Luke A. Parry

Bayesian methods outperform parsimony but at the expense of precision in the estimation of phylogeny from discrete morphological data

Different analytical methods can yield competing interpretations of evolutionary history and, currently, there is no definitive method for phylogenetic reconstruction using morphological data. Parsimony has been the primary method for analysing morphological data, but there has been a resurgence of interest in the likelihood-based Mk-model. Here, we test the performance of the Bayesian implementation of the Mk-model relative to both equal and implied-weight implementations of parsimony. Using simulated morphological data, we demonstrate that the Mk-model outperforms equal-weights parsimony in terms of topological accuracy, and implied-weights performs the most poorly. However, the Mk-model produces phylogenies that have less resolution than parsimony methods. This difference in the accuracy and precision of parsimony and Bayesian approaches to topology estimation needs to be considered when selecting a method for phylogeny reconstruction.

Uncertain-tree: Discriminating among competing approaches to the phylogenetic analysis of phenotype data

Morphological data provide the only means of classifying the majority of lifes history, but the choice between competing phylogenetic methods for the analysis of morphology is unclear. Traditionally, parsimony methods have been favoured but recent studies have shown that these approaches are less accurate than the Bayesian implementation of the Mk model. Here we expand on these findings in several ways: we assess the impact of tree shape and maximum-likelihood estimation using the Mk model, as well as analysing data composed of both binary and multistate characters. We find that all methods struggle to correctly resolve deep clades within asymmetric trees, and when analysing small character matrices. The Bayesian Mk model is the most accurate method for estimating topology, but with lower resolution than other methods. Equal weights parsimony is more accurate than implied weights parsimony, and maximum-likelihood estimation using the Mk model is the least accurate method. We conclude that the Bayesian implementation of the Mk model should be the default method for phylogenetic estimation from phenotype datasets, and we explore the implications of our simulations in reanalysing several empirical morphological character matrices. A consequence of our finding is that high levels of resolution or the ability to classify species or groups with much confidence should not be expected when using small datasets. It is now necessary to depart from the traditional parsimony paradigms of constructing character matrices, towards datasets constructed explicitly for Bayesian methods.

Cambrian stem-group annelids and a metameric origin of the annelid head

The oldest fossil annelids come from the Early Cambrian Sirius Passet and Guanshan biotas and Middle Cambrian Burgess Shale. While these are among the best preserved polychaete fossils, their relationship to living taxa is contentious, having been interpreted either as members of extant clades or as a grade outside the crown group. New morphological observations from five Cambrian species include the oldest polychaete with head appendages, a new specimen of Pygocirrus from Sirius Passet, and an undescribed form from the Burgess Shale. We propose that the palps of Canadia are on an anterior segment bearing neuropodia and that the head of Phragmochaeta is formed of a segment bearing biramous parapodia and chaetae. The unusual anatomy of these taxa suggests that the head is not differentiated into a prostomium and peristomium, that palps are derived from a modified parapodium and that the annelid head was originally a parapodium-bearing segment. Canadia, Phragmochaeta and the Marble Canyon annelid share the presence of protective notochaetae, interpreted as a primitive character state subsequently lost in Pygocirrus and Burgessochaeta, in which the head is clearly differentiated from the trunk.

Ancestral morphology of crown-group molluscs revealed by a new Ordovician stem aculiferan

Exceptionally preserved fossils provide crucial insights into extinct body plans and organismal evolution. Molluscs, one of the most disparate animal phyla, radiated rapidly during the early Cambrian period (approximately 535–520 million years ago (Ma)). The problematic fossil taxa Halkieria and Orthrozanclus (grouped in Sachitida) have been assigned variously to stem-group annelids, brachiopods, stem-group molluscs or stem-group aculiferans (Polyplacophora and Aplacophora), but their affinities have remained controversial owing to a lack of preserved diagnostic characters. Here we describe a new early sachitid, Calvapilosa kroegeri gen. et sp. nov. from the Fezouata biota of Morocco (Early Ordovician epoch, around 478 Ma). The new taxon is characterized by the presence of a single large anterior shell plate and polystichous radula bearing a median tooth and several lateral and uncinal teeth in more than 125 rows. Its flattened body is covered by hollow spinose sclerites, and a smooth, ventral girdle flanks an extensive mantle cavity. Phylogenetic analyses resolve C. kroegeri as a stem-group aculiferan together with other single-plated forms such as Maikhanella (Siphogonuchites) and Orthrozanclus; Halkieria is recovered closer to the aculiferan crown. These genera document the stepwise evolution of the aculiferan body plan from forms with a single, almost conchiferan-like shell through two-plated taxa such as Halkieria, to the eight-plated crown-group aculiferans. C. kroegeri therefore provides key evidence concerning the long debate about the crown molluscan affinities of sachitids. This new discovery strongly suggests that the possession of only a single calcareous shell plate and the presence of unmineralised sclerites are plesiomorphic (an ancestral trait) for the molluscan crown.

The impact of fossil data on annelid phylogeny inferred from discrete morphological characters

As a result of their plastic body plan, the relationships of the annelid worms and even the taxonomic makeup of the phylum have long been contentious. Morphological cladistic analyses have typically recovered a monophyletic Polychaeta, with the simple-bodied forms assigned to an early-diverging clade or grade. This is in stark contrast to molecular trees, in which polychaetes are paraphyletic and include clitellates, echiurans and sipunculans. Cambrian stem group annelid body fossils are complex-bodied polychaetes that possess well-developed parapodia and paired head appendages (palps), suggesting that the root of annelids is misplaced in morphological trees. We present a reinvestigation of the morphology of key fossil taxa and include them in a comprehensive phylogenetic analysis of annelids. Analyses using probabilistic methods and both equal- and implied-weights parsimony recover paraphyletic polychaetes and support the conclusion that echiurans and clitellates are derived polychaetes. Morphological trees including fossils depict two main clades of crown-group annelids that are similar, but not identical, to Errantia and Sedentaria, the fundamental groupings in transcriptomic analyses. Removing fossils yields trees that are often less resolved and/or root the tree in greater conflict with molecular topologies. While there are many topological similarities between the analyses herein and recent phylogenomic hypotheses, differences include the exclusion of Sipuncula from Annelida and the taxa forming the deepest crown-group divergences.

A new fireworm (Amphinomidae) from the Cretaceous of Lebanon identified from three-dimensionally preserved myoanatomy

BackgroundRollinschaeta myoplena gen. et sp. nov is described from the Late Cretaceous (Cenomanian) Konservat-Lagerstätten of Hakel and Hjoula, Lebanon. The myoanatomy of the fossils is preserved in exceptional detail in three dimensions as calcium phosphate, allowing the musculature of the body wall, gut and parapodia to be reconstructed in detail.ResultsThe major muscle groups of polychaetes can be identified in Rollinschaeta, including longitudinal muscle bands, circular muscles, oblique muscles, the parapodial muscle complex and the gut musculature, with a resolution sufficient to preserve individual fibres. To allow meaningful comparison with the phosphatized fossil specimens, extant polychaetes were stained with iodine and visualised using microCT. Rollinschaeta myoplena possesses two pairs of dorsal longitudinal muscles, dorsal and ventral circular muscles and a single pair of ventral longitudinal muscles. While six longitudinal muscle bands are known from other polychaete groups, their presence in combination with circular muscles is unique to Amphinomidae, allowing these fossils to be diagnosed to family level based solely on their myoanatomy. The elongate, rectilinear body and equally sized, laterally projecting parapodia of Rollinschaeta are found only within Amphinominae, demonstrating that the Cretaceous species is derived amongst Amphinomida.ConclusionThe uniquely preserved myoanatomy of Rollinschaeta has allowed diagnosis of a fossil annelid to subfamily level using microCT as a comparative tool for exploring myoanatomy in fossil and extant polychaetes. Our results demonstrate that fossilized muscles can provide systematically informative anatomical detail and that they should be studied when preserved.

Parsimony and Maximum Likelihood phylogenetic analyses of morphology do not generally integrate uncertainty in inferring evolutionary history: A response to Brown et al.

Our recent study evaluated the performance of parsimony and probabilistic models of phylogenetic inference based on categorical data [1]. We found that a Bayesian implementation of a probabilistic Markov model produced more accurate results than either of the competing parsimony approaches (the main method currently employed), and the maximum-likelihood implementation of the same model. This occurs principally because the results of Bayesian analyses are less resolved (less precise) as a measure of topological uncertainty is intrinsically recovered in this MCMC-based approach and can be used to construct a majority-rule consensus tree that reflects this. Of the three main methods, maximum likelihood performed the worst of all as a single exclusively bifurcating tree is estimated in this framework which does not integrate an intrinsic measure of support. In their comment on our article, Brown et al . [2] argue that our experiments are invalid because we did not employ uncertainty measures after obtaining a maximum-likelihood estimate of the topology. When bootstrapping is employed, a 50% consensus tree constructed from the bootstrap distribution is often indistinguishable from the majority-rule consensus tree constructed from the posterior sample obtained in a Bayesian analysis. This result is not entirely unexpected, as the maximum-likelihood and Bayesian statistical frameworks share many statistical similarities, including a dependence on a likelihood function that incorporates the Mk model in this context. On this basis, Brown and colleagues conclude that they cannot advocate one method of phylogenetic inference over another: Bayesian, maximum-likelihood and parsimony methods differ, and thoughtful consideration is required in order to choose among these methods. Unfortunately, their analyses do not wholly support this conclusion because they exclusively focus on the performance of …

Soft-Bodied Fossils Are Not Simply Rotten Carcasses – Toward a Holistic Understanding of Exceptional Fossil Preservation: Exceptional Fossil Preservation Is Complex and Involves the Interplay of Numerous Biological and Geological Processes

Exceptionally preserved fossils are the product of complex interplays of biological and geological processes including burial, autolysis and microbial decay, authigenic mineralization, diagenesis, metamorphism, and finally weathering and exhumation. Determining which tissues are preserved and how biases affect their preservation pathways is important for interpreting fossils in phylogenetic, ecological, and evolutionary frameworks. Although laboratory decay experiments reveal important aspects of fossilization, applying the results directly to the interpretation of exceptionally preserved fossils may overlook the impact of other key processes that remove or preserve morphological information. Investigations of fossils preserving non‐biomineralized tissues suggest that certain structures that are decay resistant (e.g., the notochord) are rarely preserved (even where carbonaceous components survive), and decay‐prone structures (e.g., nervous systems) can fossilize, albeit rarely. As we review here, decay resistance is an imperfect indicator of fossilization potential, and a suite of biological and geological processes account for the features preserved in exceptional fossils.

Multiple optimality criteria support ornithoscelida

A recent study of early dinosaur evolution using equal-weights parsimony recovered a scheme of dinosaur interrelationships and classification that differed from historical consensus in a single, but significant, respect; Ornithischia and Saurischia were not recovered as monophyletic sister-taxa, but rather Ornithischia and Theropoda formed a novel clade named Ornithoscelida. However, these analyses only used maximum parsimony, and numerous recent simulation studies have questioned the accuracy of parsimony under equal weights. Here, we provide additional support for this alternative hypothesis using Bayesian implementation of the Mkv model, as well as through number of additional parsimony analyses, including implied weighting. Using Bayesian inference and implied weighting, we recover the same fundamental topology for Dinosauria as the original study, with a monophyletic Ornithoscelida, demonstrating that the main suite of methods used in morphological phylogenetics recover this novel hypothesis. This result was further scrutinized through the systematic exclusion of different character sets. Novel characters from the original study (those not taken or adapted from previous phylogenetic studies) were found to be more important for resolving the relationships within Dinosauromorpha than the relationships within Dinosauria. Reanalysis of a modified version of the character matrix that supports the Ornithischia–Saurischia dichotomy under maximum parsimony also supports this hypothesis under implied weighting, but not under the Mkv model, with both Theropoda and Sauropodomorpha becoming paraphyletic with respect to Ornithischia.

Earth’s oldest ‘Bobbit worm’ – gigantism in a Devonian eunicidan polychaete

Whilst the fossil record of polychaete worms extends to the early Cambrian, much data on this group derive from microfossils known as scolecodonts. These are sclerotized jaw elements, which generally range from 0.1–2 mm in size, and which, in contrast to the soft-body anatomy, have good preservation potential and a continuous fossil record. Here we describe a new eunicidan polychaete, Websteroprion armstrongi gen. et sp. nov., based primarily on monospecific bedding plane assemblages from the Lower-Middle Devonian Kwataboahegan Formation of Ontario, Canada. The specimens are preserved mainly as three-dimensional moulds in the calcareous host rock, with only parts of the original sclerotized jaw walls occasionally present. This new taxon has a unique morphology and is characterized by an unexpected combination of features seen in several different Palaeozoic polychaete families. Websteroprion armstrongi was a raptorial feeder and possessed the largest jaws recorded in polychaetes from the fossil record, with maxillae reaching over one centimetre in length. Total body length of the species is estimated to have reached over one metre, which is comparable to that of extant ‘giant eunicid’ species colloquially referred to as ‘Bobbit worms’. This demonstrates that polychaete gigantism was already a phenomenon in the Palaeozoic, some 400 million years ago.