Shaping up: a geometric morphometric approach to assemblage ecomorphology

This study adopts an ecomorphological approach to test the utility of body shape as a predictor of niche relationships among a stream fish assemblage of the Tickfaw River (Lake Pontchartrain Basin) in southeastern Louisiana, U.S.A. To examine the potential influence of evolutionary constraints, analyses were performed with and without the influence of phylogeny. Fish assemblages were sampled throughout the year, and ecological data (habitat and tropic guild) and body shape (geometric morphometric) data were collected for each fish specimen. Multivariate analyses were performed to examine relationships and differences between body shape and ecological data. Results indicate that a relationship exists between body shape and trophic guild as well as flow regime, but no significant correlation between body shape and substratum was found. Body shape was a reliable indicator of position within assemblage niche space.     

Bentho-Pelagic Divergence of Cichlid Feeding Architecture Was Prodigious and Consistent during Multiple Adaptive Radiations within African Rift-Lakes

Background

How particular changes in functional morphology can repeatedly promote ecological diversification is an active area of evolutionary investigation. The African rift-lake cichlids offer a calibrated time series of the most dramatic adaptive radiations of vertebrate trophic morphology yet described, and the replicate nature of these events provides a unique opportunity to test whether common changes in functional morphology have repeatedly facilitated their ecological success.

Methodology/Principal Findings

Specimens from 87 genera of cichlid fishes endemic to Lakes Tanganyka, Malawi and Victoria were dissected in order to examine the functional morphology of cichlid feeding. We quantified shape using geometric morphometrics and compared patterns of morphological diversity using a series of analytical tests. The primary axes of divergence were conserved among all three radiations, and the most prevalent changes involved the size of the preorbital region of the skull. Even the fishes from the youngest of these lakes (Victoria), which exhibit the lowest amount of skull shape disparity, have undergone extensive preorbital evolution relative to other craniofacial traits. Such changes have large effects on feeding biomechanics, and can promote expansion into a wide array of niches along a bentho-pelagic ecomorphological axis.

Conclusions/Significance

Here we show that specific changes in trophic anatomy have evolved repeatedly in the African rift lakes, and our results suggest that simple morphological alterations that have large ecological consequences are likely to constitute critical components of adaptive radiations in functional morphology. Such shifts may precede more complex shape changes as lineages diversify into unoccupied niches. The data presented here, combined with observations of other fish lineages, suggest that the preorbital region represents an evolutionary module that can respond quickly to natural selection when fishes colonize new lakes. Characterizing the changes in cichlid trophic morphology that have contributed to their extraordinary adaptive radiations has broad evolutionary implications, and such studies are necessary for directing future investigations into the proximate mechanisms that have shaped these spectacular phenomena.     

Morphological correlates with diet of fish assemblages in brush park fisheries of tropical estuaries

Brush park fishery in Negombo estuary, Sri Lanka is a traditional fishing practice which relies on fishes attracted to artificial woody fish aggregation devices. This study investigates whether constituent species in these brush parks exhibit morphological variations in relation to their dietary habits. Fishes caught in brush parks were sampled from April 2014 to April 2016 covering rainy, intermediate and dry seasons. There were 817 specimens of 46 species belonging to 24 families. From each specimen, 17 morphological attributes were determined and diet composition of each species was analyzed in terms of relative biovolume. Trophic index of each species estimated from the proportions of dietary items and their possible trophic level in the community was significantly related to two body proportions (Maximum body height/Maximum body width and Total length/ Maximum body height) which described shape of fish. Principal component analysis of morphometric attributes and dietary habits indicated that the species in the higher trophic levels are characterized by slender, long-body shapes and those occupy lower trophic levels are predominantly laterally compressed with deep body shapes. As such, structure of coexisting species in brush parks of Negombo estuary is predominantly along the trophic dimension and is related to morphological traits of constituent species. The predictive power of ecomorphological correlates with diets of fish species other than mugilids which are attracted to brush parks, can therefore be considered as a useful tool for conducting rapid ecological assessment.     

Exploring the nature of ecological specialization in a coral reef fish community: morphology,diet and foraging microhabitat use

Patterns of ecological specialization offer invaluable information about ecosystems. Yet, specialization is rarely quantified across several ecological niche axes and variables beyond the link between morphological and dietary specialization have received little attention. Here, we provide a quantitative evaluation of ecological specialization in a coral reef fish assemblage (f. Acanthuridae) along one fundamental and two realized niche axes. Specifically, we examined ecological specialization in 10 surgeonfish species with regards to morphology and two realized niche axes associated with diet and foraging microhabitat utilization using a recently developed multidimensional framework. We then investigated the potential relationships between morphological and behavioural specialization. These relationships differed markedly from the traditional ecomorphological paradigm. While morphological specialization showed no relationship with dietary specialization, it exhibited a strong relationship with foraging microhabitat specialization. However, this relationship was inverted: species with specialized morphologies were microhabitat generalists, whereas generalized morphotypes were microhabitat specialists. Interestingly, this mirrors relationships found in plant–pollinator communities and may also be applicable to other ecosystems, highlighting the potential importance of including niche axes beyond dietary specialization into ecomorphological frameworks. On coral reefs, it appears that morphotypes commonly perceived as most generalized may, in fact, be specialized in exploiting flat and easily accessible microhabitats.     

Ecomorphological diversity of freshwater fishes as a tool for conservation priority setting: a case study from a Balkan hotspot

Biodiversity studies commonly focus on taxonomic diversity measures such as species richness and abundance. However, alternative measures based on ecomorphological traits are also critical for unveiling the processes shaping biodiversity and community assembly along environmental gradients. Our study presents the first analysis of habitat-trait-community structure in a Balkan biodiversity hotspot (Louros river, NW Greece), through the investigation of the relationships among freshwater fish assemblages’ composition, morphological traits and habitat features. In order to provide a hierarchical classification of species’ priority to protection measures, we highlight the most ecomorphologically distinct species using originality analysis. Our results suggest that the longitudinal changes of habitat variables (water temperature, depth, substrate, altitude) drive the local fish assemblages’ structure highlighting the upstream-downstream gradient. We also present evidence for environmental filtering, establishing fish assemblages according to their ecomorphological traits. The calculation of the seven available indices of ecomorphological originality indicates that Valencia letourneuxi and Cobitis hellenica, which are endemic to Louros and threatened with extinction, exhibited the highest distinctiveness; thus their protection is of great importance. The methodological approach followed and the patterns described herein can contribute further to the application of community ecology theory to conservation, highlighting the need to use ecomorphological traits as a useful ‘tool’.     

Morphological-dietary relationships within two assemblages of marine demersal fishes

In this study we have used morphological characters related to feeding and prey capture and dietary data to investigate the trophic organization within two assemblages of marine demersal fishes. Morphological and dietary disparities within fish assemblages were estimated from species similarities based on Euclidean distances plus species projections on the principal axes from multivariate analyses. The analyses of the morphological variables indicated that species in each assemblage comprised morphologically distinct groups strongly influenced by trophically linked characters. Stomach content analyses revealed that fish species in each assemblage were classified into three basic feeding groups: polychaete-shrimp feeders, crab feeders and fish feeders. These results indicated that food resource partitioning was operating within each assemblage. However, when morphological and trophic data were compared no significant correlations were found. The results did not particularly support the ecomorphological hypothesis that dietary differences are due to morphological differences, since similar diets do not correspond to similar morphologies. The patterns of trophic organization within the fish assemblages examined, possibly reflect differences among species due not only to the effect of ecological demands on morphology but also by their evolutionary history and constructional constraints imposed by phylogeny. This revised version was published online in August 2006 with corrections to the Cover Date.     

Does morphology predict behavior? Correspondence between behavioral and morphometric data in a Tyrant‐flycatcher (Tyrannidae) assemblage in the Santa Marta Mountains,Colombia

ABSTRACT Morphology is commonly used as a predictor of ecological relationships among species when studying local assemblages of Neotropical birds. Nevertheless, most evidence supporting ecomorphological correspondence in birds comes from studies of communities and not from local assemblages and, moreover, from temperate latitudes. To increase our understanding of ecomorphological correspondence in Neotropical assemblages, we used three multivariate approaches to evaluate correspondence between morphological and foraging behavior data in a tyrant‐flycatcher assemblage (N= 12 species) in the Santa Marta Mountains in Colombia. Principal components analyses revealed similar species ordinations when using morphological measurements (beak size and shape, tarsus length, wing length, and tail length) or behavioral data (behavioral types of searching for prey and prey capture) separately. Discriminant function analyses tested the ability of morphological traits to predict foraging behavior, showing that more than 90% of all measured individuals (N= 267) were correctly classified in previously defined categories of search and attack behavior. Finally, Canonical correlation analyses revealed a significant correlation between morphological data and two independent datasets of search and attack behavior. Our results demonstrate that morphology can accurately predict ecology in an assemblage of Neotropical tyrannids, and similar results have been reported in previous studies of temperate Tyrant‐flycatchers. Our results also show that bill size and shape, wing length, and tarsus length are the best predictors of foraging behavior in this assemblage. Testing for ecomorphological correspondence in other Neotropical taxa would help identify subsets of phenotypic traits that could be used for a practical, but reliable, determination of ecological relationships within different assemblages.     

Ecomorphological analysis as a complementary tool to detect changes in fish communities following major perturbations in two South African estuarine systems

Ecomorphological changes as a result of natural perturbations in estuarine fish communities were investigated in two South African estuaries (Swartvlei and East Kleinemonde), both before and after the loss of aquatic macrophyte beds in these systems. The fish communities were analysed using an ecomorphological diversity index (EMI) and the results compared to a traditional index, the Shannon-Wiener diversity index. The EMI revealed that the major changes in fish community composition recorded in both estuaries were associated with quantitative variations at the species level. Both estuaries essentially lost their macrophyte beds and ended up with the same type of bottom habitat (bare sediment). In both cases the fish morphological variability decreased immediately after aquatic macrophyte loss and then increased to end above the initial value. The ecomorphological analysis appeared to be sensitive to major ecological disturbances that occurred during the study period and this was confirmed by the morphospace configuration. The results indicate that the ecomorphology of the fish community responds to habitat changes and that this change corresponds to alterations in the representation of the different feeding types. These findings therefore contribute to the measurement of morphological changes in estuarine fish assemblages as a result of habitat changes within the ecosystem and we propose that ecomorphological analyses add another dimension to the information provided by existing diversity indices in studying changing fish communities.     

Ecomorphology of morpho‐functional relationships in the family of sparidae: A quantitative statistic approach

In many fish species, morphological similarity can be considered as a proxy for similarities in habitat use. The Sparidae family includes species that are recognized for common morphological features such as structure and positioning of the fins and specialized dentition. The aim of this study was to quantitatively describe the relationship of body shape morphology with habitat use, trophic level, and systematics in the majority of known Sparidae species (N = 92). This ecomorphological comparison was performed with a geometric morphometric approach considering as variables the Trophic Index (TROPH), the habitat (i.e., classified as demersal, benthopelagic and reef associated) and the phylogenetic relationship of species at the subfamily level. The analysis by the TROPH variable showed a positive relation with shape because the morphological features of all the species are strongly correlated with their trophic behavior (e.g., herbivore species have a smaller mouth gap that make them able to feed upon sessile resources). The morphological analysis according to the Habitat variable was used to classify species according to a feeding‐habitat niche in terms of portion of the water column and seabed space where species mostly perform their behavioral activities. We described three kinds of morphological designs in relation to a benthopelagic, demersal and reef‐associated habit. The six subfamily groups were morphologically well distinguishable and the cladogram relative to Mahalanobis' morphological distances was compared with those proposed by other authors. We also quantified the phylogenetic relationship among the different subfamilies based on the analysis of shape in relation to trophic ecology, confirming the observations of the authors. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

Seasonal changes in morphological structuring in a guild of benthic stream fishes

Summary The ecomorphological model which attempts to identify important variation in the total morphology of groups of animals has been used with some success in communities of fishes. The applicability of the model to subsets of the community, such as guilds of ecologically similar species, is uncertain, and the effects of the possible changes in correlations among morphological variables caused by demographic changes across seasons is unknown. An ecomorphological model is applied to a guild of benthic stream fishes from the Tombigbee River, Mississippi. The model is found to describe structuring in the guild based on aspects of the trophic morphology and the length of the body. Morphologically distinct groups of species are described by the model. The effect of indeterminate growth seems not to be of sufficient magnitude to change groupings across seasons. However, species associations within morphological groups change seasonally. I conclude that ecomorphological models may be properly applied to community subsets, but the interpretation of the model must consider the nature of the data set with respect of seasonality.     

Rare ecomorphological convergence on a complex adaptive landscape: Body size and diet mediate evolution of jaw shape in squirrels (Sciuridae)

Convergence is widely regarded as compelling evidence for adaptation, often being portrayed as evidence that phenotypic outcomes are predictable from ecology, overriding contingencies of history. However, repeated outcomes may be very rare unless adaptive landscapes are simple, structured by strong ecological and functional constraints. One such constraint may be a limitation on body size because performance often scales with size, allowing species to adapt to challenging functions by modifying only size. When size is constrained, species might adapt by changing shape; convergent shapes may therefore be common when size is limiting and functions are challenging. We examine the roles of size and diet as determinants of jaw shape in Sciuridae. As expected, size and diet have significant interdependent effects on jaw shape and ecomorphological convergence is rare, typically involving demanding diets and limiting sizes. More surprising is morphological without ecological convergence, which is equally common between and within dietary classes. Those cases, like rare ecomorphological convergence, may be consequences of evolving on an adaptive landscape shaped by many‐to‐many relationships between ecology and function, many‐to‐one relationships between form and performance, and one‐to‐many relationships between functionally versatile morphologies and ecology. On complex adaptive landscapes, ecological selection can yield different outcomes.     

A phylogenetic analysis of sex-specific evolution of ecological morphology in <Emphasis Type="Italic">Liolaemus</Emphasis> lizards

Adaptive radiation theory predicts that phenotypic traits involved in ecological performance evolve in different directions in populations subjected to divergent natural selection, resulting in the evolution of ecological diversity. This idea has largely been supported through comparative studies exploring relationships between ecological preferences and quantitative traits among different species. However, intersexual perspectives are often ignored. Indeed, although it is well established that intersexual competition and sex-specific parental and reproductive roles may often subject sex-linked phenotypes to antagonistic selection effects, most ecomorphological research has explored adaptive evolution on a single sex, or on means obtained from both sexes together. The few studies taking sexual differences into account reveal the occurrence of sex-specific ecomorphs in some clades of lizards, and conclude that the independent contribution of the sexes to the morphological diversity produced by adaptive radiation can be substantial. Here, we investigate whether microhabitat use results in the evolution of sex-specific ecomorphs across 44 Liolaemus lizard species. We found that microhabitat structure does not predict variation in body size and shape in either of the sexes. Yet, we found that males and females tend to occupy significantly different positions in multivariate morphological spaces, indicating that treating males and females as ecologically and phenotypically equivalent units may lead to incomplete or mistaken estimations of the diversity produced by adaptive evolution.     

庞泉沟自然保护区华北落叶松林的自组织特征映射网络分类与排序

自组织特征映射网络（SOM）是新近引入植物生态学的分析方法,对复杂问题和非线性问题具有较强的分析和求解功能。本研究应用SOM分类和排序研究了庞泉沟自然保护区华北落叶松林。研究结果表明,SOM将120个样方分为7个植物群落类型,分类结果具有明确的生态意义;样方和物种在SOM训练图上呈现一定规律的分布;7个群落类型各有其分布范围和界限,揭示了群落间的生态关系。在此基础上,通过引入一种在SOM训练图上可视化环境因子梯度的方法,能够较好地完成样方、物种和环境因子相互关系的分析,揭示了海拔是影响该区华北落叶松林生长和分布的最主要因子。生态分析表明SOM分类和排序是一种有效的梯度分析方法,适用于表征生态特征和探索群落和环境相互关系的研究。     

Should congruence between intra- and interspecific ecomorphological relationships be expected? A case study with the great tit,Parus major

We studied the relationship between leg morphology and posture while feeding in a population of great tits (Parus major) under controlled conditions to investigate to what extent morphology and ecology are linked at the individual level. From predictions generated at the interspecific level within the genus Parus (Moreno and Carrascal 1993), we tested whether intra- and interspecific ecomorphological relationships are consistent. Within our population, neither leg bone lengths nor leg muscle morphology were related to the feeding posture of individuals. However, differences in body weight were correlated with inter-individual differences in time spent hanging. These results demonstrate that the association between intra- and interspecific ecomorphological relationships is not uniform. We argue that, at the intraspecific level, body weight overrides the significance of other traits that have a functional meaning at the interspecific level (i.e. leg segment lengths, muscular morphology), due to isometric variation of morphological traits (muscular and skeletal) with body mass. Thus, the discrepancy between the ecomorphological associations at intra- and interspecific levels is the result of a problem of scale (morphological changes in evolutionary time and isometric variation of morphological traits with body mass in ecological time).     

Discrete foraging niches promote ecological, phenotypic, and genetic divergence in sympatric whitefish (Coregonus lavaretus)

Natural populations often vary in their degree of ecological, morphological and genetic divergence. This variation can be arranged along an ecological speciation continuum of increasingly discrete variation, with high inter-individual variation at one end and well defined species in the other. In postglacial fishes, evolutionary divergence has commonly resulted in the co-occurrence of a pelagic and a benthic specialist. We studied three replicate lakes supporting sympatric pelagic and benthic European whitefish (Coregonus lavaretus (L.)) morphs in search for early signs of possible further divergence into more specialized niches. Using stomach content data (recent diet) and stable isotope analyses (time-integrated measure of trophic niche use), we observed a split in the trophic niche within the benthic whitefish morph, with individuals specializing on either littoral or profundal resources. This divergence in resource use was accompanied by small but significant differences in an adaptive morphological trait (gill raker number) and significant genetic differences between fish exploiting littoral and profundal habitats and foraging resources. The same pattern of parallel divergence was found in all three lakes, suggesting similar natural selection pressures driving and/or maintaining the divergence. The two levels of divergence (a clear and robust benthic – pelagic and a more subtle littoral – profundal divergence) observed in this study apparently represent different stages in the process of ecological speciation.     

Ecomorphological disparity in an adaptive radiation: opercular bone shape and stable isotopes in Antarctic icefishes

To assess how ecological and morphological disparity is interrelated in the adaptive radiation of Antarctic notothenioid fish we used patterns of opercle bone evolution as a model to quantify shape disparity, phylogenetic patterns of shape evolution, and ecological correlates in the form of stable isotope values. Using a sample of 25 species including representatives from four major notothenioid clades, we show that opercle shape disparity is higher in the modern fauna than would be expected under the neutral evolution Brownian motion model. Phylogenetic comparative methods indicate that opercle shape data best fit a model of directional selection (Ornstein–Uhlenbeck) and are least supported by the “early burst” model of adaptive radiation. The main evolutionary axis of opercle shape change reflects movement from a broad and more symmetrically tapered opercle to one that narrows along the distal margin, but with only slight shape change on the proximal margin. We find a trend in opercle shape change along the benthic–pelagic axis, underlining the importance of this axis for diversification in the notothenioid radiation. A major impetus for the study of adaptive radiations is to uncover generalized patterns among different groups, and the evolutionary patterns in opercle shape among notothenioids are similar to those found among other adaptive radiations (three‐spined sticklebacks) promoting the utility of this approach for assessing ecomorphological interactions on a broad scale.     

Ecomorphological correlates in tropical stream fishes of southern India

Synopsis I studied ecomorphological correlations in 18 stream fish species (belonging to five families) commonly occurring in diversity rich habitats of rivers in the central Western Ghats (Southern India). Univariate and multivariate analyses indicated a clear segregation of species in morphological and ecological (habitat) space. Cluster analyses using morphological features segregated species based mainly on their body shape and feeding parameters while habitat parameters segregated species according to their position along the water column and preference to runs or pool habitats. Principal component analyses showed that body size, head dimensions, mouth position and eye diameter were important characters for species segregation in morphological space while run or pool habitat type and the position of the fish in the water column best explained segregation of species in habitat space. Consistencies in some of the species clusters obtained from analyses on morphological characteristics and habitat preferences warrant closer examination of the relationships between them. These were studied employing multivariate methods like canonical correspondence analysis and the Mantel test. The tests revealed weak correlations indicating that in addition to morphology, other factors like behavioural, physiological and evolutionary constraints together are likely to play an important role in ecosystem structuring of these complex tropical assemblages.     

Inadequacy of species-level designations for ecological studies of coastal migratory fishes

Synopsis The species is not always appropriate as a unit of measure when used in quantitative ecological studies. Analyses of fish trophic relationships in coastal areas indicate that, in many instances, more substantial ecological differences exist among life stages of a given species than among similar trophic units of different species. The use of a species in quantitative ecological studies can lead to problems of interpretation concerning the relationships of coastal fishes to complex habitats. Use of the species as a convenient unit of measure substitutes a basically taxonomic entity for more relevant life-history stages in ecological determinations. Niche breadth of a given species can be so extensive that quantitative determinations of significant ecological processes are difficult to make. Migratory coastal fishes undergo diverse ontogenetic trophic transformations. Without adequate recognition of the complex ecological stages that characterize such fishes, the oversimplification that characterizes many ecological studies in coastal areas will continue. This simplification, and the attendant overgeneralization that follows, tends to add to the continuing problem of unverified models and the inability to identify causal relationships in estuarine and coastal systems. Quantitative ecological studies would benefit from an approach that includes the use of identifiable, ontological trophic entities.     

SPECIES FLOCK IN THE NORTH AMERICAN GREAT LAKES: MOLECULAR ECOLOGY OF LAKE NIPIGON CISCOES (TELEOSTEI: COREGONIDAE: COREGONUS)

Studies on north temperate fish species indicate that new habitat availability following the last ice sheet retreat has promoted ecological speciation in postglacial lakes. Extensive ecophenotypic polymorphisms observed among the North American Great Lakes ciscoes suggest that this fish group has radiated through trophic adaptation and reproductive isolation. This study aims at relating the ecomorphological and genetic polymorphisms expressed by the Lake Nipigon ciscoes to evaluate the likelihood of an intralacustrine divergence driven by the exploitation of alternative resources. Morphological variation and trophic and spatial niches are characterized and contrasted among 203 individuals. Genetic variation at six microsatellite loci is also analyzed to appraise the extent of genetic differentiation among these morphotypes. Ecomorphological data confirm the existence of four distinct morphotypes displaying various levels of trophic and depth niche overlap and specialization. However, ecological and morphological variations were not coupled as expected, suggesting that trophic morphology is not always predictive of ecology. Although extensive genetic variability was observed, little genetic differentiation was found among morphotypes, with only one morph being slightly but significantly differentiated. Contrasting patterns of morphological, ecological, and genetic polymorphisms did not support the hypothesis of ecological speciation: the most ecologically different forms were morphologically most similar, while the only genetically differentiated morph was the least ecologically specialized. The low levels of genetic differentiation and the congruence between θ and φ estimates altogether suggest a recent (most likely postglacial) process of divergence and/or high gene flow among morphs A, C, and D, whereas higher φ estimates for comparison involving morph B suggest that this morph may be derived from another colonizing lineage exchanging little genes with the other morphs. Patterns of ecophenotypic and genetic diversity are also compatible with a more complex evolutionary history involving hybridization and introgression.     

Evolutionary convergence in Neotropical cichlids and Nearctic centrarchids: evidence from morphology,diet, and stable isotope analysis

Despite divergent evolutionary histories, Neotropical cichlids (Cichlidae) and Nearctic sunfishes (Centrarchidae) appear to have similar functional morphotypes and occupy similar ecological niches. We applied an integrative approach analyzing morphological traits, stomach contents, and stable isotope ratios (δ¹³C, δ¹⁵N) to investigate whether local assemblages of cichlids (Venezuela, Peru) and centrarchids (Texas) reveal one‐to‐one patterns of morphological and ecological convergence. Multivariate ordinations performed on diet and morphology datasets identified a broad overlap between cichlid and centrarchid assemblages. The functional morphology of the two groups has diversified in a convergent manner within the confines of ram‐suction modes of prey ingestion. Both groups had the same set of ecomorph types that corresponded to the same trophic niches, including substrate‐sifting invertivores, epibenthic invertebrate gleaners, and piscivores; the one exception was a molluscivorous sunfish, comprising a niche that was not represented in the two cichlid assemblages. Estimates of trophic positions based on stable isotope analysis revealed convergent vertical trophic structure; with few exceptions, fishes with similar morphologies had similar trophic positions. Large‐bodied piscivores had highest trophic positions, whereas small and medium‐bodied generalists and invertivores had low to intermediate trophic positions. Consistent patterns of ecomorphological convergence in these two perciform groups provide strong evidence for adaptation involving constrains in functional morphology associated with feeding. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 146–164.