Cross-disciplinary information for understanding macroevolution

Many different macroevolutionary models can produce the same observations. Despite efforts in building more complex and realistic models, it may still be difficult to distinguish the processes that have generated the biodiversity we observe. In this opinion we argue that we can make new progress by reaching out across disciplines, relying on independent data and theory to constrain macroevolutionary inference. Using mainly paleontological insights and data, we illustrate how we can eliminate less plausible or implausible models, and/or parts of parameter space, while applying comparative phylogenetic approaches. We emphasize that such cross-disciplinary insights and data can be drawn between many other disciplines relevant to macroevolution. We urge cross-disciplinary training, and collaboration using common-use databases as a platform for increasing our understanding.     

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.     

Understanding the effect of competition during evolutionary radiations: an integrated model of phenotypic and species diversification

Competition can drive macroevolutionary change, for example during adaptive radiations. However, we still lack a clear understanding of how it shapes diversification processes and patterns. To better understand the macroevolutionary consequences of competition, as well as the signal left on phylogenetic data, we developed a model linking trait evolution and species diversification in an ecological context. We find four main results: first, competition spurs trait diversity but not necessarily species richness; second, competition produces slowdowns in species diversification even in the absence of explicit ecological limits, but not in phenotypic diversification even in the presence of such limits; third, early burst patterns do not provide a reliable way of testing for adaptive radiations; and fourth, looking for phylogenetic signal in trait data and support for phenotypic models incorporating competition is a better alternative. Our results clarify the macroevolutionary consequences of competition and could help design more powerful tests of adaptive radiations in nature.     

Detecting the macroevolutionary signal of species interactions

Species interactions lie at the heart of many theories of macroevolution, from adaptive radiation to the Red Queen. Although some theories describe the imprint that interactions will have over long timescales, we are still missing a comprehensive understanding of the effects of interactions on macroevolution. Current research shows strong evidence for the impact of interactions on macroevolutionary patterns of trait evolution and diversification, yet many macroevolutionary studies have only a tenuous relationship to ecological studies of interactions over shorter timescales. We review current research in this area, highlighting approaches that explicitly model species interactions and connect them to broad‐scale macroevolutionary patterns. We also suggest that progress has been made by taking an integrative interdisciplinary look at individual clades. We focus on African cichlids as a case study of how this approach can be fruitful. Overall, although the evidence for species interactions shaping macroevolution is strong, further work using integrative and model‐based approaches is needed to spur progress towards understanding the complex dynamics that structure communities over time and space.     

Phylogenetic mixture models can reduce node-density artifacts

We investigate the performance of phylogenetic mixture models in reducing a well-known and pervasive artifact of phylogenetic inference known as the node-density effect, comparing them to partitioned analyses of the same data. The node-density effect refers to the tendency for the amount of evolutionary change in longer branches of phylogenies to be underestimated compared to that in regions of the tree where there are more nodes and thus branches are typically shorter. Mixture models allow more than one model of sequence evolution to describe the sites in an alignment without prior knowledge of the evolutionary processes that characterize the data or how they correspond to different sites. If multiple evolutionary patterns are common in sequence evolution, mixture models may be capable of reducing node-density effects by characterizing the evolutionary processes more accurately. In gene-sequence alignments simulated to have heterogeneous patterns of evolution, we find that mixture models can reduce node-density effects to negligible levels or remove them altogether, performing as well as partitioned analyses based on the known simulated patterns. The mixture models achieve this without knowledge of the patterns that generated the data and even in some cases without specifying the full or true model of sequence evolution known to underlie the data. The latter result is especially important in real applications, as the true model of evolution is seldom known. We find the same patterns of results for two real data sets with evidence of complex patterns of sequence evolution: mixture models substantially reduced node-density effects and returned better likelihoods compared to partitioning models specifically fitted to these data. We suggest that the presence of more than one pattern of evolution in the data is a common source of error in phylogenetic inference and that mixture models can often detect these patterns even without prior knowledge of their presence in the data. Routine use of mixture models alongside other approaches to phylogenetic inference may often reveal hidden or unexpected patterns of sequence evolution and can improve phylogenetic inference.     

Fitting models of continuous trait evolution to incompletely sampled comparative data using approximate Bayesian computation

In recent years, a suite of methods has been developed to fit multiple rate models to phylogenetic comparative data. However, most methods have limited utility at broad phylogenetic scales because they typically require complete sampling of both the tree and the associated phenotypic data. Here, we develop and implement a new, tree-based method called MECCA (Modeling Evolution of Continuous Characters using ABC) that uses a hybrid likelihood/approximate Bayesian computation (ABC)-Markov-Chain Monte Carlo approach to simultaneously infer rates of diversification and trait evolution from incompletely sampled phylogenies and trait data. We demonstrate via simulation that MECCA has considerable power to choose among single versus multiple evolutionary rate models, and thus can be used to test hypotheses about changes in the rate of trait evolution across an incomplete tree of life. We finally apply MECCA to an empirical example of body size evolution in carnivores, and show that there is no evidence for an elevated rate of body size evolution in the pinnipeds relative to terrestrial carnivores. ABC approaches can provide a useful alternative set of tools for future macroevolutionary studies where likelihood-dependent approaches are lacking.     

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.     

A hierarchical view of convergent evolution in microbial eukaryotes

Distinguishing convergent evolution from other causes of similarity in organisms is necessary for reconstructing phylogenetic relationships, inferring patterns of character evolution, and investigating the forces of natural selection. In contrast to animals and land plants, the pervasiveness and adaptive significance of convergent evolution in microbes has yet to be systematically explored or articulated. Convergent evolution in microbial eukaryotes, for instance, often involves very distantly related lineages with relatively limited repertoires of morphological features. These large phylogenetic distances weaken the role of ancestral developmental programs on the subsequent evolution of morphological characters, making convergent evolution between very distantly related lineages fundamentally different from convergent evolution between closely related lineages. This suggests that examples of convergence at different levels in the phylogenetic hierarchy offer different clues about the causes and processes of macroevolutionary diversification. Accordingly (and despite opinions to the contrary), I recognize three broad and overlapping categories of phenotypic convergence-"parallel", "proximate" and "ultimate"-that represent either (1) subcellular analogues, (2) subcellular analogues to multicellular systems (and vice versa), or (3) multicellular analogues. Microbial eukaryotes living in planktonic environments, interstitial environments, and the intestinal environments of metazoan hosts provide compelling examples of ultimate convergence. After describing selected examples in microbial eukaryotes, I suggest some future directions needed to more fully understand the hierarchical structure of convergent evolution and the overall history of life.     

Rates of morphological evolution are correlated with species richness in salamanders

The tempo and mode of species diversification and phenotypic evolution vary widely across the tree of life, yet the relationship between these processes is poorly known. Previous tests of the relationship between rates of phenotypic evolution and rates of species diversification have assumed that species richness increases continuously through time. If this assumption is violated, simple phylogenetic estimates of net diversification rate may bear no relationship to processes that influence the distribution of species richness among clades. Here, we demonstrate that the variation in species richness among plethodontid salamander clades is unlikely to have resulted from simple time-dependent processes, leading to fundamentally different conclusions about the relationship between rates of phenotypic evolution and species diversification. Morphological evolutionary rates of both size and shape evolution are correlated with clade species richness, but are uncorrelated with simple estimators of net diversification that assume constancy of rates through time. This coupling between species diversification and phenotypic evolution is consistent with the hypothesis that clades with high rates of morphological trait evolution may diversify more than clades with low rates. Our results indicate that assumptions about underlying processes of diversity regulation have important consequences for interpreting macroevolutionary patterns.     

After the gold rush,or before the flood? Evolutionary morphology of mushroom-forming fungi (Agaricomycetes) in the early 21st century

Mushroom-forming fungi (Agaricomycetes, approx. syn.: Homobasidiomycetes) produce a diverse array of fruiting bodies, ranging from simple crust-like forms to complex, developmentally integrated forms, such as stinkhorns and veiled agarics. The 19th century Friesian system divided the mushroom-forming fungi according to macromorphology. The Friesian taxonomy has long been regarded as artificial, but it continues to influence the language of mycology and perceptions of fungal diversity. Throughout the 20th century, the phylogenetic significance of anatomical features was elucidated, and classifications that departed strongly from the Friesian system were proposed. However, the anatomical studies left many questions and controversies unresolved, due in part to the paucity of characters, as well as the general absence of explicit phylogenetic analyses. Problems in fruiting body evolution were among the first to be addressed when molecular characters became readily accessible in the late 1980s. Today, GenBank contains about 108,000 nucleotide sequences of ‘homobasidiomycetes’, filed under 7300 unique names. Analyses of these data are providing an increasingly detailed and robust view of the phylogeny and the distribution of different fruiting body forms across the 14 major clades that make up the agaricomycetes. However, it would be wrong to suggest that all the important questions about fruiting body evolution have been resolved. Recent studies focusing on resupinate forms suggest that there may still be undetected major clades of agaricomycetes, which could have a significant impact on our estimates of the ancestral forms in this morphologically diverse group. Modern approaches, including comparative phylogenetic analyses and developmental studies, have the potential to yield novel insights into both the macroevolutionary processes and cellular mechanisms of fungal morphological evolution.     

Exploring the drivers of population structure across desert snakes can help to link micro and macroevolution

To understand the underlying mechanisms generating population genetic divergence and structure is a critical step towards understanding how biodiversity evolves at both micro‐ and macroevolutionary scales. At the population‐level, geographic isolation as well as adaptation to local environmental conditions can generate different patterns of spatial genetic variation among populations. Specific organismal traits as well as the characteristics of the environment might influence the process under which populations become spatially structured. In a From the Cover article in this issue of Molecular Ecology, Myers et al. (2019) present an integrative approach to investigate if the Cochise filter barrier (CFB), lying between the Sonoran and Chihuahuan Deserts, and the surrounding river networks were relevant in driving the population structure of 13 snake species. While local environmental conditions seem to predominantly contribute to lineage divergence, traditionally studied vicariant barriers seem to have played a minor role in shaping population structure across the studied species. This study brings insights into how population‐level processes could contribute to the formation of incipient species, which ultimately might affect the speciation rates measured at macroevolutionary scales. Hence, Myers et al. (2019) not only represents an integrative study aiming to understand the drivers of population genetic divergence, but also a potentially important contribution to our ongoing challenge in linking micro‐ and macroevolution.     

Plant scent and plant–insect interactions—Review and outlook from a macroevolutionary perspective

The astonishing diversity of plants and insects and their entangled interactions are cornerstones in terrestrial ecosystems. Co-occurring with species diversity is the diversity of plant secondary metabolites (PSMs). So far, their estimated number is more than 200 000 compounds, which are not directly involved in plant growth and development but play important roles in helping plants handle their environment including the mediation of plant–insect interactions. Here, we use plant volatile organic compounds (VOCs), a key olfactory communication channel that mediates plant–insect interactions, as a showcase of PSMs. In spite of the cumulative knowledge of the functional, ecological, and microevolutionary roles of VOCs, we still lack a macroevolutionary understanding of how they evolved with plant–insect interactions and contributed to species diversity throughout the long coevolutionary history of plants and insects. We first review the literature to summarize the current state-of-the-art research on this topic. We then present various relevant types of phylogenetic methods suitable to answer macroevolutionary questions on plant VOCs and suggest future directions for employing phylogenetic approaches in studying plant VOCs and plant–insect interactions. Overall, we found that current studies in this field are still very limited in their macroevolutionary perspective. Nevertheless, with the fast-growing development of metabolome analysis techniques and phylogenetic methods, it is becoming increasingly feasible to integrate the advances of these two areas. We highlight promising approaches to generate new testable hypotheses and gain a mechanistic understanding of the macroevolutionary roles of chemical communication in plant–insect interactions.     

INTEGRATING FOSSILS WITH MOLECULAR PHYLOGENIES IMPROVES INFERENCE OF TRAIT EVOLUTION

Comparative biologists often attempt to draw inferences about tempo and mode in evolution by comparing the fit of evolutionary models to phylogenetic comparative data consisting of a molecular phylogeny with branch lengths and trait measurements from extant taxa. These kinds of approaches ignore historical evidence for evolutionary pattern and process contained in the fossil record. In this article, we show through simulation that incorporation of fossil information dramatically improves our ability to distinguish among models of quantitative trait evolution using comparative data. We further suggest a novel Bayesian approach that allows fossil information to be integrated even when explicit phylogenetic hypotheses are lacking for extinct representatives of extant clades. By applying this approach to a comparative dataset comprising body sizes for caniform carnivorans, we show that incorporation of fossil information not only improves ancestral state estimates relative to those derived from extant taxa alone, but also results in preference of a model of evolution with trend toward large body size over alternative models such as Brownian motion or Ornstein–Uhlenbeck processes. Our approach highlights the importance of considering fossil information when making macroevolutionary inference, and provides a way to integrate the kind of sparse fossil information that is available to most evolutionary biologists.     

TRANSLATING BETWEEN MICROEVOLUTIONARY PROCESS AND MACROEVOLUTIONARY PATTERNS: THE CORRELATION STRUCTURE OF INTERSPECIFIC DATA

As species evolve along a phylogenetic tree, we expect closely related species to retain some phenotypic similarities due to their shared evolutionary histories. The amount of expected similarity depends both on the hierarchical phylogenetic structure, and on the specific magnitude and types of evolutionary changes that accumulate during each generation. In this study, we show how models of microevolutionary change can be translated into the resulting macroevolutionary patterns. We illustrate how the structure of phenotypic covariances expected in interspecific measurements can be derived, and how this structure depends on the microevolutionary forces guiding phenotypic change at each generation. We then explore the covariance structure expected from several simple microevolutionary models of phenotypic evolution, including various combinations of random genetic drift, directional selection, stabilizing selection, and environmental change, as well as models of punctuated or burst-like evolution. We find that stabilizing selection leads to patterns of exponential decrease of between species covariance with phylogenetic distance. This is different from the usual linear patterns of decrease assumed in most comparative and systematic methods. Nevertheless, linear patterns of decrease can result from many processes in addition to random genetic drift, such as directional and fluctuating selection as well as modes of punctuated change. Our framework can be used to develop methods for (1) phylogenetic reconstruction; (2) inference of the evolutionary process from comparative data; and (3) conducting or evaluating statistical analyses of comparative data while taking phylogenetic history into account.     

Convergent evolution of floral shape tied to pollinator shifts in Iochrominae (Solanaceae)*

Flower form is one of many floral features thought to be shaped by pollinator‐mediated selection. Although the drivers of variation in flower shape have often been examined in microevolutionary studies, relatively few have tested the relationship between shape evolution and shifts in pollination system across clades. In the present study, we use morphometric approaches to quantify shape variation across the Andean clade Iochrominae and estimate the relationship between changes in shape and shifts in pollination system using phylogenetic comparative methods. We infer multiple shifts from an ancestral state of narrow, tubular flowers toward open, bowl‐shaped, or campanulate flowers as well as one reversal to the tubular form. These transitions in flower shape are significantly correlated with changes in pollination system. Specifically, tubular forms tend to be hummingbird‐pollinated and the open forms tend to be insect‐pollinated, a pattern consistent with experimental work as well as classical floral syndromes. Nonetheless, our study provides one of the few empirical demonstrations of the relationship between flower shape and pollination system at a macroevolutionary scale.     

Genome evolution in polyploids

Polyploidy is a prominent process in plants and has been significant in the evolutionary history of vertebrates and other eukaryotes. In plants, interdisciplinary approaches combining phylogenetic and molecular genetic perspectives have enhanced our awareness of the myriad genetic interactions made possible by polyploidy. Here, processes and mechanisms of gene and genome evolution in polyploids are reviewed. Genes duplicated by polyploidy may retain their original or similar function, undergo diversification in protein function or regulation, or one copy may become silenced through mutational or epigenetic means. Duplicated genes also may interact through inter-locus recombination, gene conversion, or concerted evolution. Recent experiments have illuminated important processes in polyploids that operate above the organizational level of duplicated genes. These include inter-genomic chromosomal exchanges, saltational, non-Mendelian genomic evolution in nascent polyploids, inter-genomic invasion, and cytonuclear stabilization. Notwithstanding many recent insights, much remains to be learned about many aspects of polyploid evolution, including: the role of transposable elements in structural and regulatory gene evolution; processes and significance of epigenetic silencing; underlying controls of chromosome pairing; mechanisms and functional significance of rapid genome changes; cytonuclear accommodation; and coordination of regulatory factors contributed by two, sometimes divergent progenitor genomes. Continued application of molecular genetic approaches to questions of polyploid genome evolution holds promise for producing lasting insight into processes by which novel genotypes are generated and ultimately into how polyploidy facilitates evolution and adaptation.     

Ecomorphological variation in male and female wall lizards and the macroevolution of sexual dimorphism in relation to habitat use

Understanding how phenotypic diversity evolves is a major interest of evolutionary biology. Habitat use is an important factor in the evolution of phenotypic diversity of many animal species. Interestingly, male and female phenotypes have been frequently shown to respond differently to environmental variation. At the macroevolutionary level, this difference between the sexes is frequently analysed using phylogenetic comparative tools to assess variation in sexual dimorphism (SD) across taxa in relation to habitat. A shortcoming of such analyses is that they evaluate the degree of dimorphism itself and therefore they do not provide access to the evolutionary trajectories of each sex. As such, the relative contribution of male and female phenotypes on macroevolutionary patterns of sexual dimorphism cannot be directly assessed. Here, we investigate how habitat use shapes phenotypic diversity in wall lizards using phylogenetic comparative tools to simultaneously assess the tempo and mode of evolution in males, females and the degree of sexual dimorphism. We find that both sexes have globally diversified under similar, but not identical, processes, where habitat use seems to drive macroevolutionary variation in head shape, but not in body size or relative limb length. However, we also observe small differences in the evolutionary dynamics of male and female phenotypes that have a marked impact on macroevolutionary patterns of SD, with important implications for our interpretation of what drives phenotypic diversification within and between the sexes.     

A macroevolutionary perspective on species range limits

Understanding the factors that determine the geographic range limits of species is important for many questions in ecology, evolution and conservation biology. These limits arise from complex interactions among ecology and dispersal ability of species and the physical environment, but many of the underlying traits can be conserved among related species and clades. Thus, the range limits of species are likely to be influenced by their macroevolutionary history. Using palaeontological and biogeographic data for marine bivalves, we find that the range limits of genera are significantly related to their constituent species richness, but the effects of age are weak and inconsistent. In addition, we find a significant phylogenetic signal in the range limits at both genus and family levels, although the strength of this effect shows interoceanic variation. This phylogenetic conservatism of range limits gives rise to an evolutionary pattern where wide-ranging lineages have clusters of species within the biogeographic provinces, with a few extending across major boundaries.     

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.     

The Embedding Problem for Markov Models of Nucleotide Substitution

Continuous-time Markov processes are often used to model the complex natural phenomenon of sequence evolution. To make the process of sequence evolution tractable, simplifying assumptions are often made about the sequence properties and the underlying process. The validity of one such assumption, time-homogeneity, has never been explored. Violations of this assumption can be found by identifying non-embeddability. A process is non-embeddable if it can not be embedded in a continuous time-homogeneous Markov process. In this study, non-embeddability was demonstrated to exist when modelling sequence evolution with Markov models. Evidence of non-embeddability was found primarily at the third codon position, possibly resulting from changes in mutation rate over time. Outgroup edges and those with a deeper time depth were found to have an increased probability of the underlying process being non-embeddable. Overall, low levels of non-embeddability were detected when examining individual edges of triads across a diverse set of alignments. Subsequent phylogenetic reconstruction analyses demonstrated that non-embeddability could impact on the correct prediction of phylogenies, but at extremely low levels. Despite the existence of non-embeddability, there is minimal evidence of violations of the local time homogeneity assumption and consequently the impact is likely to be minor.