Variation of tooth number in mammalian dentition: connecting genetics,development, and evolution

A major question in modern biology is how gene mutations affect development and are translated into macroevolutionary changes in morphology. Variations in tooth number, a strategy used by many mammals to develop specialized dentitions, has been an important factor for species diversification. Changes in the number of teeth tend to occur in the reverse of the order teeth are formed during development, which also characterizes the general pattern of tooth loss observed during the evolution of placental mammals. To understand how changes at the molecular level affect the distinct stages of tooth development, we analyzed the ontogenesis of tooth growth arrest in sciurids and mice and in single and double knockout mutant mice. We show that the complexity of the genetic network that governs tooth development can change during ontogenetic trajectory, and these changes may be related to macroevolutionary changes. Furthermore, we show that the variation in tooth number in the affected members of human families bearing mutations in the MSX1 and PAX9 genes can help to understand how the genetic variations within a population can modulate evolutionary changes in dental patterning.     

An emerging synthesis between community ecology and evolutionary biology

A synthesis between community ecology and evolutionary biology is emerging that identifies how genetic variation and evolution within one species can shape the ecological properties of entire communities and, in turn, how community context can govern evolutionary processes and patterns. This synthesis incorporates research on the ecology and evolution within communities over short timescales (community genetics and diffuse coevolution), as well as macroevolutionary timescales (community phylogenetics and co-diversification of communities). As we discuss here, preliminary evidence supports the hypothesis that there is a dynamic interplay between ecology and evolution within communities, yet researchers have not yet demonstrated convincingly whether, and under what circumstances, it is important for biologists to bridge community ecology and evolutionary biology. Answering this question will have important implications for both basic and applied problems in biology.     

Tempo and mode of performance evolution across multiple independent origins of adhesive toe pads in lizards

Understanding macroevolutionary dynamics of trait evolution is an important endeavor in evolutionary biology. Ecological opportunity can liberate a trait as it diversifies through trait space, while genetic and selective constraints can limit diversification. While many studies have examined the dynamics of morphological traits, diverse morphological traits may yield the same or similar performance and as performance is often more proximately the target of selection, examining only morphology may give an incomplete understanding of evolutionary dynamics. Here, we ask whether convergent evolution of pad‐bearing lizards has followed similar evolutionary dynamics, or whether independent origins are accompanied by unique constraints and selective pressures over macroevolutionary time. We hypothesized that geckos and anoles each have unique evolutionary tempos and modes. Using performance data from 59 species, we modified Brownian motion (BM) and Ornstein–Uhlenbeck (OU) models to account for repeated origins estimated using Bayesian ancestral state reconstructions. We discovered that adhesive performance in geckos evolved in a fashion consistent with Brownian motion with a trend, whereas anoles evolved in bounded performance space consistent with more constrained evolution (an Ornstein–Uhlenbeck model). Our results suggest that convergent phenotypes can have quite distinctive evolutionary patterns, likely as a result of idiosyncratic constraints or ecological opportunities.     

Do arms races punctuate evolutionary stasis? Unified insights from phylogeny,phylogeography and microevolutionary processes

One of the major controversies in evolutionary biology concerns the processes underlying macroevolutionary patterns in which prolonged stasis is disrupted by rapid, short-term evolution that leads species to new adaptive zones. Recent advances in the understanding of contemporary evolution have suggested that such rapid evolution can occur in the wild as a result of environmental changes. Here, we examined a novel hypothesis that evolutionary stasis is punctuated by co-evolutionary arms races, which continuously alter adaptive peaks and landscapes. Based on the phylogeny of long-mouthed weevils in the genus Curculio , likelihood ratio tests showed that the macroevolutionary pattern of the weevils coincides with the punctuational evolution model. A coalescent analysis of a species, Curculio camelliae , the mouthpart of which has diverged considerably among populations because of an arms race with its host plant, further suggested that major evolutionary shifts had occurred within 7000 generations. Through a microevolutionary analysis of the species, we also found that natural selection acting through co-evolutionary interactions is potentially strong enough to drive rapid evolutionary shifts between adaptive zones. Overall, we posit that co-evolution is an important factor driving the history of organismal evolution.     

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.     

SCALE AND HIERARCHY IN MACROEVOLUTION

Abstract: Scale and hierarchy must be incorporated into any conceptual framework for the study of macroevolution, i.e. evolution above the species level. Expansion of temporal and spatial scales reveals evolutionary patterns and processes that are virtually inaccessible to, and unpredictable from, short‐term, localized observations. These larger‐scale phenomena range from evolutionary stasis at the species level and the mosaic assembly of complex morphologies in ancestral forms to the non‐random distribution in time and space of the origin of major evolutionary novelties, as exemplified by the Cambrian explosion and post‐extinction recoveries of metazoans, and the preferential origin of major marine groups in onshore environments and tropical waters. Virtually all of these phenomena probably involve both ecological and developmental factors, but the integration of these components with macroevolutionary theory has only just begun. Differential survival and reproduction of units can occur at several levels within a biological hierarchy that includes DNA sequences, organisms, species and clades. Evolution by natural selection can occur at any level where there is heritable variation that affects birth and death of units by virtue of interaction with the environment. This dynamic can occur when selfish DNA sequences replicate disproportionately within genomes, when organisms enjoy fitness advantages within populations (classical Darwinian selection), when differential speciation or extinction occurs within clades owing to organismic properties (effect macroevolution), and when differential speciation or extinction occurs within clades owing to emergent, species‐level properties (in the strict sense species selection). Operationally, emergent species‐level properties such as geographical range can be recognized by testing whether their macroevolutionary effects are similar regardless of the different lower‐level factors that produce them. Large‐scale evolutionary trends can be driven by transformation of species, preferential production of species in a given direction, differential origination or extinction, or any combination of these; the potential for organismic traits to hitch‐hike on other factors that promote speciation or damp extinction is high. Additional key attributes of macroevolutionary dynamics within biological hierarchies are that (1) hierarchical levels are linked by upward and downward causation, so that emergent properties at a focal level do not impart complete independence; (2) hierarchical effects are asymmetrical, so that dynamics at a given focal level need not propagate upwards, but will always cascade downwards; and (3) rates are generally, although not always, faster at lower hierarchical levels. Temporal and spatial patterns in the origin of major novelties and higher taxa are significantly discordant from those at the species and genus levels, suggesting complex hierarchical effects that remain poorly understood. Not only are many of the features promoting survivorship during background times ineffective during mass extinctions, but also they are replaced in at least some cases by higher‐level, irreducible attributes such as clade‐level geographical range. The incorporation of processes that operate across hierarchical levels and a range of temporal and spatial scales has expanded and enriched our understanding of evolution.     

Habitat transitions alter the adaptive landscape and shape phenotypic evolution in needlefishes (Belonidae)

Habitat occupancy can have a profound influence on macroevolutionary dynamics, and a switch in major habitat type may alter the evolutionary trajectory of a lineage. In this study, we investigate how evolutionary transitions between marine and freshwater habitats affect macroevolutionary adaptive landscapes, using needlefishes (Belonidae) as a model system. We examined the evolution of body shape and size in marine and freshwater needlefishes and tested for phenotypic change in response to transitions between habitats. Using micro‐computed tomographic (µCT) scanning and geometric morphometrics, we quantified body shape, size, and vertebral counts of 31 belonid species. We then examined the pattern and tempo of body shape and size evolution using phylogenetic comparative methods. Our results show that transitions from marine to freshwater habitats have altered the adaptive landscape for needlefishes and expanded morphospace relative to marine taxa. We provide further evidence that freshwater taxa attain reduced sizes either through dwarfism (as inferred from axial skeletal reduction) or through developmental truncation (as inferred from axial skeletal loss). We propose that transitions to freshwater habitats produce morphological novelty in response to novel prey resources and changes in locomotor demands. We find that repeated invasions of different habitats have prompted predictable changes in morphology.     

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.     

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.     

Rates of evolution on the time scale of the evolutionary process

A generational time scale, involving change from one generation to the next, is the time scale of evolution by natural selection. Microevolutionary and macroevolutionary patterns reflect this process on longer time scales. Rates of evolution are most efficiently expressed in haldane units, H, in standard deviations per generation, indexed by the log of the time interval. Rates from replicated selection experiments and simulations have rate-interval [RI] and log rate-log interval [LRI] scaling relations enabling directional, stationary, and random time series to be distinguished. Empirical microevolutionary and macroevolutionary data exhibit stationary scaling, but point to generational rates of evolution (H ₀) conservatively on the order of 0.2 standard deviations per generation on the time scale of the evolutionary process. This paradox of long-term stationary scaling and short-term high rates of change can be explained by considering the shape of an heuristic time-form evolutionary lattice. Cenozoic mammals occupy a lattice that is about four orders of magnitude longer in time than it has ever been wide in form. The evolutionary process is dynamic but operates within relatively narrow morphological constraints compared to the time available for change.     

Macroevolutionary synthesis of flowering plant sexual systems

Sexual system is a key determinant of genetic variation and reproductive success, affecting evolution within populations and within clades. Much research in plants has focused on evolutionary transitions away from the most common state of hermaphroditism and toward the rare state of dioecy (separate sexes). Rather than transitions predominantly toward greater sexual differentiation, however, evolution may proceed in the direction of lesser sexual differentiation. We analyzed the macroevolutionary dynamics of sexual system in angiosperm genera that contain both dioecious and nondioecious species. Our phylogenetic analyses encompass a total of 2145 species from 40 genera. Overall, we found little evidence that rates of sexual system transitions are greater in any direction. Counting the number of inferred state changes revealed a mild prevalence of transitions away from hermaphroditism and away from dioecy, toward states of intermediate sexual differentiation. We identify genera in which future studies of sexual system evolution might be especially productive, and we discuss how integrating genetic or population‐level studies of sexual system could improve the power of phylogenetic comparative analyses. Our work adds to the evidence that different selective pressures and constraints act in different groups, helping maintain the variety of sexual systems observed among plants.     

MOLECULAR PALAEOBIOLOGY

Abstract:  For more than a generation, molecular biology has been used to approach palaeontological problems, and yet only recently have attempts been made to integrate research utilizing the geological and genomic records in uncovering evolutionary history. We codify this approach as Molecular Palaeobiology for which we provide a synthetic framework for studying the interplay among genotype, phenotype and the environment, within the context of deep time. We provide examples of existing studies where molecular and morphological data have been integrated to provide novel insights within each of these variables, and an account of a case study where each variable has been tackled to understand better a single macroevolutionary event: the diversification of metazoan phyla. We show that the promise of this approach extends well beyond research into the evolutionary history of animals and, in particular, we single out plant evolution as the single greatest opportunity waiting to be exploited by molecular palaeobiology. Although most of our examples consider how novel molecular data and techniques have breathed new life into long-standing palaeontological controversies, we argue that this asymmetry in the balance of molecular and morphological evidence is an artefact of the relative 'newness' of molecular data. In particular, palaeontological data provide unique and crucial roles in unravelling evolutionary history given that extinct taxa reveal patterns of character evolution invisible to molecular biology. Finally, we argue that palaeobiologists, rather than molecular biologists, are best placed to exploit the opportunity afforded by molecular palaeobiology, though this will require incorporating the techniques and approaches of molecular biology into their skill-set.     

Biodiversity inhibits species' evolutionary responses to changing environments

Despite growing interplay between ecological and evolutionary studies, the question of how biodiversity influences evolutionary dynamics within species remains understudied. Here, using a classical model of phenotypic evolution in species occupying a patchy environment, but introducing global change affecting patch conditions, we show that biodiversity can inhibit species' evolution during global change. The presence of several species increases the chance that one or more species are pre-adapted to new conditions, which restricts the ecological opportunity for evolutionary responses in all the species. Consequently, environmental change tends to select for changes in species abundances rather than for changing phenotypes within each species. The buffering effects of species diversity that we describe might be one important but neglected explanation for widely observed niche conservatism in natural systems. Furthermore, the results show that attempts to understand biotic responses to environmental change need to consider both ecological and evolutionary processes in a realistically diverse setting.     

Eco‐evolutionary partitioning metrics: assessing the importance of ecological and evolutionary contributions to population and community change

Interest in eco‐evolutionary dynamics is rapidly increasing thanks to ground‐breaking research indicating that evolution can occur rapidly and can alter the outcome of ecological processes. A key challenge in this sub‐discipline is establishing how important the contribution of evolutionary and ecological processes and their interactions are to observed shifts in population and community characteristics. Although a variety of metrics to separate and quantify the effects of evolutionary and ecological contributions to observed trait changes have been used, they often allocate fractions of observed changes to ecology and evolution in different ways. We used a mathematical and numerical comparison of two commonly used frameworks – the Price equation and reaction norms – to reveal that the Price equation cannot partition genetic from non‐genetic trait change within lineages, whereas the reaction norm approach cannot partition among‐ from within‐lineage trait change. We developed a new metric that combines the strengths of both Price‐based and reaction norm metrics, extended all metrics to analyse community change and also incorporated extinction and colonisation of species in these metrics. Depending on whether our new metric is applied to populations or communities, it can correctly separate intraspecific, interspecific, evolutionary, non‐evolutionary and interacting eco‐evolutionary contributions to trait change.     

STABILIZING SELECTION AND THE COMPARATIVE ANALYSIS OF ADAPTATION

Comparative studies tend to differ from optimality and functionality studies in how they treat adaptation. While the comparative approach focuses on the origin and change of traits, optimality studies assume that adaptations are maintained at an optimum by stabilizing selection. This paper presents a model of adaptive evolution on a macroevolutionary time scale that includes the maintenance of traits at adaptive optima by stabilizing selection as the dominant evolutionary force. Interspecific variation is treated as variation in the position of adaptive optima. The model illustrates how phylogenetic constraints not only lead to correlations between phylogenetically related species, but also to imperfect adaptations. From this model, a statistical comparative method is derived that can be used to estimate the effect of a selective factor on adaptive optima in a way that would be consistent with an optimality study of adaptation to this factor. The method is illustrated with an analysis of dental evolution in fossil horses. The use of comparative methods to study evolutionary trends is also discussed.     

Investigating the eco-evolutionary response of microbiomes to environmental change

Microorganisms are the primary engines of biogeochemical processes and foundational to the provisioning of ecosystem services to human society. Free-living microbial communities (microbiomes) and their functioning are now known to be highly sensitive to environmental change. Given microorganisms' capacity for rapid evolution, evolutionary processes could play a role in this response. Currently, however, few models of biogeochemical processes explicitly consider how microbial evolution will affect biogeochemical responses to environmental change. Here, we propose a conceptual framework for explicitly integrating evolution into microbiome–functioning relationships. We consider how microbiomes respond simultaneously to environmental change via four interrelated processes that affect overall microbiome functioning (physiological acclimation, demography, dispersal and evolution). Recent evidence in both the laboratory and the field suggests that ecological and evolutionary dynamics occur simultaneously within microbiomes; however, the implications for biogeochemistry under environmental change will depend on the timescales over which these processes contribute to a microbiome's response. Over the long term, evolution may play an increasingly important role for microbially driven biogeochemical responses to environmental change, particularly to conditions without recent historical precedent.     

Students’ Mental Models of Evolutionary Causation: Natural Selection and Genetic Drift

In an effort to understand how to improve student learning about evolution, a focus of science education research has been to document and address students?? naive ideas. Less research has investigated how students reason about alternative scientific models that attempt to explain the same phenomenon (e.g., which causal model best accounts for evolutionary change?). Within evolutionary biology, research has yet to explore how non-adaptive factors are situated within students?? conceptual ecologies of evolutionary causation. Do students construct evolutionary explanations that include non-adaptive and adaptive factors? If so, how are non-adaptive factors structured within students?? evolutionary explanations? We used clinical interviews and two paper and pencil instruments (one open-response and one multiple-choice) to investigate the use of non-adaptive and adaptive factors in undergraduate students?? patterns of evolutionary reasoning. After instruction that included non-adaptive causal factors (e.g., genetic drift), we found them to be remarkably uncommon in students?? explanatory models of evolutionary change in both written assessments and clinical interviews. However, consistent with many evolutionary biologists?? explanations, when students used non-adaptive factors they were conceptualized as causal alternatives to selection. Interestingly, use of non-adaptive factors was not associated with greater understanding of natural selection in interviews or written assessments, or with fewer naive ideas of natural selection. Thus, reasoning using non-adaptive factors appears to be a distinct facet of evolutionary thinking. We propose a theoretical framework for an expert?Cnovice continuum of evolutionary reasoning that incorporates both adaptive and non-adaptive factors, and can be used to inform instructional efficacy in evolutionary biology.     

Phenotypic integration: studying the ecology and evolution of complex phenotypes

Phenotypic integration refers to the study of complex patterns of covariation among functionally related traits in a given organism. It has been investigated throughout the 20th century, but has only recently risen to the forefront of evolutionary ecological research. In this essay, I identify the reasons for this late flourishing of studies on integration, and discuss some of the major areas of current endeavour: the interplay of adaptation and constraints, the genetic and molecular bases of integration, the role of phenotypic plasticity, macroevolutionary studies of integration, and statistical and conceptual issues in the study of the evolution of complex phenotypes. I then conclude with a brief discussion of what I see as the major future directions of research on phenotypic integration and how they relate to our more general quest for the understanding of phenotypic evolution within the neo‐Darwinian framework. I suggest that studying integration provides a particularly stimulating and truly interdisciplinary convergence of researchers from fields as disparate as molecular genetics, developmental biology, evolutionary ecology, palaeontology and even philosophy of science.