Biology subjects

Pennell, M. W.

Publications and source records attributed to Pennell, M. W..

8 recordsLinked to original sources

bioRxiv2022

Maternal investment evolves with larger body size and higher diversification rate in sharks and rays

Across vertebrates, live-bearing has evolved at least 150 times from ancestral egg-laying into a diverse array of forms and degrees of prepartum maternal investment.1,2 A key question is how this reproductive diversity arose and whether reproductive diversification underlies species diversification?3-11 To test these questions, we evaluate the most basal jawed vertebrates, sharks, rays, chimaeras of Class Chondrichthyans, which have one of the greatest ranges of reproductive and ecological diversity among vertebrates.2,12 We reconstructed the sequence of reproductive mode evolution across a time-calibrated molecular phylogeny of 610 chondrichthyans.13 We find egg-laying is ancestral, and live-bearing evolved at least seven times. Matrotrophy (i.e. maternal contributions beyond the yolk) evolved at least 15 times, with evidence of one reversal. In sharks, transitions to live-bearing and matrotrophy are more prevalent in larger-bodied species in the tropics. Further, the evolution of live-bearing is associated with a near-doubling of the diversification rate, but, there is only a small increase in diversification associated with the appearance of matrotrophy and increased rates of speciation are associated with the colonization of novel habitats, contrary to what has been demonstrated in teleosts.3,4 This highlights a potential key difference between chondrichthyans and other fishes, specifically a slower rate of reproductive isolation following speciation, suggesting different rate-limiting mechanisms for diversification between these clades.14 The chondrichthyan diversification and radiation, particularly throughout the shallow tropical shelf seas and oceanic pelagic habitats, appears to be associated with the evolution of live-bearing and the proliferation of a wide range of maternal investment in developing offspring.

evolutionary biology↗

bioRxiv2021

Fundamental identifiability limits in molecular epidemiology

Viral phylogenies provide crucial information on the spread of infectious diseases, and many studies fit mathematical models to phylogenetic data to estimate epidemiological parameters such as the effective reproduction ratio (Re) over time. Such phylodynamic inferences often complement or even substitute for conventional surveillance data, particularly when sampling is poor or delayed. It remains generally unknown, however, how robust phylodynamic epidemiological inferences are, especially when there is uncertainty regarding pathogen prevalence and sampling intensity. Here we use recently developed mathematical techniques to fully characterize the information that can possibly be extracted from serially collected viral phylogenetic data, in the context of the commonly used birth-death-sampling model. We show that for any candidate epidemiological scenario, there exist a myriad of alternative, markedly different and yet plausible "congruent" scenarios that cannot be distinguished using phylogenetic data alone, no matter how large the dataset. In the absence of strong constraints or rate priors across the entire study period, neither maximum-likelihood fitting nor Bayesian inference can reliably reconstruct the true epidemiological dynamics from phylogenetic data alone; rather, estimators can only converge to the "congruence class" of the true dynamics. We propose concrete and feasible strategies for making more robust epidemiological inferences from viral phylogenetic data.

evolutionary biology↗

bioRxiv2021

Why extinction estimates from extant phylogenies are so often zero

Time-calibrated phylogenies comprising only extant lineages are widely used to estimate historical speciation and extinction rates. Such extinction rate estimates have long been controversial as many phylogenetic studies report zero extinction in many taxa, a finding in conflict with the fossil record. To date, the causes of this widely observed discrepancy remain unresolved. Here we provide a novel and simple explanation for these "zero-inflated" extinction rate estimates, based on the recent discovery that there exist many alternative "congruent" diversification scenarios that cannot possibly be distinguished on the sole basis of extant timetrees. Consequently, estimation methods tend to converge to some scenario congruent to (i.e., statistically indistinguishable from) the true diversification scenario, but not necessarily to the true diversification scenario itself. This congruent scenario may in principle exhibit negative extinction rates, a biologically meaningless but mathematically feasible situation, in which case estimators will tend to hit and stick to the boundary estimate of zero extinction. To test this explanation, we estimated extinction rates using maximum likelihood for a set of simulated trees and for 121 empirical trees, while either allowing or preventing negative extinction rates. We find that the existence of congruence classes and imposed bounds on extinction rates can explain the zero-inflation of previous extinction rate estimates, even for large trees (1000 tips) and in the absence of any detectable model violations. Not only do our results likely resolve a long-standing mystery in phylogenetics, they demonstrate that model congruencies can have severe consequences in practice.

evolutionary biology↗

bioRxiv2020

A General Birth-Death-Sampling Model for Epidemiology and Macroevolution

Birth-death stochastic processes are the foundation of many phylogenetic models and are widely used to make inferences about epidemiological and macroevolutionary dynamics. There are a large number of birth-death model variants that have been developed; these impose different assumptions about the temporal dynamics of the parameters and about the sampling process. As each of these variants was individually derived, it has been difficult to understand the relationships between them as well as their precise biological and mathematical assumptions. Without a common mathematical foundation, deriving new models is non-trivial. Here we unify these models into a single framework, prove that many previously developed epidemiological and macroevolutionary models are all special cases of a more general model, and illustrate the connections between these variants. This framework centers around a technique for deriving likelihood functions for arbitrarily complex birth-death(-sampling) models that will allow researchers to explore a wider array of scenarios than was previously possible. We then use this frame-work to derive general model likelihoods for both the "single-type" case in which all lineages diversify according to the same process and the "multi-type" case, where there is variation in the process among lineages. By re-deriving existing single-type birth-death sampling models we clarify and synthesize the range of explicit and implicit assumptions made by these models.

evolutionary biology↗

bioRxiv2019

Phylogenies of extant species are consistent with an infinite array of diversification histories

Time-calibrated molecular phylogenies of extant species (\"extant timetrees\") are widely used for estimating the dynamics of diversification rates (1-6) and testing for associations between these rates and environmental factors (5, 7) or species traits (8). However, there has been considerable debate surrounding the reliability of these inferences in the absence of fossil data (9-13), and to date this critical question remains unresolved. Here we mathematically clarify the precise information that can be extracted from extant timetrees under the generalized birth-death model, which underlies the majority of existing estimation methods. We prove that for a given extant timetree and a candidate diversification scenario, there exists an infinite number of alternative diversification scenarios that are equally likely to have generated a given tree. These \"congruent\" scenarios cannot possibly be distinguished using extant timetrees alone, even in the presence of infinite data. Importantly, congruent diversification scenarios can exhibit markedly different and yet plausible diversification dynamics, suggesting that many previous studies may have over-interpreted phylogenetic evidence. We show that sets of congruent models can be uniquely described using composite variables, which contain all available information about past dynamics of diversification (14); this suggests an alternative paradigm for learning about the past from extant timetrees.

evolutionary biology↗

bioRxiv2018

Macroevolutionary diversification rates show time-dependency

For centuries, biologists have been captivated by the vast disparity in species richness between different groups of organisms. Variation in diversity is widely attributed to differences between groups in how fast they speciate or go extinct. Such macroevolutionary rates have been estimated for thousands of groups and have been correlated with an incredible variety of organismal traits. Here we analyze a large collection of phylogenetic trees and fossil time series and report a hidden generality amongst these seemingly idiosyncratic results: speciation and extinction rates follow a scaling law where both depend strongly on the age of the group in which they are measured, with the fastest rates in the youngest clades. Using a series of simulations and sensitivity analyses, we demonstrate that the time-dependency is unlikely to be a result of simple statistical artifacts. As such, this time-scaling has profound implications for the interpretation of rate estimates and suggests there might be general laws governing macroevolutionary dynamics.

evolutionary biology↗

bioRxiv2018

The choice of tree prior and molecular clock does not substantially affect phylogenetic inferences of diversification rates

Comparative methods allow researchers to make inferences about evolutionary processes and patterns from phylogenetic trees. In Bayesian phylogenetics, estimating a phylogeny requires specifying priors on parameters characterizing the branching process and rates of substitution among lineages, in addition to others. However, the effect that the selection of these priors has on the inference of comparative parameters has not been thoroughly investigated. Such uncertainty may systematically bias phylogenetic reconstruction and, subsequently, parameter estimation. Here, we focus on the impact of priors in Bayesian phylogenetic inference and evaluate how they affect the estimation of parameters in macroevolutionary models of lineage diversification. Specifically, we use BEAST to simulate trees under combinations of tree priors and molecular clocks, simulate sequence data, estimate trees, and estimate diversification parameters (e.g., speciation rates and extinction rates) from these trees. When substitution rate heterogeneity is large, parameter estimates deviate substantially from those estimated under the simulation conditions when not captured by an appropriate choice of relaxed molecular clock. However, in general, we find that the choice of tree prior and molecular clock has relatively little impact on the estimation of diversification rates insofar as the sequence data are sufficiently informative and substitution rate heterogeneity among lineages is low-to-moderate.

evolutionary biology↗

bioRxiv2017

Rethinking phylogenetic comparative methods

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 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 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.

evolutionary biology↗