SPECIES SELECTION AND THE MACROEVOLUTION OF CORAL COLONIALITY AND PHOTOSYMBIOSIS

Differences in the relative diversification rates of species with variant traits are known as species selection. Species selection can produce a macroevolutionary change in the frequencies of traits by changing the relative number of species possessing each trait over time. But species selection is not the only process that can change the frequencies of traits, phyletic microevolution of traits within species and phylogenetic trait evolution among species, the tempo and mode of microevolution can also change trait frequencies. Species selection, phylogenetic, and phyletic processes can all contribute to large‐scale trends, reinforcing or canceling each other out. Even more complex interactions among macroevolutionary processes are possible when multiple covarying traits are involved. Here I present a multilevel macroevolutionary framework that is useful for understanding how macroevolutionary processes interact. It is useful for empirical studies using fossils, molecular phylogenies, or both. I illustrate the framework with the macroevolution of coloniality and photosymbiosis in scleractinian corals using a time‐calibrated molecular phylogeny. I find that standing phylogenetic variation in coloniality and photosymbiosis deflects the direction of macroevolution from the vector of species selection. Variation in these traits constrains species selection and results in a 200 million year macroevolutionary equilibrium.     

Song evolution,speciation, and vocal learning in passerine birds

Phenotypic divergence can promote reproductive isolation and speciation, suggesting a possible link between rates of phenotypic evolution and the tempo of speciation at multiple evolutionary scales. To date, most macroevolutionary studies of diversification have focused on morphological traits, whereas behavioral traits─including vocal signals─are rarely considered. Thus, although behavioral traits often mediate mate choice and gene flow, we have a limited understanding of how behavioral evolution contributes to diversification. Furthermore, the developmental mode by which behavioral traits are acquired may affect rates of behavioral evolution, although this hypothesis is seldom tested in a phylogenetic framework. Here, we examine evidence for rate shifts in vocal evolution and speciation across two major radiations of codistributed passerines: one oscine clade with learned songs (Thraupidae) and one suboscine clade with innate songs (Furnariidae). We find that evolutionary bursts in rates of speciation and song evolution are coincident in both thraupids and furnariids. Further, overall rates of vocal evolution are higher among taxa with learned rather than innate songs. Taken together, these findings suggest an association between macroevolutionary bursts in speciation and vocal evolution, and that the tempo of behavioral evolution can be influenced by variation in developmental modes among lineages.     

Morphological disparity in theropod jaws: comparing discrete characters and geometric morphometrics

Disparity, the diversity of form and function of organisms, can be assessed from cladistic or phenetic characters, and from discrete characters or continuous characters such as landmarks, outlines, or ratios. But do these different methods of assessing disparity provide comparable results? Here we provide evidence that all metrics correlate significantly with each other and capture similar patterns of morphological variation. We compare three methods of capturing morphological disparity (discrete characters, geometric morphometric outlines and geometric morphometric landmarks) in coelurosaurian dinosaurs. We standardize our study by focusing all our metrics on the mandible, so avoiding the risk of confounding disparity methods with anatomical coverage of the taxa. The correlation is strongest between the two geometric morphometric methods, and weaker between the morphometric methods and the discrete characters. By using phylogenetic simulations of discrete character and geometric morphometric data sets, we show that the strength of these correlations is significantly greater than expected from the evolution of random data under Brownian motion. All disparity metrics confirm that Maniraptoriformes had the highest disparity of all coelurosaurians, and omnivores and herbivores had higher disparity than carnivores.     

Identifying heterogeneity in rates of morphological evolution: discrete character change in the evolution of lungfish (Sarcopterygii; Dipnoi)

Quantifying rates of morphological evolution is important in many macroevolutionary studies, and critical when assessing possible adaptive radiations and episodes of punctuated equilibrium in the fossil record. However, studies of morphological rates of change have lagged behind those on taxonomic diversification, and most authors have focused on continuous characters and quantifying patterns of morphological rates over time. Here, we provide a phylogenetic approach, using discrete characters and three statistical tests to determine points on a cladogram (branches or entire clades) that are characterized by significantly high or low rates of change. These methods include a randomization approach that identifies branches with significantly high rates and likelihood ratio tests that pinpoint either branches or clades that have significantly higher or lower rates than the pooled rate of the remainder of the tree. As a test case for these methods, we analyze a discrete character dataset of lungfish, which have long been regarded as "living fossils" due to an apparent slowdown in rates since the Devonian. We find that morphological rates are highly heterogeneous across the phylogeny and recover a general pattern of decreasing rates along the phylogenetic backbone toward living taxa, from the Devonian until the present. Compared with previous work, we are able to report a more nuanced picture of lungfish evolution using these new methods.     

Overcoming problems with the use of ratios as continuous characters for phylogenetic analyses

The use of quantitative morphometric information for phylogenetic inference has been an intensely debated topic for most of the history of phylogenetic systematics. Despite several drawbacks, the most common strategy to include this sort of data into phylogenetic studies is the use of ratios, that is quotients between morphometric variables. Here, we discuss one particular problem associated with such methodology: the fact that the often arbitrary election of which variable serves as numerator and which as denominator affects the phylogenetic outcome of the analysis. We describe the cause for such an effect, and study its implications with the use of several published data matrices. Alternative coding schemes for ratio characters result in very different phylogenetic hypotheses, an effect that may even be strong enough to affect studies that combine continuous and discrete morphological information. Some of the resulting incongruence is produced by the differences in magnitude of the continuous characters involved, although different rescaling techniques are shown to decrease, but not eliminate, the confounding effect. To eliminate such problematic effect, ratios should be either log‐transformed before their use or replaced by more effective ways to capture morphometric information.     

Asymmetries in phylogenetic diversification and character change can be untangled

The analysis of diversification and character evolution using phylogenetic data attracts increasing interest from biologists. Recent statistical developments have resulted in a variety of tools for the inference of macroevolutionary processes in a phylogenetic context. In a recent paper Maddison (2006 Evolution, 60: 1743-1746) pointed out that uncareful use of some of these tools could lead to misleading conclusions on diversification or character evolution, and thus to difficulties in distinguishing both phenomena. I here present guidelines for the analyses of macroevolutionary data that may help to avoid these problems. The proper use of recently developed statistical methods may help to untangle diversification and character change, and so will allow us to address important evolutionary questions.     

Macroevolutionary integration of phenotypes within and across ant worker castes

Phenotypic traits are often integrated into evolutionary modules: sets of organismal parts that evolve together. In social insect colonies, the concepts of integration and modularity apply to sets of traits both within and among functionally and phenotypically differentiated castes. On macroevolutionary timescales, patterns of integration and modularity within and across castes can be clues to the selective and ecological factors shaping their evolution and diversification. We develop a set of hypotheses describing contrasting patterns of worker integration and apply this framework in a broad (246 species) comparative analysis of major and minor worker evolution in the hyperdiverse ant genus Pheidole. Using geometric morphometrics in a phylogenetic framework, we inferred fast and tightly integrated evolution of mesosoma shape between major and minor workers, but slower and more independent evolution of head shape between the two worker castes. Thus, Pheidole workers are evolving as a mixture of intracaste and intercaste integration and rate heterogeneity. The decoupling of homologous traits across worker castes may represent an important process facilitating the rise of social complexity.     

A phylogeny of the Platyhelminthes: towards a total-evidence solution

We advocate a total-evidence approach for the reconstruction of working phylogenies for the Turbellaria and the phylum Platyhelminthes. Few morphology-based character matrices are available in the systematic literature concerning flatworms, and molecular-based phylogenies are rapidly providing the only means by which we can estimate phylogenies cladistically. Character matrices based on gross morphology and ultrastructure are required and should be internally consistent, i.e. character coding should follow a set of a priori guidelines and character duplication and contradiction is avoided. In order to test our molecular phylogenies we need complementary data sets from morphology. To understand morphological homology we need phylogenetic evidence from independent (e.g. molecular) data. Fully complementary morphological and molecular data sets enable us to validate phylogenetic hypotheses and the combination of these sets in phylogenetic reconstruction utilises all statements of homology. Working phylogenies which include all phylogenetic information not only shed light on individual character evolution, but form a strong basis for comparative studies investigating the origin and evolutionary radiation of the taxonomic group under scrutiny. This revised version was published online in July 2006 with corrections to the Cover Date.     

How traits shape trees: new approaches for detecting character state‐dependent lineage diversification

Biologists have long sought to understand the processes underlying disparities in clade size across the tree of life and the extent to which such clade size differences can be attributed to the evolution of particular traits. The association of certain character states with species‐rich clades suggests that trait evolution can lead to increased diversification, but such a pattern could also arise due other processes, such as directional trait evolution. Recent advances in phylogenetic comparative methods have provided new statistical approaches for distinguishing between these intertwined and potentially confounded macroevolutionary processes. Here, we review the historical development of methods for detecting state‐dependent diversification and explore what new methods have revealed about classic examples of traits that affect diversification, including evolutionary dead ends, key innovations and geographic traits. Applications of these methods thus far collectively suggest that trait diversity commonly arises through the complex interplay between transition, speciation and extinction rates and that long hypothesized evolutionary dead ends and key innovations are instead often cases of directional trends in trait evolution.     

Is specialization an evolutionary dead end? Testing for differences in speciation,extinction and trait transition rates across diverse phylogenies of specialists and generalists

Specialization has often been claimed to be an evolutionary dead end, with specialist lineages having a reduced capacity to persist or diversify. In a phylogenetic comparative framework, an evolutionary dead end may be detectable from the phylogenetic distribution of specialists, if specialists rarely give rise to large, diverse clades. Previous phylogenetic studies of the influence of specialization on macroevolutionary processes have demonstrated a range of patterns, including examples where specialists have both higher and lower diversification rates than generalists, as well as examples where the rates of evolutionary transitions from generalists to specialists are higher, lower or equal to transitions from specialists to generalists. Here, we wish to ask whether these varied answers are due to the differences in macroevolutionary processes in different clades, or partly due to differences in methodology. We analysed ten phylogenies containing multiple independent origins of specialization and quantified the phylogenetic distribution of specialists by applying a common set of metrics to all datasets. We compared the tip branch lengths of specialists to generalists, the size of specialist clades arising from each evolutionary origin of a specialized trait and whether specialists tend to be clustered or scattered on phylogenies. For each of these measures, we compared the observed values to expectations under null models of trait evolution and expected outcomes under alternative macroevolutionary scenarios. We found that specialization is sometimes an evolutionary dead end: in two of the ten case studies (pollinator‐specific plants and host‐specific flies), specialization is associated with a reduced rate of diversification or trait persistence. However, in the majority of studies, we could not distinguish the observed phylogenetic distribution of specialists from null models in which specialization has no effect on diversification or trait persistence.     

Phylogenetic ANOVA: Group‐clade aggregation,biological challenges,and a refined permutation procedure

Phylogenetic regression is frequently used in macroevolutionary studies, and its statistical properties have been thoroughly investigated. By contrast, phylogenetic ANOVA has received relatively less attention, and the conditions leading to incorrect statistical and biological inferences when comparing multivariate phenotypes among groups remain underexplored. Here, we propose a refined method of randomizing residuals in a permutation procedure (RRPP) for evaluating phenotypic differences among groups while conditioning the data on the phylogeny. We show that RRPP displays appropriate statistical properties for both phylogenetic ANOVA and regression models, and for univariate and multivariate datasets. For ANOVA, we find that RRPP exhibits higher statistical power than methods utilizing phylogenetic simulation. Additionally, we investigate how group dispersion across the phylogeny affects inferences, and reveal that highly aggregated groups generate strong and significant correlations with the phylogeny, which reduce statistical power and subsequently affect biological interpretations. We discuss the broader implications of this phylogenetic group aggregation, and its relation to challenges encountered with other comparative methods where one or a few transitions in discrete traits are observed on the phylogeny. Finally, we recommend that phylogenetic comparative studies of continuous trait data use RRPP for assessing the significance of indicator variables as sources of trait variation.     

Phylogenetic and Experimental Tests of Interactions among Mutualistic Plant Defense Traits in Viburnum (Adoxaceae)

Abstract Plant traits that mediate mutualistic interactions are widespread, yet few studies have linked their macroevolutionary patterns with the ecological interactions they mediate. Here we merged phylogenetic and experimental approaches to investigate the evolution of two common mutualistic plant traits, extrafloral nectaries (EFNs) and leaf domatia. By using the flowering plant clade Viburnum, we tested whether macroevolutionary patterns support adaptive hypotheses and conducted field surveys and manipulative experiments to examine whether ecological interactions are concordant with evolutionary predictions. Phylogenetic reconstructions suggested that EFN-bearing species are monophyletic, whereas the evolution of domatia correlated with leaf production strategy (deciduous or evergreen) and climate. Domatia were also more common in the EFN clade, suggesting that the two traits may jointly mediate ecological interactions. This result was further investigated in a common-garden survey, where plants with domatia and EFNs on the leaf blade had more mutualistic mites than plants with other trait combinations, and in manipulative field experiments, where the traits additively increased mutualist abundance. Taken together, our results suggest that mutualistic traits in Viburnum are not ecologically independent, as they work in concert to attract and retain mutualists, and their long-term evolution may be influenced by complex interactions among multiple traits, mutualists, and geography.     

Journeys through discrete‐character morphospace: synthesizing phylogeny,tempo, and disparity

Palaeontologists have long employed discrete categorical data to capture morphological variation in fossil species, using the resulting character–taxon matrices to measure evolutionary tempo, infer phylogenies and capture morphological disparity. However, to date these have been seen as separate approaches despite a common goal of understanding morphological evolution over deep time. Here I argue that there are clear advantages to considering these three lines of enquiry in a single space: the phylomorphospace. Conceptually these high‐dimensional spaces capture how a phylogenetic tree explores morphospace and allow us to consider important process questions around evolutionary rates, constraints, convergence and directional trends. Currently the literature contains fundamentally different approaches used to generate such spaces, with no direct comparison between them, despite the differing evolutionary histories they imply. Here I directly compare five different phylomorphospace approaches, three with direct literature equivalents and two that are novel. I use a single empirical case study of coelurosaurian theropod dinosaurs (152 taxa, 853 characters) to show that under many analyses the literature‐derived approaches tend to reflect introduced phylogenetic (rather than the intended morphological) signal. The two novel approaches, which produce limited ancestral state estimates prior to ordination, are able to minimize this phylogenetic signal and thus exhibit more realistic amounts of phylogenetic signal, rate heterogeneity, and convergent evolution.     

Comparison of phylogenetic signal between male genitalia and non-genital characters in insect systematics

It is generally accepted that male genitalia evolve more rapidly and divergently relative to non-genital traits due to sexual selection, but there is little quantitative comparison of the pattern of evolution between these character sets. Moreover, despite the fact that genitalia are still among the most widely used characters in insect systematics, there is an idea that the rate of evolution is too rapid for genital characters to be useful in forming clades. Based on standard measures of fit used in cladistic analyses, we compare levels of homoplasy and synapomorphy between genital and non-genital characters of published data sets and demonstrate that phylogenetic signal between these two character sets is statistically similar. This pattern is found consistently across different insect orders at different taxonomic hierarchical levels. We argue that the fact that male genitalia are under sexual selection and thus diverge rapidly does not necessarily equate with the lack of phylogenetic signal, because characters that evolve by descent with modification make appropriate characters for a phylogenetic analysis, regardless of the rate of evolution. We conclude that male genitalia are a composite character consisting of different components diverging separately, which make them ideal characters for phylogenetic analyses, providing information for resolving varying levels of hierarchy.
© The Willi Hennig Society 2009.     

CORRELATED EVOLUTION OF MIGRATION AND SEXUAL DICHROMATISM IN THE NEW WORLD ORIOLES (ICTERUS)

The evolution of sexual dimorphism has long been attributed to sexual selection, specifically as it would drive repeated gains of elaborate male traits. In contrast to this pattern, New World oriole species all exhibit elaborate male plumage, and the repeated gains of sexual dichromatism observed in the genus are due to losses of female elaboration. Interestingly, most sexually dichromatic orioles belong to migratory or temperate‐breeding clades. Using character scoring and ancestral state reconstructions from two recent studies in Icterus, we tested a hypothesis of correlated evolution between migration and sexual dichromatism. We employed two discrete phylogenetic comparative approaches: the concentrated changes test and Pagel's discrete likelihood test. Our results show that the evolution of these traits is significantly correlated (CCT: uncorrected P < 0.05; ML: LRT = 12.470, P < 0.005). Indeed, our best model of character evolution suggests that gains of sexual dichromatism are 23 times more likely to occur in migratory taxa. This study demonstrates that a life‐history trait with no direct relationship with sexual selection has a strong influence on the evolution of sexual dichromatism. We recommend that researchers further investigate the role of selection on elaborate female traits in the evolution of sexual dimorphism.     

Evolution of the leaf economics spectrum in herbs: Evidence from environmental divergences in leaf physiology across Helianthus (Asteraceae)

The leaf economics spectrum (LES) describes a major axis of plant functional trait variation worldwide, defining suites of leaf traits aligned with resource‐acquisitive to resource‐conservative ecological strategies. The LES has been interpreted to arise from leaf‐level trade‐offs among ecophysiological traits common to all plants. However, it has been suggested that the defining leaf‐level trade‐offs of the LES may not hold within specific functional groups (e.g., herbs) nor within many groups of closely related species, which challenges the usefulness of the LES paradigm across evolutionary scales. Here, we examine the evolution of the LES across 28 species of the diverse herbaceous genus Helianthus (the sunflowers), which occupies a wide range of habitats and climate variation across North America. Using a phylogenetic comparative approach, we find repeated evolution of more resource‐acquisitive LES strategies in cooler, drier, and more fertile environments. We also find macroevolutionary correlations among LES traits that recapitulate aspects of the global LES, but with one major difference: leaf mass per area is uncorrelated with leaf lifespan. This indicates that whole‐plant processes likely drive variation in leaf lifespan across Helianthus, rather than leaf‐level trade‐offs. These results suggest that LES patterns do not reflect universal physiological trade‐offs at small evolutionary scales.     

Shifts from specialised to generalised pollination systems in Miconieae (Melastomataceae) and their relation with anther morphology and seed number

Most species in Melastomataceae have poricidal anthers related to specialised bee buzz‐pollination, while some have anthers with large openings associated to non‐bee pollination systems. We tracked the evolution of anther morphology and seed number on the Miconieae phylogenetic tree to understand the evolutionary shifts in such pollination systems. Anther morphometric data and seed number were recorded for 54 taxa. Pollinators (bees, flies, wasps) were recorded for 20 available species. Ancestral state reconstruction was made using Maximum Likelihood from nrITS sequences. We used phylogenetic eigenvector regressions to estimate phylogenetic signal and the adaptive component for these traits. Species pollinated by bees or bees and wasps tend to have smaller pores and fruits with more seeds. Species pollinated by flies or flies and bees and/or wasps tend to have larger pores and fruits with less seeds. Independent evolution occurred three times for anthers with large pores and twice for fruits with few seeds. We detected a phylogenetic signal in both traits, and negative correlated evolution between them. In actinomorphic small‐flowered Miconieae, changes in anther morphology can be related to generalisation in the pollination system incorporating flies and wasps as pollinators and lessening the importance of buzzing bees in such process. Differences in pollen removal and deposition may explain differences in anther morphology and seed number in Miconieae.     

A combined morphometric and phylogenetic analysis of an ecomorphological trend: pelagization in Antarctic fishes (Perciformes: Nototheniidae)

The Antarctic fish family Nototheniidae (Perciformes) presumably originated from a benthic ancestor, and several lineages have evolved to live or at least feed in the water column, a trend called pelagization. Here, we use information on phylogeny, allometric growth, and diet composition for an integrated analysis of morphological and ecological diversification in this group, mainly focusing on the subfamilies Trematominae and Pleuragramminae. A phylogenetic analysis of data published in earlier systematic studies produced eight equally parsimonious trees, all indicating that several previously recognized taxa are paraphyletic. These phylogenetic trees all suggest multiple origins of pelagic life styles. Multivariate morphometric analyses including nine species showed that juveniles and adults grow according to a common pattern of ontogenetic allometry. The morphometric differences among species are mosdy the result of lateral transpositions of the growth trajectories, indicating that embryonic and larval development is more important as a determinant of morphological variation than allometric growth as juveniles and adults. We studied patterns of interspecific variation with principal components and the covariation between morphometric variables and food composition with a partial least-squares analysis. Both analyses revealed a gradient from benthic to pelagic foragers. Measurements of structures involved in swimming have a prominent role in these analyses, suggesting adaptive evolution of these traits. Tracing morphometric traits on the phylogenetic trees revealed a considerable amount of evolutionary plasticity, showing that species related phylogenetically need not be morphologically similar, but can diverge considerably, perhaps as a response to natural selection and adaptation to different habitats and foraging modes. In accordance, a test of phylogenetically independent contrasts showed that bursts of increased morphological change accompanied habitat shifts.