Evolvability in the fossil record

The concept of evolvability—the capacity of a population to produce and maintain evolutionarily relevant variation—has become increasingly prominent in evolutionary biology. Paleontology has a long history of investigating questions of evolvability, but paleontological thinking has tended to neglect recent discussions, because many tools used in the current evolvability literature are challenging to apply to the fossil record. The fundamental difficulty is how to disentangle whether the causes of evolutionary patterns arise from variational properties of traits or lineages rather than being due to selection and ecological success. Despite these obstacles, the fossil record offers unique and growing sources of data that capture evolutionary patterns of sustained duration and significance otherwise inaccessible to evolutionary biologists. Additionally, there exist a variety of strategic possibilities for combining prominent neontological approaches to evolvability with those from paleontology. We illustrate three of these possibilities with quantitative genetics, evolutionary developmental biology, and phylogenetic models of macroevolution. In conclusion, we provide a methodological schema that focuses on the conceptualization, measurement, and testing of hypotheses to motivate and provide guidance for future empirical and theoretical studies of evolvability in the fossil record.

RAxML Grove: An empirical Phylogenetic Tree Database

The assessment of novel phylogenetic models and inference methods is routinely being conducted via experiments on simulated as well as empirical data. When generating synthetic data it is often unclear how to set simulation parameters for the models and generate trees that appropriately reflect empirical model parameter distributions and tree shapes. As a solution, we present and make available a new database called 'RAxML Grove' currently comprising more than 60,000 inferred trees and respective model parameter estimates from fully anonymized empirical data sets that were analyzed using RAxML (1) and RAxML-NG (2) on two web servers. We also describe and make available two simple applications of RAxML Grove to exemplify its usage and highlight its utility for designing realistic simulation studies and analyzing empirical model parameter and tree shape distributions. RAxML Grove is freely available at https://github.com/angtft/RAxMLGrove.

Identifying co-phylogenetic hotspots for zoonotic disease

The incidence of zoonotic diseases is increasing worldwide, which makes identifying parasites likely to become zoonotic and hosts likely to harbour zoonotic parasites a critical concern. Prior work indicates that there is a higher risk of zoonotic spillover accruing from closely related hosts and from hosts that are infected with a high phylogenetic diversity of parasites. This suggests that host and parasite evolutionary history may be important drivers of spillover, but identifying whether host–parasite associations are more strongly structured by the host, parasite or both requires co-phylogenetic analyses that combine host–parasite association data with host and parasite phylogenies. Here, we use host–parasite datasets containing associations between helminth taxa and free-range mammals in combination with phylogenetic models to explore whether host, parasite, or both host and parasite evolutionary history influences host–parasite associations. We find that host phylogenetic history is most important for driving patterns of helminth-mammal association, indicating that zoonoses are most likely to come from a host's close relatives. More broadly, our results suggest that co-phylogenetic analyses across broad taxonomic scales can provide a novel perspective for surveying potential emerging infectious diseases. This article is part of the theme issue ‘Infectious disease macroecology: parasite diversity and dynamics across the globe’.

The model-specific Markov embedding problem for symmetric group-based models

We study model embeddability, which is a variation of the famous embedding problem in probability theory, when apart from the requirement that the Markov matrix is the matrix exponential of a rate matrix, we additionally ask that the rate matrix follows the model structure. We provide a characterisation of model embeddable Markov matrices corresponding to symmetric group-based phylogenetic models. In particular, we provide necessary and sufficient conditions in terms of the eigenvalues of symmetric group-based matrices. To showcase our main result on model embeddability, we provide an application to hachimoji models, which are eight-state models for synthetic DNA. Moreover, our main result on model embeddability enables us to compute the volume of the set of model embeddable Markov matrices relative to the volume of other relevant sets of Markov matrices within the model.

Taxonomic Uncertainty and the Anomaly Zone: Phylogenomics Disentangle a Rapid Radiation to Resolve Contentious Species (Gila robusta complex) in the Colorado River

Species are indisputable units for biodiversity conservation, yet their delimitation is fraught with both conceptual and methodological difficulties. A classic example is the taxonomic controversy surrounding the Gila robusta complex in the lower Colorado River of southwestern North America. Nominal species designations were originally defined according to weakly diagnostic morphological differences, but these conflicted with subsequent genetic analyses. Given this ambiguity, the complex was re-defined as a single polytypic unit, with the proposed ‘threatened’ status under the U.S. Endangered Species Act of two elements being withdrawn. Here we re-evaluated the status of the complex by utilizing dense spatial and genomic sampling (N = 387 and >22k loci), coupled with SNP-based coalescent and polymorphism-aware phylogenetic models. In doing so, we found that all three species were indeed supported as evolutionarily independent lineages, despite widespread phylogenetic discordance. To juxtapose this discrepancy with previous studies, we first categorized those evolutionary mechanisms driving discordance, then tested (and subsequently rejected) prior hypotheses which argued phylogenetic discord in the complex was driven by the hybrid origin of Gila nigra. The inconsistent patterns of diversity we found within G. robusta were instead associated with rapid Plio-Pleistocene drainage evolution, with subsequent divergence within the ‘anomaly zone’ of tree space producing ambiguities that served to confound prior studies. Our results not only support resurrection of the three species as distinct entities, but also offer an empirical example of how phylogenetic discordance can be categorized within other recalcitrant taxa, particularly when variation is primarily partitioned at the species-level.

Tempo and mode of morphological evolution are decoupled from latitude in birds

The latitudinal diversity gradient is one of the most striking patterns in nature, yet its implications for morphological evolution are poorly understood. In particular, it has been proposed that an increased intensity of species interactions in tropical biota may either promote or constrain trait evolution, but which of these outcomes predominates remains uncertain. Here, we develop tools for fitting phylogenetic models of phenotypic evolution in which the impact of species interactions—namely, competition—can vary across lineages. Deploying these models on a global avian trait dataset to explore differences in trait divergence between tropical and temperate lineages, we find that the effect of latitude on the mode and tempo of morphological evolution is weak and clade- or trait dependent. Our results indicate that species interactions do not disproportionately impact morphological evolution in tropical bird families and question the validity of previously reported patterns of slower trait evolution in the tropics.

Source range phylogenetic community structure can predict the outcome of avian introductions

Competing phylogenetic models have been proposed to explain the success of species introduced to other communities. Here, we present a study predicting the establishment success of birds introduced to Florida, Hawaii, and New Zealand using several alternative models, considering species' phylogenetic relatedness to source and recipient range taxa, propagule pressure, and traits. We find consistent support for the predictive ability of source region phylogenetic structure. However, we find that the effects of recipient region phylogenetic structure vary in sign and magnitude depending on inclusion of source region phylogenetic structure, delineation of the recipient species pool, and the use of phylogenetic correction in the models. We argue that tests of alternative phylogenetic hypotheses including the both source and recipient community phylogenetic structure, as well as important covariates such as propagule pressure, are likely to be critical for identifying general phylogenetic patterns in introduction success, predicting future invasions, and for stimulating further exploration of the underlying mechanisms of invasibility.

Scalable total-evidence inference from molecular and continuous characters in a Bayesian framework

Time-scaled phylogenetic trees are both an ultimate goal of evolutionary biology and a necessary ingredient in comparative studies. While accumulating genomic data has moved the field closer to a full description of the tree of life, the relative timing of certain evolutionary events remains challenging even when this data is abundant, and absolute timing is impossible without external information such as fossil ages and morphology. The field of phylogenetics lacks efficient tools integrating probabilistic models for these kinds of data into unified frameworks for estimating phylogenies. Here, we implement, benchmark and validate popular phylogenetic models for the study of paleontological and neontological continuous trait data, incorporating these models into the BEAST2 platform. Our methods scale well with number of taxa and of characters. We tip-date and estimate the topology of a phylogeny of Carnivora, comparing results from different configurations of integrative models capable of leveraging ages, as well as molecular and continuous morphological data from living and extinct species. Our results illustrate and advance the paradigm of Bayesian, probabilistic total evidence, in which explanatory models are fully defined, and inferential uncertainty in all their dimensions is accounted for.

Evidence for sponges as sister to all other animals from partitioned phylogenomics with mixture models and recoding

Resolving the relationships between the major lineages in the animal tree of life is necessary to understand the origin and evolution of key animal traits. Sponges, characterized by their simple body plan, were traditionally considered the sister group of all other animal lineages, implying a gradual increase in animal complexity from unicellularity to complex multicellularity. However, the availability of genomic data has sparked tremendous controversy as some phylogenomic studies support comb jellies taking this position, requiring secondary loss or independent origins of complex traits. Here we show that incorporating site-heterogeneous mixture models and recoding into partitioned phylogenomics alleviates systematic errors that hamper commonly-applied phylogenetic models. Testing on real datasets, we show a great improvement in model-fit that attenuates branching artefacts induced by systematic error. We reanalyse key datasets and show that partitioned phylogenomics does not support comb jellies as sister to other animals at either the supermatrix or partition-specific level.