Is horizontal transmission really a problem for phylogenetic comparative methods? A simulation study using continuous cultural traits

Phylogenetic comparative methods (PCMs) provide a potentially powerful toolkit for testing hypotheses about cultural evolution. Here, we build on previous simulation work to assess the effect horizontal transmission between cultures has on the ability of both phylogenetic and non-phylogenetic methods to make inferences about trait evolution. We found that the mode of horizontal transmission of traits has important consequences for both methods. Where traits were horizontally transmitted separately, PCMs accurately reported when trait evolution was not correlated even at the highest levels of horizontal transmission. By contrast, linear regression analyses often incorrectly concluded that traits were correlated. Where simulated trait evolution was not correlated and traits were horizontally transmitted as a pair, both methods inferred increased levels of positive correlation with increasing horizontal transmission. Where simulated trait evolution was correlated, increasing rates of separate horizontal transmission led to decreasing levels of inferred correlation for both methods, but increasing rates of paired horizontal transmission did not. Furthermore, the PCM was also able to make accurate inferences about the ancestral state of traits. These results suggest that under certain conditions, PCMs can be robust to the effects of horizontal transmission. We discuss ways that future work can investigate the mode and tempo of horizontal transmission of cultural traits.     

Heterogeneity in the rate of molecular sequence evolution substantially impacts the accuracy of detecting shifts in diversification rates

As species richness varies along the tree of life, there is a great interest in identifying factors that affect the rates by which lineages speciate or go extinct. To this end, theoretical biologists have developed a suite of phylogenetic comparative methods that aim to identify where shifts in diversification rates had occurred along a phylogeny and whether they are associated with some traits. Using these methods, numerous studies have predicted that speciation and extinction rates vary across the tree of life. In this study, we show that asymmetric rates of sequence evolution lead to systematic biases in the inferred phylogeny, which in turn lead to erroneous inferences regarding lineage diversification patterns. The results demonstrate that as the asymmetry in sequence evolution rates increases, so does the tendency to select more complicated models that include the possibility of diversification rate shifts. These results thus suggest that any inference regarding shifts in diversification pattern should be treated with great caution, at least until any biases regarding the molecular substitution rate have been ruled out.     

General quantitative genetic methods for comparative biology: phylogenies,taxonomies and multi‐trait models for continuous and categorical characters

Although many of the statistical techniques used in comparative biology were originally developed in quantitative genetics, subsequent development of comparative techniques has progressed in relative isolation. Consequently, many of the new and planned developments in comparative analysis already have well‐tested solutions in quantitative genetics. In this paper, we take three recent publications that develop phylogenetic meta‐analysis, either implicitly or explicitly, and show how they can be considered as quantitative genetic models. We highlight some of the difficulties with the proposed solutions, and demonstrate that standard quantitative genetic theory and software offer solutions. We also show how results from Bayesian quantitative genetics can be used to create efficient Markov chain Monte Carlo algorithms for phylogenetic mixed models, thereby extending their generality to non‐Gaussian data. Of particular utility is the development of multinomial models for analysing the evolution of discrete traits, and the development of multi‐trait models in which traits can follow different distributions. Meta‐analyses often include a nonrandom collection of species for which the full phylogenetic tree has only been partly resolved. Using missing data theory, we show how the presented models can be used to correct for nonrandom sampling and show how taxonomies and phylogenies can be combined to give a flexible framework with which to model dependence.     

Scombroid Fishes Provide Novel Insights into the Trait/Rate Associations of Molecular Evolution

The study of which life history traits primarily affect molecular evolutionary rates is often confounded by the covariance of these traits. Scombroid fishes (billfishes, tunas, barracudas, and their relatives) are unusual in that their mass-specific metabolic rate is positively associated with body size. This study exploits this atypical pattern of trait variation, which allows for direct tests of whether mass-specific metabolic rate or body size is the more important factor of molecular evolutionary rates. We inferred a phylogeny for scombroids from a supermatrix of molecular and morphological characters and used new phylogenetic comparative approaches to assess the associations of body size and mass-specific metabolic rate with substitution rate. As predicted by the body size hypothesis, there is a negative correlation between body size and substitution rate. However, unexpectedly, we also find a negative association between mass-specific metabolic and substitution rates. These relationships are supported by analyses of the total molecular data, separate mitochondrial and nuclear genes, and individual loci, and they are robust to phylogenetic uncertainty. The molecular evolutionary rates of scombroids are primarily tied to body size. This study demonstrates that groups with novel patterns of trait variation can be particularly informative for identifying which life history traits are the primary factors of molecular evolutionary rates.     

Evolution of social learning does not explain the origin of human cumulative culture

Because culture requires transmission of information between individuals, thinking about the origin of culture has mainly focused on the genetic evolution of abilities for social learning. Current theory considers how social learning affects the adaptiveness of a single cultural trait, yet human culture consists of the accumulation of very many traits. Here we introduce a new modeling strategy that tracks the adaptive value of many cultural traits, showing that genetic evolution favors only limited social learning owing to the accumulation of maladaptive as well as adaptive culture. We further show that culture can be adaptive, and refined social learning can evolve, if individuals can identify and discard maladaptive culture. This suggests that the evolution of such "adaptive filtering" mechanisms may have been crucial for the birth of human culture.     

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.     

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.     

Joint reconstruction of divergence times and life-history evolution in placental mammals using a phylogenetic covariance model

Violation of the molecular clock has been amply documented, and is now routinely taken into account by molecular dating methods. Comparative analyses have revealed a systematic component in rate variation, relating it to the evolution of life-history traits, such as body size or generation time. Life-history evolution can be reconstructed using Brownian models. However, the resulting estimates are typically uncertain, and potentially sensitive to the underlying assumptions. As a way of obtaining more accurate ancestral trait and divergence time reconstructions, correlations between life-history traits and substitution rates could be used as an additional source of information. In this direction, a Bayesian framework for jointly reconstructing rates, traits, and dates was previously introduced. Here, we apply this model to a 17 protein-coding gene alignment for 73 placental taxa. Our analysis indicates that the coupling between molecules and life history can lead to a reevaluation of ancestral life-history profiles, in particular for groups displaying convergent evolution in body size. However, reconstructions are sensitive to fossil calibrations and to the Brownian assumption. Altogether, our analysis suggests that further integrating inference of rates and traits might be particularly useful for neontological macroevolutionary comparative studies.     

Mitochondrial DNA as a tool for reconstructing past life‐history traits in mammals

Reconstructing the ancestral characteristics of species is a major goal in evolutionary and comparative biology. Unfortunately, fossils are not always available and sufficiently informative, and phylogenetic methods based on models of character evolution can be unsatisfactory. Genomic data offer a new opportunity to estimate ancestral character states, through (i) the correlation between DNA evolutionary processes and species life‐history traits and (ii) available reliable methods for ancestral sequence inference. Here, we assess the relevance of mitochondrial DNA – the most popular molecular marker in animals – as a predictor of ancestral life‐history traits in mammals, using the order of Cetartiodactyla as a benchmark. Using the complete set of 13 mitochondrial protein‐coding genes, we show that the lineage‐specific nonsynonymous over synonymous substitution rate ratio (dN/dS) is closely correlated with the species body mass, longevity and age of sexual maturity in Cetartiodactyla and can be used as a marker of ancestral traits provided that the noise introduced by short branches is appropriately dealt with. Based on ancestral dN/dS estimates, we predict that the first cetartiodactyls were relatively small animals (around 20 kg). This finding is in accordance with Cope's rule and the fossil record but could not be recovered via continuous character evolution methods.     

The effects of sexual selection on trait divergence in a peripheral population with gene flow

The unique aspects of speciation and divergence in peripheral populations have long sparked much research. Unidirectional migration, received by some peripheral populations, can hinder the evolution of distinct differences from their founding populations. Here, we explore the effects that sexual selection, long hypothesized to drive the divergence of distinct traits used in mate choice, can play in the evolution of such traits in a partially isolated peripheral population. Using population genetic continent‐island models, we show that with phenotype matching, sexual selection increases the frequency of an island‐specific mating trait only when female preferences are of intermediate strength. We identify regions of preference strength for which sexual selection can instead cause an island‐specific trait to be lost, even when it would have otherwise been maintained at migration‐selection balance. When there are instead separate preference and trait loci, we find that sexual selection can lead to low trait frequencies or trait loss when female preferences are weak to intermediate, but that sexual selection can increase trait frequencies when preferences are strong. We also show that novel preference strengths almost universally cannot increase, under either mating mechanism, precluding the evolution of premating isolation in peripheral populations at the early stages of species divergence.     

Extant‐only comparative methods fail to recover the disparity preserved in the bird fossil record

Most extant species are in clades with poor fossil records, and recent studies of comparative methods show they have low power to infer even highly simplified models of trait evolution without fossil data. Birds are a well‐studied radiation, yet their early evolutionary patterns are still contentious. The fossil record suggests that birds underwent a rapid ecological radiation after the end‐Cretaceous mass extinction, and several smaller, subsequent radiations. This hypothesized series of repeated radiations from fossil data is difficult to test using extant data alone. By uniting morphological and phylogenetic data on 604 extant genera of birds with morphological data on 58 species of extinct birds from 50 million years ago, the “halfway point” of avian evolution, I have been able to test how well extant‐only methods predict the diversity of fossil forms. All extant‐only methods underestimate the disparity, although the ratio of within‐ to between‐clade disparity does suggest high early rates. The failure of standard models to predict high early disparity suggests that recent radiations are obscuring deep time patterns in the evolution of birds. Metrics from different models can be used in conjunction to provide more valuable insights than simply finding the model with the highest relative fit.     

Predicting rates of interspecific interaction from phylogenetic trees

Integrating phylogenetic information can potentially improve our ability to explain species' traits, patterns of community assembly, the network structure of communities, and ecosystem function. In this study, we use mathematical models to explore the ecological and evolutionary factors that modulate the explanatory power of phylogenetic information for communities of species that interact within a single trophic level. We find that phylogenetic relationships among species can influence trait evolution and rates of interaction among species, but only under particular models of species interaction. For example, when interactions within communities are mediated by a mechanism of phenotype matching, phylogenetic trees make specific predictions about trait evolution and rates of interaction. In contrast, if interactions within a community depend on a mechanism of phenotype differences, phylogenetic information has little, if any, predictive power for trait evolution and interaction rate. Together, these results make clear and testable predictions for when and how evolutionary history is expected to influence contemporary rates of species interaction.     

Euclidean nature of phylogenetic distance matrices

Phylogenies are fundamental to comparative biology as they help to identify independent events on which statistical tests rely. Two groups of phylogenetic comparative methods (PCMs) can be distinguished: those that take phylogenies into account by introducing explicit models of evolution and those that only consider phylogenies as a statistical constraint and aim at partitioning trait values into a phylogenetic component (phylogenetic inertia) and one or multiple specific components related to adaptive evolution. The way phylogenetic information is incorporated into the PCMs depends on the method used. For the first group of methods, phylogenies are converted into variance-covariance matrices of traits following a given model of evolution such as Brownian motion (BM). For the second group of methods, phylogenies are converted into distance matrices that are subsequently transformed into Euclidean distances to perform principal coordinate analyses. Here, we show that simply taking the elementwise square root of a distance matrix extracted from a phylogenetic tree ensures having a Euclidean distance matrix. This is true for any type of distances between species (patristic or nodal) and also for trees harboring multifurcating nodes. Moreover, we illustrate that this simple transformation using the square root imposes less geometric distortion than more complex transformations classically used in the literature such as the Cailliez method. Given the Euclidean nature of the elementwise square root of phylogenetic distance matrices, the positive semidefinitiveness of the phylogenetic variance-covariance matrix of a trait following a BM model, or related models of trait evolution, can be established. In that way, we build a bridge between the two groups of statistical methods widely used in comparative analysis. These results should be of great interest for ecologists and evolutionary biologists performing statistical analyses incorporating phylogenies.     

MALE CONTEST COMPETITION AND THE COEVOLUTION OF WEAPONRY AND TESTES IN PINNIPEDS

Male reproductive success is influenced by competitive interactions during precopulatory and postcopulatory selective episodes. Consequently, males can gain reproductive advantages during precopulatory contest competition by investing in weaponry and during postcopulatory sperm competition by investing in ejaculates. However, recent theory predicts male expenditure on weaponry and ejaculates should be subject to a trade‐off, and should vary under increasing risk and intensity of sperm competition. Here, we provide the first comparative analysis of the prediction that expenditure on weaponry should be negatively associated with expenditure on testes mass. Specifically, we assess how sexual selection influences the evolution of primary and secondary sexual traits among pinnipeds (seals, sea lions, and walruses). Using recently developed comparative methods, we demonstrate that sexual selection promotes rapid divergence in body mass, sexual size dimorphism (SSD), and genital morphology. We then show that genital length appears to be positively associated with the strength of postcopulatory sexual selection. However, subsequent analyses reveal that both genital length and testes mass are negatively associated with investment in precopulatory weaponry. Thus, our results are congruent with recent theoretical predictions of contest‐based sperm competition models. We discuss the possible role of trade‐offs and allometry in influencing patterns of reproductive trait evolution in pinnipeds.     

Maximizing the Power of Principal-Component Analysis of Correlated Phenotypes in Genome-wide Association Studies

Many human traits are highly correlated. This correlation can be leveraged to improve the power of genetic association tests to identify markers associated with one or more of the traits. Principal component analysis (PCA) is a useful tool that has been widely used for the multivariate analysis of correlated variables. PCA is usually applied as a dimension reduction method: the few top principal components (PCs) explaining most of total trait variance are tested for association with a predictor of interest, and the remaining components are not analyzed. In this study we review the theoretical basis of PCA and describe the behavior of PCA when testing for association between a SNP and correlated traits. We then use simulation to compare the power of various PCA-based strategies when analyzing up to 100 correlated traits. We show that contrary to widespread practice, testing only the top PCs often has low power, whereas combining signal across all PCs can have greater power. This power gain is primarily due to increased power to detect genetic variants with opposite effects on positively correlated traits and variants that are exclusively associated with a single trait. Relative to other methods, the combined-PC approach has close to optimal power in all scenarios considered while offering more flexibility and more robustness to potential confounders. Finally, we apply the proposed PCA strategy to the genome-wide association study of five correlated coagulation traits where we identify two candidate SNPs that were not found by the standard approach.     

Analysing recombination in nucleotide sequences

Throughout the living world, genetic recombination and nucleotide substitution are the primary processes that create the genetic variation upon which natural selection acts. Just as analyses of substitution patterns can reveal a great deal about evolution, so too can analyses of recombination. Evidence of genetic recombination within the genomes of apparently asexual species can equate with evidence of cryptic sexuality. In sexually reproducing species, nonrandom patterns of sequence exchange can provide direct evidence of population subdivisions that prevent certain individuals from mating. Although an interesting topic in its own right, an important reason for analysing recombination is to account for its potentially disruptive influences on various phylogenetic-based molecular evolution analyses. Specifically, the evolutionary histories of recombinant sequences cannot be accurately described by standard bifurcating phylogenetic trees. Taking recombination into account can therefore be pivotal to the success of selection, molecular clock and various other analyses that require adequate modelling of shared ancestry and draw increased power from accurately inferred phylogenetic trees. Here, we review various computational approaches to studying recombination and provide guidelines both on how to gain insights into this important evolutionary process and on how it can be properly accounted for during molecular evolution studies.     

Nonlinear relationships and phylogenetically independent contrasts

The method of phylogenetically independent contrasts is commonly used for exploring cross-taxon relationships between traits. Here we show that this phylogenetic comparative method (PCM) can fail to detect correlated evolution when the underlying relationship between traits is nonlinear. Simulations indicate that statistical power can be dramatically reduced when independent contrasts analysis is used on nonlinear relationships. We also reanalyze a published data set and demonstrate that ignoring nonlinearity can affect biological inferences. We suggest that researchers consider the shape of the relationship between traits when using independent contrasts analysis. Alternative PCMs may be more appropriate if data cannot be transformed to meet assumptions of linearity.     

Assessing current adaptation and phylogenetic inertia as explanations of trait evolution: the need for controlled comparisons

The determination of whether the pattern of trait evolution observed in a comparative analysis of species data is due to adaptation to current environments, to phylogenetic inertia, or to both of these forces requires that one control for the effects of either force when making an assessment of the evolutionary role of the other. Orzack and Sober (2001) developed the method of controlled comparisons to make such assessments; their implementation of the method focussed on a discretely varying trait. Here, we show that the method of controlled comparisons can be viewed as a meta-method, which can be implemented in many ways. We discuss which recent methods for the comparative analysis of continuously distributed traits can generate controlled comparisons and can thereby be used to properly assess whether current adaptation and/or phylogenetic inertia have influenced a trait's evolution. The implementation of controlled comparisons is illustrated by an analysis of sex-ratio data for fig wasps. This analysis suggests that current adaptation and phylogenetic inertia influence this trait.     

Comparative bioacoustics: a roadmap for quantifying and comparing animal sounds across diverse taxa

Animals produce a wide array of sounds with highly variable acoustic structures. It is possible to understand the causes and consequences of this variation across taxa with phylogenetic comparative analyses. Acoustic and evolutionary analyses are rapidly increasing in sophistication such that choosing appropriate acoustic and evolutionary approaches is increasingly difficult. However, the correct choice of analysis can have profound effects on output and evolutionary inferences. Here, we identify and address some of the challenges for this growing field by providing a roadmap for quantifying and comparing sound in a phylogenetic context for researchers with a broad range of scientific backgrounds. Sound, as a continuous, multidimensional trait can be particularly challenging to measure because it can be hard to identify variables that can be compared across taxa and it is also no small feat to process and analyse the resulting high-dimensional acoustic data using approaches that are appropriate for subsequent evolutionary analysis. Additionally, terminological inconsistencies and the role of learning in the development of acoustic traits need to be considered. Phylogenetic comparative analyses also have their own sets of caveats to consider. We provide a set of recommendations for delimiting acoustic signals into discrete, comparable acoustic units. We also present a three-stage workflow for extracting relevant acoustic data, including options for multivariate analyses and dimensionality reduction that is compatible with phylogenetic comparative analysis. We then summarize available phylogenetic comparative approaches and how they have been used in comparative bioacoustics, and address the limitations of comparative analyses with behavioural data. Lastly, we recommend how to apply these methods to acoustic data across a range of study systems. In this way, we provide an integrated framework to aid in quantitative analysis of cross-taxa variation in animal sounds for comparative phylogenetic analysis. In addition, we advocate the standardization of acoustic terminology across disciplines and taxa, adoption of automated methods for acoustic feature extraction, and establishment of strong data archival practices for acoustic recordings and data analyses. Combining such practices with our proposed workflow will greatly advance the reproducibility, biological interpretation, and longevity of comparative bioacoustic studies.