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Evolutionary history studies depend on having reliable chronologies of macroevolutionary processes. Construction of such chronologies often yields discrepancies between paleontological and molecular dates, which are sometimes viewed as conflicting. Nevertheless, each macroevolutionary process is composed of two main phases: emergence of a trait or clade and success of that trait or clade, which differ in mechanisms, drivers, and types of evidence. Moreover, emergence may be observed as gene divergence (which may be trait-coding or trait-unrelated genes), trait emergence, and clade emergence; whereas success can be observed as increase in abundance, diffusion, and/or diversity or as overall persistence over geologic time. Therefore, to fully and correctly understand any macroevolutionary process, it is of paramount importance to understand what event each date refers to, and how dates of various events and their integration reveal the complexity of macroevolutionary processes. I demonstrate this through three examples: the chronological gap between oxygenic photosynthesis emergence and the Great Oxidation Event, the chronological gap between paleontological and molecular dates of angiosperm emergence, and the evolution of plant silicon accumulation.
Toothed cetacean (Odontoceti) lineages in the Miocene and Pliocene evolved rostra that are proportionally more elongate than any other aquatic mammal or reptile, living or extinct. Their similarities in cranial proportions to billfish may suggest a convergent feeding style, where the rostrum is swept through the water to hit and stun prey. Here we calculated second moment of area from rostral cross sections of these fossil odontocete taxa, as well as from extant ecological analogues, to infer variation in feeding behavior. Our results show that the extremely long rostra of extinct toothed whales vary considerably in functionally relevant measures of shape and likely exhibited a diversity of feeding behaviors, ranging from those similar to modern odontocetes to those convergent with billfish. Eustatic sea-level and temperature maxima of the Miocene likely led to changes in prey characteristics or abundance that enabled the repeated evolution of this extreme morphotype, which later went extinct during late Pliocene climatic deterioration.
The time separating the first appearances of species from their divergences from related taxa affects assessments of macroevolutionary hypotheses about rates of anatomical or ecological change. Branch durations necessarily posit stratigraphic gaps in sampling within a clade over which we have failed to sample predecessors (ancestors) and over which there are no divergences leading to sampled relatives (sister taxa). The former reflects only sampling rates, whereas the latter reflects sampling, origination, and extinction rates. Because all three rates vary over time, the probability of a branch duration of any particular length will differ depending on when in the Phanerozoic that branch duration spans. Here, I present a birth–death-sampling model allowing interval-to-interval variation in diversification and sampling rates. Increasing either origination or sampling rates increases the probability of finding sister taxa that diverge both during and before intervals of high sampling/origination. Conversely, elevated extinction reduces the probability of divergences from sampled sister taxa before and during intervals of elevated extinction. In the case of total extinction, a Signor-Lipps will reduce expected sister taxa leading up to the extinction, with the possible effect stretching back many millions of years when sampling is low. Simulations indicate that this approach provides reasonable estimates of branch duration probabilities under a variety of circumstances. Because current probability models for describing morphological evolution are less advanced than methods for inferring diversification and sampling rates, branch duration priors allowing for time-varying diversification could be a potent tool for phylogenetic inference with fossil data.
Nonmammalian cynodonts represent a speciose and ecologically diverse group with a fossil record stretching from the late Permian until the Cretaceous. Because of their role as major components of Triassic terrestrial ecosystems and as the direct ancestors of mammals, cynodonts are an important group for understanding Mesozoic tetrapod diversity. We examine patterns of nonmammalian cynodont species richness and the quality of their fossil record. A supertree of cynodonts is constructed from recently published trees and time calibrated using a Bayesian approach. While this approach pushes the root of Cynodontia back to the earliest Guadalupian, the origins of Cynognathia and Probainognathia are close to their first appearance in the fossil record. Taxic, subsampled, and phylogenetic diversity estimates support a major cynodont radiation following the end-Permian mass extinction, but conflicting signals are observed at the end of the Triassic. The taxic diversity estimate shows high diversity in the Rhaetian and a drop across the Triassic/Jurassic boundary, while the phylogenetic diversity indicates an earlier extinction between the Norian and Rhaetian. The difference is attributed to the prevalence of taxa based solely on teeth in the Rhaetian, which are not included in the phylogenetic diversity estimate. Examining the completeness of cynodont specimens through geological time does not support a decrease in preservation potential; although the median completeness score decreases in the Late Triassic, the range of values remains consistent. Instead, the poor completeness scores are attributed to a shift in sampling and taxonomic practices: an increased prevalence in microvertebrate sampling and the naming of fragmentary material.
Geologically rapid climate change is anticipated to increase extinction risk nonuniformly across the Earth's surface. Tropical species may be more vulnerable than temperate species to current climate warming because of high tropical climate velocities and reduced seawater oxygen levels. To test whether rapid warming indeed preferentially increased the extinction risk of tropical fossil taxa, we combine a robust statistical assessment of latitudinal extinction selectivity (LES) with the dominant views on climate change occurring at ancient extinction crises. Using a global data set of marine fossil occurrences, we assess extinction rates for tropical and temperate genera, applying log ratios to assess effect size and Akaike weights for model support. Among the classical “big five” mass extinction episodes, the end-Permian mass extinction exhibits temperate preference of extinctions, whereas the Late Devonian and end-Triassic selectively hit tropical genera. Simple links between the inferred direction of climate change and LES are idiosyncratic, both during crisis and background intervals. More complex models, including sampling patterns and changes in the latitudinal distribution of continental shelf area, show tropical LES to be generally associated with raised tropical heat and temperate LES with global cold temperatures. With implications for the future, our paper demonstrates the consistency of high tropical temperatures, habitat loss, and the capacity of both to interact in generating geographic patterns in extinctions.
Deep-sea benthic ostracod assemblages covering the last 2 Myr were investigated in Integrated Ocean Drilling Program Site U1426 (at 903 m water depth) in the southern Sea of Japan. Results show that (1) orbital-scale faunal variability has been influenced by eustatic sea-level fluctuations and oxygen variability and (2) secular-scale faunal transitions are likely associated with the mid-Brunhes event (MBE, ∼0.43 Ma) and the onset of the Tsushima Warm Current (TWC, ∼1.7 Ma). Krithe, Robertsonites, and Acanthocythereis are the three most abundant genera throughout the core, accounting for 78.5% of total specimens. Multiple-regression tree analysis indicated that the TWC, the MBE, and oxygen content are the significant controlling factors of ostracod dominance. Changes in assemblages exhibit decline and recovery patterns corresponding to orbital-scale cyclicity of sea-level changes. In the Sea of Japan marginal ocean setting, this cyclicity shows a close relationship with bottom-water oxygen variability since the onset of the TWC influx. The MBE amplified the influence of the TWC and oxygen variability to the deep-sea ecosystem through larger sea-level fluctuations. Acanthocythereis dunelmensis, a circumpolar species, dominates before the TWC onset. After the TWC onset and during the mid-Pleistocene transition (MPT, ∼1.2–0.7 Ma) Krithe spp., known for their low-oxygen tolerance, substantially increase under moderate oxygen depletion. At the end of the MPT, Krithe dominance diminishes and is replaced by Robertsonites hanaii and Propontocypris spp. after the MBE. The post-MBE assemblage, characterized by R. hanaii, suggests a slightly warmer environment under the development of the TWC. In addition, the post-MBE high-amplitude climate system may have caused the increased abundance of active-swimming Propontocypris spp. due to their superior migration ability. Benthic ecosystems in marginal seas are sensitive and vulnerable to both short- and long-term climatic changes, and the MBE is suggested to be a global biotic event affecting benthic ecosystems substantially.
Deriving ecological and evolutionary descriptions of, and implications from, faunal assemblage patterns is commonly addressed by observation and a variety of exploratory techniques (scaling and clustering), along with qualitative evaluations of species occurrences and relative abundances. We argue that interpretations of faunal patterns, especially those documented by the fossil record, should be based upon the composition and structure of entire communities to provide strong conclusions and replicable results.
As an example, we use benthic foraminiferal data at high resolution (1–2 cm, corresponding to 300–1400 yr) over a section corresponding to about 20 kyr across the beginning of the Paleocene–Eocene thermal maximum (PETM). The PETM was an episode of rapid global warming about 55.5 Ma, associated with ocean acidification and lowered open oceanic productivity and deoxygenation and marked by severe turnover in benthic foraminiferal assemblages. Here we provide a stand-alone approach applicable to any dynamic faunal system, perturbation detection analysis (PDA), to recognize and identify community disruption evidenced as either positive growth or negative decline, and we use this methodical approach to obtain new information on foraminiferal communities before, during, and after the initiation of the PETM.
We conclude that the late Paleocene benthic foraminiferal community (FCOM1) was in a growth stage of positive increasing diversity, suggestive of favorable environmental conditions. This stage continued through the initial changes at the onset of the PETM, when disruption through environmental stress led to this community's termination. A second community (FCOM2) formed with declining diversity and high variability, showing a lack of adaptation to changing conditions. Knowledge of total assemblage status under both adverse and advantageous conditions is necessary, but not recognized by methods that rely upon analysis of single samples only: individual samples cannot be used to recognize disruptive changes in a community's structure, but these are easily identified using PDA.
Accurately recognizing analogues between fossil and modern ecosystems allows paleoecologists to more fully interpret fossil assemblages and modern ecologists to leverage the fossil record to address long-term ecological and environmental changes. However, this becomes increasingly difficult as taxonomic turnover increases the dissimilarity between ecosystems. Here we use a guild-based approach to compare the ecological similarity of Cretaceous cold-seep assemblages preserved in the Pierre Shale surrounding the Black Hills and modern cold-seep assemblages from five previously recognized biofacies. We modify modern assemblage data to include only those taxa with fossilizable hard parts greater than 5 mm in length to make these modern data sets more comparable to potential fossil analogues. We find that while the Black Hills assemblages are more similar in ecological guild composition to the modern thyasirid biofacies, subsets share similarities in ecological structure to the lucinid and mussel-bed biofacies. The fossil seep assemblages are also more similar to one another than are modern assemblages belonging to the same biofacies, despite greater geographic and temporal dissimilarity among the fossil samples. Furthermore, guild-level ordination analyses show a secondary faunal gradient that reflects community succession in the hard substrate–dominated modern assemblages and reveals a parallel faunal gradient in the soft sediment–dominated Cretaceous assemblages, consistent with a gradient in the influence of seep fluids on the faunas. Thus, while the Black Hills assemblages are quite homogeneous in their composition, they capture ecological variation similar to successional patterns in modern seep systems.
Vertebrate microfossil assemblages in a stratigraphic sequence often yield similar assortments of taxa but at different relative abundances, potentially indicative of marginal paleocommunity changes driven by paleoenvironmental change over time. For example, stratigraphically younger assemblages in the Dinosaur Park Formation (DPF) yield proportionally more aquatic taxa, consistent with marine transgression. However, individual deposits may have received specimens from multiple source paleocommunities over time, limiting our ability to confidently identify ecologically significant, paleocommunity differences through direct assemblage comparisons. We adapted a three-source, two-tracer Bayesian mixing model to quantify proportional contributions from different source habitats to DPF microfossil assemblages. Prior information about the compositions of separate, relatively unmixed terrestrial, freshwater, and marine assemblages from the Belly River Group allowed us to define expected taxon percent abundances for the end-member habitats likely contributing specimens to the mixed deposits. We compared the mixed assemblage and end-member distributions using 21 different combinations of vertebrate taxa. Chondrichthyan, dinosaur, and amphibian occurrence patterns ultimately allowed us to parse the contributions from the potential sources to 14 of the 15 mixed assemblages. The results confirmed a significant decline in terrestrial contributions at younger DPF sites, driven primarily by increased freshwater specimen inputs—not incursions from the adjacent marine paleocommunity. A rising base level likely increased lateral channel migration and the prevalence of freshwater habitats on the landscape, factors that contributed to increased paleocommunity mixing at younger channel deposit sites. Bayesian methods can account for source-mixing bias, which may be common in assemblages associated with major paleoenvironmental changes.
Biologic asymmetry is present in all bilaterally symmetric organisms as a result of normal developmental instability. However, fossilized organisms, which have undergone distortion due to burial, may have additional asymmetry as a result of taphonomic processes. To investigate this issue, we evaluated the magnitude of shape variation resulting from taphonomy on vertebrate bone using a novel application of fluctuating asymmetry. We quantified the amount of total variance attributed to asymmetry in a taphonomically distorted fossil taxon and compared it with that of three extant taxa. The fossil taxon had an average of 27% higher asymmetry than the extant taxa. In spite of the high amount of taphonomic input, the major axes of shape variation were not greatly altered by removal of the asymmetric component of shape variation. This presents the possibility that either underlying biologic trends drive the principal directions of shape change irrespective of asymmetric taphonomic distortion or that the symmetric taphonomic component is large enough that removing only the asymmetric component is inadequate to restore fossil shape. Our study is the first to present quantitative data on the relative magnitude of taphonomic shape change and presents a new method to further explore how taphonomic processes impact our interpretation of the fossil record.
Large herbivores can act as keystone species that strongly influence their communities. During the Pliocene and Pleistocene, Australia was dominated by a number of large to gigantic marsupial herbivore taxa. Many of these have been understudied quantitatively with regard to their ecology; and identifying the diet of these species will improve our understanding of not only their ecologies, but also of past environments. Recent research has found that cranial morphology among kangaroos and wallabies corresponds with foraging behaviors and mechanical properties of preferred plant tissues. Here we apply shape analysis and computational biomechanics to test the hypothesis: that feeding ecology is associated with craniofacial morphology across a taxonomically broad sample of diprotodont herbivores. Based on our results we predict the diet of an extinct short-faced kangaroo, Simosthenurus occidentalis. We find that biting behaviors are reflected in craniofacial morphology, but that these are more a reflection of the hardest bites required for their lifestyle, rather than diet composition alone. A combination of a very short face, robust musculoskeletal features, and dental arrangements predict that S. occidentalis was a browser, capable of consuming particularly resistant, bulky plant matter. These features were largely conserved among other short-faced kangaroos and may have offset the unpredictable availability of quality forage during the climatically variable Pleistocene epoch, contributing to their prolific diversification during this time.
This paper aims at assessing the influence of the bone ornamentation and, specifically, the associated loss of bone mass on the mechanical response of the crocodylomorph osteoderms. To this end, we have performed three-dimensional (3D) modeling and a finite element analysis on a sample that includes both extant dry bones and well-preserved fossils tracing back to the Late Triassic. We simulated an external attack under various angles on the apical surface of each osteoderm and further repeated the simulation on an equivalent set of smoothed 3D-modeled osteoderms. The comparative results indicated that the presence of an apical sculpture has no significant influence on the von Mises stress distribution in the osteoderm volume, although it produces a slight increase in its numerical score. Moreover, performing parametric analyses, we showed that the Young's modulus of the osteoderm, which may vary depending on the bone porosity, the collagen fiber orientation, or the calcification density, has no impact on the von Mises stress distribution inside the osteoderm volume. As the crocodylomorph bone ornamentation is continuously remodeled by pit resorption and secondary bone deposition, we assume that the apical sculpture may be the outcome of a trade-off between the bone mechanical resistance and the involvement in physiological functions. These physiological functions are indeed based on the setup of a bone superficial vessel network and/or the recurrent release of mineral elements into the plasma: heat transfers during basking and respiratory acidosis buffering during prolonged apnea in neosuchians and teleosaurids; compensatory homeostasis in response to general calcium deficiencies. On a general morphological basis, the osteoderm geometric variability within our sample leads us to assess that the global osteoderm geometry (whether square or rectangular) does not influence the von Mises stress, whereas the presence of a dorsal keel would somewhat reduce the stress along the vertical axis.
Constraint is a universal feature of morphological evolution. The vertebral column of synapsids (mammals and their close relatives) is a classic example of this phenotypic restriction, with greatly reduced variation in the number of vertebrae compared with the sauropsid lineage. Synapsids generally possess only three sacral vertebrae, which articulate with the ilium and play a key role in locomotion. Dicynodont anomodonts are the exception to this rule, possessing seven or more sacral vertebrae while reaching a range of body sizes rivaled among synapsids only by therian mammals. Here we explore the evolution of this unusual sacral morphology in dicynodonts by (1) hypothesizing homologies of the additional sacral vertebrae, (2) using ancestral state reconstruction and phylogenetic regressions (e.g., logistic regression, Poisson regression) to track the coevolution of sacral count and body size, and (3) proposing mechanisms by which additional sacral vertebrae were incorporated during dicynodont evolution. We find that sacral vertebral morphology covaries with sacral count in consistent ways across dicynodonts, implying that sacra with a given number of vertebrae are composed of homologous elements. There is a correlation between increased sacral count and larger body size, especially at the shift from four to five sacrals near the origin of Bidentalia. Based on position, morphology, and the consistent number of presacral vertebrae among dicynodonts, we hypothesize that the additional sacrals anterior to the plesiomorphic three are duplications of the first sacral, and that a single caudosacral was incorporated by a shift in the identity of the anteriormost caudal vertebra. Although changes in sacral count appear to be correlated with shifts in body size in dicynodonts, the evolution of general morphological conservativism in the synapsid sacrum remains to be further explored.
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