Speciation dynamics during the global radiation of extant bats

Species richness varies widely across extant clades, but the causes of this variation remain poorly understood. We investigate the role of diversification rate heterogeneity in shaping patterns of diversity across families of extant bats. To provide a robust framework for macroevolutionary inference, we assemble a time‐calibrated, species‐level phylogeny using a supermatrix of mitochondrial and nuclear sequence data. We analyze the phylogeny using a Bayesian method for modeling complex evolutionary dynamics. Surprisingly, we find that variation in family richness can largely be explained without invoking heterogeneous diversification dynamics. We document only a single well‐supported shift in diversification dynamics across bats, occurring at the base of the subfamily Stenodermatinae. Bat diversity is phylogenetically imbalanced, but—contrary to previous hypotheses—this pattern is unexplained by any simple patterns of diversification rate heterogeneity. This discordance may indicate that diversification dynamics are more complex than can be captured using the statistical tools available for modeling data at this scale. We infer that bats as a whole are almost entirely united into one macroevolutionary cohort, with decelerating speciation through time. There is also a significant relationship between clade age and richness, suggesting that global bat diversity may still be expanding.     

翼手目(蝙蝠)适应性进化分子机制的研究进展

作为哺乳动物第二大目的翼手目(Chiroptera;俗称蝙蝠)在飞行能力、回声定位与听觉系统、食性、冬眠、免疫防御等诸多方面表现出显著而独特的适应性进化,是研究生物对环境适应性进化分子机制的热点模型之一。文章综述了翼手目适应性进化分子机制的研究进展,特别是近年来在基因组水平上开展的相关研究,显示出更为复杂的分子进化模式和功能分化。随着越来越多的翼手目物种基因组数据的产生,将有望揭示新的进化机制,并为后续的功能实验奠定基础,促进人们对翼手目这一类群的认识和了解,同时也为系统认识动物适应性进化分子机制做出贡献。     

Bat Species Comparisons Based on External Morphology: A Test of Traditional versus Geometric Morphometric Approaches

External morphology is commonly used to identify bats as well as to investigate flight and foraging behavior, typically relying on simple length and area measures or ratios. However, geometric morphometrics is increasingly used in the biological sciences to analyse variation in shape and discriminate among species and populations. Here we compare the ability of traditional versus geometric morphometric methods in discriminating between closely related bat species – in this case European horseshoe bats (Rhinolophidae, Chiroptera) – based on morphology of the wing, body and tail. In addition to comparing morphometric methods, we used geometric morphometrics to detect interspecies differences as shape changes. Geometric morphometrics yielded improved species discrimination relative to traditional methods. The predicted shape for the variation along the between group principal components revealed that the largest differences between species lay in the extent to which the wing reaches in the direction of the head. This strong trend in interspecific shape variation is associated with size, which we interpret as an evolutionary allometry pattern.     

Intraspecific adaptive radiation: Competition,ecological opportunity,and phenotypic diversification within species

Intraspecific variation in resource‐use traits can have profound ecological and evolutionary implications. Among the most striking examples are resource polymorphisms, where alternative morphs that utilize different resources evolve within a population. An underappreciated aspect of their evolution is that the same conditions that favor resource polymorphism—competition and ecological opportunity—might foster additional rounds of diversification within already existing morphs. We examined these issues in spadefoot toad tadpoles that develop into either a generalist "omnivore" or a specialist "carnivore" morph. Specifically, we assessed the morphological diversity of tadpoles from natural ponds and experimentally induced carnivores reared on alternative diets. We also surveyed natural ponds to determine if the strength of intramorph competition and the diversity and abundance of dietary resources (measures of ecological opportunity) influenced the diversity of within‐morph variation. We found that five omnivore and four carnivore types were present in natural ponds; alternative diets led to shape differences, some of which mirrored variation in the wild; and both competition and ecological opportunity were associated with enhanced morphological diversity in natural ponds. Such fine‐scale intraspecific variation might represent an underappreciated form of biodiversity and might constitute a crucible of evolutionary innovation and diversification.     

Differences in Growth Generate the Diverse Palate Shapes of New World Leaf-Nosed Bats (Order Chiroptera,Family Phyllostomidae)

New World leaf-nosed bats (Family Phyllostomidae) display incredible craniofacial diversity that is associated with their broad range of dietary preferences. The short and broad palates of highly frugivorous bats are functionally linked to high bite forces, and the long and narrow palates of nectarivorous bats to flower feeding. Although the functional correlates and evolutionary history of shape variation in phyllostomid palates are beginning to be understood, the specific developmental processes that govern palate diversification remain unknown. To begin to resolve this issue, this study quantified palate morphology in seven phyllostomid species from a range of developmental stages and in adults. This sample includes species with short and broad, long and narrow, and intermediate palate shapes, and thereby covers the range of palate shapes displayed by phyllostomids. Results indicate that while initial palate shape (i.e., width vs. length) varies among species, the pattern of this variation does not match that observed in adults. In contrast, the relative growth of palate width and length in developing phyllostomids and the ratio of these axes in adults are significantly correlated. These and other results suggest that evolutionary alterations in patterns of palate growth have governed the diversification of palate shapes in adult phyllostomids. This implies that the diverse palate shapes of phyllostomids are the result of relatively subtle evolutionary changes in later rather than earlier development events.     

Sperm size evolution in African greenbuls (Passeriformes: Pycnonotidae)

Sperm morphology is highly diversified across the animal kingdom and recent comparative evidence from passerine birds suggests that postcopulatory sexual selection is a significant driver of sperm evolution. In the present study, we describe sperm size variation among 20 species of African greenbuls and one bulbul (Passeriformes: Pycnonotidae) and analyze the evolutionary differentiation of sperm size within a phylogenetic framework. We found significant interspecific variation in sperm size; with some genera exhibiting relatively long sperm (e.g. Eurillas) and others exhibiting short sperm head lengths (e.g. Phyllastrephus). However, our results suggest that contemporary levels of sperm competition are unlikely to explain sperm diversification within this clade: the coefficients of inter‐male variation (CV_bm) in sperm length were generally high, suggesting relatively low and homogeneous rates of extra‐pair paternity. Finally, in a comparison of six evolutionary or tree transformation models, we found support for both the Kappa (evolutionary change primarily at nodes) and Lambda (lineage‐specific evolutionary rates along branches) models in the evolutionary trajectories of sperm size among species. We therefore conclude that African greenbuls have more variable rates of sperm size evolution than expected from a neutral model of genetic drift. Understanding the evolutionary dynamics of sperm diversification remains a future challenge.     

Ecological and evolutionary drivers of haemoplasma infection and bacterial genotype sharing in a Neotropical bat community

Most emerging pathogens can infect multiple species, underlining the importance of understanding the ecological and evolutionary factors that allow some hosts to harbour greater infection prevalence and share pathogens with other species. However, our understanding of pathogen jumps is based primarily around viruses, despite bacteria accounting for the greatest proportion of zoonoses. Because bacterial pathogens in bats (order Chiroptera) can have conservation and human health consequences, studies that examine the ecological and evolutionary drivers of bacterial prevalence and barriers to pathogen sharing are crucially needed. Here were studied haemotropic Mycoplasma spp. (i.e., haemoplasmas) across a species‐rich bat community in Belize over two years. Across 469 bats spanning 33 species, half of individuals and two‐thirds of species were haemoplasma positive. Infection prevalence was higher for males and for species with larger body mass and colony sizes. Haemoplasmas displayed high genetic diversity (21 novel genotypes) and strong host specificity. Evolutionary patterns supported codivergence of bats and bacterial genotypes alongside phylogenetically constrained host shifts. Bat species centrality to the network of shared haemoplasma genotypes was phylogenetically clustered and unrelated to prevalence, further suggesting rare—but detectable—bacterial sharing between species. Our study highlights the importance of using fine phylogenetic scales when assessing host specificity and suggests phylogenetic similarity may play a key role in host shifts not only for viruses but also for bacteria. Such work more broadly contributes to increasing efforts to understand cross‐species transmission and the epidemiological consequences of bacterial pathogens.     

Feeding mechanisms in bats: variation within the constraints of flight

By any standard, bats are a successful group of mammals andthe evolution of flight and echolocation were certainly keyinnovations behind their success. That is only part of the story,however. Bats have diversified into trophic niches that rangefrom insectivory to feeding on blood, fruit, or nectar. Whileflight places fundamental constraints on the shape of the postcranialskeleton, skull shape in bats is remarkably diverse. Morphologicalstudies of individual families and sympatric assemblages demonstratethat variation in skull shape is clearly associated with trophicspecialization. Field experiments demonstrate that species-specificbiting behaviors during feeding are common and analyses indicatethat the evolution of cranial morphology and feeding behaviorare correlated. Modeling experiments further suggest that feeding(loading) behaviors and skull shape are functionally linked.If the skulls of bats are under selective pressure for minimalmass because of the energetic demands of flight, then they maybe more "optimized" to meet mechanical demands than are theskulls of other mammals. This would make bats a unique modelsystem for studying the evolution of diversity in skull shapeand its functional implications for the evolution of feedingstrategies in mammals.     

Adaptive evolution of butterfly wing shape: from morphology to behaviour

Butterflies display extreme variation in wing shape associated with tremendous ecological diversity. Disentangling the role of neutral versus adaptive processes in wing shape diversification remains a challenge for evolutionary biologists. Ascertaining how natural selection influences wing shape evolution requires both functional studies linking morphology to flight performance, and ecological investigations linking performance in the wild with fitness. However, direct links between morphological variation and fitness have rarely been established. The functional morphology of butterfly flight has been investigated but selective forces acting on flight behaviour and associated wing shape have received less attention. Here, we attempt to estimate the ecological relevance of morpho‐functional links established through biomechanical studies in order to understand the evolution of butterfly wing morphology. We survey the evidence for natural and sexual selection driving wing shape evolution in butterflies, and discuss how our functional knowledge may allow identification of the selective forces involved, at both the macro‐ and micro‐evolutionary scales. Our review shows that although correlations between wing shape variation and ecological factors have been established at the macro‐evolutionary level, the underlying selective pressures often remain unclear. We identify the need to investigate flight behaviour in relevant ecological contexts to detect variation in fitness‐related traits. Identifying the selective regime then should guide experimental studies towards the relevant estimates of flight performance. Habitat, predators and sex‐specific behaviours are likely to be major selective forces acting on wing shape evolution in butterflies. Some striking cases of morphological divergence driven by contrasting ecology involve both wing and body morphology, indicating that their interactions should be included in future studies investigating co‐evolution between morphology and flight behaviour.     

基因组水平蝙蝠嗅觉受体基因的分子进化

翼手目动物（俗称蝙蝠）的食性分化显著,不同食性的蝙蝠具有显著不同的嗅球大小。为了研究嗅觉是否影响了蝙蝠食性的进化,我们利用网上已公布的10种蝙蝠基因组的数据,通过同源比对的方法鉴定出所有的嗅觉受体基因,并进行嗅觉受体基因亚家族的分类,进而比较嗅觉受体基因亚家族的数目差异。结果显示,蝙蝠的嗅觉受体基因与其它哺乳动物一样,都可以分为13个单系起源的亚家族;在Yinpterochiroptera亚目中,OR1/3/7、OR2/13、OR5/8/9等3个嗅觉受体亚家族在食果蝙蝠中均发生了不同程度的扩张,基因数目显著地多于食虫蝙蝠,提示嗅觉在食果蝙蝠取食过程中具有重要的作用。因此,本研究在基因组水平上重现了蝙蝠嗅觉受体基因的进化历史,揭示了3个嗅觉受体基因亚家族的功能可能与食果蝙蝠的食性相关,突出了嗅觉对动物食性的重要作用.     

A morphospace‐based test for competitive exclusion among flying vertebrates: did birds,bats and pterosaurs get in each other's space?

Three vertebrate groups – birds, bats and pterosaurs – have evolved flapping flight over the past 200 million years. This innovation allowed each clade access to new ecological opportunities, but did the diversification of one of these groups inhibit the evolutionary radiation of any of the others? A related question is whether having the wing attached to the hindlimbs in bats and pterosaurs constrained their morphological diversity relative to birds. Fore‐ and hindlimb measurements from 894 specimens were used to construct a morphospace to assess morphological overlap and range, a possible indicator of competition, among the three clades. Neither birds nor bats entered pterosaur morphospace across the Cretaceous–Paleogene (Tertiary) extinction. Bats plot in a separate area from birds, and have a significantly smaller morphological range than either birds or pterosaurs. On the basis of these results, competitive exclusion among the three groups is not supported.     

Early diversification trend and Asian origin for extent bat lineages

Bats are a unique mammalian group, which belong to one of the largest and most diverse mammalian radiations, but their early diversification is still poorly understood, and conflicting hypotheses have emerged regarding their biogeographic history. Understanding their diversification is crucial for untangling the enigmatic evolutionary history of bats. In this study, we elucidated the rate of diversification and the biogeographic history of extant bat lineages using genus‐level chronograms. The results suggest that a rapid adaptive radiation persisted from the emergence of crown bats until the Early Eocene Climatic Optimum, whereas there was a major deceleration in diversification around 35–49 Ma. There was a positive association between changes in the palaeotemperature and the net diversification rate until 35 Ma, which suggests that the palaeotemperature may have played an important role in the regulation of ecological opportunities. By contrast, there were unexpectedly higher diversification rates around 25–35 Ma during a period characterized by intense and long‐lasting global cooling, which implies that intrinsic innovations or adaptations may have released some lineages from the intense selective pressures associated with these severe conditions. Our reconstruction of the ancestral distribution suggests an Asian origin for bats, thereby indicating that the current panglobal but disjunct distribution pattern of extant bats may be related to events involving seriate cross‐continental dispersal and local extinction, as well as the influence of geological events and the expansion and contraction of megathermal rainforests during the Tertiary.     

Sesamoids and Morphological Variation: a Hypothesis on the Origin of Rod-like Skeletal Elements in Aerial Mammals

Enigmatic rod-like skeletal structures that support compliant membranes (patagia) in aerial mammals have been often considered as neomorphic elements or as evolutionary novelties, and their origin has remained poorly understood. A potential source of skeletal plasticity and, probably, of morphofunctional innovations are sesamoids, which were recently demonstrated to have a common cellular origin with bone eminences. In this review, I compile information regarding anatomy, evolution, and development of rod-like skeletal elements in extant gliding and flying mammals and propose a working hypothesis on the origin of these structures. Rod-like skeletal elements, namely, the calcar in bats (Chiroptera), the unciform element in Anomaluridae (Rodentia), and the styliform cartilage in Pteromyini (Rodentia: Sciuridae), would derive from sesamoids, which, in turn, would have the same origin as eminences of long bones (or bones with a long-bone-like growth), i.e., calcaneus, ulna, and pisiform, respectively. Rod-like skeletal elements exhibit several features of sesamoids. However, further developmental data are needed to confirm this hypothesis, particularly whether these structures share a cellular origin and molecular developmental pathways with sesamoids and bone eminences. If this hypothesis were supported, a new role for sesamoids in generating morphofunctional innovations in mammals and, potentially, in other aerial amniotes, would be recognized. Rod-like skeletal elements, which are key in the evolution of aerial locomotion, might constitute an example of pre-existing traits that acquire novel functions through relatively little developmental plasticity.

     

Bats, clocks, and rocks: diversification patterns in Chiroptera

Identifying nonrandom clade diversification is a critical first step toward understanding the evolutionary processes underlying any radiation and how best to preserve future phylogenetic diversity. However, differences in diversification rates have not been quantitatively assessed for the majority of groups because of the lack of necessary analytical tools (e.g., complete species-level phylogenies, estimates of divergence times, and robust statistics which incorporate phylogenetic uncertainty and test appropriate null models of clade growth). Here, for the first time, we investigate diversification rate heterogeneity in one of the largest groups studied thus far, the bats (Mammalia: Chiroptera). We use a recent, robust statistical approach (whole-tree likelihood-based relative rate tests) on complete dated species-level supertree phylogenies. As has been demonstrated previously for most other groups, among-lineage diversification rate within bats has not been constant. However, we show that bat diversification is more heterogeneous than in other mammalian clades thus far studied. The whole-tree likelihood-based relative rates tests suggest that clades within the families Phyllostomidae and Molossidae underwent a number of significant changes in relative diversification rate. There is also some evidence for rate shifts within Pteropodidae, Emballonuridae, Rhinolophidae, Hipposideridae, and Vespertilionidae, but the significance of these shifts depends on polytomy resolution within each family. Diversification rate in bats has also not been constant, with the largest diversification rate shifts occurring 30-50 million years ago, a time overlapping with the greatest number of shifts in flowering plant diversification rates.     

Correlates of species richness in North American bat families

Aim A near universal truth in North America is that species richness increases from the Arctic Circle to the Central American tropics. Latitude is regarded as a major explanatory variable in species density, although it is only a surrogate for underlying ecological variables. I aimed to elucidate those underlying ecological variables that are associated with variation in bat species richness across the entire North American continent, providing a portrait of the macroecology of the order Chiroptera and its familial components. Methods I determined the number of bat species recorded for every state in Mexico and the United States, every province or territory in Canada, and every country in Central America. For each of these entities (n = 99), I also gathered basic data on mean annual precipitation, variation across the year (July vs. January) in mean temperature, mean January temperature, range in elevation (topographic relief), per cent vegetative cover and median latitude. Using a variety of linear regression and model‐fitting techniques, I analysed the strength and direction of the relationship between species richness and environmental variables for the order Chiroptera as a whole and separately for each of four familial groups: Molossidae (free‐tailed bats), Phyllostomidae (New World leaf‐nosed bats), Vespertilionidae (evening bats), and a set of six families (the Desmodontidae, Emballonuridae, Furipteridae, Natalidae, Noctilionidae, and Thyropteridae) represented in North America relatively poorly. Results and main conclusions Save for the Vespertilionidae, species richness of bats increased towards the Panamanian Isthmus. The Phyllostomidae and the set of miscellaneous families are particularly speciose in tropical Central America, with many fewer species occurring through subtropical Mexico into (in some cases) the southernmost United States. The Molossidae extends farther north, sparingly into the middle of the United States. Species density of the Vespertilionidae peaks in central and western Mexico and the southernmost United States, declining south through tropical southern Mexico and Central America and north through the central United States into Canada. Annual precipitation, January temperature, and topography are good predictors of species richness in the Chiroptera and the Molossidae, precipitation, topography, and temperature range in the Phyllostomidae, January temperature and topography in the Vespertilionidae, and precipitation alone in the collection of families. Vegetative cover explained little variation in the Chiroptera as a whole or in any family. After accounting for the effects of the environmental variables, latitude explained an insignificant amount of the residual variation in species richness. Bat families differ in their ecology, so studies of bat biogeography in North America may be misleading if they are examined only at the ordinal level.     

Evolvability and Robustness in Color Displays: Bridging the Gap between Theory and Data

Evolution of diet-derived sexual ornaments—some of the most spectacular and diverse traits in the living world—highlights the gap between modern evolutionary theory and empirical data on the origin and inheritance of complex environment-dependent traits. Specifically, current theory offers little insight into how strong environmental contingency of diet-dependent color biosynthesis and environmental variability in precursor supply can be reconciled with extensive evolutionary elaboration, diversification, and convergence of diet-dependent displays among animal taxa. Moreover, biosynthetic pathways of diet-derived displays combine seemingly irreconcilable robustness, lability, and modularity to facilitate elaboration under variable environmental conditions. Here I show that an ontogenetic decrease in the predictability of an association between organismal and environmental components of color biosynthesis and the corresponding evolutionary transition from short-term epigenetic inheritance of peripheral biosynthetic components to genetic inheritance of the most reliable upstream components link the causes of developmental variation with the causes of inheritance in diet-derived displays. Using carotenoid-based colors as an empirical model, I outline general principles of a testable evolutionary framework of diversification and functional robustness of diet-derived displays, and suggest that such a framework provides insight into the foundational question of evolutionary biology—how to connect causes of within-generation developmental variation with causes of among-generation and among-taxa variation and thus with causes of evolution?     

Complete mitochondrial genome sequences of three bats species and whole genome mitochondrial analyses reveal patterns of codon bias and lend support to a basal split in Chiroptera

Order Chiroptera is a unique group of mammals whose members have attained self-powered flight as their main mode of locomotion. Much speculation persists regarding bat evolution; however, lack of sufficient molecular data hampers evolutionary and conservation studies. Of ~ 1200 species, complete mitochondrial genome sequences are available for only eleven. Additional sequences should be generated if we are to resolve many questions concerning these fascinating mammals. Herein, we describe the complete mitochondrial genomes of three bats: Corynorhinus rafinesquii, Lasiurus borealis and Artibeus lituratus. We also compare the currently available mitochondrial genomes and analyze codon usage in Chiroptera. C. rafinesquii, L. borealis and A. lituratus mitochondrial genomes are 16438 bp, 17048 bp and 16709 bp, respectively. Genome organization and gene arrangements are similar to other bats. Phylogenetic analyses using complete mitochondrial genome sequences support previously established phylogenetic relationships and suggest utility in future studies focusing on the evolutionary aspects of these species. Comprehensive analyses of available bat mitochondrial genomes reveal distinct nucleotide patterns and synonymous codon preferences corresponding to different chiropteran families. These patterns suggest that mutational and selection forces are acting to different extents within Chiroptera and shape their mitochondrial genomes.     

Positive selection drives adaptive diversification of the 4‐coumarate: CoA ligase (4CL) gene in angiosperms

Lignin and flavonoids play a vital role in the adaption of plants to a terrestrial environment. 4‐Coumarate: coenzyme A ligase (4CL) is a key enzyme of general phenylpropanoid metabolism which provides the precursors for both lignin and flavonoids biosynthesis. However, very little is known about how such essential enzymatic functions evolve and diversify. Here, we analyze 4CL sequence variation patterns in a phylogenetic framework to further identify the evolutionary forces that lead to functional divergence. The results reveal that lignin‐biosynthetic 4CLs are under positive selection. The majority of the positively selected sites are located in the substrate‐binding pocket and the catalytic center, indicating that nonsynonymous substitutions might contribute to the functional evolution of 4CLs for lignin biosynthesis. The evolution of 4CLs involved in flavonoid biosynthesis is constrained by purifying selection and maintains the ancestral role of the protein in response to biotic and abiotic factors. Overall, our results demonstrate that protein sequence evolution via positive selection is an important evolutionary force driving adaptive diversification in 4CL proteins in angiosperms. This diversification is associated with adaption to a terrestrial environment.     

Morphology and Homology of the Chiropteran Calcar, with Comments on the Phylogenetic Relationships of Archaeopteropus

Most researchers have considered the calcar to be a unique and homologous structure within Chiroptera (e.g., the presence of this structure and its associated musculature has been cited as a synapomorphy supporting bat monophyly). However, we report that significant morphological variation exists between Microchiroptera and Megachiroptera. In microchiropterans, a calcified or cartilaginous element articulates directly with the calcaneal tuberosity of the ankle and projects into the uropatagium. In megachiropterans, a cartilaginous structure projects from the tendon of the gastrocnemius muscle into the uropatagium and has no articulation with the calcaneal tuberosity. Considerable variation also exists in the musculature associated with these structures. Phylogenetic interpretation of hindlimb morphology of extant and fossil taxa indicates that the calcar may not be homologous in all bats. We suggest retention of the term calcar for the microchiropteran structure and propose a new term, uropatagial spur, for the megachiropteran structure. The fossil bat Archaeopteropus transiens (Oligocene) has long been presumed to be a megachiropteran; however, this form has a microchiropteran-type calcar. Reconsideration of morphological evidence from this and previous studies indicates that Archaeopteropus is not a megachiropteran but, rather, a basal member of the microchiropteran lineage.