведение е бариера за митохондриалния генен поток(Castella et al. 2001, Ruedi & Castella 2003. ...
The Myotis mystacinus morphogroup is characterized by high morphological variability across the Palearctic region and four taxa M. brandtii, M. mystacinus, M. davidii and M. alcathoe are recognized on the Balkan Peninsula. Previous studies revealed several subspecies in M. mystacinus (Kuhl, 1817) (nigricans Fatio, 1869, lugubris Fatio, 1869, occidentalis Benda, 2000, caucasicus Tsytsulina, 2000) and in M. davidii (Peters, 1869) (aurascens Kuzâkin, 1935, bulgaricus Heinrich, 1936, popovi Strelkov, 1983, Myotis sp. A sensu Volleth, 1987, przewalskii senso von Helversen, 1989a, 1989b) based on their distribution and morphology.
This study is based on genetic data obtained in 258 specimens of M. mystacinus and 74 M. davidii. The sequence variation within 450 bp of the mitochondrial nd1 was compared with the variation of three nuclear introns (330 bp of ABHD11, 142 bp of ACOX2, 307 bp of ROGDI). Different methods were used to reveal details of distributions, population structure, demographic history and assess the signs of hybridization between both species. Results demonstrate that M. davidii and M. mystacinus are separate genetic lineages in all sampled regions, except the Balkan Peninsula. All individuals across the Adriatic region and most Bulgarian animals, assigned to M. davidii by the nuclear genetic marker and morphology, carried mitochondria of M. mystacinus. M. davidii individuals from Bulgaria showed reduced level of mitochondrial variation and their haplotypes resembled those of typical M. mystacinus from central Europe. Overall, of 56 analyzed animals from Bulgaria only two carried mitochondrial M. davidii haplotype which indicate almost complete replacement of their mtDNA by the M. mystacinus mtDNA.
Ancient allopatric divergence followed by subsequent secondary contact in the Balkan Peninsula might be the cause for the discrepancy between mitochondrial and nuclear genes. Mitochondrial introgression is hence preceded by hybridization events which raises the question about the effectiveness of the reproductive isolation barriers between both lineages.
... While such a refugium could be the origin of the unknown ancestral population inferred in this study, our evolutionary history models show that a species with tropical affinities was able to survive in Italy during the LGM, from where it expanded across its current European range.The inferred scenario of an Italian refugium and post-glacialEuropean recolonization concurs with the widely accepted phylogeographic paradigms for the western Palearctic(Hewitt, 1999).Among bats, Italy has been identified as a glacial refugium for Myotis myotis(Ruedi et al., 2008) and a possible refugium for Rhinolophus ferrumequinum(Rossiter et al., 2007). In a recent paper,Bogdanowicz et al. (2015) suggested that this pattern might be widespread among bat species. Focusing on Miniopterus schreibersii,Bilgin et al. (2016) suggested a new paradigm of European colonization from Anatolian populations, and although we identified an ancient population in Anatolia/Middle East, our results do not support the hypothesis of a ...
The Mediterranean Basin is a global biodiversity hotspot, hosting a number of native species belonging to families that are found almost exclusively in tropical climates. Yet, whether or not these taxa were able to survive in the Mediterranean region during the Quaternary climatic oscillations remains unknown. Focusing on the European free‐tailed bat (Tadarida teniotis), we aimed to (a) identify potential ancient populations and glacial refugia; (b) determine the post‐glacial colonization routes across the Mediterranean; and (c) evaluate current population structure and demography. Mitochondrial and nuclear markers were used to understand T. teniotis evolutionary and demographic history. We show that T. teniotis is likely restricted to the Western Palearctic, with mitochondrial phylogeny suggesting a split between an Anatolian/Middle East clade and a European clade. Nuclear data pointed to three genetic populations, one of which is an isolated and highly differentiated group in the Canary Islands, another distributed across Iberia, Morocco, and France, and a third stretching from Italy to the east, with admixture following a pattern of isolation by distance. Evolutionary and demographic reconstruction supports a pre‐Last Glacial Maximum (LGM) colonization of Italy and the Anatolian/Middle East, while the remaining populations were colonized from Italy after the Younger Dryas. We also found support for demographic expansion following the Iberian colonization. The results show that during the LGM T. teniotis persisted in Mediterranean refugia and has subsequently expanded to its current circum‐Mediterranean range. Our findings raise questions regarding the physiological and ecological traits that enabled species with tropical affinities to survive in colder climates. European free‐tailed bat populations were able to survive in Italy and Anatolia/Middle East during the LGM and have subsequently colonized the current species range. Phylogenetic reconstruction confirms a split of two main lineages, Anatolian/Middle East clade and a European clade further splitting into two subgroups. One of the groups in the European clade is exclusive to Iberia and Morocco while the other is distributed elsewhere in central and western Mediterranean. Population structure analysis revealed three main genetic populations with meaningful gene flow.
... While such a refugium could be the origin of the unknown ancestral population inferred in this study, our evolutionary history models show that a species with tropical affinities was able to survive in Italy during the LGM, from where it expanded across its current European range.The inferred scenario of an Italian refugium and post-glacialEuropean recolonization concurs with the widely accepted phylogeographic paradigms for the western Palearctic(Hewitt, 1999).Among bats, Italy has been identified as a glacial refugium for Myotis myotis(Ruedi et al., 2008) and a possible refugium for Rhinolophus ferrumequinum(Rossiter et al., 2007). In a recent paper,Bogdanowicz et al. (2015) suggested that this pattern might be widespread among bat species. Focusing on Miniopterus schreibersii,Bilgin et al. (2016) suggested a new paradigm of European colonization from Anatolian populations, and although we identified an ancient population in Anatolia/Middle East, our results do not support the hypothesis of a ...
... Additionally, the complex topography and wide latitudinal range of the Italian territory lead to a high diversity of habitat types and the associated species found therein. With over 30 bat species, Italy represents a diversity hotspot also for bats (Bogdanowicz et al., 2015). The presence of at least four species of long-eared bats (genus Plecotus) is so far confirmed for Italy (Dietz and Kiefer, 2016): P. auritus (Linnaeus, 1758) and P. austriacus (Fischer, 1829) widespread across the country, P. macrobullaris Kuzjakin 1965, restricted to the Alpine region (Alberdi et al., 2013), and P. sardus Mucedda et al. (2002) (Mucedda et al., 2002) endemic to Sardinia. ...
In recent years, many cryptic species of bats have been discovered thanks to the application of molecular techniques. The several long-eared bat species (genus Plecotus) occurring in Europe show a marked morphological similarity and occur in sympatry, so that when confusion may arise, molecular approaches have prime importance to establish the actual specific identity. Italy represents a diversity hotspot for bats in Europe, hosting 35 species among which four Plecotus species. In this study we report on the first confirmed record of the Balkan’s long-eared bat Plecotus kolombatovici for peninsular Italy, review previous unconfirmed records and analyse the species’ potential distribution in the country using a modelling approach. The species’ potential distribution is strongly associated with warm summer temperatures and relatively high winter precipitations, typical of Mediterranean climate. The modelling exercise we did highlights that P. kolombatovici may occur in much of the Italian territory, including the Tyrrhenian coast and on many islands that border it. We therefore argue that P. kolombatovici presence has been so far overlooked due to the morphological resemblance of this species with the grey long-eared bat P. austriacus. Comprehensive surveys are needed to ascertain the actual distribution and establish the conservation status in Italy of this poorly known species to adopt effective legal and practical conservation measures.
... The dashed line delineates the distribution of the species based on Hutson et al. (2008). Geolocated individuals are represented by different combination of shades and shapes according to their mitochondrial lineage (Spitzenberger et al., 2001, Kiefer et al., 2002, Pestano et al., 2003, Juste et al., 2004, Veith et al., 2004, Ibáñez et al., 2006, Spitzenberger et al., 2006, Kiefer, 2007, Galimberti et al., 2012, Kruskop et al., 2012, Çoraman et al., 2013, Bogdanowicz et al., 2015, Andriollo & Ruedi, 2018. The Sardinian lineage does not represent P. sardus, but the local lineage of P. auritus. ...
... In P. auritus, phylogeographic studies based on mitochondrial markers showed the species was highly structured across its entire range (Bogdanowicz et al., 2015;Çoraman et al., 2013;Galimberti et al., 2012;Ibáñez, García-Mudarra, Ruedi, Stadelmann, & Juste, 2006;Juste et al., 2004;Kiefer, Mayer, Kosuch, Von Helversen, & Veith, 2002;Kruskop, Borisenko, Ivanova, Lim, & Eger, 2012;Pestano, Brown, Suarez, Benzal, & Fajardo, 2003;Spitzenberger et al., 2006;Veith, Beer, Kiefer, Johannesen, & Seitz, 2004). In particular, two divergent lineages distributed in Central Europe and mainland Italy ("Western" and "Eastern" lineages in Supporting information Appendix S11) were considered to potentially deserve sub-specific division (Spitzenberger et al., 2006), and a third one (the "Abruzzo lineage" in Supporting information Appendix S11) was even qualified as an "unconfirmed candidate species" (UCS) by Galimberti et al. (2012). ...
Species are the basic units for measuring biodiversity and for comprehending biological interactions. Yet, their delineation is often contentious, especially in groups that are both diverse and phenotypically conservative. Three cryptic species of long‐eared bats, Plecotus auritus, P. austriacus, and P. macrobullaris, co‐occur over extensive areas of Western Europe. The latter is a fairly recent discovery, questioning the overall diversity of the entire Plecotus complex. Yet, high morphological and acoustic similarities compromise the reliable identification of long‐eared bats in the field. We postulate that such extensive phenotypic overlap, along with the recurrent observation of morphologically intermediate individuals, may hide rampant interspecific hybridization. Based on a geographic sampling centered on areas of sympatry in the Alps and Corsica, we assessed the level of reproductive isolation of these three Plecotus species with mitochondrial and nuclear markers, looking at both inter‐ and intraspecific genetic population structuring. No sign of hybridization was detected between these three species that appear well separated biologically. Genetic structuring of populations, however, reflected different species‐specific responses to environmental connectivity, that is, to the presence of orographic or sea barriers. While the Alpine range and the Ligurian Sea coincided with sharp genetic discontinuities in P. macrobullaris and P. austriacus, the more ubiquitous P. auritus showed no significant population structuration. There were clear phylogeographic discrepancies between microsatellite and mitochondrial markers at the intraspecific level, however, which challenges the reliance on simple barcoding approaches for the delineation of sound conservation units.
... In fact, the topology is structured in two wellsupported groups, one made up of samples corresponding to the south of the Balkan Peninsula and Anatolia and another group which includes samples from Central and Western Europe. This grouping could be also identified in a tree shown as supplementary material in a previous study on the species (Bogdanowicz et al. 2015), although the fact was not commented in that study; according to our sequences, the groups show a 1,4% K2P distance between them and point to two possible glacial refugia in the recent evolutionary history of the species, one of them in the Balkans. The new M. alcathoe from Macedonia clusters within the first group together with samples from Greece and Anatolia with which it shares haplotype. ...
Only recently separated from the Myotis mystacinus species complex, the Alcathoe whiskered bat (Myotis alcathoe) is one of the rarest tree-dwelling bats in Europe. In fact, despite the increased number of records across the continent, it is generally still poorly known. Here we present its discovery in Macedonia. A molecularly confirmed Myotis alcathoe was mist netted in the lower part of Štučka River Valley, near the Štuka village in SE Macedonia. The species is new for the bat fauna of Macedonia. This discovery brings the total number of bat species known to occur in the country to 29. In addition, the study reports the third record of the rare Western Barbastelle bat, Barbastella barbastellus (Schreber, 1774) from Macedonia.
... Subsequently, starting from these regions, northern areas were eventually re-colonized during periods of progressive climate warming, and different, subsequent cycles of cold and warmer periods led to multiple contractions and re-expansions of the distribution ranges of many vertebrate taxa (see e.g. Taberlet, et al., 1998;Hewitt, 2004;Joger et al., 2010;Bogdanowicz et al., 2015). These cyclical processes caused complex consequences, which varied in different species, such as intraspecific lineage diversification and speciation, loss of genetic diversity following population bottlenecks, recolonization of newly suitable areas, and the formation of secondary contact zones (see e.g. ...
In this work, we performed a biogeographic analysis with Bayesian binary MCMC (BBM) statistical dispersal-vicariance analysis (S-DIVA) and species distribution models (SDM) on three phylogenetically closely related Mediterranean whipsnakes (Hierophis gemonensis, H. carbonarius, H. viridiflavus), to investigate the pathways of their geographical diversification and locate putative refugial areas in the last glacial maximum (LGM). Our analysis suggests that the diversification processes between the studied species overall followed an east-west route, from eastern Greece to the Iberian Peninsula and continental France, highlighting a significant role of dispersal and vicariance processes at both inter- and intraspecific levels. In particular, the main lineage-splitting events between H. gemonensis, H. carbonarius and H. viridiflavus coincide with two events of vicariance, involving respectively eastern Greece and eastern Italy, and eastern Italy and western Italy, Iberian Peninsula and continental France. SDM analyses highlight the occurrence of multiple putative glacial refugia in the Balkans, Italy and southern France, which represent well the occurrence of distinct “refugia within refugia” in the main Mediterranean peninsulas. Furthermore, our results suggest how these refugia may have played an important role during the Quaternary climatic oscillations in shaping the current haplotype distribution of European whipsnakes.
... In effect, few other bats, including E. nilssonii, Nyctalus noctula and a few species of the genera Myotis and Pipistrellus are reported in the Lateglacial sequences of Central-Northern Europe ( Horáìek, 1995;Ochman, 2003;Horáìek & Jahelková, 2005). Moreover, according to Fladerer (2000), in the southeastern side of the Alps in the LGM the only presence of P. auritus is documented, then during the Lateglacial the area would be populated by Vespertilio Argenti et al., 2008;Salari, 2010;Salari & Kotsakis, 2011;Bogdanowicz et al., 2015), and that have returned to these lands, but even in some regions South of the Alps (e.g., Canton Ticino, Switzerland), only in the Holocene ( Horáìek, 1995Horáìek, , 2007Horáìek & Jahelková, 2005;Blant et al., 2008;Ruedi et al., 2008;Fahlke, 2009;Hutterer et al., 2012). Thus, the occurrence of E. nilssonii in the LGM at Grotta del Fossellone show that Circeo promontory played a role of glacial refugium in the Late Pleistocene for this boreal species currently distributed in Central and Northern Europe. ...
The study of the Late Pleistocene fossil assemblage of bats from the Grotta del Fossellone (Circeo promontory, Central Italy) has revealed the presence of six species, Rhinolophus ferrumequinum, Rhinolophus euryale, Myotis (Myotis) blythii, Myotis (Leuconoë) capaccinii, Eptesicus nilssonii and Miniopterus schreibersii. In the late Mousterian and Aurignacian levels of the cave (MIS 3), only M. blythii is observed, indicating open spaces around the cave. In the Gravettian levels (MIS 2) all the species mentioned are present, which
indicates a mosaic environment with forested areas alternating with open spaces (grassland or steppe) and wetlands. Particularly interesting is the presence of E. nilssonii, the only species of the assemblage currently distributed in Central and Northern Europe. The Italian Peninsula, and particularly its central and southern parts, have evidently acted as a glacial refugium during the Last Glacial Maximum for the boreal species that later, in the Lateglacial and Holocene, expanded its distribution to the northern regions recolonizing the lands liberated from the glacial coverage.
... Although the majority of the studies that support the refugia-within-refugia scenario (Gómez and Lunt 2007) have been undertaken in the Iberian Peninsula, including those on freshwater mussels (e.g. Araujo et al. 2005Araujo et al. , 2009Froufe et al. 2014Froufe et al. , 2016a, recent studies have evidenced patterns of population genetic differentiation that could also be explained by the occurrence of this scenario in Italy (e.g.; Giovannotti et al. 2010;Bogdanowicz et al. 2015;Mezzasalma et al. 2015). In this context, we aim to provide information for the conservation of freshwater mussels in the Italian Peninsula and Croatian Adriatic coast. ...
Freshwater mussels of the order Unionida have been dramatically declining globally. Despite their ecological importance, conservation of these animals has been hindered by unresolved taxonomy and a lack of data on the distribution and status of populations, especially in southern Europe. Although the Italian Peninsula has been noted as a centre of endemism and one of the major refugia of the glacial ages for several taxa, few studies have been performed on the genetic diversity of Unionida. Most importantly, the taxonomic status of several freshwater mussel populations of the Italian Peninsula is still unresolved. Here we present the first comprehensive dataset for the Unionida of the region spanning Italy and the coastal Croatian region (west of the Dinaric Alps). In total, 191 specimens were collected (85 Anodonta, 64 Unio, 17 Microcondylaea bonellii and 25 Sinanodonta woodiana) from 34 sites across the Italian Peninsula and coastal Croatian river basins for molecular identification (COI, 16S and 28S). Genetic analyses were performed to understand major phylogenetic and phylogeographic patterns. Seven species were detected: three Anodonta species (A. anatina, A. cygnea and A. exulcerata), two Unio species (U. mancus and U. elongatulus), Microcondylaea bonellii, and the invasive Sinanodonta woodiana. The presence of three endemic species (A. exulcerata, U. elongatulus and M. bonellii) confirms the importance of the region as a centre of endemism for freshwater mussels. The Apennine Mountains act as an important biogeographic barrier.
... accessed on 30 May 2016). Moreover, the IUCN assessment has so far neglected recently discovered cryptic species (e.g., Mayer and von Helversen, 2001;Bogdanowicz et al., 2015). ...
Bats are a biodiverse mammal order providing key ecosystem services such as pest suppression, pollination, and seed dispersal. Bats are also very sensitive to human actions, and significant declines in many bat populations have been recorded consequently. Many bat species find crucial roosting and foraging opportunities in European forests. Such forests have historically been exploited by humans and are still influenced by harvesting. One of the consequences of this pressure is the loss of key habitat resources, often making forests inhospitable to bats. Despite the legal protection granted to bats across Europe, the impacts of forestry on bats are still often neglected. Because forest exploitation influences forest structure at several spatial scales, economically viable forestry could become more sustainable and even favor bats. We highlight that a positive future for bat conservation that simultaneously benefits forestry is foreseeable, although more applied research is needed to develop sound management. Key future research topics include the detection of factors influencing the carrying capacity of forests, and determining the impacts of forest management and the economic importance of bats in forests. Predictive tools to inform forest managers are much needed, together with greater synergies between forest managers and bat conservationists.
... The Neotropical region is home to the greatest diversity of bats in the world, and it is well known that this fauna awaits a number of basic lines of research, among which cryptic diversity stands as one of the most relevant. Thus, despite recent efforts to address the issue, not only in the Neotropics (Clare, 2011;Clare et al., 2011;Pavan et al., 2011Pavan et al., , 2013Hernández-Dávila et al., 2012;Larsen et al., 2012;Velazco and Patterson, 2013;Parlos et al., 2014) but also in several other regions of the world (Mayer and von Helversen, 2001;Ibáñez et al., 2006;Furman et al., 2010;Raghuram et al., 2014;Bogdanowicz et al., 2015;Dammhahn et al., 2015;Has sanin et al., 2015), cryptic species complexes have become a top priority for a number of international agendas. Pteronotus parnellii is investigated here as a special case in which to study cryptic species among Neotropical bats, considering that due to its wide distribution and low morphological differentiation, the family Mormoopidae is an excellent subject for this kind of analysis. ...
One of the major challenges to understanding the evolution of Neotropical bats concerns our capacity to successfully scrutinize phylogenetic patterns associated with cases of cryptic species complexes. In this study Pteronotus parnellii is examined as a selected example of a known lineage of mormoopid bat that potentially contains several cryptic species. A samples of 452 individuals from 83 different localities, essentially covering its entire mainland distribution, was evaluated using two genetic markers: COI (mitochondrial) and DBY (nuclear) genes. The findings of this study strongly support the hypothesis of high genetic variability and identify at least six lineages within P. parnellii, some of which appear to be cryptic species.
... 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).
... et al.[21], Bray et al.[27], Çoraman et al.[16], Jesus et al.[28], Benda et al.[13], Benda et al.[8], Bogdanowicz et al.[29]). The inset provides the colour legend for each lineage. ...
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 2001 the populations of bush and forest elephants were split in two distinct species, Loxodonta africana (Blumenbach, 1797) and L. cyclotis (Matschie, 1900), using molecular data to support this separation (Roca et al., 2001). It is clear that there is a hidden biodiversity within the mammal record, the extent of which is still under discussion, but surely in some groups like chiroptera, it has a deep impact on the taxonomy (see for example Galimberti et al., 2012b andBogdanowicz et al., 2015). On the whole, the estimation of the unknown biodiversity in mammals is not so trivial, but there is an agreement on the number of about 7000 species (Reeder et al., 2007). ...
DNA barcoding is a universal molecular identification system of living beings for which efficacy and universality have been largely demonstrated in the last decade in many contexts. It is common to link DNA barcoding to phylogenetic reconstruction, and there is indeed an overlap, but identification and phylogenetic positioning/classification are two different processes. In mammals, a better phylogenetic reconstruction, able to dig in fine details the relationships among biological entities, is really welcomed, but do we need DNA barcoding too? In our opinion, the answer is positive, but not only for the identification power, nor for the supposed ability of DNA barcoding to discover new species. We do need DNA barcoding because it is a modern tool, able to create an integrated system, in which it is possible to link the many aspects of the biology of living beings starting from their identification. With 7000 species estimated and a growing interest in knowledge, exploitation and conservation, mammals are one of the best animal groups to achieve this goal. We organised our review to show how an integrative approach to taxonomy, leaded by DNA barcoding, can be effective in the twenty-first century identification and/or description of species.
... A recent review by Agnelli et al. (2008) mentioned 20 species for the region, and a few more were added by further investigations, namely the Bechstein's bat (Myotis bechsteinii Kuhl, 1817) (Di Salvo et al. 2012b), the soprano pipistrelle (Pipistrellus pygmaeus Leach, 1825) (Fichera et al. 2013) and the Maghreb mouse-eared bat (Myotis punicus Felten, 1977) (Bogdanowicz et al. 2015). The occurrence of Hypsugo cfr. ...
First record of brown long-eared bat Plecotus auritus (Chiroptera: Vespertilionidae) for Sicily island (Italy)
Understanding biogeographical patterns is a challenging task, particularly in the case of poorly studied organisms, whose phylogenetic affinities and ecological needs are not yet understood. Such a case is common among invertebrates and particularly among insects, whose extensive diversity may hamper full and deep comprehension of their ecological and evolutionary patterns. Within insects, orthopterans also represent a relatively poorly studied group. Building knowledge upon biogeography and evolution of orthopterans may provide key insights to their conservation, especially in the case of range-restricted taxa that are inherently more vulnerable, and prone to extinction. In this study we thus applied an integrated approach, combining DNA-barcoding and ecological niche modelling, for investigating the diversity of wart biters (orthoptera tettigoniidae, genus Decticus). We particularly aimed at providing a first screening of the molecular identity of species within the genus, and an assessment of their macro-ecological needs. We analysed mitochondrial DNA (cytochrome oxidase I CoI) and bioclimatic niche data for the four Decticus species that occur in the Italian Peninsula (D. verrucivorus, D. albifrons, D. loudoni, and D. aprutianus), reconstructing their phylogenetic relationships based on molecular approaches, and comparing their ecological preferences. We provide CoI sequences for all the species found in Italy, including the first one available for two endemic ones. We found a clear molecular differentiation among the four species, with D. albifrons being the most distinct and basal taxon, as based on the CoI sequence adopted. our results also bring evidence of significant ecological niche differentiation, with each species occupying a distinct portion of the climatic space available within Italy. Notably, the two range-restricted and short-winged species, D. loudoni and D. aprutianus, result as sister taxa according to CoI, and exhibit greater ecological specialisation compared to the more widespread species. Besides, we also highlight significant intra-taxon diversity for both D. verrucivorus sensu stricto and D. albifrons, suggesting that further research on potential intraspecific variability may be needed to clarify the taxonomic position of Italian populations. the observed genetic divergence and ecological niche differentiation found among wart biters suggest that adaptation to different ecological conditions may have played a role in the diversification of these range-restricted species. our results confirmed the importance of the Italian Peninsula as a biodiversity hotspot for orthoptera and provide ANCILLotto ET AL. 548 · Zootaxa 5621 (5) © 2025 Magnolia Press a solid baseline for more in-depth molecular studies, besides providing novel sequences that may be used for e.g., DNA metabarcoding or eDNA campaigns. Further research is in fact needed to explore the specific ecological factors driving niche differentiation in this and other taxa, and to investigate the evolutionary pathways that led to the genus' current diversity and distribution.
Niche partitioning is a crucial mechanism explaining species coexistence and biodiversity; however, the role of individual variation is less understood. As global changes reshuffle species communities, understanding coexistence mechanisms is vital. In this study, we use two co-occurring, morphologically similar bat species, Nathusius’ pipistrelle (Pipistrellus nathusii) and the range-expanding Kuhl’s pipistrelle (P. kuhlii), as models. We examine their niche partitioning across habitats and time, considering individual variations by analysing the spatio-temporal habitat selection of 58 radio-tracked individuals. For resource assessment, we use metabarcoding of guano samples. Our results show that individual variation in both species exceeded species-level differences. Nathusius’ pipistrelle exhibits greater between-individual variation, while the range-expanding Kuhl’s pipistrelle shows stronger within-individual variation, probably facilitating its expansion. This study emphasises the significance of individual variation in investigating animal niche partitioning. It suggests a contribution of within-individual variation in the range expansion of bat species, reshaping animal communities under global change.
Knowledge of species distribution and, for migratory species, seasonal occurrence is particularly important for vulnerable and protected animals such as bats. The former European bat species Pipistrellus pipistrellus was split into two, Pipistrelus pipistrellus s.s. and Pipistrelus pygmaeus , over 20 years ago. However, their distribution, breeding and winter ranges as well as migratory status in Eastern Europe and the Caucasus remained obscure.
In our study, we scrutinised records of both species and assessed the sex ratio during their breeding season in this region.
We show that Pipistrellus pipistrellus s.s. has a significantly smaller range than previously assumed, being restricted to the southern part of the study area. On the contrary, Pipistrelus pygmaeus has a broader distribution, covering the Caucasus and Eastern Europe, up to ca. 59° N. Hence, all historical records and long‐distance movements of Pipistrellus pipistrellus sensu lato from Eastern Europe within the inferred allopatric occurrence of Pipistrelus pygmaeus should be attributed to Pipistrelus pygmaeus .
The high portion of adult males in breeding localities, mass wintering within the breeding range and lacking evidence of long‐distance seasonal movements imply that Pipistrellus pipistrellus s.s. is a sedentary species. In Pipistrelus pygmaeus , the sex ratio among adults during the breeding season varies latitudinally. The female‐biased sex ratio, absence of mass wintering and the historical long‐distance recoveries of ringed individuals suggest that this species is migratory in Eastern Europe. The male‐biased sex ratio during the breeding season, along with late autumn records, suggests that the Caucasus represents its winter range.
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.
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.
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.
Sardinia is home to three bat species of chief conservation importance, the endemic Plecotus sardus
as well as Myotis punicus and Rhinolophus mehelyi, for which the island constitutes the Italian
stronghold. We carried out two gap analyses by overlapping the network of protected areas present
on Sardinia respectively with 1) the occurrence records of all species and 2) the binarized maps
obtained from maximum entropy models. Unlike the other two species, P. sardus known records
are confined to the central sector of the island and its suitable habitat partly overlaps with that of
M. punicus but not with R. mehelyi. Due to its uniqueness and restricted range P. sardus requires
a very specific management strategy for its protection to be successful. Both analyses led to the
conclusion that all species considered require more extensive protection than is currently granted
so that urgent measures should be taken to improve the current situation.
Mountain environments, characterized by high levels of endemism, are at risk of experiencing significant biodiversity loss due to current trends in global warming. While many acknowledge their importance and vulnerability, these ecosystems still remain poorly studied , particularly for taxa that are difficult to sample such as bats. Aiming to estimate the amount of cryptic diversity among bats of a Neotropical montane cloud forest in Talamanca Range—south-east Central America—, we performed a 15-night sampling campaign, which resulted in 90 captured bats belonging to 8 species. We sequenced their mitochon-drial cytochrome c oxidase subunit I (COI) and screened their inter-and intraspecific genetic variation. Phylogenetic relations with conspecifics and closely related species from other geographic regions were established using Maximum Likelihood and Bayesian inference methods, as well as median-joining haplotype networks. Mitochondrial lineages highly divergent from hitherto characterized populations (> 9% COI dissimilarity) were found in Myotis oxyotus and Hylonycteris underwoodi. Sturnira burtonlimi and M. keaysi also showed distinct mitochondrial structure with sibling species and/or populations. These results suggest that mountains in the region hold a high degree of endemicity potential that has previously been ignored in bats. They also warn of the high extinction risk montane bats may be facing due to climatic change, particularly in isolated mountain systems like Tala-manca Range.
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.
During the Pleistocene, the habitat of the noctule bat (Nyctalus noctula) was limited to small refuge areas located in Southern Europe, whereas the species is now widespread across this continent. Using mtDNA (control region and ND1 gene) polymorphisms, we asked whether this recolonization occurred through bottlenecks and whether it was accompanied by population growth. Sequences of the second hypervariable domain of the control region were obtained from 364 noctule bats representing 18 colonies sampled across Europe. This yielded 108 haplotypes that were depicted on a minimum spanning tree that showed a starlike structure with two long branches. Additional sequences obtained from the ND1 gene confirmed that the different parts of the MST correspond to three clades which diverged before the Last Glacial Maximum (18,000 yrC14 BP), leading to the conclusion that the noctule bat survived in several isolated refugia. Partitioning populations into coherent geographical groups divided our samples (φ(CT) = 0.17; P = 0.01) into a group of highly variable nursing colonies from central and eastern Europe and less variable, isolated colonies from western and southern Europe. Demographic analyses suggest that populations of the former group underwent demographic expansions either after the Younger Dryas (11,000-10,000 yrC14 BP), assuming a fast mutation rate for HV II, or during the Pleistocene, assuming a conventional mutation rate. We discuss the fact that the high genetic variability (h = 0.69-0.96; π = 0.006-0.013) observed in nursing colonies that are located some distance from potential Pleistocene refugia is probably due to the combined effect of rapid evolution of the control region in growing populations and a range shift of noctule populations parallel to the recovery of forests in Europe after the last 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.
Sequences of the mitochondrial cytochrome b (1140 bp) and nuclear Rag 2 (1148 bp) genes were used to assess the evolutionary history of the cosmopolitan bat genus Myotis, based on a worldwide sampling of over 88 named species plus 7 species with uncertain nomenclature. Phylogenetic reconstructions of this comprehensive taxon sampling show that most radiation of species occurred independently within each biogeographic region. Our molecular study supports an early divergence of species from the New World, where all Nearctic and Neotropical species plus a lineage from the Palaearctic constitute a monophyletic clade, sister to the remaining Old World taxa. The major Old World clade includes all remaining Eurasian taxa, most Oriental species, one Oceanian, and all Ethiopian species. Another lineage, including M. latirostris from Taiwan, appears at the base of these two major biogeographic clades and, because it bears nyctalodont molars, could be considered as a distinct genus. However, this molar configuration is also found in crown-group species, indicating that these dental characters are variable in the genus Myotis and may confound interpretation of the fossil record. Molecular datings suggest an origin of all recent Myotis in the early Miocene (about 21 MYA with 95% highest posterior density interval 23-20 MYA). This period was characterized by a global climatic cooling that reduced the availability of tropical habitats and favoured the development of more temperate vegetation. This sharp climatic change might have triggered the evolution of Myotis in the Northern continents, because Myotis ancestors seem to have been well adapted and successful in such temperate habitats. Ancestral area reconstructions based on the molecular phylogeny suggest that the eastern portion of the Asian continent was an important centre of origin for the early diversification of all Myotis lineages, and involved relatively few subsequent transcontinental range expansions.
The Vespertilionidae is the largest family of bats, characterized by high occurrence of morphologically convergent groups, which impedes the study of their evolutionary history. The situation is even more complicated in the tropics, where certain regions remain under-sampled.
Two hundred and thirteen vespertilionid bats from Senegal (West Africa) were studied with the use of non-differentially stained karyotypes and multi-locus sequence data analysed with maximum likelihood and Bayesian methods. These bats were identified as 10 different taxa, five of which were distinctive from their nominate species (Pipistrellus hesperidus, Nycticeinops schlieffenii, Scotoecus hirundo, Neoromicia nana and N. somalica), based on both karyotypes and molecular data. These five cryptic taxa are unrelated, suggesting that these West African populations have long been isolated from other African regions. Additionally, we phylogenetically analysed 166 vespertilionid taxa from localities worldwide using GenBank data (some 80% of the genera of the family) and 14 representatives of closely related groups, together with our Senegalese specimens. The systematic position of several taxa differed from previous studies and the tribes Pipistrellini and Vespertilionini were redefined. The African Pipistrellus rueppellii was basal to the Pipistrellus/Nyctalus clade and the Oriental species Glischropus tylopus was basal to the East Asian pipistrelles within the tribe Pipistrellini. The African genus Neoromicia was confirmed to be diphyletic. Based on GenBank data, Eptesicus was polyphyletic, with the Asian E. nasutus and E. dimissus both supported as phylogenetically distinct from the Eptesicus clade. The subfamily Scotophilinae was confirmed as one of the basal branches of Vespertilionidae.
New taxa and new systematic arrangements show that there is still much to resolve in the vespertilionids and that West Africa is a biogeographic hotspot with more diversity to be discovered.
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.
Bat wing morphology is considered in relation to flight performance and flight behaviour to clarify the functional basis for eco-morphological correlations in flying animals. Bivariate correlations are presented between wing dimensions and body mass for a range of bat families and feeding classes, and principal-components analysis is used to measure overall size, wing size and wing shape. The principal components representing wing size and wing shape (as opposed to overall size) are interpreted as being equivalent to wing loading and to aspect ratio. Relative length and area of the hand-wing or wingtip are determined independently of wing size, and are used to derive a wingtip shape index, which measures the degree of roundedness or pointedness of the wingtip. The optimal wing form for bats adapted for different modes of flight is predicted by means of mechanical and aerodynamic models. We identify and model aspects of performance likely to influence flight adaptation significantly; these include selective pressures for economic forward flight (low energy per unit time or per unit distance (equal to cost of transport)), for flight at high or low speeds, for hovering, and for turning. Turning performance is measured by two quantities: manoeuvrability, referring to the minimum space required for a turn at a given speed; and agility, relating to the rate at which a turn can be initiated. High flight speed correlates with high wing loading, good manoeuvrability is favoured by low wing loading, and turning agility should be associated with fast flight and with high wing loading. Other factors influencing wing adaptations, such as migration, flying with a foetus or young or carrying loads in flight (all of which favour large wing area), flight in cluttered environments (short wings) and modes of landing, are identified. The mechanical predictions are cast into a size-independent principal-components form, and are related to the morphology and the observed flight behaviour of different species and families of bats. In this way we provide a broadly based functional interpretation of the selective forces that influence wing morphology in bats. Measured flight speeds in bats permit testing of these predictions. Comparison of open-field free-flight speeds with morphology confirms that speed correlates with mass, wing loading and wingtip proportions as expected; there is no direct relation between speed and aspect ratio. Some adaptive trends in bat wing morphology are clear from this analysis. Insectivores hunt in a range of different ways, which are reflected in their morphology. Bats hawking high-flying insects have small, pointed wings which give good agility, high flight speeds and low cost of transport. Bats hunting for insects among vegetation, and perhaps gleaning, have very short and rounded wingtips, and often relatively short, broad wings, giving good manoeuvrability at low flight speeds. Many insectivorous species forage by `flycatching' (perching while seeking prey) and have somewhat similar morphology to gleaners. Insectivorous species foraging in more open habitats usually have slightly longer wings, and hence lower cost of transport. Piscivores forage over open stretches of water, and have very long wings giving low flight power and cost of transport, and unusually long, rounded tips for control and stability in flight. Carnivores must carry heavy loads, and thus have relatively large wing areas; their foraging strategies consist of perching, hunting and gleaning, and wing structure is similar to that of insectivorous species with similar behaviour. Perching and hovering nectarivores both have a relatively small wing area: this surprising result may result from environmental pressure for a short wingspan or from the advantage of high speed during commuting flights; the large wingtips of these bats are valuable for lift generation in slow flight. The relation between flight morphology (as an indicator of flight behaviour) and echolocation is considered. It is demonstrated that adaptive trends in wing adaptations are predictably and closely paralleled by echolocation call structure, owing to the joint constraints of flying and locating food in different ways. Pressures on flight morphology depend also on size, with most aspects of performance favouring smaller animals. Power rises rapidly as mass increases; in smaller bats the available energy margin is greater than in larger species, and they may have a more generalized repertoire of flight behaviour. Trophic pressures related to feeding strategy and behaviour are also important, and may restrict the size ranges of different feeding classes: insectivores and primary nectarivores must be relatively small, carnivores and frugivores somewhat larger. The relation of these results to bat community ecology is considered, as our predictions may be tested through comparisons between comparable, sympatric species. Our mechanical predictions apply to all bats and to all kinds of bat communities, but other factors (for example echolocation) may also contribute to specialization in feeding or behaviour, and species separation may not be determined solely by wing morphology or flight behaviour. None the less, we believe that our approach, of identifying functional correlates of bat flight behaviour and identifying these with morphological adaptations, clarifies the eco-morphological relationships of bats.
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.
While it is generally accepted that patterns of intra-specific genetic differentiation are substantially affected by glacial history, population genetic processes occurring during Pleistocene glaciations are still poorly understood. In this study, we address the question of the genetic consequences of Pleistocene glaciations for European grey wolves. Combining our data with data from published studies, we analysed phylogenetic relationships and geographic distribution of mitochondrial DNA haplotypes for 947 contemporary European wolves. We also compared the contemporary wolf sequences with published sequences of 24 ancient European wolves.
We found that haplotypes representing two haplogroups, 1 and 2, overlap geographically, but substantially differ in frequency between populations from south-western and eastern Europe. A comparison between haplotypes from Europe and other continents showed that both haplogroups are spread throughout Eurasia, while only haplogroup 1 occurs in contemporary North American wolves. All ancient wolf samples from western Europe that dated from between 44,000 and 1,200 years B.P. belonged to haplogroup 2, suggesting the long-term predominance of this haplogroup in this region. Moreover, a comparison of current and past frequencies and distributions of the two haplogroups in Europe suggested that haplogroup 2 became outnumbered by haplogroup 1 during the last several thousand years.
Parallel haplogroup replacement, with haplogroup 2 being totally replaced by haplogroup 1, has been reported for North American grey wolves. Taking into account the similarity of diets reported for the late Pleistocene wolves from Europe and North America, the correspondence between these haplogroup frequency changes may suggest that they were associated with ecological changes occurring after the Last Glacial Maximum.
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.
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.
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 leas...
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.
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.
The concept of microrefugia is widely accepted to explain the post-glacial colonization of continents, which led to the present-day biotic configuration of the Earth. However, so far, microrefugia are no more than a ‘theoretical necessity’ without an appropriate biogeographical and ecological characterization. Here, a tentative definition and a classification of microrefugia, based on the existing literature, are proposed for discussion. A deeper biogeographical analysis of the concept is suggested using novel ecological models and methods, in order to develop new hypotheses to be tested with palaeoecological and molecular phylogenetic tools.
Genetic divergence in bat communities was assessed on both sides of the Straits of Gibraltar and cryptic diversity was examined. Screening was carried out using partial sequences of the mitochondrial (mt)DNA cytochrome b gene on 399 individual bats belonging to the 18 species found on both sides of the Straits of Gibraltar. For those bats that showed important genetic discontinuities, molecular markers (ND1 and nuclear RAG2 genes) were added to expand the sampling process. Phylogenetic reconstructions were obtained using maximum parsinomy, genetic distances, maximum likelihood, and Bayesian criteria. As an estimate of bats' flight performance, we measured for each species the wing aspect ratio and wing loading indexes, and correlated them with the maximum pairwise genetic distances obtained between southern Iberian and northern Moroccan populations. Genetic mtDNA distances between populations on both continents exceed 5% in seven out of 18 bat species analysed and unknown lineages were uncovered within the species complexes Myotis nattereri and Myotis mystacinus. We did not find a general pattern in the degree of permeability of the Straits of Gibraltar for bats. Genetic distances were not correlated with the ability to cross the Straits. Our study shows that the cryptic diversity uncovered among bats continues to increase as more regions are studied. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96, 434–450.
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 barbastelle (Barbastella barbastellus) is a rare forest bat with a wide distribution in Europe. Here, we combine results from the analysis of two mtDNA fragments with species distribution modelling to determine glacial refugia and postglacial colonization routes. We also investigated whether niche conservatism occurs in this species. Glacial refugia were identified in the three southern European peninsulas: Iberia, Italy and the Balkans. These latter two refugia played a major role in the postglacial colonization process, with their populations expanding to England and central Europe, respectively. Palaeo-distribution models predicted that suitable climatic conditions existed in the inferred refugia during the last glacial maximum (LGM). Nevertheless, the overlap between the current and the LGM distributions was almost inexistent in Italy and in the Balkans, meaning that B. barbastellus populations were forced to shift range between glacial and interglacial periods, a process that probably caused some local extinctions. In contrast, Iberian populations showed a 'refugia within refugium' pattern, with two unconnected areas containing stable populations (populations that subsisted during both glacial and interglacial phases). Moreover, the match between LGM models and the refugial areas determined by molecular analysis supported the hypothesis of niche conservatism in B. barbastellus. We argue that geographic patterns of genetic structuring, altogether with the modelling results, indicate the existence of four management units for conservation: Morocco, Iberia, Italy and UK, and Balkans and central Europe. In addition, all countries sampled possessed unique gene pools, thus stressing the need for the conservation of local populations.
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.
The older history of hybrid zones is explored through consideration of recent advances in climatology, paleontology and phylogeography in the Late Cenozoic, particularly the Quaternary Period with its major climatic cycles. The fossil record shows that these ice ages and their nested millennial oscillations caused substantial changes in species distributions and with genetic evidence allows deduction of refugia and colonization routes in arctic, temperate, desert and tropical regions. The age of divergence between hybridizing lineages varies from the Late Pleistocene to the Late Miocene, implying much range change and varying selection on sister lineages. Hybridizing lineages in the Tropical and Temperate regions range in age from young to old, but those studied in the Arctic are no more than a few ice ages old and their refugial roots are not clear. Mid to low latitude regions often show parapatric patchworks of lineages and multiple refugia stable through many climatic oscillations. Particular hybrid zones may have formed more than once; while some expansions were not the same, producing reticulation and introgression in previous glacial cycles. Hybrid-zone roots are complex and deep, and considerations of their complexity can reveal evolutionary pathways of species. They are indeed windows on evolution.
Resurgent interest in the genetics of population divergence and speciation coincides with recent critical evaluation of species concepts and proposals for species delimitation. An important result of these parallel trends is a slight but important conceptual shift in focus away from species diagnoses based on prior species concepts or definitions, and toward analyses of the processes acting on lineages of metapopulations that eventually lead to differences recognizable as species taxa. An advantage of this approach is that it identifies quantitative metapopulation differences in continuous variables, rather than discrete entities that do or do not conform to a prior species concept, and species taxa are recognized as an emergent property of population-level processes. The tension between species concepts and diagnosis versus emergent recognition of species taxa is at least as old as Darwin, and is unlikely to be resolved soon in favor of either view, because the products of both approaches (discrete utilitarian taxon names for species, process-based understanding of the origins of differentiated metapopulations) continue to have important applications.
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.
Global climate has fluctuated greatly during the past three million years, leading to the recent major ice ages. An inescapable consequence for most living organisms is great changes in their distribution, which are expressed differently in boreal, temperate and tropical zones. Such range changes can be expected to have genetic consequences, and the advent of DNA technology provides most suitable markers to examine these. Several good data sets are now available, which provide tests of expectations, insights into species colonization and unexpected genetic subdivision and mixture of species. The genetic structure of human populations may be viewed in the same context. The present genetic structure of populations, species and communities has been mainly formed by Quaternary ice ages, and genetic, fossil and physical data combined can greatly help our understanding of how organisms were so affected.