Resource partitioning in rhinolophoid bats revisited

We assessed the ecomorphological structure of a guild of rhinolophoid bats in a Malaysian rainforest first described by Heller and von Helversen (1989). These authors found that the distribution of echolocation call frequencies used by 12 syntopic species was more even than expected from allometric relationships or in randomly generated communities, and that the observed minimal ratio was greater than expected by chance alone. In this study we were able to expand their guild to 15 species, but in doing so it became apparent that call frequencies might be less evenly distributed across the total frequency range than previously proposed. We replicated Heller and von Helversen’s (1989) analyses with the full 15-species complement but were unable to support their suggestion that rhinolophoid bats exhibit resource partitioning through differences in frequency bands. We adopted a multivariate approach and incorporated measures of body size and wing morphology into the analysis. We used phylogenetic autocorrelation to ensure that the species were statistically independentand principal component analysis to describe the morphological space occupied by the 15 species in the community and four additional species representing the extremes of phenotypic variation. We derived interspecific Euclidean distances and tested the mean values and SDs of these distances against those of 100 guilds of ”synthetic” species created randomly within the principal component space. The guild of Rhinolophoidea was not distributed randomly in multivariate space. Instead we found evidence of morphological overdispersion of the most similar species, which suggests niche differentiation in response to competition. Less similar species were nearer in morphological space than expected, and we suggest this is a consequence of ecological constraints on parameter combinations. Despite this underdispersion, many of the more distant neighbours were evenly rather than randomly spaced or clumped in morphospace, suggesting that, given the environmental constraints on morphology, species in this guild do experience limits to their similarity. Finally, we tested the influence of the relative abundance of species on morphological displacement, and found no evidence that abundant, spatially correlated species reduce interspecific overlap in morphological space. Received: 10 April 1999 / Accepted: 28 February 2000     

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.     

Adaptation of brain regions to habitat complexity: a comparative analysis in bats (Chiroptera)

Vertebrate brains are organized in modules which process information from sensory inputs selectively. Therefore they are probably under different evolutionary pressures. We investigated the impact of environmental influences on specific brain centres in bats. We showed in a phylogenetically independent contrast analysis that the wing area of a species corrected for body size correlated with estimates of habitat complexity. We subsequently compared wing area, as an indirect measure of habitat complexity, with the size of regions associated with hearing, olfaction and spatial memory, while controlling for phylogeny and body mass. The inferior colliculi, the largest sub-cortical auditory centre, showed a strong positive correlation with wing area in echolocating bats. The size of the main olfactory bulb did not increase with wing area, suggesting that the need for olfaction may not increase during the localization of food and orientation in denser habitat. As expected, a larger wing area was linked to a larger hippocampus in all bats. Our results suggest that morphological adaptations related to flight and neuronal capabilities as reflected by the sizes of brain regions coevolved under similar ecological pressures. Thus, habitat complexity presumably influenced and shaped sensory abilities in this mammalian order independently of each other.     

Evolutionary constraints in hind wing shape in Chinese dung beetles (Coleoptera: Scarabaeinae)

This study examines the evolution hindwing shape in Chinese dung beetle species using morphometric and phylogenetic analyses. Previous studies have analyzed the evolution of wing shape within a single or very few species, or by comparing only a few wing traits. No study has analyzed wing shape evolution of a large number of species, or quantitatively compared morphological variation of wings with proposed phylogenetic relationships. This study examines the morphological variation of hindwings based on 19 landmarks, 119 morphological characters, and 81 beetle species. Only one most parsimonious tree (MPT) was found based on 119 wing and body characters. To better understand the possible role of the hindwing in the evolution of Scarabaeinae, additional phylogenetic analyses were proposed based on the only body features (106 characters, wing characters excluded). Two MPT were found based on 106 body characters, and five nodes were collapsed in a strict consensus. There was a strong correlation between the morphometric tree and all phylogenetic trees (r>0.5). Reconstructions of the ancestral wing forms suggest that Scarabaeinae hindwing morphology has not changed substantially over time, but the morphological changes that do occur are focused at the base of the wing. These results suggest that flight has been important since the origin of Scarabaeinae, and that variation in hindwing morphology has been limited by functional constraints. Comparison of metric disparity values and relative evolutionary sequences among Scarabaeinae tribes suggest that the primitive dung beetles had relatively diverse hindwing morphologies, while advanced dung beetles have relatively similar wing morphologies. The strong correlation between the morphometric tree and phylogenetic trees suggest that hindwing features reflect the evolution of whole body morphology and that wing characters are suitable for the phylogenetic analyses. By integrating morphometric and cladistic approaches, this paper sheds new light on the evolution of dung beetle hind wings.     

EVOLUTION AND COADAPTATION OF THERMOREGULATORY BEHAVIOR AND WING PIGMENTATION PATTERN IN PIERID BUTTERFLIES

This paper addresses the question of how the relationship between morphological structure and functional performance differs in related groups of organisms. I describe the relationship between a suite of phenotypic characters (behavioral posture and the pattern of wing pigmentation) and one function of these characters (thermoregulatory performance) for two groups of butterflies in the family Pieridae, focusing on how behavior and wing pattern interact to affect specific aspects of thermoregulation. Using both natural and experimentally created variation in wing-melanization patterns, I develop and test a series of predictions about the relations among thermoregulatory posture, melanization pattern, body temperature, and flight activity. Results show that increased melanization in different wing regions has positive, negative, or neutral effects in increasing body temperature of Pieris butterflies. The angle of the wings used during basking alters the relative importance of different modes of heat transfer and thereby determines the contribution of different dorsal wing regions to thermoregulation. Experimentally increased dorsal melanization can either increase or decrease the onset of flight activity and can directly alter thermoregulatory posture. For Pieris, dorsal melanization affects basking and flight, while ventral melanization primarily affects overheating. These results are used to generate a functional map relating melanization pattern to thermoregulatory performance in Pieris. Reflectance-basking posture, white background color, and melanization pattern represent coadapted characters in Pieris that interact to determine thermoregulatory performance. The differences in thermoregulatory posture and background color between pierid butterflies in the subfamilies Pierinae and Coliadinae have led to a reorganization and partial reversal of the thermoregulatory effects of melanization pattern. I suggest that this change in the physical mechanism of thermoregulatory adaption in pierids has qualitatively altered the nature of selection on wing-melanization pattern.     

Flight style in bats as predicted from wing morphometry: the effects of specimen preservation

An as yet unconsidered potential error in studies that predict flight style from morphological measurements of bats is the effect of the specimen type employed. On the basis of the finding that morphological measurements taken from fluid-preserved bat specimens may not yield values equivalent to those taken from the live animal, we compared the values of several variables (lifting surface area, wingspan, mass, aspect ratio, wing loading and minimum power speed) for live and fluid-preserved little brown bats ( Myotis lucifugus ) with the accepted standards for this species given by Norberg & Rayner (1987). Significant differences were detected for lifting surface area, wingspan, mass, aspect ratio and wing loading values taken from live bats and their respective values reported by Norberg & Rayner. Differences between preserved bats and Norberg & Rayner's numbers were limited to lifting surface area and wingspan (extended wing positions only), aspect ratio (all wing positions), and mass (both 70% ethanol- and 45% isopropyl alcohol-preserved specimens). Thus, Norberg & Rayner's values correspond most closely to values obtained from preserved museum specimens, a fact reflecting the source of their data in this instance. This and other limitations involved in attempting to predict the flight style of bats from a few morphological characters are discussed.     

PATTERNS OF QUANTITATIVE VARIATION IN LEPIDOPTERAN WING MORPHOLOGY: THE CONVERGENT GROUPS HELICONIINAE AND ITHOMIINAE (PAPILIONOIDEA: NYMPHALIDAE)

Wing morphology has historically been a major focus in taxonomic and evolutionary studies of lepidopterans. However, general patterns of quantitative variation and diversification in wing sizes and shapes and the factors underlying them have been unexplored. A morphometric study of wing variation in the convergent heliconine and ithomine butterflies reveals remarkable similarities, both in their morphologies at a given size and in their patterns of allometry and variability. The groups differ primarily in the relative lengths of inner and outer forewing margins, with larger species being more similar across groups than smaller ones. Allometric size-scaling variation accounts for more than 90% of the total morphological variation in the two groups and thus seems to be the major determinant of wing shape. Forewings and hind wings are isometric in size (area) with respect to one another; however, wing shape within and among groups is significantly allometric, resulting in considerable shape differences between small and large species. A strong trend of increasing variability from anterior to posterior along the wings is consistent with hypotheses of aerodynamic constraint. Wings and bodies represent classical morphological “character suites” in that size and shape variation are more tightly correlated within suites than among them. Such complexes argue against the overriding importance of aerodynamic factors, such as wing load and muscle development, in constraining gross morphology.     

Parallel evolution of auditory genes for echolocation in bats and toothed whales

The ability of bats and toothed whales to echolocate is a remarkable case of convergent evolution. Previous genetic studies have documented parallel evolution of nucleotide sequences in Prestin and KCNQ4, both of which are associated with voltage motility during the cochlear amplification of signals. Echolocation involves complex mechanisms. The most important factors include cochlear amplification, nerve transmission, and signal re-coding. Herein, we screen three genes that play different roles in this auditory system. Cadherin 23 (Cdh23) and its ligand, protocadherin 15 (Pcdh15), are essential for bundling motility in the sensory hair. Otoferlin (Otof) responds to nerve signal transmission in the auditory inner hair cell. Signals of parallel evolution occur in all three genes in the three groups of echolocators--two groups of bats (Yangochiroptera and Rhinolophoidea) plus the dolphin. Significant signals of positive selection also occur in Cdh23 in the Rhinolophoidea and dolphin, and Pcdh15 in Yangochiroptera. In addition, adult echolocating bats have higher levels of Otof expression in the auditory cortex than do their embryos and non-echolocation bats. Cdh23 and Pcdh15 encode the upper and lower parts of tip-links, and both genes show signals of convergent evolution and positive selection in echolocators, implying that they may co-evolve to optimize cochlear amplification. Convergent evolution and expression patterns of Otof suggest the potential role of nerve and brain in echolocation. Our synthesis of gene sequence and gene expression analyses reveals that positive selection, parallel evolution, and perhaps co-evolution and gene expression affect multiple hearing genes that play different roles in audition, including voltage and bundle motility in cochlear amplification, nerve transmission, and brain function.     

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.     

Evolution of the placenta and associated reproductive characters in bats

Recent advances in molecular phylogenetics indicate that the order Chiroptera is monophyletic and that one of four lineages of microbats (Rhinolophoidea) shares a common origin with megabats. Against this background we undertook a comprehensive analysis of placental evolution in bats. We defined a range of characters and character states associated with female reproduction, early development, placentation and the neonate. These were then mapped on a pre-existing hypothesis of bat relationships that represents the current view from molecular studies. Our purpose was threefold. First, on the assumption of bat monophyly, we wished to establish the stem species pattern of extant chiropterans. Secondly, we asked whether there are derived character conditions in support of a common origin for Rhinolophoidea and the megabats. Thirdly, we looked for evolutionary character transformations that characterize higher-level clades within Chiroptera, i.e. the megabats and the four lineages of microbats. The character condition occurring in the last common ancestor of Chiroptera was unequivocal for 21 of the 25 characters included in the analysis. The data did not offer support for a megabat-rhinolophoid clade or the implication that microbats are paraphyletic. However, analysis of early development, placentation and other reproductive parameters resulted in derived character conditions for the megabats as well as for each of the four major lineages of microbats.     

Variation of wing venation in Elachistidae (Lepidoptera: Gelechioidea): methodology and implications to systematics

We introduce a method to transform wing venation data to a numerical form so that the venation pattern can be analysed and compared regardless of wing size and displacement of the pattern. We use the method for assessing the intraspecific variation and asymmetry within the individual of relative positions of forewing veins in ten species of elachistid moths. Both the intraspecific variation and intra-individual asymmetry were found to be greater than the differences frequently used as systematic characters on various levels within Elachistidae, and to some extent in other Lepidoptera. At least in Elachistidae, major alterations to the current classification will have to be made. Wing characters subject to intraspecific variation should not be used to delimit groups unless they are based on examination of population samples and supported by other characters.     

Reuse of voucher specimens provides insights into the genomic associations and taxonomic value of wing colour and genitalic differences in a pest group (Lepidoptera: Tortricidae: Choristoneura)

Subtle morphological differences can be essential to diagnosing closely related species, and an understanding of the genetic basis of these characters can contribute to understanding their divergences. We used voucher specimens from previous genetic analyses of population structure to subsequently analyse genome-wide associations linking morphology to genetic variation in spruce budworms, a group of economically important and morphologically similar forest pests. In particular, we assessed the taxonomic value and genetic architecture of two morphological traits (wing pattern and genitalic spicule abundance) that have been reported to differ among spruce budworm species. Our results suggest that phallic spicule number has greater taxonomic utility than wing pattern for distinguishing Choristoneura fumiferana (Clemens) from Choristoneura occidentalis occidentalis Freeman and Choristoneura occidentalis biennis Freeman. However, there was considerable overlap among taxa for all phenotypic characters analysed. In a genome-wide association study, wing pattern variation was significantly associated with four single nucleotide polymorphism (SNP) loci, including two adjacent SNPs. One SNP was flanked by sequence resembling RNA-directed DNA polymerase from mobile element jockey-like. This locus is a promising candidate for the study of wing pattern development in spruce budworms, as jockey-like transposable elements and polymerases have documented roles in wing spot production in other Lepidoptera. Our study links classical taxonomic characters and genomic data to provide insights into the potential genetic architecture of species differences. It also demonstrates previously untapped morphological and taxonomic value in voucher specimens from earlier molecular genetic analyses.     

Variability of morphological traits in Drosophila bipectinata complex

Phenotypic or morphological differences among different populations and sexual dimorphism in certain metric traits were analysed in D. bipectinata complex. It was noticed that different populations of D. bipectinata species group harbour large amount of variation for these characters. In all the populations, morphometric characters such as lengths of femur, tibia and wing length, wing width, number of sternopleural bristles and bristles on epandrium varied significantly among populations. The study indicates that the morphological variations are due to the interplay of genetic and environmental endowments. Further, females had significantly larger values, for lengths of femur, tibia and wing length, wing width and sternopleural bristles.     

PHENOTYPIC CORRELATION STRUCTURE AMONG ELEMENTS OF THE COLOR PATTERN IN PRECIS COENIA (LEPIDOPTERA: NYMPHALIDAE)

The component parts of butterfly wing patterns are arranged in sets of serially homologous pattern elements, repeated from wing cell to wing cell. Measurements were made on the sizes and positions of these elements on two successive, independent, sets of specimens in order to elucidate the phenotypic correlation structure among pattern elements. That portion of the correlation between measures due to overall size variation was accounted for through two alternate methods: multiple regression on two vein length measures, which represent wing size, and a Wright-style factor analysis. The sizes of pattern elements belonging to a homologous series were found to be significantly correlated whereas those of non-homologous elements varied independently. The degree of correlation among homologs varied, and, in the case of eyespot sizes, appeared to be inversely related to the degree of their morphological divergence. Although not correlated in size, the positions of non-homologous elements that lie within the same wing cell are moderately correlated. The results support current developmental models for the ontogeny of butterfly color pattern.     

Phylogeny of the riodinid butterfly subtribe Theopeina (Lepidoptera: Riodinidae: Nymphidiini)

Abstract The almost exclusively Neotropical butterfly family Riodinidae is poorly represented in both ecological and systematic studies of Lepidoptera. A comparative morphological study of all seventy-five species in subtribe Theopeina (tribe Nymphidiini) yielded 104 characters, predominantly from wing pattern, male and female genitalia, and abdominal structures. All morphological characters and adults representing the range of wing pattern variation are illustrated. Phylogenetic analysis of the data produced a large number of most parsimonious cladograms, but the strict consensus of these, both when using equal weights and after successive weighting, is well resolved and the majority of terminal clades have high character and branch support. Theopeina is found to consist of five monophyletic genera, Protonymphidia , Archaeonympha , Calicosama , Behemothia and Theope (=  Parnes and Dinoplotis ), with the largest genus Theope containing thirteen monophyletic species groups, which are delineated to facilitate a discussion of broad evolutionary patterns in this morphologically diverse subtribe.     

Anthropometric variationin the Yanadi: Population structure and sex differences

Anthropometric variation and sex differences were investigated among the Yanadi tribe, who live in different regions and show differences in population structure variables and form regional breeding populations. In case of within population variation in anthropometric characters, both males and females show greater variation in a few specific characters (e.g., HB, LL) and almost no variation in FB, but least variation in HL and NB in males and in ZB, LB in females and show sex differences. Overall, females showed greater variation in more number of characters than males. In case of between population variation a few traits show clinal trend between male-female comparisons. Each character shows a specific pattern (e.g., HB, ZB, EL, GB) which vary according to the spatial distribution of the regional populations. The curves also indicate least average differences corresponding to within regional homogeneity among males and females (e.g., HB, ECD, EB) and increasing differences with males and females of other regions. A comparison of anthropometric profiles of the five populations show significant sex differences in IY subpopulation. The three mainland subpopulations show wide morphological differentiation with two coastal subpopulations, who also differ in subsistence pattern and geographically isolated. A comparison of anthropometric profiles between males and females across five populations show positive association between P1, HF and P₂ populations, whereas significant negative association with CY and HF. The correllelographs based on the male-female comparisons also indicate greater morphological similarity between sexes in cases of within regional population. They also show clinal changes of either decreasing or increasing trends of morphological variation between populations in association with spatial distribution and population structure differences. The results obtained are in agreement with the expectations from the population structure of the tribe.     

Within-island geographic variation of the dangerous Taiwanese snake, Trimeresurus stejnegeri, in relation to ecology

Multivariate analysis shows that geographic variation occurs in the scalation and body proportions of the dangerously venomous snake Tritneresurus stejnegeri , within the island of Taiwan. Canonical correlation analysis reveals a high correlation between constellations of morphological characters and ecological factors. Numerical hypothesis testing, using partial Mantel tests, provides evidence of a causal relationship with ecology. Head shape was found to be primarily associated with mean annual temperature and altitude, and head scalation with the annual range of temperature. Body scalation was found to be influenced by altitude, mean annual temperature and mean annual rainfall. Tail length is primarily associated with the range of temperature and rainfall and secondarily with the mean annual temperature and altitude. Geographic proximity was found to be less important in the explanation of the observed geographic pattern than some ecological factors, supporting the hypothesis of an ecogenetic origin of morphological variation.     

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.     

Intraspecific variation in Anolis sagrei mirrors the adaptive radiation of Greater Antillean anoles

Anolis lizards of the Greater Antilles represent one of the classic examples of vertebrate adaptive radiation. The same morphological types ('ecomorphs') have evolved repeatedly in response to similar ecological pressures on different islands. We tested whether patterns of within species diversification were congruent with between species patterns and the processes leading to the adaptive radiation of Greater Antillean anoles by measuring variation in performance-related morphological characters in the brown anole, Anolis sagrei . We measured morphological and genetic variation in two different habitat types on each of five islands in the Bahamas. We estimated population structure and rates of gene flow within and among islands using eight microsatellite markers. Intraspecific variation in performance-related morphological characters was similar to the pattern of interspecific variation that characterizes the adaptive radiation of this group in the Greater Antilles. For example, limb length was correlated with perch diameter within A. sagrei as has also been shown among species of anole. Morphological divergence in traits has occurred despite relatively high levels of gene flow both within and among islands. These results are discussed in the context of the divergence-with-gene-flow model of speciation. The results provide important intraspecific evidence that the diversification of anoles has been shaped by natural selection and show how ecologically-based selection pressures explain diversification at both the population and species levels.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 90 , 189–199.