Skeletal completeness of the non‐avian theropod dinosaur fossil record

Non‐avian theropods were a highly successful clade of bipedal, predominantly carnivorous, dinosaurs. Their diversity and macroevolutionary patterns have been the subject of many studies. Changes in fossil specimen completeness through time and space can bias our understanding of macroevolution. Here, we quantify the completeness of 455 non‐avian theropod species using the skeletal completeness metric (SCM), which calculates the proportion of a complete skeleton preserved for a specimen. Temporal patterns of theropod skeletal completeness show peaks in the Carnian, Oxfordian–Kimmeridgian and Barremian–Aptian, and lows in the Berriasian and Hauterivian. Lagerstätten primarily drive the peaks in completeness and observed taxonomic diversity in the Oxfordian–Kimmeridgian and the Barremian–Aptian. Theropods have a significantly lower distribution of completeness scores than contemporary sauropodomorph dinosaurs but change in completeness through time for the two groups shows a significant correlation when conservation Lagerstätten are excluded, possibly indicating that both records are primarily driven by geology and sampling availability. Our results reveal relatively weak temporal sampling biases acting on the theropod record but relatively strong spatial and environmental biases. Asia has a significantly more complete record than any other continent, the mid northern latitudes have the highest abundance of finds, and most complete theropod skeletons come from lacustrine and aeolian environments. We suggest that these patterns result from historical research focus, modern climate dynamics, and depositional transportation energy plus association with conservation Lagerstätten, respectively. Furthermore, we find possible ecological biases acting on different theropod subgroups, but body size does not influence theropod completeness on a global scale.     

Ten more years of discovery: revisiting the quality of the sauropodomorph dinosaur fossil record

Spatiotemporal changes in fossil specimen completeness can bias our understanding of a group's evolutionary history. The quality of the sauropodomorph fossil record was assessed a decade ago, but the number of valid species has since increased by 60%, and 17% of the taxa from that study have since undergone taxonomic revision. Here, we assess how 10 years of additional research has changed our outlook on the group's fossil record. We quantified the completeness of all 307 sauropodomorph species currently considered valid using the skeletal completeness metric, which calculates the proportion of a complete skeleton preserved for each taxon. Taxonomic and stratigraphic age revisions, rather than new species, are the drivers of the most significant differences between the current results and those of the previous assessment. No statistical differences appeared when we use our new dataset to generate temporal completeness curves based solely on taxa known in 2009 or 1999. We now observe a severe drop in mean completeness values across the Jurassic–Cretaceous boundary that never recovers to pre-Cretaceous levels. Explaining this pattern is difficult, as we find no convincing evidence that it is related to environmental preferences or body size changes. Instead, it might result from: (1) reduction of terrestrial fossil preservation space due to sea level rise; (2) ecological specificities and relatively high diagnosability of Cretaceous species; and/or (3) increased sampling of newly explored sites with many previously unknown taxa. Revisiting patterns in this manner allows us to test the longevity of conclusions made in previous quantitative studies.     

Fossil preservation and the stratigraphic ranges of taxa

The incompleteness of the fossil record hinders the inference of evolutionary rates and patterns. Here, we derive relationships among true taxonomic durations, preservation probability, and observed taxonomic ranges. We use these relationships to estimate original distributions of taxonomic durations, preservation probability, and completeness (proportion of taxa preserved), given only the observed ranges. No data on occurrences within the ranges of taxa are required. When preservation is random and the original distribution of durations is exponential, the inference of durations, preservability, and completeness is exact. However, reasonable approximations are possible given non-exponential duration distributions and temporal and taxonomic variation in preservability. Thus, the approaches we describe have great potential in studies of taphonomy, evolutionary rates and patterns, and genealogy. Analyses of Upper Cambrian-Lower Ordovician trilobite species, Paleozoic crinoid genera, Jurassic bivalve species, and Cenozoic mammal species yield the following results: (1) The preservation probability inferred from stratigraphic ranges alone agrees with that inferred from the analysis of stratigraphic gaps when data on the latter are available. (2) Whereas median durations based on simple tabulations of observed ranges are biased by stratigraphic resolution, our estimates of median duration, extinction rate, and completeness are not biased.(3) The shorter geologic ranges of mammalian species relative to those of bivalves cannot be attributed to a difference in preservation potential. However, we cannot rule out the contribution of taxonomic practice to this difference. (4) In the groups studied, completeness (proportion of species [trilobites, bivalves, mammals] or genera [crinoids] preserved) ranges from 60% to 90%. The higher estimates of completeness at smaller geographic scales support previous suggestions that the incompleteness of the fossil record reflects loss of fossiliferous rock more than failure of species to enter the fossil record in the first place.     

Evolutionary genetics of birds IV rates of protein divergence in waterfowl (Anatidae)

An electrophoretic comparison of proteins in 26 species of waterfowl (Anatidae), representing two major subfamilies and six subfamilial tribes, led to the following major conclusions: (1) the genetic data, analyzed phenetically and cladistically, generally support traditional concepts of evolutionary relationships, although some areas of disagreement are apparent; (2) species and genera within Anatidae exhibit smaller genetic distances at protein-coding loci than do most non-avian vertebrates of equivalent taxonomic rank; (3) the conservative pattern of protein differentiation in Anatidae parallels patterns previously reported in Passeriforme birds. If previous taxonomic assignments and ages of anatid fossils are reliable, it would appear that the conservative levels of protein divergence among living species may not be due to recent age of the family, but rather to a several-fold deceleration in rate of protein evolution relative to non-avian vertebrates. Since it now appears quite possible that homologous proteins can evolve at different rates in different phylads, molecular-based conclusions about absolute divergence times for species with a poor fossil record should remain appropriately reserved. However, the recognition and study of the phenomenon of apparent heterogeneity in rates of protein divergence across phylads may eventually enhance our understanding of molecular and organismal evolution.     

Is evolutionary history repeatedly rewritten in light of new fossil discoveries?

Mass media and popular science journals commonly report that new fossil discoveries have ‘rewritten evolutionary history’. Is this merely journalistic hyperbole or is our sampling of systematic diversity so limited that attempts to derive evolutionary history from these datasets are premature? We use two exemplars—catarrhine primates (Old World monkeys and apes) and non-avian dinosaurs—to investigate how the maturity of datasets can be assessed. Both groups have been intensively studied over the past 200 years and so should represent pinnacles in our knowledge of vertebrate systematic diversity. We test the maturity of these datasets by assessing the completeness of their fossil records, their susceptibility to changes in macroevolutionary hypotheses and the balance of their phylogenies through study time. Catarrhines have shown prolonged stability, with discoveries of new species being evenly distributed across the phylogeny, and thus have had little impact on our understanding of their fossil record, diversification and evolution. The reverse is true for dinosaurs, where the addition of new species has been non-random and, consequentially, their fossil record, tree shape and our understanding of their diversification is rapidly changing. The conclusions derived from these analyses are relevant more generally: the maturity of systematic datasets can and should be assessed before they are exploited to derive grand macroevolutionary hypotheses.     

Preservational bias controls the fossil record of pterosaurs

Pterosaurs, a Mesozoic group of flying archosaurs, have become a focal point for debates pertaining to the impact of sampling biases on our reading of the fossil record, as well as the utility of sampling proxies in palaeo‐diversity reconstructions. The completeness of the pterosaur fossil specimens themselves potentially provides additional information that is not captured in existing sampling proxies, and might shed new light on the group's evolutionary history. Here we assess the quality of the pterosaur fossil record via a character completeness metric based on the number of phylogenetic characters that can be scored for all known skeletons of 172 valid species, with averaged completeness values calculated for each geological stage. The fossil record of pterosaurs is observed to be strongly influenced by the occurrence and distribution of Lagerstätten. Peaks in completeness correlate with Lagerstätten deposits, and a recovered correlation between completeness and observed diversity is rendered non‐significant when Lagerstätten species are excluded. Intervals previously regarded as potential extinction events are shown to lack Lagerstätten and exhibit low completeness values: as such, the apparent low diversity in these intervals might be at least partly the result of poor fossil record quality. A positive correlation between temporal patterns in completeness of Cretaceous pterosaurs and birds further demonstrates the prominent role that Lagerstätten deposits have on the preservation of smaller bodied organisms, contrasting with a lack of correlation with the completeness of large‐bodied sauropodomorphs. However, we unexpectedly find a strong correlation between sauropodomorph and pterosaur completeness within the Triassic–Jurassic, but not the Cretaceous, potentially relating to a shared shift in environmental preference and thus preservation style through time. This study highlights the importance of understanding the relationship between various taphonomic controls when correcting for sampling bias, and provides additional evidence for the prominent role of sampling on observed patterns in pterosaur macroevolution.     

Quantifying the effects of the break up of Pangaea on global terrestrial diversification with neutral theory

The historic richness of most taxonomic groups increases substantially over geological time. Explanations for this fall broadly into two categories: bias in the fossil record and elevated net rates of diversification in recent periods. For example, the break up of Pangaea and isolation between continents might have increased net diversification rates. In this study, we investigate the effect on terrestrial diversification rates of the increased isolation between land masses brought about by continental drift. We use ecological neutral theory as a means to study geologically complex scenarios tractably. Our models show the effects of simulated geological events that affect all species equally, without the added complexity of further ecological processes. We find that continental drift leads to an increase in diversity only where isolation between continents leads to additional speciation through vicariance, and where higher taxa with very low global diversity are considered. We conclude that continental drift by itself is not sufficient to account for the increase in terrestrial species richness observed in the fossil record.     

How Accurate are Paleoecological Reconstructions of Early Paleontological and Archaeological Sites?

Paleoecology allows construction of paleoenvironmental models, faunal changes and evolutionary trends of paleontological taxa using modern analogs. However, when linking modern analogs to paleontological taxa in paleoecological reconstruction, differential taxonomic preservation in the fossil record has to be taken into account. Paleontologists have known the biased nature of the fossil record since Efremov’s publication on taphonomy in 1940, yet many ecological models of habitats associated with hominins in paleontological and archaeological sites in Africa and elsewhere barely address the complexity of the fossil record. We use randomly sampled ungulates from modern biomes in a comparative taxonomic abundance to demonstrate how the combination of modern thanatocoenoses and taphocoenoses, when used in reference to habitat-specific biocoenosis, produce better inferences of past habitats in paleontological and archaeological sites than approaches currently used.     

Small Theropod Teeth from the Late Cretaceous of the San Juan Basin,Northwestern New Mexico and Their Implications for Understanding Latest Cretaceous Dinosaur Evolution

Studying the evolution and biogeographic distribution of dinosaurs during the latest Cretaceous is critical for better understanding the end-Cretaceous extinction event that killed off all non-avian dinosaurs. Western North America contains among the best records of Late Cretaceous terrestrial vertebrates in the world, but is biased against small-bodied dinosaurs. Isolated teeth are the primary evidence for understanding the diversity and evolution of small-bodied theropod dinosaurs during the Late Cretaceous, but few such specimens have been well documented from outside of the northern Rockies, making it difficult to assess Late Cretaceous dinosaur diversity and biogeographic patterns. We describe small theropod teeth from the San Juan Basin of northwestern New Mexico. These specimens were collected from strata spanning Santonian – Maastrichtian. We grouped isolated theropod teeth into several morphotypes, which we assigned to higher-level theropod clades based on possession of phylogenetic synapomorphies. We then used principal components analysis and discriminant function analyses to gauge whether the San Juan Basin teeth overlap with, or are quantitatively distinct from, similar tooth morphotypes from other geographic areas. The San Juan Basin contains a diverse record of small theropods. Late Campanian assemblages differ from approximately co-eval assemblages of the northern Rockies in being less diverse with only rare representatives of troodontids and a Dromaeosaurus-like taxon. We also provide evidence that erect and recurved morphs of a Richardoestesia-like taxon represent a single heterodont species. A late Maastrichtian assemblage is dominated by a distinct troodontid. The differences between northern and southern faunas based on isolated theropod teeth provide evidence for provinciality in the late Campanian and the late Maastrichtian of North America. However, there is no indication that major components of small-bodied theropod diversity were lost during the Maastrichtian in New Mexico. The same pattern seen in northern faunas, which may provide evidence for an abrupt dinosaur extinction.     

The mosasaur fossil record through the lens of fossil completeness

The quality of the fossil record affects our understanding of macroevolutionary patterns. Palaeodiversity is filtered through geological and human processes; efforts to correct for these biases are part of a debate concerning the role of sampling proxies and standardization in biodiversity models. We analyse the fossil record of mosasaurs in terms of fossil completeness as a measure of fossil quality, using three novel, correlating metrics of fossil completeness and 4083 specimens. A new qualitative measure of character completeness (QCM) correlates with the phylogenetic character completeness metric. Mean completeness by species decreases with specimen count; average completeness by substage varies significantly. Mean specimen completeness is higher for species‐named fossils than those identified to genus and family. We consider the effect of tooth‐only specimens. Importantly, we find that completeness of species does not correlate with completeness of specimens. Completeness varies by palaeogeography: North American specimens show higher completeness than those from Eurasia and Gondwana. These metrics can be used to identify exceptional preservation; specimen completeness varies significantly by both formation and lithology. The Belgian Ciply Formation displays the highest completeness; clay lithologies show higher completeness values. Neither species diversity nor sea level correlates significantly with fossil completeness. A generalized least squares (GLS) analysis using multiple variables agrees with this result, but reveals two variables with significant predictive value for modelling averaged diversity: sea level, and mosasaur and plesiosaur‐bearing formations (the latter is redundant with diversity). Mosasaur completeness is not driven by sea level, nor does completeness limit the mosasaur diversity signal.     

Large-scale heterogeneity of the fossil record: implications for Phanerozoic biodiversity studies

Patterns of origination, extinction and standing diversity through time have been inferred from tallies of taxa preserved in the fossil record. This approach assumes that sampling of the fossil record is effectively uniform over time. Although recent evidence suggests that our sampling of the available rock record has indeed been very thorough and effective, there is also overwhelming evidence that the rock record available for sampling is itself distorted by major systematic biases. Data on rock outcrop area compiled for post-Palaeozoic sediments from Western Europe at stage level are presented. These show a strongly cyclical pattern corresponding to first- and second-order sequence stratigraphical depositional cycles. Standing diversity increases over time and, at the coarsest scale, is decoupled from surface outcrop area. This increasing trend can therefore be considered a real pattern. Changes in standing diversity and origination rates over time-scales measured in tens of millions of years, however, are strongly correlated with surface outcrop area. Extinction peaks conform to a random-walk model, but larger peaks occur at just two positions with respect to second-order stratigraphical sequences, towards the culmination of stacked transgressive system tracts and close to system bases, precisely the positions where taxonomic last occurrences are predicted to cluster under a random distribution model. Many of the taxonomic patterns that have been described from the fossil record conform to a species-area effect. Whether this arises primarily from sampling bias, or from changing surface area of marine shelf seas through time and its effect on biodiversity, remains problematic.     

The effects of taxonomic standardization on sampling-standardized estimates of historical diversity

Occurrence-based databases such as the Palaeobiology database (PBDB) provide means of accommodating the heterogeneities of the fossil record when evaluating historical diversity patterns. Although palaeontologists have given ample attention to the effects of taxonomic practice on diversity patterns derived from synoptic databases (those using first and last appearances of taxa), workers have not examined the effects of taxonomic error on occurrence-based diversity studies. Here, we contrast diversity patterns and diversity dynamics between raw data and taxonomically vetted data in the PBDB to evaluate the effects of taxonomic errors. We examine three groups: Palaeozoic gastropods, Jurassic bivalves and Cenozoic bivalves. We contrast genus-level diversity patterns based on: (i) all occurrences assigned to a genus (i.e. both species records and records identifying only the genus), (ii) only occurrences for which a species is identified, and (iii) only occurrences for which a species is identified, but after vetting the genus to which the species is assigned.Extensive generic reassignments elevate origination and extinction rates within Palaeozoic gastropods and origination rates within Cenozoic bivalves. However, vetting increases generic richness markedly only for Cenozoic bivalves, and even then the increase is less than 10%. Moreover, the patterns of standing generic richness are highly similar under all three data treatments. Unless our results are unusual, taxonomic standardization can elevate diversity dynamics in some cases, but it will not greatly change inferred richness over time.     

Systematics and palaeoecology of middle Toarcian Asteroidea (Echinodermata) from the “Seuil du Poitou”, Western France

Complete, articulated starfish fossils are rare. However, more frequently encountered dissociated skeletal elements (ossicles) permit reliable taxonomic identification, making them a valuable data source for diversity estimates. Nearly 300 asteroid ossicles, collected from the middle Toarcian marls in western France can be assigned to five species. Four species and two genera are described: Comptoniaster vrinensis nov. sp. (Goniasteridae), Poncetaster crateri nov. gen. nov. sp. (Stauranderasteridae), Galbaster recurrans nov. gen. nov. sp. (Goniasteridae) and Pentasteria? liasica nov. sp. (Astropectinidae). The known diversity of Early Jurassic asteroids is increased from 12 to 16 species. These taxa illustrate the diversification of crown-group asteroids early in the Jurassic, following the Permo-Triassic crisis. They also reflect bias of the fossil record, and imply the existence of numerous ghost lineages in the evolutionary trees of extant groups. Variation in asteroid diversity across the “Seuil du Poitou” was driven by ecological constraints. The relative frequency (abundance of ossicles and diversity) of goniasterids and stauranderasterids increases in shallower environments. The Benthopectinidae, represented by Plesiastropecten hallovensis, occurred primarily from deep-shelf sediments. Similar ecological patterns are observed for more recent fossil and extant relatives, which further supports the idea of conservative evolution in post-Palaeozoic starfishes since the Early Jurassic.     

Comparative experimental taphonomy of eight marine arthropods indicates distinct differences in preservation potential

Global biodiversity patterns in deep time can only be understood fully when the relative preservation potential of each clade is known. The relative preservation potential of marine arthropod clades, a diverse and ecologically important component of modern and past ecosystems, is poorly known. We tackled this issue by carrying out a 205‐day long comprehensive, comparative, taphonomic experiment in a laboratory by scoring up to ten taphonomic characters for multiple specimens of seven crustacean and one chelicerate species (two true crabs, one shrimp, one lobster, one hermit crab, one stomatopod, one barnacle and one horseshoe crab). Although the results are preliminary because we used a single experimental setup and algal growth partially hampered observations, some parts of hermit crabs, stomatopods, swimming crabs and barnacles decayed slowly relative to other parts, implying differential preservation potentials within species, largely consistent with the fossil record of these groups. An inferred parasitic isopod, manifested by a bopyriform swelling within a hermit crab carapace, decayed relatively fast. We found limited variation in the decay rate between conspecifics, and we did not observe size‐related trends in decay rate. Conversely, substantial differences in the decay rate between species were seen after c. 50 days, with shrimps and stomatopods decaying fastest, suggesting a relatively low preservation potential, whereas the lobster, calico crabs, horseshoe crabs and barnacles showed relatively slow decay rates, suggesting a higher preservation potential. These results are supported by two modern and fossil record‐based preservation potential metrics that are significantly correlated to decay rate ranks. Furthermore, we speculate that stemward slippage may not be ubiquitous in marine arthropods. Our results imply that diversity studies of true crabs, lobsters, horseshoe crabs and barnacles are more likely to yield patterns that are closer to their true biodiversity patterns than those for stomatopods, shrimps and hermit crabs.     

HOW DO GEOLOGICAL SAMPLING BIASES AFFECT STUDIES OF MORPHOLOGICAL EVOLUTION IN DEEP TIME? A CASE STUDY OF PTEROSAUR (REPTILIA: ARCHOSAURIA) DISPARITY

A fundamental contribution of paleobiology to macroevolutionary theory has been the illumination of deep time patterns of diversification. However, recent work has suggested that taxonomic diversity counts taken from the fossil record may be strongly biased by uneven spatiotemporal sampling. Although morphological diversity (disparity) is also frequently used to examine evolutionary radiations, no empirical work has yet addressed how disparity might be affected by uneven fossil record sampling. Here, we use pterosaurs (Mesozoic flying reptiles) as an exemplar group to address this problem. We calculate multiple disparity metrics based upon a comprehensive anatomical dataset including a novel phylogenetic correction for missing data, statistically compare these metrics to four geological sampling proxies, and use multiple regression modeling to assess the importance of uneven sampling and exceptional fossil deposits (Lagerstätten). We find that range‐based disparity metrics are strongly affected by uneven fossil record sampling, and should therefore be interpreted cautiously. The robustness of variance‐based metrics to sample size and geological sampling suggests that they can be more confidently interpreted as reflecting true biological signals. In addition, our results highlight the problem of high levels of missing data for disparity analyses, indicating a pressing need for more theoretical and empirical work.     

Evolution of olfaction in non-avian theropod dinosaurs and birds

Little is known about the olfactory capabilities of extinct basal (non-neornithine) birds or the evolutionary changes in olfaction that occurred from non-avian theropods through modern birds. Although modern birds are known to have diverse olfactory capabilities, olfaction is generally considered to have declined during avian evolution as visual and vestibular sensory enhancements occurred in association with flight. To test the hypothesis that olfaction diminished through avian evolution, we assessed relative olfactory bulb size, here used as a neuroanatomical proxy for olfactory capabilities, in 157 species of non-avian theropods, fossil birds and living birds. We show that relative olfactory bulb size increased during non-avian maniraptoriform evolution, remained stable across the non-avian theropod/bird transition, and increased during basal bird and early neornithine evolution. From early neornithines through a major part of neornithine evolution, the relative size of the olfactory bulbs remained stable before decreasing in derived neoavian clades. Our results show that, rather than decreasing, the importance of olfaction actually increased during early bird evolution, representing a previously unrecognized sensory enhancement. The relatively larger olfactory bulbs of earliest neornithines, compared with those of basal birds, may have endowed neornithines with improved olfaction for more effective foraging or navigation skills, which in turn may have been a factor allowing them to survive the end-Cretaceous mass extinction.     

Fossilized embryos are widespread but the record is temporally and taxonomically biased

We report new discoveries of embryos and egg capsules from the Lower Cambrian of Siberia, Middle Cambrian of Australia and Lower Ordovician of North America. Together with existing records, embryos have now been recorded from four of the seven continents. However, the new discoveries highlight secular and systematic biases in the fossil record of embryonic stages. The temporal window within which the embryos and egg capsules are found is of relatively short duration; it ends in the Early Ordovician and is roughly coincident with that of typical "Orsten"-type faunas. The reduced occurrence of such fossils has been attributed to reducing levels of phosphate in marine waters during the early Paleozoic, but may also be owing to the increasing depth of sediment mixing by infaunal metazoans. Furthermore, most records younger than the earliest Cambrian are of a single kind-large eggs and embryos of the priapulid-like scalidophoran Markuelia. We explore alternative explanations for the low taxonomic diversity of embryos recovered thus far, including sampling, size, anatomy, ecology, and environment, concluding that the preponderance of Markuelia embryos is due to its precocious development of cuticle at an embryonic stage, predisposing it to preservation through action as a substrate on which microbially mediated precipitation of authigenic calcium phosphate may occur. The fossil record of embryos may be limited to a late Neoproterozoic to early Ordovician snapshot that is subject to dramatic systematic bias. Together, these biases must be considered seriously in attempts to use the fossil record to arbitrate between hypotheses of developmental and life history evolution implicated in the origin of metazoan clades.     

Early tetrapodomorph biogeography: Controlling for fossil record bias in macroevolutionary analyses

The fossil record provides direct empirical data for understanding macroevolutionary patterns and processes. Inherent biases in the fossil record are well known to confound analyses of this data. Sampling bias proxies have been used as covariates in regression models to test for such biases. Proxies, such as formation count, are associated with paleobiodiversity, but are insufficient for explaining species dispersal owing to a lack of geographic context. Here, we develop a sampling bias proxy that incorporates geographic information and test it with a case study on early tetrapodomorph biogeography. We use recently-developed Bayesian phylogeographic models and a new supertree of early tetrapodomorphs to estimate dispersal rates and ancestral habitat locations. We find strong evidence that geographic sampling bias explains supposed radiations in dispersal rate (potential adaptive radiations). Our study highlights the necessity of accounting for geographic sampling bias in macroevolutionary and phylogenetic analyses and provides an approach to test for its effect.