Combining Molecular, Macroevolutionary, and Macroecological Perspectives on the Generation of Diversity.

Charles Darwin presented a unified process of diversification driven by the gradual accumulation of heritable variation. The growth in DNA databases and the increase in genomic sequencing, combined with advances in molecular phylogenetic analyses, gives us an opportunity to realize Darwin's vision, connecting the generation of variation to the diversification of lineages. The rate of molecular evolution is correlated with the rate of diversification across animals and plants, but the relationship between genome change and speciation is complex: Mutation rates evolve in response to life history and niche; substitution rates are influenced by mutation, selection, and population size; rates of acquisition of reproductive isolation vary between populations; and traits, niches, and distribution can influence diversification rates. The connection between mutation rate and diversification rate is one part of the complex and varied story of speciation, which has theoretical importance for understanding the generation of biodiversity and also practical impacts on the use of DNA to understand the dynamics of speciation over macroevolutionary timescales.

Neighbours and relatives: accounting for spatial distribution when testing causal hypotheses in cultural evolution.

Many important and interesting hypotheses about cultural evolution are evaluated using cross-cultural correlations: if knowing one particular feature of a culture (e.g. environmental conditions such as temperature, humidity or parasite load) allows you to predict other features (e.g. language features, religious beliefs, cuisine), it is often interpreted as indicating a causal link between the two (e.g. hotter climates carry greater disease risk, which encourages belief in supernatural forces and favours the use of antimicrobial ingredients in food preparation; dry climates make the production of distinct tones more difficult). However, testing such hypotheses from cross-cultural comparisons requires us to take proximity of cultures into account: nearby cultures share many aspects of their environment and are more likely to be similar in many culturally inherited traits. This can generate indirect associations between environment and culture which could be misinterpreted as signals of a direct causal link. Evaluating examples of cross-cultural correlations from the literature, we show that significant correlations interpreted as causal relationships can often be explained as a result of similarity between neighbouring cultures. We discuss some strategies for sorting the explanatory wheat from the co-varying chaff, distinguishing incidental correlations from causal relationships.

Investigating the reliability of molecular estimates of evolutionary time when substitution rates and speciation rates vary.

BACKGROUND: An accurate timescale of evolutionary history is essential to testing hypotheses about the influence of historical events and processes, and the timescale for evolution is increasingly derived from analysis of DNA sequences. But variation in the rate of molecular evolution complicates the inference of time from DNA. Evidence is growing for numerous factors, such as life history and habitat, that are linked both to the molecular processes of mutation and fixation and to rates of macroevolutionary diversification. However, the most widely used methods rely on idealised models of rate variation, such as the uncorrelated and autocorrelated clocks, and molecular dating methods are rarely tested against complex models of rate change. One relationship that is not accounted for in molecular dating is the potential for interaction between molecular substitution rates and speciation, a relationship that has been supported by empirical studies in a growing number of taxa. If these relationships are as widespread as current evidence suggests, they may have a significant influence on molecular dates. RESULTS: We simulate phylogenies and molecular sequences under three different realistic rate variation models-one in which speciation rates and substitution rates both vary but are unlinked, one in which they covary continuously and one punctuated model in which molecular change is concentrated in speciation events, using empirical case studies to parameterise realistic simulations. We test three commonly used "relaxed clock" molecular dating methods against these realistic simulations to explore the degree of error in molecular dates under each model. We find average divergence time inference errors ranging from 12% of node age for the unlinked model when reconstructed under an uncorrelated rate prior using BEAST 2, to up to 91% when sequences evolved under the punctuated model are reconstructed under an autocorrelated prior using PAML. CONCLUSIONS: We demonstrate the potential for substantial errors in molecular dates when both speciation rates and substitution rates vary between lineages. This study highlights the need for tests of molecular dating methods against realistic models of rate variation generated from empirical parameters and known relationships.

Diversification Rate is Associated with Rate of Molecular Evolution in Ray-Finned Fish (Actinopterygii).

Understanding the factors that drive diversification of taxa across the tree of life is a key focus of macroevolutionary research. While the effects of life history, ecology, climate and geography on diversity have been studied for many taxa, the relationship between molecular evolution and diversification has received less attention. However, correlations between rates of molecular evolution and diversification rate have been detected in a range of taxa, including reptiles, plants and birds. A correlation between rates of molecular evolution and diversification rate is a prediction of several evolutionary theories, including the evolutionary speed hypothesis which links variation in mutation rates to differences in speciation rates. If it is widespread, such correlations could also have significant practical impacts, if they are not adequately accounted for in phylogenetic inference of evolutionary rates and timescales. Ray-finned fish (Actinopterygii) offer a prime target to test for this relationship due to their extreme variation in clade size suggesting a wide range of diversification rates. We employ both a sister-pairs approach and a whole-tree approach to test for correlations between substitution rate and net diversification. We also collect life history and ecological trait data and account for potential confounding factors including body size, latitude, max depth and reef association. We find evidence to support a relationship between diversification and synonymous rates of nuclear evolution across two published backbone phylogenies, as well as weak evidence for a relationship between mitochondrial nonsynonymous rates and diversification at the genus level.

Global predictors of language endangerment and the future of linguistic diversity.

Language diversity is under threat. While each language is subject to specific social, demographic and political pressures, there may also be common threatening processes. We use an analysis of 6,511 spoken languages with 51 predictor variables spanning aspects of population, documentation, legal recognition, education policy, socioeconomic indicators and environmental features to show that, counter to common perception, contact with other languages per se is not a driver of language loss. However, greater road density, which may encourage population movement, is associated with increased endangerment. Higher average years of schooling is also associated with greater endangerment, evidence that formal education can contribute to loss of language diversity. Without intervention, language loss could triple within 40 years, with at least one language lost per month. To avoid the loss of over 1,500 languages by the end of the century, urgent investment is needed in language documentation, bilingual education programmes and other community-based programmes.

There is little evidence that spicy food in hot countries is an adaptation to reducing infection risk.

Spicier food in hot countries has been explained in terms of natural selection on human cultures, with spices with antimicrobial effects considered to be an adaptation to increased risk of foodborne infection. However, correlations between culture and environment are difficult to interpret, because many cultural traits are inherited together from shared ancestors, neighbouring cultures are exposed to similar conditions, and many cultural and environmental variables show strong covariation. Here, using a global dataset of 33,750 recipes from 70 cuisines containing 93 different spices, we demonstrate that variation in spice use is not explained by temperature and that spice use cannot be accounted for by diversity of cultures, plants, crops or naturally occurring spices. Patterns of spice use are not consistent with an infection-mitigation mechanism, but are part of a broader association between spice, health, and poverty. This study highlights the challenges inherent in interpreting patterns of human cultural variation in terms of evolutionary pressures.

Modeling colonization rates over time: Generating null models and testing model adequacy in phylogenetic analyses of species assemblages.

A central theme connecting macroevolutionary processes to macroecological patterns is the shaping of regional biodiversity over time through speciation, extinction, migration, and range shifts. The use of phylogenies to explore the dynamics of diversification due to variation in speciation and extinction rates has been well-developed and there are established methods for inferring speciation times from phylogenies and generating its null distributions (as represented by node heights on molecular phylogenies). But inferring colonization events from phylogenies is more challenging. Unlike speciation events, represented by nodes, colonization events could occur at any point along a branch connecting species in the assemblage to the regional pool. We account for uncertainty in identification of colonization lineages and timing of colonization events by using an efficient analytical solution to inferring the distribution of colonization times from an assemblage phylogeny. Using the same solution, we efficiently derive the null distribution of colonization times, which provides us with a general approach to testing the adequacy of a model to describe colonization events into the assemblage. We illustrate this approach by demonstrating how the movement of squamate lineages into Madagascar has been uneven over time, peaking in the early Cenozoic when ocean conditions favored colonization.

Macroevolutionary and macroecological approaches to understanding the evolution of stress tolerance in plants.

Environmental stress response in plants has been studied using a wide range of approaches, from lab-based investigation of biochemistry and genetics, to glasshouse studies of physiology and growth rates, to field-based trials and ecological surveys. It is also possible to investigate the evolution of environmental stress responses using macroevolutionary and macroecological analyses, analysing data from many different species, providing a new perspective on the way that environmental stress shapes the evolution and distribution of biodiversity. "Macroevoeco" approaches can produce intriguing results and new ways of looking at old problems. In this review, we focus on studies using phylogenetic analysis to illuminate macroevolutionary patterns in the evolution of environmental stress tolerance in plants. We follow a particular thread from our own research-evolution of salt tolerance-as a case study that illustrates a macroevolutionary way of thinking that opens up a range of broader questions on the evolution of environmental stress tolerances. We consider some potential future applications of macroevolutionary and macroecological analyses to understanding how diverse groups of plants evolve in response to environmental stress, which may allow better prediction of current stress tolerance and a way of predicting the capacity of species to adapt to changing environmental stresses over time.

A phylogenomic approach reveals a low somatic mutation rate in a long-lived plant.

Somatic mutations can have important effects on the life history, ecology, and evolution of plants, but the rate at which they accumulate is poorly understood and difficult to measure directly. Here, we develop a method to measure somatic mutations in individual plants and use it to estimate the somatic mutation rate in a large, long-lived, phenotypically mosaic Eucalyptus melliodora tree. Despite being 100 times larger than Arabidopsis, this tree has a per-generation mutation rate only ten times greater, which suggests that this species may have evolved mechanisms to reduce the mutation rate per unit of growth. This adds to a growing body of evidence that illuminates the correlated evolutionary shifts in mutation rate and life history in plants.

The ecological drivers of variation in global language diversity.

Language diversity is distributed unevenly over the globe. Intriguingly, patterns of language diversity resemble biodiversity patterns, leading to suggestions that similar mechanisms may underlie both linguistic and biological diversification. Here we present the first global analysis of language diversity that compares the relative importance of two key ecological mechanisms - isolation and ecological risk - after correcting for spatial autocorrelation and phylogenetic non-independence. We find significant effects of climate on language diversity, consistent with the ecological risk hypothesis that areas of high year-round productivity lead to more languages by supporting human cultural groups with smaller distributions. Climate has a much stronger effect on language diversity than landscape features, such as altitudinal range and river density, which might contribute to isolation of cultural groups. The association between biodiversity and language diversity appears to be an incidental effect of their covariation with climate, rather than a causal link between the two.

Six Impossible Things before Breakfast: Assumptions, Models, and Belief in Molecular Dating.

Confidence in molecular dating analyses has grown with the increasing sophistication of the methods. Some problematic cases where molecular dates disagreed with paleontological estimates appear to have been resolved with a growing agreement between molecules and fossils. But we cannot relax just yet. The growing analytical sophistication of many molecular dating methods relies on an increasingly large number of assumptions about evolutionary history and processes. Many of these assumptions are based on statistical tractability rather than being informed by improved understanding of molecular evolution, yet changing the assumptions can influence molecular dates. How can we tell if the answers we get are driven more by the assumptions we make than by the molecular data being analyzed?

Parasites and politics: why cross-cultural studies must control for relatedness, proximity and covariation.

A growing number of studies seek to identify predictors of broad-scale patterns in human cultural diversity, but three sources of non-independence in human cultural variables can bias the results of cross-cultural studies. First, related cultures tend to have many traits in common, regardless of whether those traits are functionally linked. Second, societies in geographical proximity will share many aspects of culture, environment and demography. Third, many cultural traits covary, leading to spurious relationships between traits. Here, we demonstrate tractable methods for dealing with all three sources of bias. We use cross-cultural analyses of proposed associations between human cultural traits and parasite load to illustrate the potential problems of failing to correct for these three forms of statistical non-independence. Associations between parasite stress and sociosexuality, authoritarianism, democracy and language diversity are weak or absent once relatedness and proximity are taken into account, and parasite load has no more power to explain variation in traditionalism, religiosity and collectivism than other measures of biodiversity, climate or population size do. Without correction for statistical non-independence and covariation in cross-cultural analyses, we risk misinterpreting associations between culture and environment.

Population Size and the Rate of Language Evolution: A Test Across Indo-European, Austronesian, and Bantu Languages.

What role does speaker population size play in shaping rates of language evolution? There has been little consensus on the expected relationship between rates and patterns of language change and speaker population size, with some predicting faster rates of change in smaller populations, and others expecting greater change in larger populations. The growth of comparative databases has allowed population size effects to be investigated across a wide range of language groups, with mixed results. One recent study of a group of Polynesian languages revealed greater rates of word gain in larger populations and greater rates of word loss in smaller populations. However, that test was restricted to 20 closely related languages from small Oceanic islands. Here, we test if this pattern is a general feature of language evolution across a larger and more diverse sample of languages from both continental and island populations. We analyzed comparative language data for 153 pairs of closely-related sister languages from three of the world's largest language families: Austronesian, Indo-European, and Niger-Congo. We find some evidence that rates of word loss are significantly greater in smaller languages for the Indo-European comparisons, but we find no significant patterns in the other two language families. These results suggest either that the influence of population size on rates and patterns of language evolution is not universal, or that it is sufficiently weak that it may be overwhelmed by other influences in some cases. Further investigation, for a greater number of language comparisons and a wider range of language features, may determine which of these explanations holds true.

Bayesian molecular dating: opening up the black box.

Molecular dating analyses allow evolutionary timescales to be estimated from genetic data, offering an unprecedented capacity for investigating the evolutionary past of all species. These methods require us to make assumptions about the relationship between genetic change and evolutionary time, often referred to as a 'molecular clock'. Although initially regarded with scepticism, molecular dating has now been adopted in many areas of biology. This broad uptake has been due partly to the development of Bayesian methods that allow complex aspects of molecular evolution, such as variation in rates of change across lineages, to be taken into account. But in order to do this, Bayesian dating methods rely on a range of assumptions about the evolutionary process, which vary in their degree of biological realism and empirical support. These assumptions can have substantial impacts on the estimates produced by molecular dating analyses. The aim of this review is to open the 'black box' of Bayesian molecular dating and have a look at the machinery inside. We explain the components of these dating methods, the important decisions that researchers must make in their analyses, and the factors that need to be considered when interpreting results. We illustrate the effects that the choices of different models and priors can have on the outcome of the analysis, and suggest ways to explore these impacts. We describe some major research directions that may improve the reliability of Bayesian dating. The goal of our review is to help researchers to make informed choices when using Bayesian phylogenetic methods to estimate evolutionary rates and timescales.

The phylogeny and biogeography of Hakea (Proteaceae) reveals the role of biome shifts in a continental plant radiation.

The frequency of evolutionary biome shifts during diversification has important implications for our ability to explain geographic patterns of plant diversity. Recent studies present several examples of biome shifts, but whether frequencies of biome shifts closely reflect geographic proximity or environmental similarity of biomes remains poorly known. We explore this question by using phylogenomic methods to estimate the phylogeny of Hakea, a diverse Australian genus occupying a wide range of biomes. Model-based estimation of ancestral regions indicates that Hakea began diversifying in the Mediterranean biome of southern Australia in the Middle Eocene-Early Oligocene, and dispersed repeatedly into other biomes across the continent. We infer around 47 shifts between biomes. Frequencies of shifts between pairs of biomes are usually similar to those expected from their geographic connectedness or climatic similarity, but in some cases are substantially higher or lower than expected, perhaps reflecting how readily key physiological traits can be modified to adapt lineages to new environments. The history of frequent biome-shifting is reflected in the structure of present-day assemblages, which tend to be more phylogenetically diverse than null-model expectations. The case of Hakea demonstrates that the radiation of large plant clades across wide geographic areas need not be constrained by dispersal limitation or conserved adaptations to particular environments.

Darwinism for the Genomic Age: Connecting Mutation to Diversification.

A growing body of evidence suggests that rates of diversification of biological lineages are correlated with differences in genome-wide mutation rate. Given that most research into differential patterns of diversification rate have focused on species traits or ecological parameters, a connection to the biochemical processes of genome change is an unexpected observation. While the empirical evidence for a significant association between mutation rate and diversification rate is mounting, there has been less effort in explaining the factors that mediate this connection between genetic change and species richness. Here we draw together empirical studies and theoretical concepts that may help to build links in the explanatory chain that connects mutation to diversification. First we consider the way that mutation rates vary between species. We then explore how differences in mutation rates have flow-through effects to the rate at which populations acquire substitutions, which in turn influences the speed at which populations become reproductively isolated from each other due to the acquisition of genomic incompatibilities. Since diversification rate is commonly measured from phylogenetic analyses, we propose a conceptual approach for relating events of reproductive isolation to bifurcations on molecular phylogenies. As we examine each of these relationships, we consider theoretical models that might shine a light on the observed association between rate of molecular evolution and diversification rate, and critically evaluate the empirical evidence for these links, focusing on phylogenetic comparative studies. Finally, we ask whether we are getting closer to a real understanding of the way that the processes of molecular evolution connect to the observable patterns of diversification.

Interdisciplinary research has consistently lower funding success.

Interdisciplinary research is widely considered a hothouse for innovation, and the only plausible approach to complex problems such as climate change. One barrier to interdisciplinary research is the widespread perception that interdisciplinary projects are less likely to be funded than those with a narrower focus. However, this commonly held belief has been difficult to evaluate objectively, partly because of lack of a comparable, quantitative measure of degree of interdisciplinarity that can be applied to funding application data. Here we compare the degree to which research proposals span disparate fields by using a biodiversity metric that captures the relative representation of different fields (balance) and their degree of difference (disparity). The Australian Research Council's Discovery Programme provides an ideal test case, because a single annual nationwide competitive grants scheme covers fundamental research in all disciplines, including arts, humanities and sciences. Using data on all 18,476 proposals submitted to the scheme over 5 consecutive years, including successful and unsuccessful applications, we show that the greater the degree of interdisciplinarity, the lower the probability of being funded. The negative impact of interdisciplinarity is significant even when number of collaborators, primary research field and type of institution are taken into account. This is the first broad-scale quantitative assessment of success rates of interdisciplinary research proposals. The interdisciplinary distance metric allows efficient evaluation of trends in research funding, and could be used to identify proposals that require assessment strategies appropriate to interdisciplinary research.

Testing hypotheses in macroevolution.

Experimental manipulation of microevolution (changes in frequency of heritable traits in populations) has shed much light on evolutionary processes. But many evolutionary processes occur on scales that are not amenable to experimental manipulation. Indeed, one of the reasons that macroevolution (changes in biodiversity over time, space and lineages) has sometimes been a controversial topic is that processes underlying the generation of biological diversity generally operate at scales that are not open to direct observation or manipulation. Macroevolutionary hypotheses can be tested by using them to generate predictions then asking whether observations from the biological world match those predictions. Each study that identifies significant correlations between evolutionary events, processes or outcomes can generate new predictions that can be further tested with different datasets, allowing a cumulative process that may narrow down on plausible explanations, or lead to rejection of other explanations as inconsistent or unsupported. A similar approach can be taken even for unique events, for example by comparing patterns in different regions, lineages, or time periods. I will illustrate the promise and pitfalls of these approaches using a range of examples, and discuss the problems of inferring causality from significant evolutionary associations.