Age-dependent extinction and the neutral theory of biodiversity.

Red Queen (RQ) theory states that adaptation does not protect species from extinction because their competitors are continually adapting alongside them. RQ was founded on the apparent independence of extinction risk and fossil taxon age, but analytical developments have since demonstrated that age-dependent extinction is widespread, usually most intense among young species. Here, we develop ecological neutral theory as a general framework for modeling fossil species survivorship under incomplete sampling. We show that it provides an excellent fit to a high-resolution dataset of species durations for Paleozoic zooplankton and more broadly can account for age-dependent extinction seen throughout the fossil record. Unlike widely used alternative models, the neutral model has parameters with biological meaning, thereby generating testable hypotheses on changes in ancient ecosystems. The success of this approach suggests reinterpretations of mass extinctions and of scaling in eco-evolutionary systems. Intense extinction among young species does not necessarily refute RQ or require a special explanation but can instead be parsimoniously explained by neutral dynamics operating across species regardless of age.

Measurement theory and paleobiology.

Measurement theory, a branch of applied mathematics, offers guiding principles for extracting meaning from empirical observations and is applicable to any science involving measurements. Measurement theory is highly relevant in paleobiology because statistical approaches assuming ratio-scaled variables are commonly used on data belonging to nominal and ordinal scale types. We provide an informal introduction to representational measurement theory and argue for its importance in robust scientific inquiry. Although measurement theory is widely applicable in paleobiology research, we use the study of disparity to illustrate measurement theoretical challenges in the quantitative study of the fossil record. Respecting the inherent properties of different measurements enables meaningful inferences about evolutionary and ecological processes from paleontological data.

Conceptual and empirical bridges between micro- and macroevolution.

Explaining broad molecular, phenotypic and species biodiversity patterns necessitates a unifying framework spanning multiple evolutionary scales. Here we argue that although substantial effort has been made to reconcile microevolution and macroevolution, much work remains to identify the links between biological processes at play. We highlight four major questions of evolutionary biology whose solutions require conceptual bridges between micro and macroevolution. We review potential avenues for future research to establish how mechanisms at one scale (drift, mutation, migration, selection) translate to processes at the other scale (speciation, extinction, biogeographic dispersal) and vice versa. We propose ways in which current comparative methods to infer molecular evolution, phenotypic evolution and species diversification could be improved to specifically address these questions. We conclude that researchers are in a better position than ever before to build a synthesis to understand how microevolutionary dynamics unfold over millions of years.

Cross-disciplinary information for understanding macroevolution.

Many different macroevolutionary models can produce the same observations. Despite efforts in building more complex and realistic models, it may still be difficult to distinguish the processes that have generated the biodiversity we observe. In this opinion we argue that we can make new progress by reaching out across disciplines, relying on independent data and theory to constrain macroevolutionary inference. Using mainly paleontological insights and data, we illustrate how we can eliminate less plausible or implausible models, and/or parts of parameter space, while applying comparative phylogenetic approaches. We emphasize that such cross-disciplinary insights and data can be drawn between many other disciplines relevant to macroevolution. We urge cross-disciplinary training, and collaboration using common-use databases as a platform for increasing our understanding.

Changing allometric relationships among fossil and Recent populations in two colonial species.

Allometry is vital for understanding the mechanisms underlying phenotypic evolution. Despite a large body of literature on allometry, studies based on fossil time series are limited for solitary organisms and nonexistent for colonial organisms. Allometric relationships have been found to be relatively constant across Recent populations of the same species, separated by space, but variable among fossil populations separated by thousands of years. How stable are allometric relationships at the module level for colonial organisms? We address this question using two extant species of the cheilostome bryozoan Microporella with fossil records spanning the Pleistocene of New Zealand. We investigate size covariation between feeding modules and three traits with separate functions (reproductive, resource uptake, and defense). We found that within-population (static) allometry can change on timescales of at least 0.1 million years. These within-population relationships do not consistently predict overintraspecific evolutionary allometry, which in turn does not predict those estimated at the genus level. Different functional traits are constrained to different extents by module size with defensive traits being the least constrained and most evolvable, compared with reproductive and resource uptake traits. Our study highlights the potential of colonial organisms in understanding the constraints and drivers of long-term phenotypic change.

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.

Paleozoic origins of cheilostome bryozoans and their parental care inferred by a new genome-skimmed phylogeny.

Phylogenetic relationships and the timing of evolutionary events are essential for understanding evolution on longer time scales. Cheilostome bryozoans are a group of ubiquitous, species-rich, marine colonial organisms with an excellent fossil record but lack phylogenetic relationships inferred from molecular data. We present genome-skimmed data for 395 cheilostomes and combine these with 315 published sequences to infer relationships and the timing of key events among c. 500 cheilostome species. We find that named cheilostome genera and species are phylogenetically coherent, rendering fossil or contemporary specimens readily delimited using only skeletal morphology. Our phylogeny shows that parental care in the form of brooding evolved several times independently but was never lost in cheilostomes. Our fossil calibration, robust to varied assumptions, indicates that the cheilostome lineage and parental care therein could have Paleozoic origins, much older than the first known fossil record of cheilostomes in the Late Jurassic.

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.

A molecular phylogeny of historical and contemporary specimens of an under-studied micro-invertebrate group.

Resolution of relationships at lower taxonomic levels is crucial for answering many evolutionary questions, and as such, sufficiently varied species representation is vital. This latter goal is not always achievable with relatively fresh samples. To alleviate the difficulties in procuring rarer taxa, we have seen increasing utilization of historical specimens in building molecular phylogenies using high throughput sequencing. This effort, however, has mainly focused on large-bodied or well-studied groups, with small-bodied and under-studied taxa under-prioritized. Here, we utilize both historical and contemporary specimens, to increase the resolution of phylogenetic relationships among a group of under-studied and small-bodied metazoans, namely, cheilostome bryozoans. In this study, we pioneer the sequencing of air-dried cheilostomes, utilizing a recently developed library preparation method for low DNA input. We evaluate a de novo mitogenome assembly and two iterative methods, using the sequenced target specimen as a reference for mapping, for our sequences. In doing so, we present mitochondrial and ribosomal RNA sequences of 43 cheilostomes representing 37 species, including 14 from historical samples ranging from 50 to 149 years old. The inferred phylogenetic relationships of these samples, analyzed together with publicly available sequence data, are shown in a statistically well-supported 65 taxa and 17 genes cheilostome tree, which is also the most broadly sampled and largest to date. The robust phylogenetic placement of historical samples whose contemporary conspecifics and/or congenerics have been sequenced verifies the appropriateness of our workflow and gives confidence in the phylogenetic placement of those historical samples for which there are no close relatives sequenced. The success of our workflow is highlighted by the circularization of a total of 27 mitogenomes, seven from historical cheilostome samples. Our study highlights the potential of utilizing DNA from micro-invertebrate specimens stored in natural history collections for resolving phylogenetic relationships among species.

Trait-fitness associations do not predict within-species phenotypic evolution over 2 million years.

Long-term patterns of phenotypic change are the cumulative results of tens of thousands to millions of years of evolution. Yet, empirical and theoretical studies of phenotypic selection are largely based on contemporary populations. The challenges in studying phenotypic evolution, in particular trait-fitness associations in the deep past, are barriers to linking micro- and macroevolution. Here, we capitalize on the unique opportunity offered by a marine colonial organism commonly preserved in the fossil record to investigate trait-fitness associations over 2 Myr. We use the density of female polymorphs in colonies of Antartothoa tongima as a proxy for fecundity, a fitness component, and investigate multivariate signals of trait-fitness associations in six time intervals on the backdrop of Pleistocene climatic shifts. We detect negative trait-fitness associations for feeding polymorph (autozooid) sizes, positive associations for autozooid shape but no particular relationship between fecundity and brood chamber size. In addition, we demonstrate that long-term trait patterns are explained by palaeoclimate (as approximated by ∂18O), and to a lesser extent by ecological interactions (i.e. overgrowth competition and substrate crowding). Our analyses show that macroevolutionary outcomes of trait evolution are not a simple scaling-up from the trait-fitness associations.

New species of Adeonellopsis (Bryozoa: Adeonidae) from southern Zealandia and the western Tasman Sea.

Seven new species of Adeonellopsis MacGillivray, 1886 are described: Adeonellopsis macewindui, A. gracilis (endemic to New Zealand), A. gemina (New Zealand and Norfolk Island shelf), A. tasmanensis (Norfolk Island shelf and Gascoyne Seamount), A. periculosa Norfolk Island shelf) and A. wassi and A. minor (New South Wales shelf). All have flattened staghorn branches, which range in width from 0.8 to 5 mm, depending on species. Based on underwater photos, the largest species, A. macewindui n. sp. forms locally significant habitat on fiord walls and parts of the continental shelf in New Zealand, sometimes in association with A. gemina n. sp.. The latter can survive as isolated fragments that can regenerate from broken ends. Three species have a number of large gonozooids at selected locations on their branches and two of these species have vestigial ooecia in their gonozooids, recorded for the first time in Adeonidae. The remaining four species have among their autozooids only a few zooids that are a little larger, with larger compound spiramina. These are suggested to function as gonozooids, representing the larger end of a size spectrum for reproductive zooids, of which those at the lower end are the same size as autozooids. The encrusting Australian species known as Adeonellopsis baccata (Hutton, 1878) is transferred to Reptadeonella as Reptadeonella baccata n. comb..

A genome-skimmed phylogeny of a widespread bryozoan family, Adeonidae.

BACKGROUND: Understanding the phylogenetic relationships among species is one of the main goals of systematic biology. Simultaneously, credible phylogenetic hypotheses are often the first requirement for unveiling the evolutionary history of traits and for modelling macroevolutionary processes. However, many non-model taxa have not yet been sequenced to an extent such that statistically well-supported molecular phylogenies can be constructed for these purposes. Here, we use a genome-skimming approach to extract sequence information for 15 mitochondrial and 2 ribosomal operon genes from the cheilostome bryozoan family, Adeonidae, Busk, 1884, whose current systematics is based purely on morphological traits. The members of the Adeonidae are, like all cheilostome bryozoans, benthic, colonial, marine organisms. Adeonids are also geographically widely-distributed, often locally common, and are sometimes important habitat-builders. RESULTS: We successfully genome-skimmed 35 adeonid colonies representing 6 genera (Adeona, Adeonellopsis, Bracebridgia, Adeonella, Laminopora and Cucullipora). We also contributed 16 new, circularised mitochondrial genomes to the eight previously published for cheilostome bryozoans. Using the aforementioned mitochondrial and ribosomal genes, we inferred the relationships among these 35 samples. Contrary to some previous suggestions, the Adeonidae is a robustly supported monophyletic clade. However, the genera Adeonella and Laminopora are in need of revision: Adeonella is polyphyletic and Laminopora paraphyletically forms a clade with some Adeonella species. Additionally, we assign a sequence clustering identity using cox1 barcoding region of 99% at the species and 83% at the genus level. CONCLUSIONS: We provide sequence data, obtained via genome-skimming, that greatly increases the resolution of the phylogenetic relationships within the adeonids. We present a highly-supported topology based on 17 genes and substantially increase availability of circularised cheilostome mitochondrial genomes, and highlight how we can extend our pipeline to other bryozoans.

Cope's Rule in a modular organism: Directional evolution without an overarching macroevolutionary trend.

Cope's Rule describes increasing body size in evolutionary lineages through geological time. This pattern has been documented in unitary organisms but does it also apply to module size in colonial organisms? We address this question using 1169 cheilostome bryozoans ranging through the entire 150 million years of their evolutionary history. The temporal pattern evident in cheilostomes as a whole shows no overall change in zooid (module) size. However, individual subclades show size increases: within a genus, younger species often have larger zooids than older species. Analyses of (paleo)latitudinal shifts show that this pattern cannot be explained by latitudinal effects (Bergmann's Rule) coupled with younger species occupying higher latitudes than older species (an "out of the tropics" hypothesis). While it is plausible that size increase was linked to the advantages of large zooids in feeding, competition for trophic resources and living space, other proposed mechanisms for Cope's Rule in unitary organisms are either inapplicable to cheilostome zooid size or cannot be evaluated. Patterns and mechanisms in colonial organisms cannot and should not be extrapolated from the better-studied unitary organisms. And even if macroevolution simply comprises repeated rounds of microevolution, evolutionary processes occurring within lineages are not always detectable from macroevolutionary patterns.

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.

Model Adequacy and Microevolutionary Explanations for Stasis in the Fossil Record.

Long-term phenotypic stasis is frequently observed in the fossil record, but not readily predicted from microevolutionary theory. To test competing explanations for stasis on macroevolutionary timescales we need reliably estimated parameters from appropriate evolutionary models that adequately describe the evolutionary trait dynamics. Here, we develop tests to assess the adequacy of the most commonly used stasis model in evolutionary biology and apply them to time series of phenotypic traits from fossil lineages. Of the 572 fossil time series we analyzed from the literature, 263 time series showed a better fit to the stasis model relative to alternative models, but only 172 of those fitted the stasis model in both relative and absolute terms. The estimated trait variances from these 172 time series do not correlate with rough proxies of effective population size. Our preliminary investigation of the fixed-optimum hypothesis hence fails to give empirical support to the idea that genetic drift around a constant trait optimum is an explanation for stasis in the fossil record. We argue that optima following stationary processes on the adaptive landscape is a viable hypothesis for stasis that needs further investigation. We end by discussing how investigations of model adequacy can be a valuable approach for increasing our understanding of the dynamics of the adaptive landscape on macroevolutionary timescales.

Finding Evolutionary Processes Hidden in Cryptic Species.

Cryptic species could represent a substantial fraction of biodiversity. However, inconsistent definitions and taxonomic treatment of cryptic species prevent informed estimates of their contribution to biodiversity and impede our understanding of their evolutionary and ecological significance. We propose a conceptual framework that recognizes cryptic species based on their low levels of phenotypic (morphological) disparity relative to their degree of genetic differentiation and divergence times as compared with non-cryptic species. We discuss how application of a more rigorous definition of cryptic species in taxonomic practice will lead to more accurate estimates of their prevalence in nature, better understanding of their distribution patterns on the tree of life, and increased abilities to resolve the processes underlying their evolution.

Millions of Years Behind: Slow Adaptation of Ruminants to Grasslands.

The Late Cretaceous appearance of grasses, followed by the Cenozoic advancement of grasslands as dominant biomes, has contributed to the evolution of a range of specialized herbivores adapted to new diets, as well as to increasingly open and arid habitats. Many mammals including ruminants, the most diversified ungulate suborder, evolved high-crowned (hypsodont) teeth as an adaptation to tooth-wearing diets and habitats. The impact of different causes of tooth wear is still a matter of debate, and the temporal pattern of hypsodonty evolution in relation to the evolution of grasslands remains unclear. We present an improved time-calibrated molecular phylogeny of Cetartiodactyla, with phylogenetic reconstruction of ancestral ruminant diets and habitats, based on characteristics of extant taxa. Using this timeline, as well as the fossil record of grasslands, we conduct phylogenetic comparative analyses showing that hypsodonty in ruminants evolved as an adaptation to both diet and habitat. Our results demonstrate a slow, perhaps constrained, evolution of hypsodonty toward estimated optimal states, excluding the possibility of immediate adaptation. This augments recent findings that slow adaptation is not uncommon on million-year time scales.

Common species link global ecosystems to climate change: dynamical evidence in the planktonic fossil record.

Common species shape the world around us, and changes in their commonness signify large-scale shifts in ecosystem structure and function. However, our understanding of long-term ecosystem response to environmental forcing in the deep past is centred on species richness, neglecting the disproportional impact of common species. Here, we use common and widespread species of planktonic foraminifera in deep-sea sediments to track changes in observed global occupancy (proportion of sampled sites at which a species is present and observed) through the turbulent climatic history of the last 65 Myr. Our approach is sensitive to relative changes in global abundance of the species set and robust to factors that bias richness estimators. Using three independent methods for detecting causality, we show that the observed global occupancy of planktonic foraminifera has been dynamically coupled to past oceanographic changes captured in deep-ocean temperature reconstructions. The causal inference does not imply a direct mechanism, but is consistent with an indirect, time-delayed causal linkage. Given the strong quantitative evidence that a dynamical coupling exists, we hypothesize that mixotrophy (symbiont hosting) may be an ecological factor linking the global abundance of planktonic foraminifera to long-term climate changes via the relative extent of oligotrophic oceans.