As a result of the process of descent with modification, closely related species tend to be similar to one another in a myriad different ways. In statistical terms, this means that traits measured on one species will not be independent of traits measured on others. Since their introduction in the 1980s, phylogenetic comparative methods (PCMs) have been framed as a solution to this problem. In this article, we argue that this way of thinking about PCMs is deeply misleading. Not only has this sowed widespread confusion in the literature about what PCMs are doing but has led us to develop methods that are susceptible to the very thing we sought to build defenses against-unreplicated evolutionary events. Through three Case Studies, we demonstrate that the susceptibility to singular events is indeed a recurring problem in comparative biology that links several seemingly unrelated controversies. In each Case Study, we propose a potential solution to the problem. While the details of our proposed solutions differ, they share a common theme: unifying hypothesis testing with data-driven approaches (which we term "phylogenetic natural history") to disentangle the impact of singular evolutionary events from that of the factors we are investigating. More broadly, we argue that our field has, at times, been sloppy when weighing evidence in support of causal hypotheses. We suggest that one way to refine our inferences is to re-imagine phylogenies as probabilistic graphical models; adopting this way of thinking will help clarify precisely what we are testing and what evidence supports our claims.
As a result of the process of descent with modification, closely related species tend to be similar to one another in a myriad different ways. In statistical terms, this 20 means that traits measured on one species will not be independent of traits measured on others. Since their introduction in the 1980s, phylogenetic comparative methods (PCMs) have been framed as a solution to this problem. In this paper, we argue that this way of thinking about PCMs is deeply misleading. Not only has this sowed widespread confusion in the literature about what PCMs are doing but 25 has led us to develop methods that are susceptible to the very thing we sought to build defenses against -unreplicated evolutionary events. Through three Case Studies, we demonstrate that the susceptibility to singular events indeed a recurring problem in comparative biology that links several seemingly unrelated controversies. In each Case Study we propose a potential solution to the problem. 30While the details of our proposed solutions differ, they share a common theme: unifying hypothesis testing with data-driven approaches (which we term "phylogenetic natural history") to disentangle the impact of singular evolutionary events from that of the factors we are investigating. More broadly, we argue that our field has, at times, been sloppy when weighing evidence in support of causal hypothe-35 ses. We suggest that one way to refine our inferences is to re-imagine phylogenies as probabilistic graphical models; adopting this way of thinking will help clarify precisely what we are testing and what evidence supports our claims.
If particular traits consistently affect rates of speciation and extinction, broad macroevolutionary patterns can be interpreted as consequences of selection at high levels of the biological hierarchy. Identifying traits associated with diversification rates is difficult because of the wide variety of characters under consideration and the statistical challenges of testing for associations from comparative phylogenetic data. Ploidy (diploid vs polyploid states) and breeding system (self-incompatible vs self-compatible states) are both thought to be drivers of differential diversification in angiosperms.We fit 29 diversification models to extensive trait and phylogenetic data in Solanaceae and investigate how speciation and extinction rate differences are associated with ploidy, breeding system, and the interaction between these traits.We show that diversification patterns in Solanaceae are better explained by breeding system and an additional unobserved factor, rather than by ploidy. We also find that the most common evolutionary pathway to polyploidy in Solanaceae occurs via direct breakdown of self-incompatibility by whole genome duplication, rather than indirectly via breakdown followed by polyploidization.Comparing multiple stochastic diversification models that include complex trait interactions alongside hidden states enhances our understanding of the macroevolutionary patterns in plant phylogenies.Among life history traits, reproductive characters that determine mating patterns are perhaps the most influential in governing macroevolution.
Although numerous studies have surveyed the frequency with which different plant characters are associated with polyploidy, few statistical tools are available to identify the factors that potentially facilitate polyploidy. We describe a new probabilistic model, BiChroM, designed to associate the frequency of polyploidy and chromosomal change with a binary phenotypic character in a phylogeny. BiChroM provides a robust statistical framework for testing differences in rates of polyploidy associated with phenotypic characters along a phylogeny while simultaneously allowing for evolutionary transitions between character states. We used BiChroM to test whether polyploidy is more frequent in woody or herbaceous plants, based on tree with 4711 eudicot species. Although polyploidy occurs in woody species, rates of chromosome doubling were over six times higher in herbaceous species. Rates of single chromosome increases or decreases were also far higher in herbaceous than woody species. Simulation experiments indicate that BiChroM performs well with little to no bias and relatively little variance at a wide range of tree depths when trees have at least 500 taxa. Thus, BiChroM provides a first step toward a rigorous statistical framework for assessing the traits that facilitate polyploidy.
Estimating time-dependent rates of speciation and extinction from dated phylogenetic trees of extant species (timetrees), and determining how and why they vary, is key to understanding how ecological and evolutionary processes shape biodiversity. Due to an increasing availability of phylogenetic trees, a growing number of process-based methods relying on the birth-death model have been developed in the last decade to address a variety of questions in macroevolution. However, this methodological progress has regularly been criticised such that one may wonder how reliable the estimations of speciation and extinction rates are. In particular, using lineages-through-time (LTT) plots, a recent study (Louca and Pennell, 2020) has shown that there are an infinite number of equally likely diversification scenarios that can generate any timetree. This has led to questioning whether or not diversification rates should be estimated at all. Here we summarize, clarify, and highlight technical considerations on recent findings regarding the capacity of models to disentangle diversification histories. Using simulations we illustrate the characteristics of newly-proposed “pulled rates” and their utility. We recognize that the recent findings are a step forward in understanding the behavior of macroevolutionary modelling, but they in no way suggest we should abandon diversification modelling altogether. On the contrary, the study of macroevolution using phylogenetic trees has never been more exciting and promising than today. We still face important limitations in regard to data availability and methods, but by acknowledging them we can better target our joint efforts as a scientific community.
Premise of the StudyPolyploidy has profound evolutionary consequences for land plants. Despite the availability of large phylogenetic and chromosomal data sets, estimating the rates of polyploidy and chromosomal evolution across the tree of life remains a challenging, computationally complex problem. We introduce the R package chromploid, which allows scientists to perform inference of chromosomal evolution rates across large phylogenetic trees.Methods and Resultschromploid is an open‐source package in the R environment that calculates the likelihood function of models of chromosome evolution. Models of discrete character evolution can be customized using chromploid. We demonstrate the performance of the BiChroM model, testing for associations between rates of chromosome doubling (as a proxy for polyploidy) and a binary phenotypic character, within chromploid using simulations and empirical data from Solanum. In simulations, estimated chromosome‐doubling rates were unbiased and the variance decreased with larger trees, but distinguishing small differences in rates of chromosome doubling, even from large data sets, remains challenging. In the Solanum data set, a custom model of chromosome number evolution demonstrated higher rates of chromosome doubling in herbaceous species compared to woody.Conclusionschromploid enables researchers to perform robust likelihood‐based inferences using complex models of chromosome number evolution across large phylogenies.
The complex island archipelagoes of Wallacea and Melanesia have provided empirical data behind integral theories in evolutionary biology, including allopatric speciation and island biogeography. Yet, questions regarding the relative impact of the layered biogeographic barriers, such as deep-water trenches and isolated island systems, on faunal diversification remain underexplored. One such barrier is Wallace’s Line, a significant biogeographic boundary that largely separates Australian and Asian biodiversity. To assess the relative roles of biogeographic barriers—specifically isolated island systems and Wallace’s Line—we investigated the tempo and mode of diversification in a diverse avian radiation, Corvides (Crows and Jays, Birds-of-paradise, Vangas, and allies). We combined a genus-level dataset of thousands of ultraconserved elements (UCEs) and a species-level, 12-gene Sanger sequence matrix to produce a well-resolved supermatrix tree that we leveraged to explore the group’s historical biogeography and effects of biogeographic barriers on their macroevolutionary dynamics. The tree is well-resolved and differs substantially from what has been used extensively for past comparative analyses within this group. We confirmed that Corvides, and its major constituent clades, arose in Australia and that a burst of dispersals west across Wallace’s Line occurred after the uplift of Wallacea during the mid-Miocene. We found that dispersal across this biogeographic barrier were generally rare, though westward dispersals were two times more frequent than eastward dispersals. Wallacea’s central position between Sundaland and Sahul no doubt acted as a bridge for island-hopping dispersal out of Australia, across Wallace’s Line, to colonize the rest of Earth. In addition, we found that the complex island archipelagoes east of Wallace’s Line harbor the highest rates of net diversification and are a substantial source of colonists to continental systems on both sides of this biogeographic barrier. Our results support emerging evidence that island systems, particularly the geologically complex archipelagoes of the Indo-pacific, are drivers of species diversification.
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