Jonathan Chang

Is BAMM Flawed? Theoretical and Practical Concerns in the Analysis of Multi-Rate Diversification Models

&NA; Bayesian analysis of macroevolutionary mixtures (BAMM) is a statistical framework that uses reversible jump Markov chain Monte Carlo to infer complex macroevolutionary dynamics of diversification and phenotypic evolution on phylogenetic trees. A recent article by Moore et al. (MEA) reported a number of theoretical and practical concerns with BAMM. Major claims from MEA are that (i) BAMM’s likelihood function is incorrect, because it does not account for unobserved rate shifts; (ii) the posterior distribution on the number of rate shifts is overly sensitive to the prior; and (iii) diversification rate estimates from BAMM are unreliable. Here, we show that these and other conclusions from MEA are generally incorrect or unjustified. We first demonstrate that MEA’s numerical assessment of the BAMM likelihood is compromised by their use of an invalid likelihood function. We then show that “unobserved rate shifts” appear to be irrelevant for biologically plausible parameterizations of the diversification process. We find that the purportedly extreme prior sensitivity reported by MEA cannot be replicated with standard usage of BAMM v2.5, or with any other version when conventional Bayesian model selection is performed. Finally, we demonstrate that BAMM performs very well at estimating diversification rate variation across the ∼20% of simulated trees in MEA’s data set for which it is theoretically possible to infer rate shifts with confidence. Due to ascertainment bias, the remaining 80% of their purportedly variable‐rate phylogenies are statistically indistinguishable from those produced by a constant‐rate birth‐death process and were thus poorly suited for the summary statistics used in their performance assessment. We demonstrate that inferences about diversification rates have been accurate and consistent across all major previous releases of the BAMM software. We recognize an acute need to address the theoretical foundations of rate‐shift models for phylogenetic trees, and we expect BAMM and other modeling frameworks to improve in response to mathematical and computational innovations. However, we remain optimistic that that the imperfect tools currently available to comparative biologists have provided and will continue to provide important insights into the diversification of life on Earth.

Genome-wide ultraconserved elements exhibit higher phylogenetic informativeness than traditional gene markers in percomorph fishes

Ultraconserved elements (UCEs) have become popular markers in phylogenomic studies because of their cost effectiveness and their potential to resolve problematic phylogenetic relationships. Although UCE datasets typically contain a much larger number of loci and sites than more traditional datasets of PCR-amplified, single-copy, protein coding genes, a fraction of UCE sites are expected to be part of a nearly invariant core, and the relative performance of UCE datasets versus protein coding gene datasets is poorly understood. Here we use phylogenetic informativeness (PI) to compare the resolving power of multi-locus and UCE datasets in a sample of percomorph fishes with sequenced genomes (genome-enabled). We compare three data sets: UCE core regions, flanking sequence adjacent to the UCE core and a set of ten protein coding genes commonly used in fish systematics. We found the net informativeness of UCE core and flank regions to be roughly ten-fold and 100-fold more informative than that of the protein coding genes. On a per locus basis UCEs and protein coding genes exhibited similar levels of phylogenetic informativeness. Our results suggest that UCEs offer enormous potential for resolving relationships across the percomorph tree of life.

Crowdsourced geometric morphometrics enable rapid large‐scale collection and analysis of phenotypic data

Summary Advances in genomics and informatics have enabled the production of large phylogenetic trees. However, the ability to collect large phenotypic data sets has not kept pace. Here, we present a method to quickly and accurately gather morphometric data using crowdsourced image-based landmarking. We find that crowdsourced workers perform similarly to experienced morphologists on the same digitization tasks. We also demonstrate the speed and accuracy of our method on seven families of ray-finned fishes (Actinopterygii). Crowdsourcing will enable the collection of morphological data across vast radiations of organisms and can facilitate richer inference on the macroevolutionary processes that shape phenotypic diversity across the tree of life.

An inverse latitudinal gradient in speciation rate for marine fishes

Far more species of organisms are found in the tropics than in temperate and polar regions, but the evolutionary and ecological causes of this pattern remain controversial1,2. Tropical marine fish communities are much more diverse than cold-water fish communities found at higher latitudes3,4, and several explanations for this latitudinal diversity gradient propose that warm reef environments serve as evolutionary ‘hotspots’ for species formation5–8. Here we test the relationship between latitude, species richness and speciation rate across marine fishes. We assembled a time-calibrated phylogeny of all ray-finned fishes (31,526 tips, of which 11,638 had genetic data) and used this framework to describe the spatial dynamics of speciation in the marine realm. We show that the fastest rates of speciation occur in species-poor regions outside the tropics, and that high-latitude fish lineages form new species at much faster rates than their tropical counterparts. High rates of speciation occur in geographical regions that are characterized by low surface temperatures and high endemism. Our results reject a broad class of mechanisms under which the tropics serve as an evolutionary cradle for marine fish diversity and raise new questions about why the coldest oceans on Earth are present-day hotspots of species formation.Contrary to previous hypotheses, high-latitude fish lineages form new species at much faster rates than their tropical counterparts especially in geographical regions that are characterized by low surface temperatures and high endemism.

How Well Can We Estimate Diversity Dynamics for Clades in Diversity Decline

&NA; The fossil record shows that the vast majority of all species that ever existed are extinct and that most lineages go through an expansion and decline in diversity. However, macroevolutionary analyses based upon molecular phylogenies have difficulty inferring extinction dynamics, raising questions about whether the neontological record can contribute to an understanding of the decline phenomenon. Two recently developed diversification methods for molecular phylogenies (RPANDA and BAMM) incorporate models that theoretically have the capacity to capture decline dynamics by allowing extinction to be higher than speciation. However, the performance of these frameworks over a wide range of decline scenarios has not been studied. Here, we investigate the behavior of these methods under decline scenarios caused by decreasing speciation and increasing extinction through time on simulated trees at fixed intervals over diversity trajectories with expansion and decline phases. We also compared method performance over a comprehensive data set of 214 empirical trees. Our results show that both methods perform equally well when varying speciation rates control decline. When decline was only caused by an increase in extinction rates both methods wrongly assign the variation in net diversification to a drop in speciation, even though the positive gamma values of those trees would suggest otherwise. We also found a tendency for RPANDA to favor increasing extinction and BAMM to favor decreasing speciation as the most common cause of decline in empirical trees. Overall our results shed light on the limitations of both methods, encouraging researchers to carefully interpret the results from diversification studies.

Competition and Extinction Explain the Evolution of Diversity in American Automobiles

One of the most remarkable aspects of our species is that while we show surprisingly little genetic diversity, we demonstrate astonishing amounts of cultural diversity. Perhaps most impressive is the diversity of our technologies, broadly defined as all the physical objects we produce and the skills we use to produce them. Despite considerable focus on the evolution of technology by social scientists and philosophers, there have been few attempts to systematically quantify technological diversity, and therefore the dynamics of technological change remain poorly understood. Here we show a novel Bayesian model for examining technological diversification adopted from palaeontological analysis of occurrence data. We use this framework to estimate the tempo of diversification in American car and truck models produced between 1896 and 2014, and to test the relative importance of competition and extrinsic factors in shaping changes in macro-evolutionary rates. Our results identify a four-fold decrease in the origination and extinction rates of car models, and a negative net diversification rate over the last 30 years. We also demonstrate that competition played a more significant role in car model diversification than either changes in oil prices or gross domestic product. Together our analyses provide a set of tools that can enhance current research on technological and cultural evolution by providing a flexible and quantitative framework for exploring the dynamics of diversification.

A phylogenomic perspective on the robust capuchin monkey (Sapajus) radiation: First evidence for extensive population admixture across South America

Phylogenetic relationships amongst the robust capuchin monkeys (genus Sapajus) are poorly understood. Morphology-based taxonomies have recognized anywhere from one to twelve different species. The current IUCN (2017) classification lists eight robust capuchins: S. xanthosternos, S. nigritus, S. robustus, S. flavius, S. libidinosus, S. cay, S. apella and S. macrocephalus. Here, we assembled the first phylogenomic data set for Sapajus using ultra-conserved elements (UCEs) to reconstruct a capuchin phylogeny. All phylogenomic analyses strongly supported a deep divergence of Sapajus and Cebus clades within the capuchin monkeys, and provided support for Sapajus nigritus, S. robustus and S. xanthosternos as distinct species. However, the UCE phylogeny lumped the putative species S. cay, S. libidinosus, S. apella, S. macrocephalus, and S. flavius together as a single widespread lineage. A SNP phylogeny constructed from the UCE data was better resolved and recovered S. flavius and S. libidinosus as sister species; however, S. apella, S. macrocephalus, and S. cay individuals were recovered in two geographic clades, from northeastern and southwestern Amazon, rather than clustering by currently defined morphospecies. STRUCTURE analysis of population clustering revealed widespread admixture among Sapajus populations within the Amazon and even into the Cerrado and Atlantic Forest. Difficulty in assigning species by morphology may be a result of widespread population admixture facilitated through frequent movement across major rivers and even ecosystems by robust capuchin monkeys.

Buccal venom gland associates with increased of diversification rate in the fang blenny fish Meiacanthus (Blenniidae; Teleostei)

At the macroevolutionary level, many mechanisms have been proposed to explain explosive species diversification. Among them morphological and/or physiological novelty is considered to have a great impact on the tempo and the mode of diversification. Meiacanthus is a genus of Blenniidae possessing a unique buccal venom gland at the base of an elongated canine tooth. This unusual trait has been hypothesized to aid escape from predation and thus potentially play an important role in their pattern of diversification. Here, we produce the first time-calibrated phylogeny of Blenniidae and we test the impact of two morphological novelties on their diversification, i.e. the presence of swim bladder and buccal venom gland, using various comparative methods. We found an increase in the tempo of lineage diversification at the root of the Meiacanthus clade, associated with the evolution of the buccal venom gland, but not the swim bladder. Neither morphological novelty was associated with the pattern of size disparification in blennies. Our results support the hypothesis that the buccal venom gland has contributed to the explosive diversification of Meiacanthus, but further analyses are needed to fully understand the factors sustaining this burst of speciation.

Ice ages and butterflyfishes: Phylogenomics elucidates the ecological and evolutionary history of reef fishes in an endemism hotspot

Abstract For tropical marine species, hotspots of endemism occur in peripheral areas furthest from the center of diversity, but the evolutionary processes that lead to their origin remain elusive. We test several hypotheses related to the evolution of peripheral endemics by sequencing ultraconserved element (UCE) loci to produce a genome‐scale phylogeny of 47 butterflyfish species (family Chaetodontidae) that includes all shallow water butterflyfish from the coastal waters of the Arabian Peninsula (i.e., Red Sea to Arabian Gulf) and their close relatives. Bayesian tree building methods produced a well‐resolved phylogeny that elucidated the origins of butterflyfishes in this hotspots of endemism. We show that UCEs, often used to resolve deep evolutionary relationships, represent an important tool to assess the mechanisms underlying recently diverged taxa. Our analyses indicate that unique environmental conditions in the coastal waters of the Arabian Peninsula probably contributed to the formation of endemic butterflyfishes. Older endemic species are also associated with narrow versus broad depth ranges, suggesting that adaptation to deeper coral reefs in this region occurred only recently (<1.75 Ma). Even though deep reef environments were drastically reduced during the extreme low sea level stands of glacial ages, shallow reefs persisted, and as such there was no evidence supporting mass extirpation of fauna in this region.