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Unraveling the diversification mechanisms of organisms is a fundamental and important macroevolutionary question regarding the diversity, ecological niche, and morphological divergence of life. However, many studies have only explored diversification mechanisms via isolated factors. Here, based on comparative phylogenetic analysis, we performed a macroevolutionary examination of horseshoe bats (Chiroptera: Rhinolophidae: Rhinolophus), to reveal the inter-relationships among diversification, intrinsic/extrinsic factors, and climatic ecological niche characteristics. Results showed a general slowing trajectory during diversification, with two dispersal events from Asia into Southeast Asia and Africa playing key roles in shaping regional heterogeneous diversity. Morphospace expansions of the investigated traits (e.g., body size, echolocation, and climate niche) revealed a decoupled pattern between diversification trajectory and trait divergence, suggesting that other factors (e.g., biotic interactions) potentially played a key role in recent diversification. Based on ancestral traits and pathway analyses, most Rhinolophus lineages belonging to the same region overlapped with each other geographically and were positively associated with the diversification rate, implying a competitive prelude to speciation. Overall, our study showed that multiple approaches need to be integrated to address diversification history. Rather than a single factor, the joint effects of multiple factors (biogeography, environmental drivers, and competition) are responsible for the current diversity patterns in horseshoe bats, and a corresponding multifaceted strategy is recommended to study these patterns in the future.
We examined patterns of genetic variation in Rousettus madagascariensis from Madagascar and R. obliviosus from the Comoros (Grande Comore, Anjouan, and Mohéli). Genetic distances among individuals on the basis of 1,130 base pairs of the mitochondrial cytochrome b (Cytb) locus were estimated from specimens collected from 17 sites on Madagascar, 3 sites on Grande Comore, 3 sites on Anjouan, and 2 sites on Mohéli. We observed little variation in Madagascar and nearshore island samples (maximum 1.1%) and interisland Comoros samples (maximum 1.8%). In contrast, pairwise distances between different sampled sites on Madagascar and the Comoros varied from 8.5% to 13.2%. For 131 Malagasy animals, 69 unique haplotypes were recovered with 86 variable sites, and for 44 Comorian individuals, 17 unique haplotypes were found with 30 variable sites. No haplotype was shared between Madagascar and the Comoros, adding to previous morphological evidence that these 2 populations should be considered separate species. Cytb data showed that Rousettus populations of Madagascar (including nearshore islands) and the Comoros are respectively monophyletic and display no geographic structure in haplotype diversity, and that R. madagascariensis and R. obliviosus are strongly supported as sister to each other relative to other Rousettus species. Genotypic data from 6 microsatellite loci confirm lack of geographic structure in either of the 2 species. In pairwise tests of population differentiation, the only significant values were between samples from the Comoro Islands and Madagascar (including nearshore islands). Estimates of current and historical demographic parameters support population expansion in both the Comoros and Madagascar. These data suggest a more recent and rapid demographic expansion in Madagascar in comparison with greater population stability on the Comoros. On the basis of available evidence, open-water crossings approaching 300 km seem rarely traversed by Rousettus, and, if successful, can result in genetic isolation and subsequent differentiation.
Despite their obvious utility, detailed species-level phylogenies are lacking for many groups, including several major mammalian lineages such as bats. Here we provide a cytochrome b genealogy of over 50% of bat species (648 terminal taxa). Based on prior analyzes of related mammal groups, cytb emerges as a particularly reliable phylogenetic marker, and given that our results are broadly congruent with prior knowledge, the phylogeny should be a useful tool for comparative analyzes. Nevertheless, we stress that a single-gene analysis of such a large and old group cannot be interpreted as more than a crude estimate of the bat species tree. Analysis of the full dataset supports the traditional division of bats into macro- and microchiroptera, but not the recently proposed division into Yinpterochiroptera and Yangochiroptera. However, our results only weakly reject the former and strongly support the latter group, and furthermore, a time calibrated analysis of a pruned dataset where most included taxa have the entire 1140bp cytb sequence finds monophyletic Yinpterochiroptera. Most bat families and many higher level groups are supported, however, relationships among families are in general weakly supported, as are many of the deeper nodes of the tree. The exceptions are in most cases apparently due to the misplacement of species with little available data, while in a few cases the results suggest putative problems with current classification, such as the non-monophyly of Mormoopidae. We provide this phylogenetic hypothesis, and an analysis of divergence times, as tools for evolutionary and ecological studies that will be useful until more inclusive studies using multiple loci become available.
The Stripe-headed Round-eared bat, Tonatia saurophila, includes three subspecies: Tonatia saurophila saurophila (known only from subfossil records in Jamaica), Tonatia saurophila bakeri (distributed from southeastern Mexico to northern Colombia, Venezuela west and north of the Cordillera de Mérida, and northwestern Ecuador), and Tonatia saurophila maresi (distributed in Venezuela east and south of the Cordillera de Mérida, the Guianas, Trinidad and Tobago, northeastern Brazil, and along the upper Amazon basin in Colombia, Ecuador, Peru, and Bolivia). The last two subspecies are an attractive example to test predictions about the historical role of the Andes in mammalian diversification. Based on morphological descriptions, morphometric analyses, and phylogenetic reconstruction using the mitochondrial gene Cyt-b and the nuclear exon RAG2, this study evaluates the intraspecific relationships within Tonatia saurophila and the taxonomic status of the taxon. The three subspecies of T. saurophila are recognizable as full species: Tonatia bakeri, Tonatia maresi, and Tonatia saurophila. The latter is restricted to its type locality and possibly is extinct. Tonatia bakeri, in addition to being larger than T. maresi, is morphologically distinguishable by possessing an acute apex at the posterior edge of the skull, a well-developed clinoid process, and relatively robust mandibular condyles, and by lacking a diastema between the canine and the first lower premolar. The genetic distance between T. bakeri and T. maresi is 7.65%.
Morphological variation between individuals can increase niche segregation and decrease intraspecific competition when heterogeneous individuals explore their environment in different ways. Among bat species, wing shape correlates with flight maneuverability and habitat use, with species that possess broader wings typically foraging in more cluttered habitats. However, few studies have investigated the role of morphological variation in bats for niche partitioning at the individual level. To determine the relationship between wing shape and diet, we studied a population of the insectivorous bat species Pteronotus mesoamericanus in the dry forest of Costa Rica. Individual diet was resolved using DNA metabarcoding, and bat wing shape was assessed using geometric morphometric analysis. Inter-individual variation in wing shape showed a significant relationship with both dietary dissimilarity based on Bray-Curtis estimates, and nestedness derived from an ecological network. Individual bats with broader and more rounded wings were found to feed on a greater diversity of arthropods (less nested) in comparison to individuals with triangular and pointed wings (more nested). We conclude that individual variation in bat wing morphology can impact foraging efficiency leading to the observed overall patterns of diet specialization and differentiation within the population.
Bats of the family Phyllostomidae show a unique diversity in feeding specializations. This taxon includes species that are highly specialized on insects, blood, small vertebrates, fruits or nectar, and pollen. Feeding specialization is accompanied by morphological, physiological and behavioural adaptations. Several attempts were made to resolve the phylogenetic relationships within this family in order to reconstruct the evolutionary transitions accompanied by nutritional specialization. Nevertheless, the evolution of nectarivory remained equivocal.
The revision of the sub-order Microchiroptera is one of the most intriguing outcomes in recent mammalian molecular phylogeny. The unexpected sister-taxon relationship between rhinolophoid microbats and megabats, with the exclusion of other microbats, suggests that megabats arose in a relatively short period of time from a microbat-like ancestor. In order to understand the genetic mechanism underlying adaptive evolution in megabats, we determined the whole-genome sequences of two rousette megabats, Leschenault's rousette (Rousettus leschenaultia) and the Egyptian fruit bat (R. aegyptiacus). The sequences were compared with those of 22 other mammals, including nine bats, available in the database. We identified that megabat genomes are distinct in that they have extremely low activity of SINE retrotranspositions, expansion of two chemosensory gene families, including the trace amine receptor (TAAR) and olfactory receptor (OR), and elevation of the dN/dS ratio in genes for immunity and protein catabolism. The adaptive signatures discovered in the genomes of megabats may provide crucial insight into their distinct evolution, including key processes such as virus resistance, loss of echolocation, and frugivorous feeding.
Previous studies on bats from this laboratory have revealed the presence of exceptionally high circulating levels of glucocorticoids in two species of the sub-order Megachiroptera. In the present study, the following questions were asked: (1) what effect does the routine handling and examination of captive bats have on the activity of their hypothalamic-pituitary-adrenocortical (HPA) axis?; (2) are the unusually high plasma levels of cortisol and corticosterone found in Pteropus hypomelanus associated with high levels of circulating adrenocorticotropic hormone (ACTH)?; (3) are there diurnal changes in stress responsivity in this species?; and (4) how do levels of glucocorticoids in P. hypomelanus compare with those found in other species of Chiroptera (both micro and megachiropteran species)? Of five species examined, P. hypomelanus had slightly higher total glucocorticoid levels than P. pumulis, but approximately 8-fold higher levels than in three species of Microchiroptera (Artibeus jamaicensis, Carollia perspicillata, and Myotis lucifigus). There was a pronounced diurnal rhythm in glucocorticoid levels in one species (M. lucifigus) for which this was determined. A 1-h period of restraint stress increased glucose and glucocorticoid levels in P. pumulis, and also increased ACTH and glucocorticoids in P. hypomelanus. Fifteen minutes of routine handling (weighting, measuring, etc.) elicited a significant rise in plasma glucocorticoids in P. hypomelanus to combined peak (cortisol plus corticosterone) levels of over 1,000 ng/ml (100 micrograms%). There was no significant difference in the response to handling in bats tested in the morning or evening. Basal ACTH levels as detected by radioimmunoassay were low in P. hypomelanus, in spite of high steroid levels.(ABSTRACT TRUNCATED AT 250 WORDS)
Dermanura Gervais, 1856 is represented by small frugivorous bats of the Stenodermatinae subfamily. The taxonomy of this group presents controversies and has been subject to changes, especially since the morphological characters evaluated have left gaps that are difficult to fill regarding good species characterization. Previous studies performed in Dermanura cinerea Gervais, 1856 found that the karyotype of this species has a diploid number of chromosomes equal to 30 and 56 autosomal arms. The objective of the present study was to describe, for the first time, the karyotypes of the species Dermanura anderseni (Osgood, 1916) and Dermanura gnoma (Handley, 1987) based on classical cytogenetic markers. For both species, the diploid number found was 2n = 30 and NFa = 56. Two pairs of chromosomes showed markings of the nucleolus organizing regions (AgNORs) in the species D. anderseni and only one pair in D. gnoma, differing from what has already been described for D. cinerea. The two species analyzed here also showed differences in the sex chromosome system, with D. gnoma showing a neo-XY type system while in D. anderseni the classic XY sexual system was observed. In both species, visualization of the constitutive heterochromatin occurred in the pericentromeric region of all chromosomes, as well as in the short arms of the subtelocentric chromosomes. The present work represents an important expansion of karyotypic information for the subfamily Stenodermatinae, bringing chromosomal features that are possible to use in the taxonomic implications of the group.
Since the last systematic review of Chiroderma (big-eyed bats) more than two decades ago, we report on biodiversity surveys that expand the distribution and species diversity of this Neotropical genus. The Caribbean endemic species Chiroderma improvisum is documented for the first time from Nevis in the northern Lesser Antilles. A broader geographic sampling for a molecular analysis identifies a paraphyletic relationship in Chiroderma trinitatum with respect to Chiroderma doriae. Cis-Andean populations of C. trinitatum are most closely related to the morphologically distinctive and allopatrically distributed C. doriae in the Cerrado and Atlantic Forest of Brazil and Paraguay. The sister taxon to this grouping includes trans-Andean populations of C. trinitatum, which we recommend to elevate to species status as C. gorgasi. This is an example of a cryptic species because C. gorgasi was previously considered morphologically similar to C. trinitatum, but more detailed examination revealed that it lacks a posterolabial accessory cusp on the lower second premolar and has a narrower breadth of the braincase. We provide an amended description of Chiroderma gorgasi.
Insectivorous bats provide important ecosystem services, especially by suppressing and controlling the insects' biomass. To empirically quantify the number of insects consumed by European vespertilionid bats per night, we estimated their ratio of dry mass of feces to mass of consumed insects. This study combines the results of feeding in captivity and the data obtained in field surveys; dry mass of feces was measured in both cases. In captivity, we analyzed the effect of species, age and sex of bats, species of insects consumed and the mass of food portion on the dry mass of feces. Using coefficients of the regression model, we estimated the number of insects consumed by free-ranging bats based on dry mass of their feces. According to our estimates, on average, one individual of one of the largest European bat species, Nyctalusnoctula, consumes 2.2 g (ranging from 0.5 to 8.2 g) of insects per one feeding night, while the smallest European bats of genus Pipistrellus consume 0.4 g (ranging from 0.1 to 1.3 g), further confirming the importance of insectivorous bats for ecosystem services. This publication offers the novel method for the estimation of insects' biomass consumed by bats.
The family Pteropodidae comprises bats commonly known as megabats or Old World fruit bats. Molecular phylogenetic studies of pteropodids have provided considerable insight into intrafamilial relationships, but these studies have included only a fraction of the extant diversity (a maximum of 26 out of the 46 currently recognized genera) and have failed to resolve deep relationships among internal clades. Here we readdress the systematics of pteropodids by applying a strategy to try to resolve ancient relationships within Pteropodidae, while providing further insight into subgroup membership, by 1) increasing the taxonomic sample to 42 genera; 2) increasing the number of characters (to >8,000 bp) and nuclear genomic representation; 3) minimizing missing data; 4) controlling for sequence bias; and 5) using appropriate data partitioning and models of sequence evolution.
Temperature regulation is an indispensable physiological activity critical for animal survival. However, relatively little is known about the origin of thermoregulatory regimes in a phylogenetic context, or the genetic mechanisms driving the evolution of these regimes. Using bats as a study system, we examined the evolution of three thermoregulatory regimes (hibernation, daily heterothermy, and homeothermy) in relation to the evolution of leptin, a protein implicated in regulation of torpor bouts in mammals, including bats. A threshold model was used to test for a correlation between lineages with positively selected lep, the gene encoding leptin, and the thermoregulatory regimes of those lineages. Although evidence for episodic positive selection of lep was found, positive selection was not correlated with lineages of heterothermic bats, a finding that contradicts results from previous studies. Evidence from our ancestral state reconstructions suggests that the most recent common ancestor of bats used daily heterothermy and that the presence of hibernation is highly unlikely at this node. Hibernation likely evolved independently at least four times in bats-once in the common ancestor of Vespertilionidae and Molossidae, once in the clade containing Rhinolophidae and Rhinopomatidae, and again independently in the lineages leading to Taphozous melanopogon and Mystacina tuberculata. Our reconstructions revealed that thermoregulatory regimes never transitioned directly from hibernation to homeothermy, or the reverse, in the evolutionary history of bats. This, in addition to recent evidence that heterothermy is best described along a continuum, suggests that thermoregulatory regimes in mammals are best represented as an ordered continuous trait (homeothermy ← → daily torpor ← → hibernation) rather than as the three discrete regimes that evolve in an unordered fashion. These results have important implications for methodological approaches in future physiological and evolutionary research.
The family Phyllostomidae (Chiroptera) shows wide morphological, molecular and cytogenetic variation; many disagreements regarding its phylogeny and taxonomy remains to be resolved. In this study, we use chromosome painting with whole chromosome probes from the Phyllostomidae Phyllostomus hastatus and Carollia brevicauda to determine the rearrangements among several genera of the Nullicauda group (subfamilies Gliphonycterinae, Carolliinae, Rhinophyllinae and Stenodermatinae).
Rhodopsin, encoded by the gene Rhodopsin (RH1), is extremely sensitive to light, and is responsible for dim-light vision. Bats are nocturnal mammals that inhabit poor light environments. Megabats (Old-World fruit bats) generally have well-developed eyes, while microbats (insectivorous bats) have developed echolocation and in general their eyes were degraded, however, dramatic differences in the eyes, and their reliance on vision, exist in this group. In this study, we examined the rod opsin gene (RH1), and compared its evolution to that of two cone opsin genes (SWS1 and M/LWS). While phylogenetic reconstruction with the cone opsin genes SWS1 and M/LWS generated a species tree in accord with expectations, the RH1 gene tree united Pteropodidae (Old-World fruit bats) and Yangochiroptera, with very high bootstrap values, suggesting the possibility of convergent evolution. The hypothesis of convergent evolution was further supported when nonsynonymous sites or amino acid sequences were used to construct phylogenies. Reconstructed RH1 sequences at internal nodes of the bat species phylogeny showed that: (1) Old-World fruit bats share an amino acid change (S270G) with the tomb bat; (2) Miniopterus share two amino acid changes (V104I, M183L) with Rhinolophoidea; (3) the amino acid replacement I123V occurred independently on four branches, and the replacements L99M, L266V and I286V occurred each on two branches. The multiple parallel amino acid replacements that occurred in the evolution of bat RH1 suggest the possibility of multiple convergences of their ecological specialization (i.e., various photic environments) during adaptation for the nocturnal lifestyle, and suggest that further attention is needed on the study of the ecology and behavior of bats.
The Old World leaf-nosed bats (Hipposideridae) are aerial and gleaning insectivores that occur throughout the Paleotropics. Both their taxonomic and phylogenetic histories are confused. Until recently, the family included genera now allocated to the Rhinonycteridae and was recognized as a subfamily of Rhinolophidae. Evidence that Hipposideridae diverged from both Rhinolophidae and Rhinonycteridae in the Eocene confirmed their family rank, but their intrafamilial relationships remain poorly resolved. We examined genetic variation in the Afrotropical hipposiderids Doryrhina, Hipposideros, and Macronycteris using relatively dense taxon-sampling throughout East Africa and neighboring regions. Variation in both mitochondrial (cyt-b) and four nuclear intron sequences (ACOX2, COPS, ROGDI, STAT5) were analyzed using both maximum likelihood and Bayesian inference methods. We used intron sequences and the lineage delimitation method BPP-a multilocus, multi-species coalescent approach-on supported mitochondrial clades to identify those acting as independent evolutionary lineages. The program StarBEAST was used on the intron sequences to produce a species tree of the sampled Afrotropical hipposiderids. All genetic analyses strongly support generic monophyly, with Doryrhina and Macronycteris as Afrotropical sister genera distinct from a Paleotropical Hipposideros; mitochondrial analyses interpose the genera Aselliscus, Coelops, and Asellia between these clades. Mitochondrial analyses also suggest at least two separate colonizations of Africa by Asian groups of Hipposideros, but the actual number and direction of faunal interchanges will hinge on placement of the unsampled African-Arabian species H. megalotis. Mitochondrial sequences further identify a large number of geographically structured clades within species of all three genera. However, in sharp contrast to this pattern, the four nuclear introns fail to distinguish many of these groups and their geographic structuring disappears. Various distinctive mitochondrial clades are consolidated in the intron-based gene trees and delimitation analyses, calling into question their evolutionary independence or else indicating their very recent divergence. At the same time, there is now compelling genetic evidence in both mitochondrial and nuclear sequences for several additional unnamed species among the Afrotropical Hipposideros. Conflicting appraisals of differentiation among the Afrotropical hipposiderids based on mitochondrial and nuclear loci must be adjudicated by large-scale integrative analyses of echolocation calls, quantitative morphology, and geometric morphometrics. Integrative analyses will also help to resolve the challenging taxonomic issues posed by the diversification of the many lineages associated with H. caffer and H. ruber.
Two or more species are cryptic, if they are morphologically similar, biologically distinct, and misclassified as a single species. Cryptic species complexes were recently discovered within many bat species and we suspect that the bent-wing bat, Miniopterus schreibersii, found in Europe, northern Africa, and Asia Minor, could also form such a complex. Populations of M. schreibersii decline in most of the European countries and the species is currently listed as Near Threatened in the IUCN Red List. Finding that M. schreibersii is not a single species, but a species complex, would have a considerable impact on its conservation strategies, as the abundance of each component taxon would be much smaller than the one estimated for the nominal species.
A trade-off between the sensory modalities of vision and hearing is likely to have occurred in echolocating bats as the sophisticated mechanism of laryngeal echolocation requires considerable neural processing and has reduced the reliance of echolocating bats on vision for perceiving the environment. If such a trade-off exists, it is reasonable to hypothesize that some genes involved in visual function may have undergone relaxed selection or even functional loss in echolocating bats. The Gap junction protein, alpha 10 (Gja10, encoded by Gja10 gene) is expressed abundantly in mammal retinal horizontal cells and plays an important role in horizontal cell coupling. The interphotoreceptor retinoid-binding protein (Irbp, encoded by the Rbp3 gene) is mainly expressed in interphotoreceptor matrix and is known to be critical for normal functioning of the visual cycle. We sequenced Gja10 and Rbp3 genes in a taxonomically wide range of bats with divergent auditory characteristics (35 and 18 species for Gja10 and Rbp3, respectively). Both genes have became pseudogenes in species from the families Hipposideridae and Rhinolophidae that emit constant frequency echolocation calls with Doppler shift compensation at high-duty-cycles (the most sophisticated form of biosonar known), and in some bat species that emit echolocation calls at low-duty-cycles. Our study thus provides further evidence for the hypothesis that a trade-off occurs at the genetic level between vision and echolocation in bats.
Phenotypes of distantly related species may converge through adaptation to similar habitats and/or because they share biological constraints that limit the phenotypic variants produced. A common theme in bats is the sympatric occurrence of cryptic species that are convergent in morphology but divergent in echolocation frequency, suggesting that echolocation may facilitate niche partitioning, reducing competition. If so, allopatric populations freed from competition, could converge in both morphology and echolocation provided they occupy similar niches or share biological constraints. We investigated the evolutionary history of a widely distributed African horseshoe bat, Rhinolophus darlingi, in the context of phenotypic convergence. We used phylogenetic inference to identify and date lineage divergence together with phenotypic comparisons and ecological niche modelling to identify morphological and geographical correlates of those lineages. Our results indicate that R. darlingi is paraphyletic, the eastern and western parts of its distribution forming two distinct non-sister lineages that diverged ~9.7 Mya. We retain R. darlingi for the eastern lineage and argue that the western lineage, currently the sub-species R. d. damarensis, should be elevated to full species status. R. damarensis comprises two lineages that diverged ~5 Mya. Our findings concur with patterns of divergence of other co-distributed taxa which are associated with increased regional aridification between 7-5 Mya suggesting possible vicariant evolution. The morphology and echolocation calls of R. darlingi and R. damarensis are convergent despite occupying different biomes. This suggests that adaptation to similar habitats is not responsible for the convergence. Furthermore, R. darlingi forms part of a clade comprising species that are bigger and echolocate at lower frequencies than R. darlingi, suggesting that biological constraints are unlikely to have influenced the convergence. Instead, the striking similarity in morphology and sensory biology are probably the result of neutral evolutionary processes, resulting in the independent evolution of similar phenotypes.
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