The 'Tully monster' is a vertebrate.

Problematic fossils, extinct taxa of enigmatic morphology that cannot be assigned to a known major group, were once a major issue in palaeontology. A long-favoured solution to the 'problem of the problematica', particularly the 'weird wonders' of the Cambrian Burgess Shale, was to consider them representatives of extinct phyla. A combination of new evidence and modern approaches to phylogenetic analysis has now resolved the affinities of most of these forms. Perhaps the most notable exception is Tullimonstrum gregarium, popularly known as the Tully monster, a large soft-bodied organism from the late Carboniferous Mazon Creek biota (approximately 309-307 million years ago) of Illinois, USA, which was designated the official state fossil of Illinois in 1989. Its phylogenetic position has remained uncertain and it has been compared with nemerteans, polychaetes, gastropods, conodonts, and the stem arthropod Opabinia. Here we review the morphology of Tullimonstrum based on an analysis of more than 1,200 specimens. We find that the anterior proboscis ends in a buccal apparatus containing teeth, the eyes project laterally on a long rigid bar, and the elongate segmented body bears a caudal fin with dorsal and ventral lobes. We describe new evidence for a notochord, cartilaginous arcualia, gill pouches, articulations within the proboscis, and multiple tooth rows adjacent to the mouth. This combination of characters, supported by phylogenetic analysis, identifies Tullimonstrum as a vertebrate, and places it on the stem lineage to lampreys (Petromyzontida). In addition to increasing the known morphological disparity of extinct lampreys, a chordate affinity for T. gregarium resolves the nature of a soft-bodied fossil which has been debated for more than 50 years.

When fossil clades 'compete': local dominance, global diversification dynamics and causation.

Examining the supposition that local-scale competition drives macroevolutionary patterns has become a familiar goal in fossil biodiversity studies. However, it is an elusive goal, hampered by inadequate confirmation of ecological equivalence and interactive processes between clades, patchy sampling, few comparative analyses of local species assemblages over long geological intervals, and a dearth of appropriate statistical tools. We address these concerns by reevaluating one of the classic examples of clade displacement in the fossil record, in which cheilostome bryozoans surpass the once dominant cyclostomes. Here, we analyse a newly expanded and vetted compilation of 40 190 fossil species occurrences to estimate cheilostome and cyclostome patterns of species proportions within assemblages, global genus richness and genus origination and extinction rates while accounting for sampling. Comparison of time-series models using linear stochastic differential equations suggests that inter-clade genus origination and extinction rates are causally linked to each other in a complex feedback relationship rather than by simple correlations or unidirectional relationships, and that these rates are not causally linked to changing within-assemblage proportions of cheilostome versus cyclostome species.

Text-mined fossil biodiversity dynamics using machine learning.

Documented occurrences of fossil taxa are the empirical foundation for understanding large-scale biodiversity changes and evolutionary dynamics in deep time. The fossil record contains vast amounts of understudied taxa. Yet the compilation of huge volumes of data remains a labour-intensive impediment to a more complete understanding of Earth's biodiversity history. Even so, many occurrence records of species and genera in these taxa can be uncovered in the palaeontological literature. Here, we extract observations of fossils and their inferred ages from unstructured text in books and scientific articles using machine-learning approaches. We use Bryozoa, a group of marine invertebrates with a rich fossil record, as a case study. Building on recent advances in computational linguistics, we develop a pipeline to recognize taxonomic names and geologic time intervals in published literature and use supervised learning to machine-read whether the species in question occurred in a given age interval. Intermediate machine error rates appear comparable to human error rates in a simple trial, and resulting genus richness curves capture the main features of published fossil diversity studies of bryozoans. We believe our automated pipeline, that greatly reduced the time required to compile our dataset, can help others compile similar data for other taxa.

Rethinking Living Fossils.

Biologists would be mistaken if they relegated living fossils to paleontological inquiry or assumed that the concept is dead. It is now used to describe entities ranging from viruses to higher taxa, despite recent warnings of misleading inferences. Current work on character evolution illustrates how analyzing living fossils and stasis in terms of parts (characters) and wholes (e.g., organisms and lineages) advances our understanding of prolonged stasis at many hierarchical levels. Instead of viewing the concept's task as categorizing living fossils, we show how its primary role is to mark out what is in need of explanation, accounting for the persistence of both molecular and morphological traits. Rethinking different conceptions of living fossils as specific hypotheses reveals novel avenues for research that integrate phylogenetics, ecological and evolutionary modeling, and evo-devo to produce a more unified theoretical outlook.

Corrigendum: Rethinking Living Fossils.

[This corrects the article DOI: 10.1093/biosci/biy084.].

Simple versus complex models of trait evolution and stasis as a response to environmental change.

Previous analyses of evolutionary patterns, or modes, in fossil lineages have focused overwhelmingly on three simple models: stasis, random walks, and directional evolution. Here we use likelihood methods to fit an expanded set of evolutionary models to a large compilation of ancestor-descendant series of populations from the fossil record. In addition to the standard three models, we assess more complex models with punctuations and shifts from one evolutionary mode to another. As in previous studies, we find that stasis is common in the fossil record, as is a strict version of stasis that entails no real evolutionary changes. Incidence of directional evolution is relatively low (13%), but higher than in previous studies because our analytical approach can more sensitively detect noisy trends. Complex evolutionary models are often favored, overwhelmingly so for sequences comprising many samples. This finding is consistent with evolutionary dynamics that are, in reality, more complex than any of the models we consider. Furthermore, the timing of shifts in evolutionary dynamics varies among traits measured from the same series. Finally, we use our empirical collection of evolutionary sequences and a long and highly resolved proxy for global climate to inform simulations in which traits adaptively track temperature changes over time. When realistically calibrated, we find that this simple model can reproduce important aspects of our paleontological results. We conclude that observed paleontological patterns, including the prevalence of stasis, need not be inconsistent with adaptive evolution, even in the face of unstable physical environments.

Moving Past the Systematics Wars.

It is time to escape the constraints of the Systematics Wars narrative and pursue new questions that are better positioned to establish the relevance of the field in this time period to broader issues in the history of biology and history of science. To date, the underlying assumptions of the Systematics Wars narrative have led historians to prioritize theory over practice and the conflicts of a few leading theorists over the less-polarized interactions of systematists at large. We show how shifting to a practice-oriented view of methodology, centered on the trajectory of mathematization in systematics, demonstrates problems with the common view that one camp (cladistics) straightforwardly "won" over the other (phenetics). In particular, we critique David Hull's historical account in Science as a Process by demonstrating exactly the sort of intermediate level of positive sharing between phenetic and cladistic theories that undermines their mutually exclusive individuality as conceptual systems over time. It is misleading, or at least inadequate, to treat them simply as holistically opposed theories that can only interact by competition to the death. Looking to the future, we suggest that the concept of workflow provides an important new perspective on the history of mathematization and computerization in biology after World War II.

Evolutionary mode routinely varies among morphological traits within fossil species lineages.

Recent studies have revitalized interest in methods for detecting evolutionary modes in both fossil sequences and phylogenies. Most of these studies examine single size or shape traits, often implicitly assuming that single phenotypic traits are adequate representations of species-level change. We test the validity of this assumption by tallying the frequency with which traits vary in evolutionary mode within fossil species lineages. After fitting models of directional change, unbiased random walk, and stasis to a dataset of 635 traits across 153 species lineages, we find that within the majority of lineages, evolutionary mode varies across traits and the likelihood of conflicting within-lineage patterns increases with the number of traits analyzed. In addition, single traits may show variation in evolutionary mode even in situations where the overall morphological evolution of the lineage is dominated by one type of mode. These quantified, stratigraphically based findings validate the idea that morphological patterns of mosaic evolution are pervasive across groups of organisms throughout Earth's history.

Enhancing georeferenced biodiversity inventories: automated information extraction from literature records reveal the gaps.

We use natural language processing (NLP) to retrieve location data for cheilostome bryozoan species (text-mined occurrences (TMO)) in an automated procedure. We compare these results with data combined from two major public databases (DB): the Ocean Biodiversity Information System (OBIS), and the Global Biodiversity Information Facility (GBIF). Using DB and TMO data separately and in combination, we present latitudinal species richness curves using standard estimators (Chao2 and the Jackknife) and range-through approaches. Our combined DB and TMO species richness curves quantitatively document a bimodal global latitudinal diversity gradient for extant cheilostomes for the first time, with peaks in the temperate zones. A total of 79% of the georeferenced species we retrieved from TMO (N = 1,408) and DB (N = 4,549) are non-overlapping. Despite clear indications that global location data compiled for cheilostomes should be improved with concerted effort, our study supports the view that many marine latitudinal species richness patterns deviate from the canonical latitudinal diversity gradient (LDG). Moreover, combining online biodiversity databases with automated information retrieval from the published literature is a promising avenue for expanding taxon-location datasets.

Controlling the error probabilities of model selection information criteria using bootstrapping.

The Akaike Information Criterion (AIC) and related information criteria are powerful and increasingly popular tools for comparing multiple, non-nested models without the specification of a null model. However, existing procedures for information-theoretic model selection do not provide explicit and uniform control over error rates for the choice between models, a key feature of classical hypothesis testing. We show how to extend notions of Type-I and Type-II error to more than two models without requiring a null. We then present the Error Control for Information Criteria (ECIC) method, a bootstrap approach to controlling Type-I error using Difference of Goodness of Fit (DGOF) distributions. We apply ECIC to empirical and simulated data in time series and regression contexts to illustrate its value for parametric Neyman-Pearson classification. An R package implementing the bootstrap method is publicly available.

Chemical signatures of soft tissues distinguish between vertebrates and invertebrates from the Carboniferous Mazon Creek Lagerstätte of Illinois.

The chemical composition of fossil soft tissues is a potentially powerful and yet underutilized tool for elucidating the affinity of problematic fossil organisms. In some cases, it has proven difficult to assign a problematic fossil even to the invertebrates or vertebrates (more generally chordates) based on often incompletely preserved morphology alone, and chemical composition may help to resolve such questions. Here, we use in situ Raman microspectroscopy to investigate the chemistry of a diverse array of invertebrate and vertebrate fossils from the Pennsylvanian Mazon Creek Lagerstätte of Illinois, and we generate a ChemoSpace through principal component analysis (PCA) of the in situ Raman spectra. Invertebrate soft tissues characterized by chitin (polysaccharide) fossilization products and vertebrate soft tissues characterized by protein fossilization products plot in completely separate, non-overlapping regions of the ChemoSpace, demonstrating the utility of certain soft tissue molecular signatures as biomarkers for the original soft tissue composition of fossil organisms. The controversial problematicum Tullimonstrum, known as the Tully Monster, groups with the vertebrates, providing strong evidence of a vertebrate rather than invertebrate affinity.

The origin of ascophoran bryozoans was historically contingent but likely.

The degree to which evolutionary outcomes are historically contingent remains unresolved, with studies at different levels of the biological hierarchy reaching different conclusions. Here we examine historical contingency in the origin of two evolutionary novelties in bryozoans, a phylum of colonial animals whose fossil record is as complete as that of any major group. In cheilostomes, the dominant living bryozoans, key innovations were the costal shield and ascus, which first appeared in the Cretaceous 85-95 Myr ago. We establish the parallel origin of these structures less than 12 Myr ago in an extant bryozoan genus, Cauloramphus, with transitional stages remarkably similar to those inferred for a Cretaceous clade. By one measure, long lag times in the first origins of costal shield and ascus suggest a high degree of historical contingency. This, however, does not equate with dependence on a narrow set of initial conditions or a low probability of evolution. More than one set of initial conditions may lead to an evolutionary outcome, and alternative sets are not entirely independent. We argue that, although historically contingent, the origin of ascus and costal shield was highly likely with sufficient possibilities afforded by time.

Matrotrophy and placentation in invertebrates: a new paradigm.

Matrotrophy, the continuous extra-vitelline supply of nutrients from the parent to the progeny during gestation, is one of the masterpieces of nature, contributing to offspring fitness and often correlated with evolutionary diversification. The most elaborate form of matrotrophy-placentotrophy-is well known for its broad occurrence among vertebrates, but the comparative distribution and structural diversity of matrotrophic expression among invertebrates is wanting. In the first comprehensive analysis of matrotrophy across the animal kingdom, we report that regardless of the degree of expression, it is established or inferred in at least 21 of 34 animal phyla, significantly exceeding previous accounts and changing the old paradigm that these phenomena are infrequent among invertebrates. In 10 phyla, matrotrophy is represented by only one or a few species, whereas in 11 it is either not uncommon or widespread and even pervasive. Among invertebrate phyla, Platyhelminthes, Arthropoda and Bryozoa dominate, with 162, 83 and 53 partly or wholly matrotrophic families, respectively. In comparison, Chordata has more than 220 families that include or consist entirely of matrotrophic species. We analysed the distribution of reproductive patterns among and within invertebrate phyla using recently published molecular phylogenies: matrotrophy has seemingly evolved at least 140 times in all major superclades: Parazoa and Eumetazoa, Radiata and Bilateria, Protostomia and Deuterostomia, Lophotrochozoa and Ecdysozoa. In Cycliophora and some Digenea, it may have evolved twice in the same life cycle. The provisioning of developing young is associated with almost all known types of incubation chambers, with matrotrophic viviparity more widespread (20 phyla) than brooding (10 phyla). In nine phyla, both matrotrophic incubation types are present. Matrotrophy is expressed in five nutritive modes, of which histotrophy and placentotrophy are most prevalent. Oophagy, embryophagy and histophagy are rarer, plausibly evolving through heterochronous development of the embryonic mouthparts and digestive system. During gestation, matrotrophic modes can shift, intergrade, and be performed simultaneously. Invertebrate matrotrophic adaptations are less complex structurally than in chordates, but they are more diverse, being formed either by a parent, embryo, or both. In a broad and still preliminary sense, there are indications of trends or grades of evolutionarily increasing complexity of nutritive structures: formation of (i) local zones of enhanced nutritional transport (placental analogues), including specialized parent-offspring cell complexes and various appendages increasing the entire secreting and absorbing surfaces as well as the contact surface between embryo and parent, (ii) compartmentalization of the common incubatory space into more compact and 'isolated' chambers with presumably more effective nutritional relationships, and (iii) internal secretory ('milk') glands. Some placental analogues in onychophorans and arthropods mimic the simplest placental variants in vertebrates, comprising striking examples of convergent evolution acting at all levels-positional, structural and physiological.

Spatial patterns of diversity in the sea: bryozoan species richness in the North Atlantic.

1. We have examined large-scale geographical patterns in species richness for continental shelf bryozoan assemblages in the North Atlantic. Bryozoans are common and often abundant benthic organisms, but they have not previously been examined at this scale of resolution. 2. Assemblage species richness was estimated by sample species richness. This was highest at intermediate depths (10-75 m) at all latitudes where there were sufficient data, but there was no statistically significant variation with depth for the overall data set (all latitudes pooled). Mean assemblage species richness showed no significant variation with latitude, although the highest individual values were generally from lower latitudes. There is thus as yet no convincing evidence for a latitudinal cline in the alpha diversity of North Atlantic bryozoans. 3. Pooling of data into bins of 10 degrees of latitude, or into biogeographic provinces, to estimate regional species richness revealed significant undersampling. Two independent techniques to correct for this undersampling revealed a latitudinal cline in the regional species richness of North Atlantic bryozoans, with a peak around 10-30°N, and a steady decrease in richness north to 80°N. 4. Two measures of beta diversity (Whittaker and Jaccard) revealed relatively high turnover, presumably related to habitat heterogeneity within regional bins or to significant environmental variation across bins. There was a tendency for beta diversity to be higher at lower latitudes, as would be expected from a combination of a latitudinal cline in regional diversity with a mean assemblage species richness invariant with latitude. Null models were used to clarify the expected relationship between the two measures of beta diversity, and these indicated a strong influence of species-abundance structure in the North Atlantic bryozoan data.

The normative structure of mathematization in systematic biology.

We argue that the mathematization of science should be understood as a normative activity of advocating for a particular methodology with its own criteria for evaluating good research. As a case study, we examine the mathematization of taxonomic classification in systematic biology. We show how mathematization is a normative activity by contrasting its distinctive features in numerical taxonomy in the 1960s with an earlier reform advocated by Ernst Mayr starting in the 1940s. Both Mayr and the numerical taxonomists sought to formalize the work of classification, but Mayr introduced a qualitative formalism based on human judgment for determining the taxonomic rank of populations, while the numerical taxonomists introduced a quantitative formalism based on automated procedures for computing classifications. The key contrast between Mayr and the numerical taxonomists is how they conceptualized the temporal structure of the workflow of classification, specifically where they allowed meta-level discourse about difficulties in producing the classification.

Individuals at the center of biology: Rudolf Leuckart's Polymorphismus der Individuen and the ongoing narrative of parts and wholes. With an annotated translation.

Rudolf Leuckart's 1851 pamphlet Ueber den Polymorphismus der Individuen (On the polymorphism of individuals) stood at the heart of naturalists' discussions on biological individuals, parts and wholes in mid-nineteenth-century Britain and Europe. Our analysis, which accompanies the first translation of this pamphlet into English, situates Leuckart's contribution to these discussions in two ways. First, we present it as part of a complex conceptual knot involving not only individuality and the understanding of compound organisms, but also the alternation of generations, the division of labor in nature, and the possibility of finding general laws of the organic world. Leuckart's pamphlet is important as a novel attempt to give order to the strands of this knot. It also solved a set of key biological problems in a way that avoided some of the drawbacks of an earlier teleological tradition. Second, we situate the pamphlet within a longer trajectory of inquiry into part-whole relations in biology from the mid-eighteenth century to the present. We argue that biological individuality, along with the problem-complexes with which it engaged, was as central a problem to naturalists before 1859 as evolution, and that Leuckart's contributions to it left a long legacy that persisted well into the twentieth century. As biologists' interests in part-whole relations are once again on the upswing, the longue durée of this problem merits renewed consideration.

Abundance distributions imply elevated complexity of post-Paleozoic marine ecosystems.

Likelihood analyses of 1176 fossil assemblages of marine organisms from Phanerozoic (i.e., Cambrian to Recent) assemblages indicate a shift in typical relative-abundance distributions after the Paleozoic. Ecological theory associated with these abundance distributions implies that complex ecosystems are far more common among Meso-Cenozoic assemblages than among the Paleozoic assemblages that preceded them. This transition coincides not with any major change in the way fossils are preserved or collected but with a shift from communities dominated by sessile epifaunal suspension feeders to communities with elevated diversities of mobile and infaunal taxa. This suggests that the end-Permian extinction permanently altered prevailing marine ecosystem structure and precipitated high levels of ecological complexity and alpha diversity in the Meso-Cenozoic.