A nuclear DNA phylogenetic perspective on the evolution of echolocation and historical biogeography of extant bats (chiroptera)

Bats (Order Chiroptera), the only mammals capable of powered flight and sophisticated laryngeal echolocation, represent one of the most species-rich and ubiquitous orders of mammals. However, phylogenetic relationships within this group are poorly resolved. A robust evolutionary tree of Chiroptera is essential for evaluating the phylogeny of echolocation within Chiroptera, as well as for understanding their biogeographical history. We generated 4 kb of sequence data from portions of four novel nuclear intron markers for multiple representatives of 17 of the 18 recognized extant bat families, as well as the putative bat family Miniopteridae. Three echolocation-call characters were examined by mapping them onto the combined topology: (1) high-duty cycle versus low-duty cycle, (2) high-intensity versus low-intensity call emission, and (3) oral versus nasal emission. Echolocation seems to be highly convergent, and the mapping of echolocation-call design onto our phylogeny does not appear to resolve the question of whether echolocation had a single or two origins. Fossil taxa may also provide insight into the evolution of bats; we therefore evaluate 195 morphological characters in light of our nuclear DNA phylogeny. All but 24 of the morphological characters were found to be homoplasious when mapped onto the supermatrix topology, while the remaining characters provided insufficient information to reconstruct the placement of the fossil bat taxa with respect to extant families. However, a morphological synapomorphy characterizing the Rhinolophoidea was identified and is suggestive of a separate origin of echolocation in this clade. Dispersal-Vicariance analysis together with a relaxed Bayesian clock were used to evaluate possible biogeographic scenarios that could account for the current distribution pattern of extant bat families. Africa was reconstructed as the center of origin of modern-day bat families.     

The digital tendon locking mechanism of the avian foot (Aves)

Summary Representatives of all avian orders were studied in order to establish that the tendon-locking mechanism (TLM), consisting of local specialization of the flexor tendons and the adjacent portion of the flexor tendon sheath, is by no means rare, but rather, constitutes the prevalent condition in a large majority of the avian species sampled. The areas of tubercles on the tendons and the adjacent sheath plications intermesh with one another thereby forming a true tendon-locking mechanism that maintains the distal and other interphalangeal joints of the digits in the flexed position. The TLM seems to function not only in perching, but in a wide variety of other activities of the avian foot including swimming, wading, prey-grasping, clinging, hanging, and tree climbing. The basic structural components of the mechanism are remarkably similar in the divergent avian groups adapted for these activities. Ultrastructural detail of the TLM was studied by means of scanning and transmission electron microscopy. Interdigital variation in distribution of the TLM in all of the digits of individuals were made as were comparisons of the interspecific distribution of the TLM. An analysis of the biomechanics involved in engaging the elements of the TLM and how they produce locking of the flexed joints of the digits includes a consideration of the roles of the podothecal pads, ungual flexor processes, and the elastic flexor and extensor ligaments of the toes. The components of the TLM are differentiated in early fetal development establishing that the TLM components are not acquired adventitiously in response to such factors as posthatching mechanical stresses.     

Chiropteran vomeronasal complex and the interfamilial relationships of bats

Within the extant orders of living mammals, the distribution of the vomeronasal organ (VNO) and associated structures is very stable, being universally present in the vast majority or universally absent in cetaceans and sirenians. Chiroptera is the most noteworthy exception, with variation in the absence or presence of the vomeronasal complex occurring even at the species level in some instances. The VNO and/or its component structures, such as the accessory olfactory bulb, were studied in serially sectioned snouts and brains from 114 genera and 292 species representing all extant chiropteran families except Myzopodidae and Antrozoidae. Taxa were scored for the following characters: (1) degree of formation of the vomeronasal epithelial tube, (2) shape of the vomeronasal cartilage, (3) occurrence of the nasopalatine duct, and (4) occurrence of the accessory olfactory bulb. To reconstruct the evolutionary history of the bat vomeronasal complex, the distributions of these four characters were mapped, using the computer program MacClade, onto chiropteran phylogenies in the literature derived from other data sets. In all phylogenies, these four characters exhibit a high degree of homoplasy, only part of which is accounted for by several polymorphic taxa. However, perhaps the most remarkable result is that in the most parsimonious solutions the absence of the vomeronasal epithelial tube and accessory olfactory bulb is identified as primitive for Chiroptera, with both structures reevolving numerous times: such a scenario would be unique to bats among mammals. An alternative, though less parsimonious interpretation, which does not require reevolution of this very complex system, is that a well-developed vomeronasal epithelial tube is primitive for Chiroptera, as in nearly all other orders of mammals, but has been reduced or lost in the majority of families. Explication of the peculiar evolutionary history of the vomeronasal system in bats awaits studies on the adult morphology in the more than 630 species not yet examined and, in particular, on ontogeny, which to date is known for only a handful of taxa.A preliminary account of this research was presented at the Tenth International Bat Research Conference and Twenty-Fifth North American Bat Research Symposium held at Boston University, Massachusetts, on 6–11 August 1995.     

Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective

Secondary metabolites, at least the major ones present in a plant, apparently function as defence (against herbivores, microbes, viruses or competing plants) and signal compounds (to attract pollinating or seed dispersing animals). They are thus important for the plant's survival and reproductive fitness. Secondary metabolites therefore represent adaptive characters that have been subjected to natural selection during evolution. Molecular phylogenies of the Fabaceae, Solanaceae and Lamiaceae were reconstructed and employed as a framework to map and to interpret the distribution of some major defence compounds that are typical for the respective plant families; quinolizidine alkaloids and non-protein amino acids for legumes; tropane and steroidal alkaloids for Solanaceae, and iridoids and essential oils for labiates. The distribution of the respective compounds appears to be almost mutually exclusive in the families studied, implying a strong phylogenetic and ecological component. However, on a closer look, remarkable exceptions can be observed, in that certain metabolites are absent (or present) in a given taxon, although all the neighbouring and ancestral taxa express (or do not express, respectively) the particular trait. It is argued that these patterns might reflect differential expression of the corresponding genes that have evolved earlier in plant evolution. The inconsistent secondary metabolite profiles mean that the systematic value of chemical characters becomes a matter of interpretation in the same way as traditional morphological markers. Thus, the distribution of secondary metabolites has some value for taxonomy but their occurrence apparently reflects adaptations and particular life strategies embedded in a given phylogenetic framework.     

A phylogenetic and biogeographic perspective on the evolution of poeciliid fishes

Phylogenetic relationships of members of the subfamily Poeciliinae (Cyprinodontiformes) are investigated to test alternate hypotheses of diversification resulting from the assembly of the Central America and the Caribbean from the Cretaceous period onwards. We use 4333 aligned base pairs of mitochondrial DNA and 1549 aligned base pairs of nuclear DNA from 55 samples representing 48 ingroup and seven outgroup species to test this hypothesis. Mitochondrial genes analyzed include those encoding the 12S and 16S ribosomal RNAs; transfer RNAs coding for valine, leucine, isoleucine, glutamine, methionine, tryptophan, alanine, asparagine, cysteine and tyrosine; and complete cytochrome b and NADH dehydrogenase subunit I and II; nuclear gene analyzed included the third exon of the recombination activation gene 1 (RAG1). Analyses of combined mtDNA and nuclear DNA data sets result in a well-supported phylogenetic hypothesis. This hypothesis is in conflict with the classical taxonomic assignment of genera into tribes and phylogenetic hypotheses based on the taxonomy; however, the molecular hypothesis defines nine clades that are geographically restricted and consistent with the geological evolution of Central America and the Caribbean. Our analyses support multiple colonization events of Middle America followed by a mix of vicariance and dispersal events.     

The evolution of flight and echolocation in bats: another leap in the dark

The earliest known complete bats, from the Eocene (49–53 Mya), were already capable of flapping flight and echolocation. In the absence of direct fossil evidence there have been many speculative scenarios advanced to explain the evolution of these behaviours and their distributions in extant bats. Theories assuming chiropteran monophyly have generally presumed the ancestral pre‐bat was nocturnal, arboreal and insectivorous. Following this assumption hypotheses can be divided into the echolocation first, flight first and tandem development hypotheses, all of which assume that flight evolved only once in the lineage. In contrast, the chiropteran diphyly hypothesis suggests that flight evolved twice. Evidence supporting and refuting the different hypotheses are reviewed. It is concluded that there are significant problems attached to all the current models. A novel hypothesis is advanced, which starts from the assumption that bats are monophyletic and the ancestral pre‐bat was arboreal, but diurnal and frugivorous. After the evolution of flight it is suggested that these animals were driven into the nocturnal niche by the evolution of raptorial birds, and different groups evolved either specialised nocturnal vision (megachiropterans) or echolocation (microchiropterans). A block on sensory modality transfer has retained this distribution of perceptual capabilities ever since, despite some Megachiroptera evolving rudimentary echolocation, and the dietary convergence of some Microchiroptera with the Megachiroptera. The new hypothesis overcomes many of the problems identified in previous treatments.     

Evolution of eye development in arthropods: phylogenetic aspects

The architecture of the adult arthropod visual system for many decades has contributed important character sets that are useful for reconstructing the phylogenetic relationships within this group. In the current paper we explore whether aspects of eye development can also contribute new arguments to the discussion of arthropod phylogeny. We review the current knowledge on eye formation in Trilobita, Xiphosura, Myriapoda, Hexapoda, and Crustacea. All euarthropod taxa share the motif of a proliferation zone at the side of the developing eye field that contributes new eye elements. Two major variations of this common motif can be distinguished: 1. The “row by row type” of Trilobita, Xiphosura, and Diplopoda. In this type, the proliferation zone at the side of the eye field generates new single, large elements with a high and variable cell number, which are added to the side of the eye and extend rows of existing eye elements. Cell proliferation, differentiation and ommatidial assembly seem to be separated in time but spatially confined within the precursors of the optic units which grow continuously once they are formed (intercalary growth). 2. The “morphogenetic front type” of eye formation in Crustacea + Hexapoda (Tetraconata). In this type, there is a clear temporal and spatial separation of the formation and differentiation processes. Proliferation and the initial steps of pattern formation take place in linear and parallel mitotic and morphogenetic fronts (the mitotic waves and the morphogenetic furrow/transition zone) and numerous but small new elements with a strictly fixed set of cells are added to the eye field. In Tetraconata, once formed, the individual ommatidia do not grow any more. Scutigeromorph chilopods take an intermediate position between these two major types. We suggest that the “row by row type” as seen in Trilobita, Xiphosura and Diplopoda represents the plesiomorphic developmental mode of eye formation from the euarthropod ground pattern whereas the “morphogenetic front type” is apomorphic for the Tetraconata. Our data are discussed with regard to two competing hypotheses on arthropod phylogeny, the “Tracheata” versus “Tetraconata” concept. The modes of eye development in Myriapoda is more parsimonious to explain in the Tetraconata hypothesis so that our data raise the possibility that myriapod eyes may not be secondarily reconstructed insect eyes as the prevailing hypothesis suggests.     

Trapped in the darkness of the night: thermal and energetic constraints of daylight flight in bats

Bats are one of the most successful mammalian groups, even though their foraging activities are restricted to the hours of twilight and night-time. Some studies suggested that bats became nocturnal because of overheating when flying in daylight. This is because--in contrast to feathered wings of birds--dark and naked wing membranes of bats efficiently absorb short-wave solar radiation. We hypothesized that bats face elevated flight costs during daylight flights, since we expected them to alter wing-beat kinematics to reduce heat load by solar radiation. To test this assumption, we measured metabolic rate and body temperature during short flights in the tropical short-tailed fruit bat Carollia perspicillata at night and during the day. Core body temperature of flying bats differed by no more than 2°C between night and daytime flights, whereas mass-specific CO(2) production rates were higher by 15 per cent during daytime. We conclude that increased flight costs only render diurnal bat flights profitable when the relative energy gain during daytime is high and risk of predation is low. Ancestral bats possibly have evolved dark-skinned wing membranes to reduce nocturnal predation, but a low degree of reflectance of wing membranes made them also prone to overheating and elevated energy costs during daylight flights. In consequence, bats may have become trapped in the darkness of the night once dark-skinned wing membranes had evolved.     

Distribution and underground habitats of cave-dwelling bats in China

To understand the distribution and relative abundance of cave-dwelling bats and to identify those sites that would be important for conservation of bat species, 25 underground sites that had not been previously surveyed were investigated in this 3-year study (from December 2003 to April 2006) in Funiu Mountain of Henan province, China. Approximately 80 000 bats were recorded, representing 12 species. The most abundant species were Rhinolophus affini s, Miniopterus schreibersi and Hipposideros pratti . The roosts were evaluated for their conservation importance. The most important sites in the area are Yunhua and Nanzhao caves, which serve as hibernaculums and nursery roosts to c . 13 740 and 11 803 bats, respectively, representing seven species. By means of cluster and correspondence analysis, the distribution of bat species was different between the two sides of the mountain and was highly dependent on the size of the cave. The underground sites in the south region hosted c . 80% of the total bats, representing 11 species. The sites in the north region hosted 20% of the total bats, representing seven species. Presently, none of the caves in the region has adequate protection and some bat populations are under serious threat. Many large caves that contained large bat populations and several species of concern had been developed as tourist sites, and so some advice on protecting the most important local habitats was sought based on the assessment of the conservation status of underground sites. This paper presents basic data concerning the distribution of cave-dwelling bats and the patterns of cave use on Funiu Mountain. The data will help local governments and policy-makers develop suitable strategies to promote local tourisms while protecting important habitats of animal species.     

Molecular phylogenetic perspective on the evolution of the deep-sea fish genusCyclothone (Stomiiformes: Gonostomatidae)

A portion of mitochondrially encoded 12S and 16S ribosomal RNA genes were sequenced from 13 currently recognized species of the midwater deep-sea fish genusCyclothone (Stomiiformes: Gonostomatidae) and three gonostomatid outgroup taxa. Phylogenetic analyses using maximum parsimony and maximum likelihood methods were performed on unambiguously aligned, combined sequences (803 bp) of the two genes. The resultant tree topologies from the two methods were congruent, being robust and supported by various tree statistics, enabling the evolutionary history ofCyclothone to be described in detail. The molecular phylogeny demonstrated striking inconsistencies with previously proposed “natural groups”, although the latter could be confidently refuted by the molecular data. The most significant characteristic of the evolutionary history ofCyclothone was the independent acquisition of an apomorphic depth habitat from the relatively ancestral, lower mesopelagic habitat, by each of three major distinct lineages that had diverged earlier in their evolution. Moreover, such macroevolutionary habitat shifts had been necessarily accompanied by morphological and ecological novelties, presumably originating from paedomorphosis. Repeated evolution of such changes strongly suggests ontogenetic plasticity inCyclothone which could enable these fishes to acquire larval-like, simple organization of body structure. Such a body plan could help them subsist in food-poor surroundings and regulate reproductive variables that take advantage of increasing larval survival toward shallower depths. Recent speciation events, on the contrary, have produced contemporary sister species of allopatric (or microallopatric) distributions, but few morphological and ecological differences. Even if remarkable miniaturization has occurred, such as in the Mediterranean endemicC. pygmaea, it had to have been a simple truncation of ancestral species' ontogeny without attendance of any discernible paedomorphic features. On the basis of the fossil record, geological history of the Mediterranean region, and ectotherm molecular divergence rate, it was estimated thatCyclothone radiation had already started in the early-middle Miocene (17–20 million years ago).     

Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process

By their very nature oceanic island ecosystems offer great opportunities for the study of evolution and have for a long time been recognized as natural laboratories for studying evolution owing to their discrete geographical nature and diversity of species and habitats. The development of molecular genetic methods for phylogenetic reconstruction has been a significant advance for evolutionary biologists, providing a tool for answering questions about the diversity among the flora and fauna on such islands. These questions relate to both the origin and causes of species diversity both within an archipelago and on individual islands. Within a phylogenetic framework one can answer fundamental questions such as whether ecologically and/or morphologically similar species on different islands are the result of island colonization or convergent evolution. Testing hypotheses about ages of the individual species groups or entire community assemblages is also possible within a phylogenetic framework. Evolutionary biologists and ecologists are increasingly turning to molecular phylogenetics for studying oceanic island plant and animal communities and it is important to review what has been attempted and achieved so far, with some cautionary notes about interpreting phylogeographical pattern on oceanic islands.     

Barriers and benefits: implications of artificial night-lighting for the distribution of common bats in Britain and Ireland

Artificial lighting is a particular problem for animals active at night. Approximately 69% of mammal species are nocturnal, and one-third of these are bats. Due to their extensive movements—both on a nightly basis to exploit ephemeral food supplies, and during migration between roosts—bats have an unusually high probability of encountering artificial light in the landscape. This paper reviews the impacts of lighting on bats and their prey, exploring the direct and indirect consequences of lighting intensity and spectral composition. In addition, new data from large-scale surveys involving more than 265 000 bat calls at more than 600 locations in two countries are presented, showing that prevalent street-lighting types are not generally linked with increased activity of common and widespread bat species. Such bats, which are important to ecosystem function, are generally considered ‘light-attracted’ and likely to benefit from the insect congregations that form at lights. Leisler''s bat (Nyctalus leisleri) may be an exception, being more frequent in lit than dark transects. For common pipistrelle bats (Pipistrellus pipistrellus), lighting is negatively associated with their distribution on a landscape scale, but there may be local increases in habitats with good tree cover. Research is now needed on the impacts of sky glow and glare for bat navigation, and to explore the implications of lighting for habitat matrix permeability.     

A phylogenetic study of the Plantaginaceae

In a study based on morphological, embryological and chemical data of the Plantaginaceae, within the subclass Sympetalae or Asteridae, the superorder Lamianae is shown to be monophyletic. However, it was not possible to reconstruct the phylogeny within Lamianae or to find a sister-group for the monophyletic Plantaginaceae – Hydrostachyaceae for the latter is rejected. Three or rarely four genera have previously been recognized within Plantaginaceae, but in both cases Plantago appears as polyphyletic, which is considered unacceptable. Six clades are recognized as subgenera within Plantago: subgen. Plantago (c. 131 species), subgen. Coronopus (c. 11 species), subgen. Littorella (three species), subgen. Psyllium (c. 16 species), subgen. Bougueria (one species), and subgen. Albicans (51 species). Within P. subgen. Plantago, the paraphyletic sect. Plantago (c. 42 species) is found in all parts of the world except South America, New Zealand, Australia, and New Guinea, where sect. Oliganthos and sect. Mesembryniae vicariate. It is not possible to infer the phylogeny within sect. Plantago, for example between the endemic species from distant Pacific Islands; their common ancestor might be a species that once had a very wide distribution. Keys to genera, subgenera, sections and series are given. Only one genus, Plantago L., is recognized. The following proposals are made in the Appendix: P. ser. Oliganthos Rahn, ser. nov.; P. ser. Carpophorae (Rahn) Rahn, stat. nov. (= sect. C.); P. ser. Microcalyx (Pilg.) Rahn, stat. nov. (= sect. M.); P. unibrackteata Rahn, nom. nov. (=P. uniflora Hook.f. non L.); P. subgen. Littorella (P. J. Bergius) Rahn, stat. nov. (=Littorella P. J. Bergius); P. araucana Rahn, nom. nov. (=Littorella australis Griseb. non Plantago australis Lam.); P. americana (Fernald) Rahn, comb. nov.(=Littorella a.); P. subgen. Bougueria (Decne.) Rahn, stat. nov. (=Bougueria Decne.); P. nubicola (Decne.) Rahn, comb. nov. (=Bougueria n. Decne.); P. subgen. Albicans Rahn, subgen. nov. Ten lectotypes are selected.     

Rainfall, food abundance and timing of parturition in African bats

We used published results from studies in Africa to test the hypothesis that the timing of parturition in the Chiroptera is constrained by rainfall. Comparison of year-round rainfall and insect data at various latitudes showed that insect abundance peaks approximately a month after peak rainfall. A similar comparison of parturition time to rainfall showed that with the possible exception of the molossids, the Microchiroptera commonly give birth a month before peak rainfall. With an average 6-week lactation period in the Microchiroptera, the timing of parturition is such that young bats are weaned just before the period of maximum insect abundance. We suggest that the needs of the young in this post-weaning period may be more important than the energetic demands of lactation on the mother in determining the timing of parturition on an evolutionary scale. A similar conclusion is implied for the African Megachiroptera, but there is insufficient information on their reproduction to adequately test the main hypothesis for these bats. Received: 4 October 1996 / Accepted: 14 March 1997