Andrew Meade

Bayesian Estimation of Ancestral Character States on Phylogenies

Biologists frequently attempt to infer the character states at ancestral nodes of a phylogeny from the distribution of traits observed in contemporary organisms. Because phylogenies are normally inferences from data, it is desirable to account for the uncertainty in estimates of the tree and its branch lengths when making inferences about ancestral states or other comparative parameters. Here we present a general Bayesian approach for testing comparative hypotheses across statistically justified samples of phylogenies, focusing on the specific issue of reconstructing ancestral states. The method uses Markov chain Monte Carlo techniques for sampling phylogenetic trees and for investigating the parameters of a statistical model of trait evolution. We describe how to combine information about the uncertainty of the phylogeny with uncertainty in the estimate of the ancestral state. Our approach does not constrain the sample of trees only to those that contain the ancestral node or nodes of interest, and we show how to reconstruct ancestral states of uncertain nodes using a most-recent-common-ancestor approach. We illustrate the methods with data on ribonuclease evolution in the Artiodactyla. Software implementing the methods (BayesMultiState) is available from the authors.

Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo.

We describe a Bayesian method for investigating correlated evolution of discrete binary traits on phylogenetic trees. The method fits a continuous‐time Markov model to a pair of traits, seeking the best fitting models that describe their joint evolution on a phylogeny. We employ the methodology of reversible‐jump (RJ) Markov chain Monte Carlo to search among the large number of possible models, some of which conform to independent evolution of the two traits, others to correlated evolution. The RJ Markov chain visits these models in proportion to their posterior probabilities, thereby directly estimating the support for the hypothesis of correlated evolution. In addition, the RJ Markov chain simultaneously estimates the posterior distributions of the rate parameters of the model of trait evolution. These posterior distributions can be used to test among alternative evolutionary scenarios to explain the observed data. All results are integrated over a sample of phylogenetic trees to account for phylogenetic uncertainty. We implement the method in a program called RJ Discrete and illustrate it by analyzing the question of whether mating system and advertisement of estrus by females have coevolved in the Old World monkeys and great apes.

Detecting Regular Sound Changes in Linguistics as Events of Concerted Evolution

Summary Background Concerted evolution is normally used to describe parallel changes at different sites in a genome, but it is also observed in languages where a specific phoneme changes to the same other phoneme in many words in the lexicon—a phenomenon known as regular sound change. We develop a general statistical model that can detect concerted changes in aligned sequence data and apply it to study regular sound changes in the Turkic language family. Results Linguistic evolution, unlike the genetic substitutional process, is dominated by events of concerted evolutionary change. Our model identified more than 70 historical events of regular sound change that occurred throughout the evolution of the Turkic language family, while simultaneously inferring a dated phylogenetic tree. Including regular sound changes yielded an approximately 4-fold improvement in the characterization of linguistic change over a simpler model of sporadic change, improved phylogenetic inference, and returned more reliable and plausible dates for events on the phylogenies. The historical timings of the concerted changes closely follow a Poisson process model, and the sound transition networks derived from our model mirror linguistic expectations. Conclusions We demonstrate that a model with no prior knowledge of complex concerted or regular changes can nevertheless infer the historical timings and genealogical placements of events of concerted change from the signals left in contemporary data. Our model can be applied wherever discrete elements—such as genes, words, cultural trends, technologies, or morphological traits—can change in parallel within an organism or other evolving group.

Frequency of word-use predicts rates of lexical evolution throughout Indo-European history

Greek speakers say “ουρ”, Germans “schwanz” and the French “queue” to describe what English speakers call a ‘tail’, but all of these languages use a related form of ‘two’ to describe the number after one. Among more than 100 Indo-European languages and dialects, the words for some meanings (such as ‘tail’) evolve rapidly, being expressed across languages by dozens of unrelated words, while others evolve much more slowly—such as the number ‘two’, for which all Indo-European language speakers use the same related word-form. No general linguistic mechanism has been advanced to explain this striking variation in rates of lexical replacement among meanings. Here we use four large and divergent language corpora (English, Spanish, Russian and Greek) and a comparative database of 200 fundamental vocabulary meanings in 87 Indo-European languages to show that the frequency with which these words are used in modern language predicts their rate of replacement over thousands of years of Indo-European language evolution. Across all 200 meanings, frequently used words evolve at slower rates and infrequently used words evolve more rapidly. This relationship holds separately and identically across parts of speech for each of the four language corpora, and accounts for approximately 50% of the variation in historical rates of lexical replacement. We propose that the frequency with which specific words are used in everyday language exerts a general and law-like influence on their rates of evolution. Our findings are consistent with social models of word change that emphasize the role of selection, and suggest that owing to the ways that humans use language, some words will evolve slowly and others rapidly across all languages.

Origin of avian genome size and structure in non-avian dinosaurs

Avian genomes are small and streamlined compared with those of other amniotes by virtue of having fewer repetitive elements and less non-coding DNA. This condition has been suggested to represent a key adaptation for flight in birds, by reducing the metabolic costs associated with having large genome and cell sizes. However, the evolution of genome architecture in birds, or any other lineage, is difficult to study because genomic information is often absent for long-extinct relatives. Here we use a novel bayesian comparative method to show that bone-cell size correlates well with genome size in extant vertebrates, and hence use this relationship to estimate the genome sizes of 31 species of extinct dinosaur, including several species of extinct birds. Our results indicate that the small genomes typically associated with avian flight evolved in the saurischian dinosaur lineage between 230 and 250 million years ago, long before this lineage gave rise to the first birds. By comparison, ornithischian dinosaurs are inferred to have had much larger genomes, which were probably typical for ancestral Dinosauria. Using comparative genomic data, we estimate that genome-wide interspersed mobile elements, a class of repetitive DNA, comprised 5–12% of the total genome size in the saurischian dinosaur lineage, but was 7–19% of total genome size in ornithischian dinosaurs, suggesting that repetitive elements became less active in the saurischian lineage. These genomic characteristics should be added to the list of attributes previously considered avian but now thought to have arisen in non-avian dinosaurs, such as feathers, pulmonary innovations, and parental care and nesting.

Languages evolve in punctuational bursts

Linguists speculate that human languages often evolve in rapid or punctuational bursts, sometimes associated with their emergence from other languages, but this phenomenon has never been demonstrated. We used vocabulary data from three of the worlds major language groups—Bantu, Indo-European, and Austronesian—to show that 10 to 33% of the overall vocabulary differences among these languages arose from rapid bursts of change associated with language-splitting events. Our findings identify a general tendency for increased rates of linguistic evolution in fledgling languages, perhaps arising from a linguistic founder effect or a desire to establish a distinct social identity.

Multiple routes to mammalian diversity

The radiation of the mammals provides a 165-million-year test case for evolutionary theories of how species occupy and then fill ecological niches. It is widely assumed that species often diverge rapidly early in their evolution, and that this is followed by a longer, drawn-out period of slower evolutionary fine-tuning as natural selection fits organisms into an increasingly occupied niche space. But recent studies have hinted that the process may not be so simple. Here we apply statistical methods that automatically detect temporal shifts in the rate of evolution through time to a comprehensive mammalian phylogeny and data set of body sizes of 3,185 extant species. Unexpectedly, the majority of mammal species, including two of the most speciose orders (Rodentia and Chiroptera), have no history of substantial and sustained increases in the rates of evolution. Instead, a subset of the mammals has experienced an explosive increase (between 10- and 52-fold) in the rate of evolution along the single branch leading to the common ancestor of their monophyletic group (for example Chiroptera), followed by a quick return to lower or background levels. The remaining species are a taxonomically diverse assemblage showing a significant, sustained increase or decrease in their rates of evolution. These results necessarily decouple morphological diversification from speciation and suggest that the processes that give rise to the morphological diversity of a class of animals are far more free to vary than previously considered. Niches do not seem to fill up, and diversity seems to arise whenever, wherever and at whatever rate it is advantageous.

Phylogenies reveal new interpretation of speciation and the Red Queen

The Red Queen describes a view of nature in which species continually evolve but do not become better adapted. It is one of the more distinctive metaphors of evolutionary biology, but no test of its claim that speciation occurs at a constant rate has ever been made against competing models that can predict virtually identical outcomes, nor has any mechanism been proposed that could cause the constant-rate phenomenon. Here we use 101 phylogenies of animal, plant and fungal taxa to test the constant-rate claim against four competing models. Phylogenetic branch lengths record the amount of time or evolutionary change between successive events of speciation. The models predict the distribution of these lengths by specifying how factors combine to bring about speciation, or by describing how rates of speciation vary throughout a tree. We find that the hypotheses that speciation follows the accumulation of many small events that act either multiplicatively or additively found support in 8% and none of the trees, respectively. A further 8% of trees hinted that the probability of speciation changes according to the amount of divergence from the ancestral species, and 6% suggested speciation rates vary among taxa. By comparison, 78% of the trees fit the simplest model in which new species emerge from single events, each rare but individually sufficient to cause speciation. This model predicts a constant rate of speciation, and provides a new interpretation of the Red Queen: the metaphor of species losing a race against a deteriorating environment is replaced by a view linking speciation to rare stochastic events that cause reproductive isolation. Attempts to understand species-radiations or why some groups have more or fewer species should look to the size of the catalogue of potential causes of speciation shared by a group of closely related organisms rather than to how those causes combine.

Ultraconserved words point to deep language ancestry across Eurasia

The search for ever deeper relationships among the World’s languages is bedeviled by the fact that most words evolve too rapidly to preserve evidence of their ancestry beyond 5,000 to 9,000 y. On the other hand, quantitative modeling indicates that some “ultraconserved” words exist that might be used to find evidence for deep linguistic relationships beyond that time barrier. Here we use a statistical model, which takes into account the frequency with which words are used in common everyday speech, to predict the existence of a set of such highly conserved words among seven language families of Eurasia postulated to form a linguistic superfamily that evolved from a common ancestor around 15,000 y ago. We derive a dated phylogenetic tree of this proposed superfamily with a time-depth of ∼14,450 y, implying that some frequently used words have been retained in related forms since the end of the last ice age. Words used more than once per 1,000 in everyday speech were 7- to 10-times more likely to show deep ancestry on this tree. Our results suggest a remarkable fidelity in the transmission of some words and give theoretical justification to the search for features of language that might be preserved across wide spans of time and geography.

Bantu expansion shows that habitat alters the route and pace of human dispersals

Significance Humans are uniquely capable of using cultural innovations to occupy a range of environments, raising the intriguing question of whether historical human migrations have followed familiar habitats or moved relatively independently of them. Beginning ∼5,000 y ago, savannah-dwelling populations of Bantu-speaking peoples swept out of West Central Africa, eventually occupying a vast geographical area. We show that this expansion avoided unfamiliar rainforest habitats by following savannah corridors that emerged from the Congo rainforest, probably from climate change. When Bantu speakers did move into the rainforest, migration rates were delayed by on average 300 y compared with similar movements on the savannah. Despite unmatched abilities to produce innovations culturally, unfamiliar habitats significantly alter the route and pace of human dispersals. Unlike most other biological species, humans can use cultural innovations to occupy a range of environments, raising the intriguing question of whether human migrations move relatively independently of habitat or show preferences for familiar ones. The Bantu expansion that swept out of West Central Africa beginning ∼5,000 y ago is one of the most influential cultural events of its kind, eventually spreading over a vast geographical area a new way of life in which farming played an increasingly important role. We use a new dated phylogeny of ∼400 Bantu languages to show that migrating Bantu-speaking populations did not expand from their ancestral homeland in a “random walk” but, rather, followed emerging savannah corridors, with rainforest habitats repeatedly imposing temporal barriers to movement. When populations did move from savannah into rainforest, rates of migration were slowed, delaying the occupation of the rainforest by on average 300 y, compared with similar migratory movements exclusively within savannah or within rainforest by established rainforest populations. Despite unmatched abilities to produce innovations culturally, unfamiliar habitats significantly alter the route and pace of human dispersals.