Jennifer F. Hoyal Cuthill

Fractal branching organizations of Ediacaran rangeomorph fronds reveal a lost Proterozoic body plan

Significance Rangeomorph fronds characterize the late Ediacaran Period (575–541 Ma), representing some of the earliest large organisms. As such, they offer key insights into the early evolution of multicellular eukaryotes. However, their extraordinary branching morphology differs from all other organisms and has proved highly enigmatic. Here we provide a unified mathematical model of rangeomorph branching, allowing us to reconstruct 3D morphologies of 11 taxa and measure their functional properties. This reveals an adaptive radiation of fractal morphologies which maximized body surface area, consistent with diffusive nutrient uptake (osmotrophy). Rangeomorphs were adaptively optimal for the low-competition, high-nutrient conditions of Ediacaran oceans. With the Cambrian explosion in animal diversity (from 541 Ma), fundamental changes in ecological and geochemical conditions led to their extinction. The branching morphology of Ediacaran rangeomorph fronds has no exact counterpart in other complex macroorganisms. As such, these fossils pose major questions as to growth patterns, functional morphology, modes of feeding, and adaptive optimality. Here, using parametric Lindenmayer systems, a formal model of rangeomorph morphologies reveals a fractal body plan characterized by self-similar, axial, apical, alternate branching. Consequent morphological reconstruction for 11 taxa demonstrates an adaptive radiation based on 3D space-filling strategies. The fractal body plan of rangeomorphs is shown to maximize surface area, consistent with diffusive nutrient uptake from the water column (osmotrophy). The enigmas of rangeomorph morphology, evolution, and extinction are resolved by the realization that they were adaptively optimized for unique ecological and geochemical conditions in the late Proterozoic. Changes in ocean conditions associated with the Cambrian explosion sealed their fate.

Phylogenetic Codivergence Supports Coevolution of Mimetic Heliconius Butterflies

The unpalatable and warning-patterned butterflies Heliconius erato and Heliconius melpomene provide the best studied example of mutualistic Müllerian mimicry, thought–but rarely demonstrated–to promote coevolution. Some of the strongest available evidence for coevolution comes from phylogenetic codivergence, the parallel divergence of ecologically associated lineages. Early evolutionary reconstructions suggested codivergence between mimetic populations of H. erato and H. melpomene, and this was initially hailed as one of the most striking known cases of coevolution. However, subsequent molecular phylogenetic analyses found discrepancies in phylogenetic branching patterns and timing (topological and temporal incongruence) that argued against codivergence. We present the first explicit cophylogenetic test of codivergence between mimetic populations of H. erato and H. melpomene, and re-examine the timing of these radiations. We find statistically significant topological congruence between multilocus coalescent population phylogenies of H. erato and H. melpomene. Cophylogenetic historical reconstructions support repeated codivergence of mimetic populations, from the base of the sampled radiations. Pairwise distance correlation tests, based on our coalescent analyses plus recently published AFLP and wing colour pattern gene data, also suggest that the phylogenies of H. erato and H. melpomene show significant topological congruence. Divergence time estimates, based on a Bayesian coalescent model, suggest that the evolutionary radiations of H. erato and H. melpomene occurred over the same time period, and are compatible with a series of temporally congruent codivergence events. Our results suggest that differences in within-species genetic divergence are the result of a greater overall effective population size for H. erato relative to H. melpomene and do not imply incongruence in the timing of their phylogenetic radiations. Repeated codivergence between Müllerian co-mimics, predicted to exert mutual selection pressures, strongly suggests coevolution. Our results therefore support a history of reciprocal coevolution between Müllerian co-mimics characterised by phylogenetic codivergence and parallel phenotypic change.

A simple model explains the dynamics of preferential host switching among mammal RNA viruses.

A growing number of studies support a tendency toward preferential host switching, by parasites and pathogens, over relatively short phylogenetic distances. This suggests that a host switch is more probable if a potential host is closely related to the original host than if it is a more distant relative. However, despite its importance for the health of humans, livestock, and wildlife, the detailed dynamics of preferential host switching have, so far, been little studied. We present an empirical test of two theoretical models of preferential host switching, using observed phylogenetic distributions of host species for RNA viruses of three mammal orders (primates, carnivores, and ungulates). The analysis focuses on multihost RNA virus species, because their presence on multiple hosts and their estimated ages of origin indicate recent host switching. Approximate Bayesian computation was used to compare observed phylogenetic distances between hosts with those simulated under the theoretical models. The results support a decreasing sigmoidal model of preferential host switching, with a strong effect from increasing phylogenetic distance, on all three studied host phylogenies. This suggests that the dynamics of host switching are fundamentally similar for RNA viruses of different mammal orders and, potentially, a wider range of coevolutionary systems.

A formula for maximum possible steps in multistate characters: isolating matrix parameter effects on measures of evolutionary convergence

To identify a biological signal in the distribution of homoplasy, it is first necessary to isolate non‐biological factors affecting its measurement. The number of states per character in a phylogenetic data matrix may indicate evolutionary flexibility and, consequently, the likelihood of recurrent evolution. However, we show here that the number of states per character limits the maximum number of steps that may be inferred using parsimony. A formula is provided for the maximum number of steps that may be taken by a character with a given number of states and taxa. We show that as more character states are included the maximum proportion of steps that can be attributed to homoplasy falls, and the greatest amount of homoplasy measurable with the consistency index declines.

The size of the character state space affects the occurrence and detection of homoplasy: modelling the probability of incompatibility for unordered phylogenetic characters.

This study models the probability of incompatibility versus compatibility for binary or unordered multistate phylogenetic characters, by treating the allocation of taxa to character states as a classical occupancy problem in probability. It is shown that, under this model, the number of character states has a non-linear effect on the probability of character incompatibility, which is also affected by the number of taxa. Effects on homoplasy from the number of character states are further explored using evolutionary computer simulations. The results indicate that the character state space affects both the known levels of homoplasy (recorded during simulated evolution) and those inferred from parsimony analysis of the resulting character data, with particular relevance for morphological phylogenetic analyses which generally use the parsimony method. When the evolvable state space is large (more potential states per character) there is a reduction in the known occurrence of homoplasy (as reported previously). However, this is not always reflected in the levels of homoplasy detected in a parsimony analysis, because higher numbers of states per character can lead to an increase in the probability of character incompatibility (as well as the maximum homoplasy measurable with some indices). As a result, inferred trends in homoplasy can differ markedly from the underlying trend (that recorded during evolutionary simulation). In such cases, inferred homoplasy can be entirely misleading with regard to tree quality (with higher levels of homoplasy inferred for better quality trees). When rates of evolution are low, commonly used indices such as the number of extra steps (H) and the consistency index (CI) provide relatively good measures of homoplasy. However, at higher rates, estimates may be improved by using the retention index (RI), and particularly by accounting for homoplasy measured among randomised character data using the homoplasy excess ratio (HER).

Wing patterning genes and coevolution of Müllerian mimicry in Heliconius butterflies: Support from phylogeography, cophylogeny, and divergence times

Examples of long‐term coevolution are rare among free‐living organisms. Müllerian mimicry in Heliconius butterflies had been suggested as a key example of coevolution by early genetic studies. However, research over the last two decades has been dominated by the idea that the best‐studied comimics, H. erato and H. melpomene, did not coevolve at all. Recently sequenced genes associated with wing color pattern phenotype offer a new opportunity to resolve this controversy. Here, we test the hypothesis of coevolution between H. erato and H. melpomene using Bayesian multilocus analysis of five color pattern genes and five neutral genetic markers. We first explore the extent of phylogenetic agreement versus conflict between the different genes. Coevolution is then tested against three aspects of the mimicry diversifications: phylogenetic branching patterns, divergence times, and, for the first time, phylogeographic histories. We show that all three lines of evidence are compatible with strict coevolution of the diverse mimicry wing patterns, contrary to some recent suggestions. Instead, these findings tally with a coevolutionary diversification driven primarily by the ecological force of Müllerian mimicry.

Australian spiny mountain crayfish and their temnocephalan ectosymbionts: an ancient association on the edge of coextinction?

Australian spiny mountain crayfish (Euastacus, Parastacidae) and their ecotosymbiotic temnocephalan flatworms (Temnocephalida, Platyhelminthes) may have co-occurred and interacted through deep time, during a period of major environmental change. Therefore, reconstructing the history of their association is of evolutionary, ecological, and conservation significance. Here, time-calibrated Bayesian phylogenies of Euastacus species and their temnocephalans (Temnohaswellia and Temnosewellia) indicate near-synchronous diversifications from the Cretaceous. Statistically significant cophylogeny correlations between associated clades suggest linked evolutionary histories. However, there is a stronger signal of codivergence and greater host specificity in Temnosewellia, which co-occurs with Euastacus across its range. Phylogeography and analyses of evolutionary distinctiveness (ED) suggest that regional differences in the impact of climate warming and drying had major effects both on crayfish and associated temnocephalans. In particular, Euastacus and Temnosewellia show strong latitudinal gradients in ED and, conversely, in geographical range size, with the most distinctive, northern lineages facing the greatest risk of extinction. Therefore, environmental change has, in some cases, strengthened ecological and evolutionary associations, leaving host-specific temnocephalans vulnerable to coextinction with endangered hosts. Consequently, the extinction of all Euastacus species currently endangered (75%) predicts coextinction of approximately 60% of the studied temnocephalans, with greatest loss of the most evolutionarily distinctive lineages.

Hunting Darwin's Snark: which maps shall we use?

The 11 contributions to this thematic volume touch on a large range of issues concerning the landscape of biological possibilities and the manner by which it may be traversed by evolving life forms. The contributors also consider how this landscape might be mapped by evolutionary biologists, with an emphasis on how one might identify the limits of such maps. While some agreements emerge on the question of limits on evolution, not surprisingly few contributors look towards the same horizons. Rather than providing a potted summary of the 11 papers, our aim in this introduction is to identify eight principal themes that might serve as common ground and, as importantly, to listen out for the sound of rushing subterranean waters that hint at caverns of concealed knowledge. By no means all of these themes are addressed by all authors, but in gathering the many strands of enquiry we hope that this will allow us to ask: What, if any, are the limits to evolution?