Rates of phenotypic evolution vary markedly across the tree of life, from the accelerated evolution apparent in adaptive radiations to the remarkable evolutionary stasis exhibited by so-called “living fossils.” Such rate variation has important consequences for large-scale evolutionary dynamics, generating vast disparities in phenotypic diversity across space, time, and taxa. Despite this, most methods for estimating trait evolution rates assume rates vary deterministically with respect to some variable of interest or change infrequently during a clade’s history. These assumptions may cause underfitting of trait evolution models and mislead hypothesis testing. Here, we develop a new trait evolution model that allows rates to vary gradually and stochastically across a clade. Further, we extend this model to accommodate generally decreasing or increasing rates over time, allowing for flexible modeling of “early/late bursts” of trait evolution. We implement a Bayesian method, termed “evolving rates” (evorates for short), to efficiently fit this model to comparative data. Through simulation, we demonstrate that evorates can reliably infer both how and in which lineages trait evolution rates varied during a clade’s history. We apply this method to body size evolution in cetaceans, recovering substantial support for an overall slowdown in body size evolution over time with recent bursts among some oceanic dolphins and relative stasis among beaked whales of the genus Mesoplodon. These results unify and expand on previous research, demonstrating the empirical utility of evorates. [cetacea; macroevolution; comparative methods; phenotypic diversity; disparity; early burst; late burst]
Understanding phenotypic disparity across the tree of life requires identifying where and when evolutionary rates change on phylogeny. A primary methodological challenge in macroevolution is therefore to develop methods for accurate inference of among-lineage variation in rates of phenotypic evolution. Here, we describe a method for inferring among-lineage evolutionary rate heterogeneity in both continuous and discrete traits. The method assumes that the present-day distribution of a trait is shaped by a variable-rate process arising from a mixture of constant-rate processes and uses a single-pass tree traversal algorithm to estimate branch-specific evolutionary rates. By employing dynamic programming optimization techniques and approximate maximum likelihood estimators where appropriate, our method permits rapid exploration of the tempo and mode of phenotypic evolution. Simulations indicate that the method reconstructs rates of trait evolution with high accuracy. Application of the method to data sets on squamate reptile reproduction and turtle body size recovers patterns of rate heterogeneity identified by previous studies but with computational costs reduced by many orders of magnitude. Our results expand the set of tools available for detecting macroevolutionary rate heterogeneity and point to the utility of fast, approximate methods for studying large-scale biodiversity dynamics. [Brownian motion; continuous characters; discrete characters; macroevolution; Markov process; rate heterogeneity.]
more » « less- Award ID(s):
- 1939128
- NSF-PAR ID:
- 10373541
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Systematic Biology
- Volume:
- 71
- Issue:
- 6
- ISSN:
- 1063-5157
- Page Range / eLocation ID:
- p. 1307-1318
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Reconstructing ancestral states for discrete characters is essential for understanding trait evolution in organisms. However, most existing methods are limited to individual characters and often overlook the hierarchical and interactive nature of traits. Recent advances in phylogenetics now offer the possibility of integrating knowledge from anatomy ontologies to reconstruct multiple discrete character histories. Nonetheless, practical applications that fully harness the potential of these new approaches are still lacking.
This paper introduces
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In recent years it has become increasingly popular to use phylogenetic comparative methods to investigate heterogeneity in the rate or process of quantitative trait evolution across the branches or clades of a phylogenetic tree. Here, I present a new method for modeling variability in the rate of evolution of a continuously-valued character trait on a reconstructed phylogeny. The underlying model of evolution is stochastic diffusion (Brownian motion), but in which the instantaneous diffusion rate (σ 2 ) also evolves by Brownian motion on a logarithmic scale. Unfortunately, it’s not possible to simultaneously estimate the rates of evolution along each edge of the tree and the rate of evolution of σ 2 itself using Maximum Likelihood. As such, I propose a penalized-likelihood method in which the penalty term is equal to the log-transformed probability density of the rates under a Brownian model, multiplied by a ‘smoothing’ coefficient, λ, selected by the user. λ determines the magnitude of penalty that’s applied to rate variation between edges. Lower values of λ penalize rate variation relatively little; whereas larger λ values result in minimal rate variation among edges of the tree in the fitted model, eventually converging on a single value of σ 2 for all of the branches of the tree. In addition to presenting this model here, I have also implemented it as part of my phytools R package in the function multirateBM . Using different values of the penalty coefficient, λ, I fit the model to simulated data with: Brownian rate variation among edges (the model assumption); uncorrelated rate variation; rate changes that occur in discrete places on the tree; and no rate variation at all among the branches of the phylogeny. I then compare the estimated values of σ 2 to their known true values. In addition, I use the method to analyze a simple empirical dataset of body mass evolution in mammals. Finally, I discuss the relationship between the method of this article and other models from the phylogenetic comparative methods and finance literature, as well as some applications and limitations of the approach.more » « less
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Abstract Phenotypic data are crucial for understanding genotype–phenotype relationships, assessing the tree of life and revealing trends in trait diversity over time. Large‐scale description of whole organisms for quantitative analyses (phenomics) presents several challenges, and technological advances in the collection of genomic data outpace those for phenomic data. Reasons for this disparity include the time‐consuming and expensive nature of collecting discrete phenotypic data and mining previously published data on a given species (both often requiring anatomical expertise across taxa), and computational challenges involved with analysing high‐dimensional datasets.
One approach to building approximations of organismal phenomes is to combine published datasets of discrete characters assembled for phylogenetic analyses into a phenomic dataset. Despite a wealth of legacy datasets in the literature for many groups, relatively few methods exist for automating the assembly, analysis, and visualization of phenomic datasets in phylogenetic contexts. Here, we introduce a new
r packagephenotools for integrating (fusing original or legacy datasets), curating (finding and removing duplicates) and visualizing phenomic datasets.We demonstrate the utility of the proposed toolkit with a morphological dataset for flightless birds and two morphological datasets for theropod dinosaurs and provide recommendations for character construction to maximize accessibility in future workflows. Visualization tools allow rapid identification of anatomical subregions with difficult or problematic histories of homology.
We anticipate these tools aiding automation of the assembly and visualization of phenomic datasets to inform evolutionary relationships and rates of phenotypic evolution.
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Abstract An important goal of evolutionary genomics is to identify genomic regions whose substitution rates differ among lineages. For example, genomic regions experiencing accelerated molecular evolution in some lineages may provide insight into links between genotype and phenotype. Several comparative genomics methods have been developed to identify genomic accelerations between species, including a Bayesian method called PhyloAcc, which models shifts in substitution rate in multiple target lineages on a phylogeny. However, few methods consider the possibility of discordance between the trees of individual loci and the species tree due to incomplete lineage sorting, which might cause false positives. Here, we present PhyloAcc-GT, which extends PhyloAcc by modeling gene tree heterogeneity. Given a species tree, we adopt the multispecies coalescent model as the prior distribution of gene trees, use Markov chain Monte Carlo (MCMC) for inference, and design novel MCMC moves to sample gene trees efficiently. Through extensive simulations, we show that PhyloAcc-GT outperforms PhyloAcc and other methods in identifying target lineage-specific accelerations and detecting complex patterns of rate shifts, and is robust to specification of population size parameters. PhyloAcc-GT is usually more conservative than PhyloAcc in calling convergent rate shifts because it identifies more accelerations on ancestral than on terminal branches. We apply PhyloAcc-GT to two examples of convergent evolution: flightlessness in ratites and marine mammal adaptations, and show that PhyloAcc-GT is a robust tool to identify shifts in substitution rate associated with specific target lineages while accounting for incomplete lineage sorting.
