ALLOMETRIC CONSTRAINTS AND THE EVOLUTION OF ALLOMETRY

Morphological traits often covary within and among species according to simple power laws referred to as allometry. Such allometric relationships may result from common growth regulation, and this has given rise to the hypothesis that allometric exponents may have low evolvability and constrain trait evolution. We formalize hypotheses for how allometry may constrain morphological trait evolution across taxa, and test these using more than 300 empirical estimates of static (within‐species) allometric relations of animal morphological traits. Although we find evidence for evolutionary changes in allometric parameters on million‐year, cross‐species time scales, there is limited evidence for microevolutionary changes in allometric slopes. Accordingly, we find that static allometries often predict evolutionary allometries on the subspecies level, but less so across species. Although there is a large body of work on allometry in a broad sense that includes all kinds of morphological trait–size relationships, we found relatively little information about the evolution of allometry in the narrow sense of a power relationship. Despite the many claims of microevolutionary changes of static allometries in the literature, hardly any of these apply to narrow‐sense allometry, and we argue that the hypothesis of strongly constrained static allometric slopes remains viable.     

Phylogeny, regression, and the allometry of physiological traits

Physiological and ecological allometries often pose linear regression problems characterized by (1) noncausal, phylogenetically autocorrelated independent (x) and dependent (y) variables (characters); (2) random variation in both variables; and (3) a focus on regression slopes (allometric exponents). Remedies for the phylogenetic autocorrelation of species values (phylogenetically independent contrasts) and variance structure of the data (reduced major axis [RMA] regression) have been developed, but most functional allometries are reported as ordinary least squares (OLS) regression without use of phylogenetically independent contrasts. We simulated Brownian diffusive evolution of functionally related characters and examined the importance of regression methodologies and phylogenetic contrasts in estimating regression slopes for phylogenetically constrained data. Simulations showed that both OLS and RMA regressions exhibit serious bias in estimated regression slopes under different circumstances but that a modified orthogonal (least squares variance-oriented residual [LSVOR]) regression was less biased than either OLS or RMA regressions. For strongly phylogenetically structured data, failure to use phylogenetic contrasts as regression data resulted in overestimation of the strength of the regression relationship and a significant increase in the variance of the slope estimate. Censoring of data sets by simulated extinction of taxa did not affect the importance of appropriate regression models or the use of phylogenetic contrasts.     

The consequences of size dependent foraging for food web topology

A general question in biology is how processes at one scale, for example that of individual organisms, influence patterns at larger scales, for example communities of interacting individuals. Here we ask how changing the size‐dependence of the foraging behaviour of individuals can influence the structure of food webs. We assembled communities using a model in which species interactions are determined by allometric foraging rules of (1) handling time and (2) attack rates, and also (3) the distribution of body sizes. We systematically varied these three factors and examined their effects on three community level, food web allometries: the generality ‐ mass correlation, the vulnerability ‐ mass correlation and the trophic height ‐ mass correlation. The results demonstrate how allometries of individual foraging behaviour (handling time and attack rates) are linked across scales of organisation: different community level allometries are influenced by different individual level allometries. For example, generality allometries in the community are most affected by the individual allometric relationships of the attack rate, whereas trophic level allometries in the community are more strongly influenced by variation in individual handling time allometries. Importantly, we also find that the shape of the body size distribution from which species are drawn has a substantial influence on how these links between scales operate. This study suggests that understanding the variation of size structure among ecological networks requires knowledge about the causes of variation in individual foraging behaviour and determinants of the regional body size distribution.     

Combining geometric morphometrics with pattern recognition for the investigation of species complexes

The parasitoid Hymenoptera contain a large number of species complexes that are as yet unresolved by traditional taxonomic studies. Evolutionary studies as well as biological control programmes often require further investigations which cannot rely on simple qualitative morphological characters; in many cases, particularly with dried specimens housed in museums, molecular approaches cannot be used. Recent developments in geometric morphometrics and statistical exploratory approaches open new perspectives for the objective evaluation of morphological characters in this taxonomic context. In this study, geometric morphometrics and pattern recognition approaches were applied to the wing shape and venation of two closely related braconid species considered to differ by subtle qualitative morphological head characters. Exploratory analyses such as kernel density estimates and Gaussian mixture analyses were used to explore the structure of the data in the multivariate morphometric space. Discrimination techniques (linear discriminant functions and neural networks combined with cross‐validations) were used to estimate the taxonomic value of qualitative characters. Gaussian mixtures highlighted the existence of two non‐overlapping groups. A good congruence was found between one of the two groups and the a priori defined Bassus tumidulus. The misclassification rate was higher for B. tegularis specimens, which also appeared morphometrically heterogeneous. Discrimination between the two a priori defined species was incomplete with misclassification rates higher than, or equal to, 6%. In most cases, the lack of congruence between species and morphometrically defined subgroups could be related to specimens that exhibited ambiguous qualitative character states. In summary, if two entities are present, they still need to be defined morphologically, while B. tegularis heterogeneity calls for further investigation of specimens of known origin and hosts. © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 80, 89–98.     

Relationship between song characters and morphology in New World pigeons

We studied the pattern of variation in song characters among 16 New World pigeon species belonging to different taxonomic groups defined by morphological characters. Structural, temporal and frequency characters of the song were analysed. Principal components analyses showed that species belonging to the same taxonomic group were also grouped together by their song characters. In addition, individuals were correctly assigned into taxonomic groups by discriminant function analyses in more than 87.8% of cases. These analyses also showed that more than 87.5% of the individuals could be correctly classified by species when all song characters were included. Correct classification of individuals by species and taxonomic groups dropped when character types were analysed separately, thus showing that structural, as well as temporal and frequency characters are fundamental to define species- and group-specific identities of New World pigeon's songs. Correspondence between patterns of vocal and morphological variation found in this study can be a consequence of evolutionary changes in morphology affecting song production, as for example body size changes that constrain the syrinx to produce certain acoustic frequencies.     

Post-weaning cranial ontogeny in two bandicoots (Mammalia,Peramelomorphia, Peramelidae) and comparison with carnivorous marsupials

The ontogeny of the skull has been studied in several marsupial groups such as didelphids, microbiotheriids, and dasyurids. Here, we describe and compare the post-weaning ontogeny of the skull in two species of bandicoots, Echymipera kalubu (Echymiperinae) and Isoodon macrourus (Peramelinae), analyzing specific allometric trends in both groups, describing common (and specific) patterns, and discussing them on functional and phylogenetic grounds. Growth patterns were analyzed both qualitatively and quantitatively, including bivariate and multivariate analyses of allometry. We also evaluated character transformation and phylogenetic signals of the allometric patterns in several groups of marsupials and some placentals. We identified morphological changes between juvenile and adult stages in both species of peramelids, many related to the development of the trophic apparatus. Notable differences were detected in the patterns of growth, suggesting divergences in ontogenetic trajectories between both species. Both bivariate and multivariate methods indicate that positive allometries in E. kalubu apply to longitudinal dimensions, whereas in I. macrourus, positive allometries are restricted to vertical dimensions of the skull. The comparison of the allometric trends of two bandicoots with previously studied taxa reveals that although peramelids exhibit a particularly short gestation period and divergent morphology compared to other marsupials, their pattern does not show any particular trend. Some allometric trends seem to be highly conserved among the species studied, showing weak phylogenetic signal. Marsupials in general do not show particular patterns of post-weaning skull growth compared with placentals.     

Taxonomic versus allometric constraints on non‐linear interaction strengths

Recently, the importance of body mass and allometric scaling for the structure and dynamics of ecological networks has been highlighted in several ground‐breaking studies. However, advances in the understanding of generalities across ecosystem types are impeded to a considerable extent by a methodological dichotomy contrasting a considerable portion of marine ecology on the one hand opposite to traditional community ecology on the other hand. Many marine ecologists are bound to the taxonomy‐neglecting size spectrum approach when describing and analysing community patterns. In contrast, the mindset of the other school is focused on taxonomies according to the Linnean system at the cost of obscuring information due to applying species or population averages of body masses and other traits. Following other pioneering studies, we addressed this lingering gap, and studied non‐linear interaction strengths (i.e. functional responses) between two taxonomically‐distinct terrestrial arthropod predators (centipedes and spiders) of varying individual body masses and their prey. We fitted three non‐linear functional response models to the data: (1) a taxonomic model not accounting for variance in body masses amongst predator individuals, (2) an allometric model ignoring taxonomic differences between predator individuals, and (3) a combined model including body mass and taxonomic effects. Ranked according to their AICs, the combined model performs better than the allometric model, which provides a superior fit to the data than the taxonomic model. These results strongly indicate that the body masses of predator and prey individuals were responsible for most of the variation in non‐linear interaction strengths. Taxonomy explained some specific patterns in allometric exponents between groups and revealed mechanistic insights in predation efficiencies. Reconciling quantitative allometric models as employed by the marine size‐spectrum approach with taxonomic information may thus yield quantitative results that are generalized across ecosystem types and taxonomic groups. Using these quantitative models as novel null models should also strengthen subsequent taxonomic analyses.     

Variation in the ontogenetic allometry of horn length in bovids along a body mass continuum

Allometric relationships describe the proportional covariation between morphological, physiological, or life‐history traits and the size of the organisms. Evolutionary allometries estimated among species are expected to result from species differences in ontogenetic allometry, but it remains uncertain whether ontogenetic allometric parameters and particularly the ontogenetic slope can evolve. In bovids, the nonlinear evolutionary allometry between horn length and body mass in males suggests systematic changes in ontogenetic allometry with increasing species body mass. To test this hypothesis, we estimated ontogenetic allometry between horn length and body mass in males and females of 19 bovid species ranging from ca. 5 to 700 kg. Ontogenetic allometry changed systematically with species body mass from steep ontogenetic allometries over a short period of horn growth in small species to shallow allometry with the growth period of horns matching the period of body mass increase in the largest species. Intermediate species displayed steep allometry over long period of horn growth. Females tended to display shallower ontogenetic allometry with longer horn growth compared to males, but these differences were weak and highly variable. These findings show that ontogenetic allometric slope evolved across species possibly as a response to size‐related changes in the selection pressures acting on horn length and body mass.     

Geometric and traditional morphometrics for the assessment of character state identity: multivariate statistical analyses of character variation in the genus Arrenurus (Acari,Hydrachnidia, Arrenuridae)

Geometric and traditional morphometric approaches are tested to describe and reveal taxonomic characters and character states in variation of shape and size of idiosoma morphology in the Arrenuridae. Patterns of variation of idiosoma and glandularia features of males from 11 Mexican species of Arrenurus (Megaluracarus) and two species of subgenus Dadayella were explored with five landmark configurations and three sets of interlandmark distances. Separate principal component analyses (PCA) and canonical variate analyses (CVA) were performed for each data set. The eight multivariate analyses of variance among 13 a priori groups (species) detected significantly different morphometric variants, which were interpreted as different taxonomic character states. Patterns of character state similarity among species were examined with unweighted‐pair grouping method using averages (UPGMA) cluster analyses on Mahalanobis distances. Analyses of five landmark configurations revealed important taxonomical variation in the anterior idiosoma outline (10 character states), the outline of the posterior region or cauda (13 states), the distribution of postocularia, and the second and third pairs of dorsoglandularia (nine states), the fourth pair of dorsoglandularia (three states), and ventroglandularia on the posterior side of idiosoma (nine character states). Multivariate analyses of three sets of distance measurements also resulted in the detection of potential taxonomic characters related to idiosoma size (12 character states), postocularia and dorsoglandularia (13 states), and ventroglandularia (nine character states). Morphometric analyses of distances and shapes provide a formal basis for the interpretation of taxonomic characters, and for the discovery of character states. These characters should be investigated further in a wider sample of species for the phylogenetic systematics of these water mites. In the meantime, idiosoma regions and structures were tested for congruence in a phylogenetic analysis, and were proposed as homologous among the species sampled.     

Profile or group discriminative techniques? Generating reliable species distribution models using pseudo‐absences and target‐group absences from natural history collections

Aim The presence‐only data stored in natural history collections is the most important source of information available regarding the distribution of organisms. These data and profile techniques can be used to generate species distribution models (SDMs), but pseudo‐absences must be generated to use group discriminative techniques. In this study, we evaluated whether the SDMs generated with pseudo‐absences are reliable and also if there are differences in the results obtained with profile and group discriminative techniques. Location Ecuador, South America. Methods The SDMs were generated with a training data set for each of the five species of Anthurium and six different methods: two profile techniques (BIOCLIM and Gower’s distance index), three group discriminative techniques [logistic multiple regression (LMR), multivariate adaptative regression splines (MARS) and Maxent ] and a mixed modelling approach genetic algorithm for rule‐set production (GARP), which employs a combination of profile and group discriminative techniques and generates its own pseudo‐absences. For LMR, MARS and Maxent , three types of absences were generated: (1) random pseudo‐absences in equal number to presences and excluding a buffer area around presences (except for Maxent , which assumes that this background sample includes presences), (2) a large number (10,000) of random pseudo‐absences, also excluding a buffer area around each presence and (3) ‘target‐group absences’ (TGA), consisting of sites where other species of the group have been collected by the specialist, but not the species being modelled. To compare the predictive performance of the SDMs, the area under the curve statistic was calculated using an independent testing data set for each species. Results MARS, Maxent and LMR produce better results than the profile techniques. The models created with TGA are generally more accurate than those generated with pseudo‐absences. Main conclusions The advantages and disadvantages of different options for using pseudo‐absences and TGA with profile and group discriminative modelling techniques are explained and recommendations are made for the future.     

Multivariate analysis of morphological variation among closely related species Bromus japonicus, B. squarrosus and B. arvensis (Poaceae) in comparison with isozyme evidences

Morphological variation and taxonomic continuum of 110 specimens of Bromus arvensis, B. japonicus and B. squarrosus were analysed to assess the morphological variability of these close taxa. The importance of every morphological character was estimated by the GLM procedure. Stepwise discriminant analysis was used in order to find a set of morphological characters that maximises differences among the species. According to this, the most important characters appeared to be the length of anthers, width of lemma and lemma margin angle shape. The most important characters for the determination of Bromus arvensis was the length of anthers and for B. squarrosus width of lemma. According to the UPGMA cluster analysis, canonical discriminant, classificatory discriminant and principal component analyses, all specimens were separated into three moderately distinct groups which corresponded to the three traditional species. The study showed that qualitative characters were the best for the delimitation of the tax a by statistical analyses and demonstrated the incongruity between the pattern of morphological and genetic (allozyme) variation among the three Bromus species.     

Evolutionary trends in Tetrastigma (Vitaceae): Morphological diversity and taxonomic implications

Tetrastigma (Miq.) Planch. (Vitaceae) is a genus with ca. 100 species showing great morphological diversity. Previous molecular phylogenetic studies suggested that traditional classification systems are not consistent with the molecular phylogeny, and Tetrastigma is undergoing further systematic investigation. We traced the evolutionary trends of 20 morphological characters within a robust phylogenetic framework. Our results revealed that many morphological characters show either multiple transitions or few state changes, however, some characters show distinct variation. The two subgenera in Tetrastigma (subgen. Tetrastigma and subgen. Palmicirrata) based on unbranched/bifurcate versus digitately branched tendrils are not supported because subgen. Tetrastigma is paraphyletic. However, the unbranched versus bifurcate/digitately branched tendril is of taxonomic utility to characterize some of the major clades. Inflorescences in Tetrastigma appear axillary, but are leaf‐opposed on a compressed axillary shoot. We found most of the species in Tetrastigma retained the ancestral compound dichasial inflorescence, except those of clade IV that have derived pseudo‐umbellate inflorescences. Other characters including habit, leaf organization, and berry shape provide additional morphological support for the major clades. Our morphological analysis and recent molecular study suggest each of the five major clades within Tetrastigma be treated as distinct taxonomic sections (five sections in the genus).     

The limited value of traditional morphometric features in stromatoporoid taxonomy

The morphological variation of stromatoporoids, which are solitary organisms, is partitioned into its presumably genetic and environmental components. Potentially heritable, environmentally mediated and residual components of morphological variability were estimated in a test set containing Devonian stromatoporoids of the genus Gerronostromaria from southern Poland using analysis of variance. The taxonomic importance of traditional morphometric features is limited, because they are dominated by the intra‐skeletal component of variance. Conventional metrics were therefore replaced by stereological and textural quantities. Both stereological and textural features are dominated by the inter‐skeletal and inter‐locality components of variation and thus may be valuable in taxonomic and environmental studies of stromatoporoids. Statistical analyses of these characters (principal component analysis and cluster analysis) were performed. Of 13 characters considered most useful in taxonomic studies, only five have been used previously in conventional species definitions.     

Grass allometry and estimation of above‐ground biomass in tropical alpine tussock grasslands

The puna/páramo grasslands span across the highest altitudes of the tropical Andes, and their ecosystem dynamics are still poorly understood. In this study we examined the above‐ground biomass and developed species specific and multispecies power‐law allometric equations for four tussock grass species in Peruvian high altitude grasslands, considering maximum height (h_max), elliptical crown area and elliptical basal area. Although these predictors are commonly used among allometric literature, they have not previously been used for estimating puna grassland biomass. Total above‐ground biomass was estimated to be of 6.7 ± 0.2 Mg ha^?1 (3.35 ± 0.1 Mg C ha^?1). All allometric relationships fitted to similar power‐law models, with basal area and crown area as the most influential predictors, although the fit improved when tussock maximum height was included in the model. Multispecies allometries gave better fits than the other species‐specific equations, but the best equation should be used depending on the species composition of the target grassland. These allometric equations provide an useful approach for measuring above‐ground biomass and productivity in high‐altitude Andean grasslands, where destructive sampling can be challenging and difficult because of the remoteness of the area. These equations can be also applicable for establishing above‐ground reference levels before the adoption of carbon compensation mechanisms or grassland management policies, as well as for measuring the impact of land use changes in Andean ecosystems.     

Some ‘ant’swers: Application of a layered barcode approach to problems in ant taxonomy

DNA barcoding has emerged as a routine tool in modern taxonomy. Although straightforward, this approach faces new challenges, when applied to difficult situation such as defining cryptic biodiversity. Ants are prime examples for high degrees of cryptic biodiversity due to complex population differentiation, hybridization and speciation processes. Here, we test the DNA barcoding region, cytochrome c oxidase 1 and two supplementary markers, 28S ribosomal DNA and long‐wavelength rhodopsin, commonly used in ant taxonomy, for their potential in a layered, character‐based barcoding approach across different taxonomic levels. Furthermore, we assess performance of the character‐based barcoding approach to determine cryptic species diversity in ants. We found (i) that the barcode potential of a specific genetic marker varied widely among taxonomic levels in ants; (ii) that application of a layered, character‐based barcode for identification of specimens can be a solution to taxonomical challenging groups; (iii) that the character‐based barcoding approach allows us to differentiate specimens even within locations based on pure characters. In summary, (layered) character‐based barcoding offers a reliable alternative for problematic species identification in ants and can be used as a fast and cost‐efficient approach to estimate presence, absence or frequency of cryptic species.     

Identification of cryptic species of Miniopterus bats (Chiroptera: Miniopteridae) from Madagascar and the Comoros using bioacoustics overlaid on molecular genetic and morphological characters

The number of Miniopterus bat species on Madagascar and the nearby Comoros islands (Malagasy region) has risen from four to 11. These recently described cryptic taxa have been differentiated primarily based on molecular markers and associated a posteriori morphological characters that corroborate the different clades. Members of this Old World genus are notably conservative in morphology across their range. Several sites on Madagascar hold up to four small‐bodied taxa of this genus that are morphologically similar to one another, although they can be distinguished based on the tragus, an ear structure associated with echolocation. Miniopterus often emit species‐specific calls. In the present study, we analyze the bioacoustics of the 11 species of Miniopterus currently recognized from the Malagasy region, with an initial identification of the 87 recorded and collected individuals based on molecular markers and certain morphological characters. In most cases, bioacoustic parameters differentiate species and have taxonomic utility. Miniopterus griveaudi populations, which occur on three islands (Madagascar, Anjouan, and Grande Comore), showed no significant differences in peak echolocation frequencies. After running a discriminant function analysis based on five bioacoustic parameters, some mismatched assignments of Malagasy species were found, which include allopatric sister‐taxa and sympatric, phylogenetically not closely‐related species of similar body size. Because the peak echolocation frequencies of two species (Miniopterus sororculus and Miniopterus aelleni) were independent of body size, they were acoustically distinguishable from cryptic sympatric congeners. The small variation around the allometric relationship between body size and peak echolocation frequency of Malagasy Miniopterus species suggests that intraspecific communication rather than competition or prey detection may be the driver for the acoustic divergence of these two species. Our well‐defined echolocation data allow detailed ecological work to commence aiming to test predictions about the relative roles of competition, prey availability, and social communication on the evolution of echolocation in Malagasy Miniopterus species. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 284–302.     

Flower-fruit size allometry at three taxonomic levels in Crepis (Asteraceae)

The present investigation utilizes the major axis technique to examine the allometric relationship between flower and fruit size, two developmentally related characters. Regression of log (corolla length) on log (fruit length) using data from 188 species of Crepis , 52 populations of C. tectorum and 40 sibships from a population of C. tectorum demonstrated that flower size shows a decelerating increase with increasing fruit size at all taxonomic levels, with the allometric slope varying from 0.53 to 0.69. The null hypothesis of isometry was rejected in analyses using species or sibships as observations, while the comparison of populations revealed a slope significantly different from 1 only if two outliers were excluded from the analysis. Numerous species and populations have escaped the constraint linking flower and fruit size, including C. tectorum (which has a high ratio of flower to fruit size within the genus) and C. tectorum subsp. pumila (which has a high ratio of flower to fruit size within the species).     

MOLECULAR AND MORPHOMETRIC DATA PINPOINT SPECIES BOUNDARIES IN HALIMEDA SECTION RHIPSALIS (BRYOPSIDALES,CHLOROPHYTA)1

Molecular systematic studies have changed the face of algal taxonomy. Particularly at the species level, molecular phylogenetic research has revealed the inaccuracy of morphology‐based taxonomy: Cryptic and pseudo‐cryptic species were shown to exist within many morphologically conceived species. This study focused on section Rhipsalis of the green algal genus Halimeda. This section was known to contain cryptic diversity and to comprise species with overlapping morphological boundaries. In the present study, species diversity within the section and identity of individual specimens were assessed using ITS1–5.8S–ITS2 (nrDNA) and rps3 (cpDNA) sequence data. The sequences grouped in a number of clear‐cut genotypic clusters that were considered species. The same specimens were subjected to morphometric analysis of external morphological and anatomical structures. Morphological differences between the genotypic cluster species were assessed using discriminant analysis. It was shown that significant morphological differences exist between genetically delineated species and that allocation of specimens to species on the basis of morphometric variables is nearly perfect. Anatomical characters yielded better results than external morphological characters. Two approaches were offered to allow future morphological identifications: a probabilistic approach based on classification functions of discriminant analyses and the classical approach of an identification key.     

Tree height–diameter allometry across the United States

The relationship between tree height and diameter is fundamental in determining community and ecosystem structure as well as estimates of biomass and carbon storage. Yet our understanding of how tree allometry relates to climate and whole organismal function is limited. We used the Forest Inventory and Analysis National Program database to determine height–diameter allometries of 2,976,937 individuals of 293 tree species across the United States. The shape of the allometric relationship was determined by comparing linear and nonlinear functional forms. Mixed‐effects models were used to test for allometric differences due to climate and floristic (between angiosperms and gymnosperms) and functional groups (leaf habit and shade tolerance). Tree allometry significantly differed across the United States largely because of climate. Temperature, and to some extent precipitation, in part explained tree allometric variation. The magnitude of allometric variation due to climate, however, had a phylogenetic signal. Specifically, angiosperm allometry was more sensitive to differences in temperature compared to gymnosperms. Most notably, angiosperm height was more negatively influenced by increasing temperature variability, whereas gymnosperm height was negatively influenced by decreasing precipitation and increasing altitude. There was little evidence to suggest that shade tolerance influenced tree allometry except for very shade‐intolerant trees which were taller for any given diameter. Tree allometry is plastic rather than fixed and scaling parameters vary around predicted central tendencies. This allometric variation provides insight into life‐history strategies, phylogenetic history, and environmental limitations at biogeographical scales.