Are rates of species diversification correlated with rates of morphological evolution?

Some major evolutionary theories predict a relationship between rates of proliferation of new species (species diversification) and rates of morphological divergence between them. However, this relationship has not been rigorously tested using phylogeny-based approaches. Here, we test this relationship with morphological and phylogenetic data from 190 species of plethodontid salamanders. Surprisingly, we find that rates of species diversification and morphological evolution are not significantly correlated, such that rapid diversification can occur with little morphological change, and vice versa. We also find that most clades have undergone remarkably similar patterns of morphological evolution (despite extensive sympatry) and that those relatively novel phenotypes are not associated with rapid diversification. Finally, we find a strong relationship between rates of size and shape evolution, which has not been previously tested.     

Phylogenetic effects, the loss of complex characters, and the evolution of development in calyptraeid gastropods

Abstract Despite considerable theoretical and empirical work on the population genetic effects of mode of development in benthic marine invertebrates, it is unclear what factors generate and maintain interspecific variation in mode of development and few studies have examined such variation in a phylogenetic context. Here I combine data on mode of development with a molecular phylogeny of 72 calyptraeid species to test the following hypotheses about the evolution of mode of development: (1) Is the loss of feeding larvae irreversible? (2) Is there a phylogenetic effect on the evolution of mode of development? (3) Do embryos of direct‐developing species lose the structures necessary for larval feeding and swimming and, if so, is the degree of embryonic modification correlated with the genetic distance between species? The results of these analyses suggest that mode of development evolves rapidly and with little phylogenetic inertia. There are three cases of the possible regain of feeding larvae, in all cases from direct development with nurse eggs. It appears that species with planktotrophic, lecithotrophic, or direct development with nurse eggs all have equal evolutionary potential and retain the possibility of subsequent evolution of a different mode of development. However, species with direct development from large yolky eggs appear to be subject to phylogenetic constraints and may not be able to subsequently evolve a different mode of development. Finally, species that have more recently evolved direct development have less highly modified embryos than older direct‐developing species. Since species with nurse eggs generally have fewer embryonic modifications than those from large yolky eggs, this embryological difference may be the underlying cause of the difference in evolutionary potential.     

The utility of cranial ontogeny for phylogenetic inference: a case study in crocodylians using geometric morphometrics

The degree to which the ontogeny of organisms could facilitate our understanding of phylogenetic relationships has long been a subject of contention in evolutionary biology. The famed notion that ‘ontogeny recapitulates phylogeny’ has been largely discredited, but there remains an expectation that closely related organisms undergo similar morphological transformations throughout ontogeny. To test this assumption, we used three‐dimensional geometric morphometric methods to characterize the cranial morphology of 10 extant crocodylian species and construct allometric trajectories that model the post‐natal ontogenetic shape changes. Using time‐calibrated molecular and morphological trees, we employed a suite of comparative phylogenetic methods to assess the extent of phylogenetic signal in these trajectories. All analyses largely demonstrated a lack of significant phylogenetic signal, indicating that ontogenetic shape changes contain little phylogenetic information. Notably, some Mantel tests yielded marginally significant results when analysed with the morphological tree, which suggest that the underlying signal in these trajectories is correlated with similarities in the adult cranial morphology. However, despite these instances, all other analyses, including more powerful tests for phylogenetic signal, recovered statistical and visual evidence against the assumption that similarities in ontogenetic shape changes are commensurate with phylogenetic relatedness and thus bring into question the efficacy of using allometric trajectories for phylogenetic inference.     

Do different disparity proxies converge on a common signal? Insights from the cranial morphometrics and evolutionary history of Pterosauria (Diapsida: Archosauria)

Disparity, or morphological diversity, is often quantified by evolutionary biologists investigating the macroevolutionary history of clades over geological timescales. Disparity is typically quantified using proxies for morphology, such as measurements, discrete anatomical characters, or geometric morphometrics. If different proxies produce differing results, then the accurate quantification of disparity in deep time may be problematic. However, despite this, few studies have attempted to examine disparity of a single clade using multiple morphological proxies. Here, as a case study for this question, we examine the disparity of the volant Mesozoic fossil reptile clade Pterosauria, an intensively studied group that achieved substantial morphological, ecological and taxonomic diversity during their 145+ million-year evolutionary history. We characterize broadscale patterns of cranial morphological disparity for pterosaurs for the first time using landmark-based geometric morphometrics and make comparisons to calculations of pterosaur disparity based on alternative metrics. Landmark-based disparity calculations suggest that monofenestratan pterosaurs were more diverse cranially than basal non-monofenestratan pterosaurs (at least when the aberrant anurognathids are excluded), and that peak cranial disparity may have occurred in the Early Cretaceous, relatively late in pterosaur evolution. Significantly, our cranial disparity results are broadly congruent with those based on whole skeleton discrete character and limb proportion data sets, indicating that these divergent approaches document a consistent pattern of pterosaur morphological evolution. Therefore, pterosaurs provide an exemplar case demonstrating that different proxies for morphological form can converge on the same disparity signal, which is encouraging because often only one such proxy is available for extinct clades represented by fossils. Furthermore, mapping phylogeny into cranial morphospace demonstrates that pterosaur cranial morphology is significantly correlated with, and potentially constrained by, phylogenetic relationships.     

A targeted next‐generation sequencing toolkit for exon‐based cichlid phylogenomics

Cichlid fishes (family Cichlidae) are models for evolutionary and ecological research. Massively parallel sequencing approaches have been successfully applied to study relatively recent diversification in groups of African and Neotropical cichlids, but such technologies have yet to be used for addressing larger‐scale phylogenetic questions of cichlid evolution. Here, we describe a process for identifying putative single‐copy exons from five African cichlid genomes and sequence the targeted exons for a range of divergent (>tens of millions of years) taxa with probes designed from a single reference species (Oreochromis niloticus, Nile tilapia). Targeted sequencing of 923 exons across 10 cichlid species that represent the family's major lineages and geographic distribution resulted in a complete taxon matrix of 564 exons (649 549 bp), representing 559 genes. Maximum likelihood and Bayesian analyses in both species tree and concatenation frameworks yielded the same fully resolved and highly supported topology, which matched the expected backbone phylogeny of the major cichlid lineages. This work adds to the body of evidence that it is possible to use a relatively divergent reference genome for exon target design and successful capture across a broad phylogenetic range of species. Furthermore, our results show that the use of a third‐party laboratory coupled with accessible bioinformatics tools makes such phylogenomics projects feasible for research groups that lack direct access to genomic facilities. We expect that these resources will be used in further cichlid evolution studies and hope the protocols and identified targets will also be useful for phylogenetic studies of a wider range of organisms.     

Allometric space and allometric disparity: a developmental perspective in the macroevolutionary analysis of morphological disparity

Here, we advance novel uses of allometric spaces--multidimensional spaces specifically defined by allometric coefficients--with the goal of investigating the focal role of development in shaping the evolution of morphological disparity. From their examination, operational measures of allometric disparity can be derived, complementing standard signals of morphological disparity through an intuitive and process-oriented refinement of established analytical protocols used in disparity studies. Allometric spaces thereby become a promising context to reveal different patterns of evolutionary developmental changes and to assess their relative prevalence and importance. Such spaces offer a novel domain of investigation of phenotypic variation and should help in detecting large-scale trends, thus placing various macroevolutionary phenomena in an explicitly developmental context. Ammonoidea (Cephalopoda) at the Lower-Middle Jurassic transition were chosen as a case study to illustrate this methodological approach. We constructed two phenotypic spaces: a static, adult one (adult morphospace) and a dynamic, developmental one (allometric space). Comparative disparity analyses show a strikingly stable occupation in both spaces, despite extensive change in taxonomic composition. In contrast, disparity analyses of subclades reveal clearly distinct morphological and allometric disparity dynamics. Allometric approaches allow developmental insights into morphological diversification otherwise intractable from the analysis of adult morphospace alone.     

Integrating micro- and macroevolution of development through the study of horned beetles

A major challenge in evolutionary developmental biology is to understand how developmental evolution on the level of populations and closely related species relates to macroevolutionary transitions and the origin of evolutionary novelty. Here, I review the genetic, developmental, endocrine, and ecological basis of beetle horns, a morphological novelty that exhibits remarkable diversity both below and above the species level. Integrating from a variety of approaches three major insights emerge: the origin of beetle horns relied at least in part on the redeployment of already existing genetic, developmental and endocrine mechanisms. At the same time little to no phylogenetic distance appeared to have been necessary for the evolution of diverse modifier mechanisms that permit substantial modulation of trait expression at different time points during development in different species, sexes, alternative male morphs or even different tissue regions of the same individual. Lastly, at least a subset of these modifier mechanisms can evolve rapidly in geographically isolated populations, apparently driven by relatively simple, and probably ubiquitous, changes in ecological conditions. I discuss the implications of these results for our understanding of the genesis of morphological novelty and diversity.     

Evaluating evolutionary pressures and phylogenetic signal in earthworms: a case study – the number of typhlosole lamellae in Hormogastridae (Annelida,Oligochaeta)

Rarely have phylogenetic comparative methods been used to study the correlation between phenotypic traits and environmental variables in invertebrates. With the widespread convergence and conservativeness of the morphological characters used in earthworms, these comparative methods could be useful to improve our understanding of their evolution and systematics. One of the most prominent morphological characters in the family Hormogastridae, endemic to Mediterranean areas, is their multilamellar typhlosole, traditionally thought to be an adaptation to soils poor in nutrients. We tested the correlation of body size and soil characteristics with the number of typhlosole lamellae through a phylogenetic generalized least squares (PGLS) analysis. An ultrametric phylogenetic hypothesis was built with a 2580‐bp DNA sequence from 90 populations, used in combination with three morphological and 11 soil variables. The best‐supported model, based on the Akaike information criterion, was obtained by optimizing the parameters lambda (λ), kappa (κ), and delta (δ). The phylogenetic signal was strong for the number of typhlosole lamellae and average body weight, and was lower for soil variables. Increasing body weight appeared to be the main evolutionary pressure behind the increase in the number of typhlosole lamellae, with soil texture and soil richness having a weaker but significant effect. Information on the evolutionary rate of the number of typhlosole lamellae suggested that the early evolution of this character could have strongly shaped its variability, as is found in an adaptive radiation. This work highlights the importance of implementing the phylogenetic comparative method to test evolutionary hypotheses in invertebrate taxa.     

A phylogenetic hot spot for evolutionary novelty in Middle American treefrogs

Among the various types of evolutionary changes in morphology, the origin of novel structures may be the most rare and intriguing. Here we show statistically that the origins of different novel structures may be correlated and phylogenetically clustered into "hot spots" of evolutionary novelty, in a case study involving skull elements in treefrogs. We reconstruct phylogenetic relationships within a clade of Middle American treefrogs based on data from 10 nuclear and four mitochondrial genes and then analyze morphological evolution across this tree. New cranial elements are rare among anurans and tetrapods in general, but three novel elements have evolved within this clade, with a 40% increase in the number of skull roof elements in some species. Two of these elements also evolved in a related clade of treefrogs, and these two novel elements may have each evolved repeatedly within one or both clades. The molecular phylogeny suggests striking homoplasy in cranial morphology and shows that parsimony and Bayesian analyses of the morphological data have produced misleading results with strong statistical support. The origins of the novel elements are associated with an overall increase in the ossification of dermal skull roof elements (suggesting peramorphosis) and with the evolution of a novel adaptive behavior. Our study may be the first to statistically document significant phylogenetic clustering and correlation in the origins of novel structures, and to demonstrate the strongly misleading effects of peramorphosis on phylogenetic analysis.     

Overcoming phylogenetic and geographic uncertainties to test for correlates of range size evolution in gymnophthalmid lizards

Patterns of range size evolution are important for developing an evolutionary biogeographical theory and supporting conservation actions. Determining those patterns is however hampered by multiple factors acting on range size and by our uncertainty with regard to species' phylogenetic relationships and geographic distribution. In addition, given the diversity of analytic approaches existing in the literature, there are concerns regarding whether different methods might lead to different patterns. Here, we addressed these uncertainties in order to test for correlations between the evolution of morphology (body size and shape) and range size. We studied lizards of the family Gymnophthalmidae, representing changes of an order of magnitude in body size and also two independent lineages with limb‐reduced (snake‐like) morphs. We used phylogenetic multivariate methods (pPCA) to control for allometric effects of body size over shape. Then, we performed multiple regressions under three approaches: ‘naive’ least squares, Bayesian comparative methods that accounted for uncertainties in trait optimization, tree topology and branch length, and a novel permutative procedure based on phylogenetic generalized least squares (pGLS) to assess the robustness of our relationships to uncertainties in the range sizes of the species studied. All approaches led to the same answer: only body size was related to range size. While bigger gymnophthalmids tend to have relatively large ranges, small species can have either small or large ones. Our results’ robustness to strong uncertainties in both phylogenetic relationships and range sizes shows there are opportunities for overcoming those problems and produce reliable patterns of range size evolution. However, interpretation of the processes driving patterns of range size evolution will still require advances in phylogenetic and taxonomic knowledge. We discuss the application of morphology–range size relationships to conservation planning in the light of existing uncertainties in the geographic knowledge of our studied species group and workarounds for data availability.     

Differing evolutionary patterns underlie convergence on elongate morphology in endemic fishes of Lake Waccamaw, North Carolina

An extensive body of research has recently demonstrated patterns of parallel and/or convergent evolution that arise from divergent natural selection pressures exerted across environmental gradients. These studies, although providing some of our best empirical evidence for natural selection, have focused on rather narrow phylogenetic scopes, more often than not comparing patterns of morphological change among closely‐related taxa within a single genus. Organisms in replicated populations in these studies are often assumed to have accomplished convergence via similar underlying processes. However, such assumptions cannot be made when looking at evolution across broader phylogenetic and ecological spectra. In the present study, we assessed morphological change across a much broader scale to test whether similar evolutionary and developmental patterns underlie convergence. Specifically, we studied morphological change that has occurred in a novel lake environment (Lake Waccamaw, North Carolina, USA) where three phylogenetically‐disparate fishes representing different orders have speciated and independently evolved streamlined morphologies relative to their deeper‐bodied progenitors occupying nearby streams and coastal regions. Geometric morphometric analyses revealed that, although the bulk of shape change between environments is similar across taxa, significant species‐specific responses, concordant with differing expectations based on the ecologies of these taxa, were also found. Moreover, allometry analyses indicated that the developmental patterns underlying this change also differ across taxa. The present study provides evidence that, within a common environment, convergence can be achieved by different evolutionary and developmental patterns in phylogenetically‐ and ecologically‐disparate taxa. Finally, these results contradict the commonly‐held hypothesis that fishes should be more streamlined in streams than lakes and emphasize the need to also consider other environmental characteristics, such as water clarity and physical complexity, in studies of divergence. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98 , 636–645.     

A phylogenetic analysis of macroevolutionary patterns in fermentative yeasts

When novel sources of ecological opportunity are available, physiological innovations can trigger adaptive radiations. This could be the case of yeasts (Saccharomycotina), in which an evolutionary novelty is represented by the capacity to exploit simple sugars from fruits (fermentation). During adaptive radiations, diversification and morphological evolution are predicted to slow‐down after early bursts of diversification. Here, we performed the first comparative phylogenetic analysis in yeasts, testing the “early burst” prediction on species diversification and also on traits of putative ecological relevance (cell‐size and fermentation versatility). We found that speciation rates are constant during the time‐range we considered (ca., 150 millions of years). Phylogenetic signal of both traits was significant (but lower for cell‐size), suggesting that lineages resemble each other in trait‐values. Disparity analysis suggested accelerated evolution (diversification in trait values above Brownian Motion expectations) in cell‐size. We also found a significant phylogenetic regression between cell‐size and fermentation versatility (R² = 0.10), which suggests correlated evolution between both traits. Overall, our results do not support the early burst prediction both in species and traits, but suggest a number of interesting evolutionary patterns, that warrant further exploration. For instance, we show that the Whole Genomic Duplication that affected a whole clade of yeasts, does not seems to have a statistically detectable phenotypic effect at our level of analysis. In this regard, further studies of fermentation under common‐garden conditions combined with comparative analyses are warranted.     

Categorical versus geometric morphometric approaches to characterizing the evolution of morphological disparity in Osteostraci (Vertebrata,stem Gnathostomata)

Morphological variation (disparity) is almost invariably characterized by two non-mutually exclusive approaches: (1) quantitatively, through geometric morphometrics; and (2) in terms of discrete, ‘cladistic’, or categorical characters. Uncertainty over the comparability of these approaches diminishes the potential to obtain nomothetic insights into the evolution of morphological disparity and the few benchmarking studies conducted so far show contrasting results. Here, we apply both approaches to characterizing morphology in the stem-gnathostome clade Osteostraci in order to assess congruence between these alternative methods as well as to explore the evolutionary patterns of the group in terms of temporal disparity and the influence of phylogenetic relationships and habitat on morphospace occupation. Our results suggest that both approaches yield similar results in morphospace occupation and clustering, but also some differences indicating that these metrics may capture different aspects of morphology. Phylomorphospaces reveal convergence towards a generalized ‘horseshoe’-shaped cranial morphology and two strong trends involving major groups of osteostracans (benneviaspidids and thyestiids), which probably reflect adaptations to different lifestyles. Temporal patterns of disparity obtained from categorical and morphometric approaches appear congruent, however, disparity maxima occur at different times in the evolutionary history of the group. The results of our analyses indicate that categorical and continuous data sets may characterize different patterns of morphological disparity and that discrepancies could reflect preservational limitations of morphometric data and differences in the potential of each data type for characterizing more or less inclusive aspects of overall phenotype.     

How species longevity, intraspecific morphological variation, and geographic range size are related: a comparison using late Cambrian trilobites

Phenotypic variation is fundamental to evolutionary change. Variation not only evinces the connectivity of populations but it is also associated with the adaptability and evolvability of taxa. Despite the potential importance of morphological variation in structuring evolutionary patterns, little is known about how relative differences in intraspecific morphological variation and its geographic structure are linked to differences in species longevity. This study offers a novel combination of analyses that reveal the quantitative relationships among intraspecific variation, geographic range size and duration in the fossil record using late Cambrian trilobites. Results show that geographic range size and duration are positively correlated. Surprisingly, longer lived species tend to have less intraspecific variation. Phylogenetic effects were also explored and found not to determine the association between these variables. However, the distribution of geographic range sizes shows strong phylogenetic signal. In light of previous work, one possible explanation for these results is that species with shorter durations have comparatively higher rates of morphological evolution, reflected in higher phenotypic variation overall.     

Comparative methods as a statistical fix: the dangers of ignoring an evolutionary model

Abstract Comparative methods are widely used in ecology and evolution. The most frequently used comparative methods are based on an explicit evolutionary model. However, recent approaches have been popularized that are without an evolutionary basis or an underlying null model. Here we highlight the limitations of such techniques in comparative analyses by using simulations to compare two commonly used comparative methods with and without evolutionary basis, respectively: generalized least squares (GLS) and phylogenetic eigenvector regression (PVR). We find that GLS methods are more efficient at estimating model parameters and produce lower variance in parameter estimates, lower phylogenetic signal in residuals, and lower Type I error rates than PVR methods. These results can very likely be generalized to eigenvector methods that control for space and both space and phylogeny. We highlight that GLS methods can be adapted in numerous ways and that the variance structure used in these models can be flexibly optimized to each data set.     

Sequence capture using AFLP‐generated baits: A cost‐effective method for high‐throughput phylogenetic and phylogeographic analysis

Target sequence capture is an efficient technique to enrich specific genomic regions for high‐throughput sequencing in ecological and evolutionary studies. In recent years, many sequence capture approaches have been proposed, but most of them rely on commercial synthetic baits which make the experiment expensive. Here, we present a novel sequence capture approach called AFLP‐based genome sequence capture (AFLP Capture). This method uses the AFLP (amplified fragment length polymorphism) technique to generate homemade capture baits without the need for prior genome information, thus is applicable to any organisms. In this approach, biotinylated AFLP fragments representing a random fraction of the genome are used as baits to capture the homologous fragments from genomic shotgun sequencing libraries. In a trial study, by using AFLP Capture, we successfully obtained 511 orthologous loci (>700,000 bp in total length) from 11 Odorrana species and more than 100,000 single nucleotide polymorphisms (SNPs) in four analyzed individuals of an Odorrana species. This result shows that our method can be used to address questions of various evolutionary depths (from interspecies level to intraspecies level). We also discuss the flexibility in bait preparation and how the sequencing data are analyzed. In summary, AFLP Capture is a rapid and flexible tool and can significantly reduce the experimental cost for phylogenetic studies that require analyzing genome‐scale data (hundreds or thousands of loci).     

Behavioural,ecological, and evolutionary aspects of diversity in frog colour patterns

The role of colours and colour patterns in behavioural ecology has been extensively studied in a variety of contexts and taxa, while almost overlooked in many others. For decades anurans have been the focus of research on acoustic signalling due to the prominence of vocalisations in their communication. Much less attention has been paid to the enormous diversity of colours, colour patterns, and other types of putative visual signals exhibited by frogs. With the exception of some anecdotal observations and studies, the link between colour patterns and the behavioural and evolutionary ecology of anurans had not been addressed until approximately two decades ago. Since then, there has been ever‐increasing interest in studying how colouration is tied to different aspects of frog behaviour, ecology and evolution. Here I review the literature on three different contexts in which frog colouration has been recently studied: predator–prey interactions, intraspecific communication, and habitat use; and I highlight those aspects that make frogs an excellent, yet understudied, group to examine the role of colour in the evolution of anti‐predation strategies and animal communication systems. Further, I argue that in addition to natural‐history observations, more experiments are needed in order to elucidate the functions of anuran colouration and the selective pressures involved in its diversity. To conclude, I encourage researchers to strengthen current experimental approaches, and suggest future directions that may broaden our current understanding of the adaptive value of anuran colour pattern diversity.     

Weighted parsimony outperforms other methods of phylogenetic inference under models appropriate for morphology

One of the lasting controversies in phylogenetic inference is the degree to which specific evolutionary models should influence the choice of methods. Model‐based approaches to phylogenetic inference (likelihood, Bayesian) are defended on the premise that without explicit statistical models there is no science, and parsimony is defended on the grounds that it provides the best rationalization of the data, while refraining from assigning specific probabilities to trees or character‐state reconstructions. Authors who favour model‐based approaches often focus on the statistical properties of the methods and models themselves, but this is of only limited use in deciding the best method for phylogenetic inference—such decision also requires considering the conditions of evolution that prevail in nature. Another approach is to compare the performance of parsimony and model‐based methods in simulations, which traditionally have been used to defend the use of models of evolution for DNA sequences. Some recent papers, however, have promoted the use of model‐based approaches to phylogenetic inference for discrete morphological data as well. These papers simulated data under models already known to be unfavourable to parsimony, and modelled morphological evolution as if it evolved just like DNA, with probabilities of change for all characters changing in concert along tree branches. The present paper discusses these issues, showing that under reasonable and less restrictive models of evolution for discrete characters, equally weighted parsimony performs as well or better than model‐based methods, and that parsimony under implied weights clearly outperforms all other methods.