The Occurrence Birth–Death Process for Combined-Evidence Analysis in Macroevolution and Epidemiology

Abstract

Phylodynamic models generally aim at jointly inferring phylogenetic relationships, model parameters, and more recently, the number of lineages through time, based on molecular sequence data. In the fields of epidemiology and macroevolution, these models can be used to estimate, respectively, the past number of infected individuals (prevalence) or the past number of species (paleodiversity) through time. Recent years have seen the development of “total-evidence” analyses, which combine molecular and morphological data from extant and past sampled individuals in a unified Bayesian inference framework. Even sampled individuals characterized only by their sampling time, that is, lacking morphological and molecular data, which we call occurrences, provide invaluable information to estimate the past number of lineages. Here, we present new methodological developments around the fossilized birth–death process enabling us to (i) incorporate occurrence data in the likelihood function; (ii) consider piecewise-constant birth, death, and sampling rates; and (iii) estimate the past number of lineages, with or without knowledge of the underlying tree. We implement our method in the RevBayes software environment, enabling its use along with a large set of models of molecular and morphological evolution, and validate the inference workflow using simulations under a wide range of conditions. We finally illustrate our new implementation using two empirical data sets stemming from the fields of epidemiology and macroevolution. In epidemiology, we infer the prevalence of the coronavirus disease 2019 outbreak on the Diamond Princess ship, by taking into account jointly the case count record (occurrences) along with viral sequences for a fraction of infected individuals. In macroevolution, we infer the diversity trajectory of cetaceans using molecular and morphological data from extant taxa, morphological data from fossils, as well as numerous fossil occurrences. The joint modeling of occurrences and trees holds the promise to further bridge the gap between traditional epidemiology and pathogen genomics, as well as paleontology and molecular phylogenetics. [Birth–death model; epidemiology; fossils; macroevolution; occurrences; phylogenetics; skyline.]

Exploring congruent diversification histories with flexibility and parsimony

“…Congruence classes have been characterized beyond classical birth-death models, for example in the context of the fossilized birth-death process. This process contains an additional rate for incorporating samples over time into the phylogeny, interpreted as fossils in macroevolutionary studies and genetic samples in epidemiological analyses (Andréoletti et al, 2022; MacPherson et al, 2022). Although this model has been demonstrated to be non-identifiable in the (macroevolutionarily unrealistic) case where lineages go extinct upon sampling (Louca et al, 2021), a more general demonstration is lacking and a method for sampling within this congruence class has not been established.…”

Combining palaeontological and neontological data shows a delayed diversification burst of carcharhiniform sharks likely mediated by environmental change

“…In addition, tree-based approaches are challenging for most groups because both molecular data (for extant species) and morphological data (for extant and extinct taxa) are needed, which requires a considerable amount of time and comes with issues. For instance, the dynamics of carcharhiniform rates of diversification and diversity could have been analysed with the occurrence birth–death process 33 . However, the lack of existing morphological character matrix hinders the placement of fossil carcharhiniform species in the tree, and the clade size makes the analyses computationally intensive (J. Andréoletti pers.…”

“…Integrating palaeontological and neontological data has mostly relied on tree-based approaches 27 , including supertree 28 or metatree 29 methods. Alternatively, total-evidence dating 30 or tip dating 31 methods rely on the fossilised-birth-death model 32 or the occurrence birth-death process 33 to simultaneously infer a time-calibrated phylogeny including extant and extinct lineages in a single framework based on both morphological and molecular data (total-evidence dating) or morphology only (tip dating). While these approaches and their recent methodological developments offer a powerful phylogenetic framework to estimate past diversification events 34 , reconstructing such dated phylogenies still come with some methodological issues (e.g., effects of fossil sampling, missing data, settings of morphological clocks) that are not yet fully understood [35][36][37][38] .…”

“…Despite these limitations, this approach is relevant for clades with a poor fossil record in recent times combined with recent diversification events that are not entirely captured by the fossil record. Although methods for correcting Ts-Te of sampled taxa have been developed, one of the main challenges in palaeodiversity estimates is the inference of non-sampled taxa 33,122 . This is particularly problematic for clades like Carcharhiniformes, for www.nature.com/scientificreports/ which lineages from some environments (deep-sea) and periods of time (Oligocene, upper Miocene-Recent) are weakly sampled.…”

Exploring congruent diversification histories with flexibility and parsimony

“…Congruence classes have been characterized beyond classical birth-death models, for example, in the context of the fossilized birth-death process. This process contains an additional rate for incorporating samples over time into the phylogeny, interpreted as fossils in macroevolutionary studies and genetic samples in epidemiological analyses (Andréoletti et al, 2022;MacPherson et al, 2022).…”