Fossil biomolecules reveal an avian metabolism in the ancestral dinosaur.

Birds and mammals independently evolved the highest metabolic rates among living animals1. Their metabolism generates heat that enables active thermoregulation1, shaping the ecological niches they can occupy and their adaptability to environmental change2. The metabolic performance of birds, which exceeds that of mammals, is thought to have evolved along their stem lineage3-10. However, there is no proxy that enables the direct reconstruction of metabolic rates from fossils. Here we use in situ Raman and Fourier-transform infrared spectroscopy to quantify the in vivo accumulation of metabolic lipoxidation signals in modern and fossil amniote bones. We observe no correlation between atmospheric oxygen concentrations11 and metabolic rates. Inferred ancestral states reveal that the metabolic rates consistent with endothermy evolved independently in mammals and plesiosaurs, and are ancestral to ornithodirans, with increasing rates along the avian lineage. High metabolic rates were acquired in pterosaurs, ornithischians, sauropods and theropods well before the advent of energetically costly adaptations, such as flight in birds. Although they had higher metabolic rates ancestrally, ornithischians reduced their metabolic abilities towards ectothermy. The physiological activities of such ectotherms were dependent on environmental and behavioural thermoregulation12, in contrast to the active lifestyles of endotherms1. Giant sauropods and theropods were not gigantothermic9,10, but true endotherms. Endothermy in many Late Cretaceous taxa, in addition to crown mammals and birds, suggests that attributes other than metabolism determined their fate during the terminal Cretaceous mass extinction.

Pliocene decoupling of equatorial Pacific temperature and pH gradients.

Ocean dynamics in the equatorial Pacific drive tropical climate patterns that affect marine and terrestrial ecosystems worldwide. How this region will respond to global warming has profound implications for global climate, economic stability and ecosystem health. As a result, numerous studies have investigated equatorial Pacific dynamics during the Pliocene (5.3-2.6 million years ago) and late Miocene (around 6 million years ago) as an analogue for the future behaviour of the region under global warming1-12. Palaeoceanographic records from this time present an apparent paradox with proxy evidence of a reduced east-west sea surface temperature gradient along the equatorial Pacific1,3,7,8-indicative of reduced wind-driven upwelling-conflicting with evidence of enhanced biological productivity in the east Pacific13-15 that typically results from stronger upwelling. Here we reconcile these observations by providing new evidence for a radically different-from-modern circulation regime in the early Pliocene/late Miocene16 that results in older, more acidic and more nutrient-rich water reaching the equatorial Pacific. These results provide a mechanism for enhanced productivity in the early Pliocene/late Miocene east Pacific even in the presence of weaker wind-driven upwelling. Our findings shed new light on equatorial Pacific dynamics and help to constrain the potential changes they will undergo in the near future, given that the Earth is expected to reach Pliocene-like levels of warming in the next century.

Sensitivity of ocean circulation to warming during the Early Eocene greenhouse.

Multiple abrupt warming events ("hyperthermals") punctuated the Early Eocene and were associated with deep-sea temperature increases of 2 to 4 °C, seafloor carbonate dissolution, and negative carbon isotope (δ13C) excursions. Whether hyperthermals were associated with changes in the global ocean overturning circulation is important for understanding their driving mechanisms and feedbacks and for gaining insight into the circulation's sensitivity to climatic warming. Here, we present high-resolution benthic foraminiferal stable isotope records (δ13C and δ18O) throughout the Early Eocene Climate Optimum (~53.26 to 49.14 Ma) from the deep equatorial and North Atlantic. Combined with existing records from the South Atlantic and Pacific, these indicate consistently amplified δ13C excursion sizes during hyperthermals in the deep equatorial Atlantic. We compare these observations with results from an intermediate complexity Earth system model to demonstrate that this spatial pattern of δ13C excursion size is a predictable consequence of global warming-induced changes in ocean overturning circulation. In our model, transient warming drives the weakening of Southern Ocean-sourced overturning circulation, strengthens Atlantic meridional water mass aging gradients, and amplifies the magnitude of negative δ13C excursions in the equatorial to North Atlantic. Based on model-data consistency, we conclude that Eocene hyperthermals coincided with repeated weakening of the global overturning circulation. Not accounting for ocean circulation impacts on δ13C excursions will lead to incorrect estimates of the magnitude of carbon release driving hyperthermals. Our finding of weakening overturning in response to past transient climatic warming is consistent with predictions of declining Atlantic Ocean overturning strength in our warm future.

The latitudinal temperature gradient and its climate dependence as inferred from foraminiferal δ18O over the past 95 million years.

SignificanceThe temperature difference between low and high latitudes is one measure of the efficiency of the global climate system in redistributing heat and is used to test the ability of models to represent the climate system through time. Here, we show that the latitudinal temperature gradient has exhibited a consistent inverse relationship with global mean sea-surface temperature for at least the past 95 million years. Our results help reduce conflicts between climate models and empirical estimates of temperature and argue for a fundamental consistency in the dynamics of heat transport and radiative transfer across vastly different background states.

Revisiting the sedimentary record of the rise of diatoms.

Diatoms are a major primary producer in the modern oceans and play a critical role in the marine silica cycle. Their rise to dominance is recognized as one of the largest shifts in Cenozoic marine ecosystems, but the timing of this transition is debated. Here, we use a diagenetic model to examine the effect of sedimentation rate and temperature on the burial efficiency of biogenic silica over the past 66 million years (i.e., the Cenozoic). We find that the changing preservation potential of siliceous microfossils during that time would have overprinted the primary signal of diatom and radiolarian abundance. We generate a taphonomic null hypothesis of the diatom fossil record by assuming a constant flux of diatoms to the sea floor and having diagenetic conditions driven by observed shifts in temperature and sedimentation rate. This null hypothesis produces a late Cenozoic (∼5 Ma to 20 Ma) increase in the relative abundance of fossilized diatoms that is comparable to current empirical records. This suggests that the observed increase in diatom abundance in the sedimentary record may be driven by changing preservation potential. A late Cenozoic rise in diatoms has been causally tied to the rise of grasslands and baleen whales and to declining atmospheric CO2 levels. Here we suggest that the similarity among these records primarily arises from a common driver-the cooling climate system-that drove enhanced diatom preservation as well as the rise of grasslands and whales, rather than a causal link among them.

The enigma of Oligocene climate and global surface temperature evolution.

Falling atmospheric CO2 levels led to cooling through the Eocene and the expansion of Antarctic ice sheets close to their modern size near the beginning of the Oligocene, a period of poorly documented climate. Here, we present a record of climate evolution across the entire Oligocene (33.9 to 23.0 Ma) based on TEX86 sea surface temperature (SST) estimates from southwestern Atlantic Deep Sea Drilling Project Site 516 (paleolatitude ∼36°S) and western equatorial Atlantic Ocean Drilling Project Site 929 (paleolatitude ∼0°), combined with a compilation of existing SST records and climate modeling. In this relatively low CO2 Oligocene world (∼300 to 700 ppm), warm climates similar to those of the late Eocene continued with only brief interruptions, while the Antarctic ice sheet waxed and waned. SSTs are spatially heterogenous, but generally support late Oligocene warming coincident with declining atmospheric CO2 This Oligocene warmth, especially at high latitudes, belies a simple relationship between climate and atmospheric CO2 and/or ocean gateways, and is only partially explained by current climate models. Although the dominant climate drivers of this enigmatic Oligocene world remain unclear, our results help fill a gap in understanding past Cenozoic climates and the way long-term climate sensitivity responded to varying background climate states.

Rapid ocean acidification and protracted Earth system recovery followed the end-Cretaceous Chicxulub impact.

Mass extinction at the Cretaceous-Paleogene (K-Pg) boundary coincides with the Chicxulub bolide impact and also falls within the broader time frame of Deccan trap emplacement. Critically, though, empirical evidence as to how either of these factors could have driven observed extinction patterns and carbon cycle perturbations is still lacking. Here, using boron isotopes in foraminifera, we document a geologically rapid surface-ocean pH drop following the Chicxulub impact, supporting impact-induced ocean acidification as a mechanism for ecological collapse in the marine realm. Subsequently, surface water pH rebounded sharply with the extinction of marine calcifiers and the associated imbalance in the global carbon cycle. Our reconstructed water-column pH gradients, combined with Earth system modeling, indicate that a partial ∼50% reduction in global marine primary productivity is sufficient to explain observed marine carbon isotope patterns at the K-Pg, due to the underlying action of the solubility pump. While primary productivity recovered within a few tens of thousands of years, inefficiency in carbon export to the deep sea lasted much longer. This phased recovery scenario reconciles competing hypotheses previously put forward to explain the K-Pg carbon isotope records, and explains both spatially variable patterns of change in marine productivity across the event and a lack of extinction at the deep sea floor. In sum, we provide insights into the drivers of the last mass extinction, the recovery of marine carbon cycling in a postextinction world, and the way in which marine life imprints its isotopic signal onto the geological record.

Towards quantifying the mass extinction debt of the Anthropocene.

To make sense of our present biodiversity crises, the modern rate of species extinctions is commonly compared to a benchmark, or 'background,' rate derived from the fossil record. These estimates are critical for bounding the scale of modern diversity loss, but are yet to fully account for the fundamental structure of extinction rates through time. Namely, a substantial fraction of extinctions within the fossil record occurs within relatively short-lived extinction pulses, and not during intervals characterized by background rates of extinction. Accordingly, it is more appropriate to compare the modern event to these pulses than to the long-term average rate. Unfortunately, neither the duration of extinction pulses in the geological record nor the ultimate magnitude of the extinction pulse today is resolved, making assessments of their relative sizes difficult. In addition, the common metric used to compare current and past extinction rates does not correct for large differences in observation duration. Here, we propose a new predictive metric that may be used to ascertain the ultimate extent of the ongoing extinction threat, building on the observation that extinction magnitude in the marine fossil record is correlated to the magnitude of sedimentary turnover. Thus, we propose that the ultimate number of species destined for extinction today can be predicted by way of a quantitative appraisal of humanity's modification of ecosystems as recorded in sediments-that is, by comparing our future rock record with that of the past. The ubiquity of habitat disruption worldwide suggests that a profound mass extinction debt exists today, but one that might yet be averted by preserving and restoring ecosystems and their geological traces.

Rarity in mass extinctions and the future of ecosystems.

The fossil record provides striking case studies of biodiversity loss and global ecosystem upheaval. Because of this, many studies have sought to assess the magnitude of the current biodiversity crisis relative to past crises-a task greatly complicated by the need to extrapolate extinction rates. Here we challenge this approach by showing that the rarity of previously abundant taxa may be more important than extinction in the cascade of events leading to global changes in the biosphere. Mass rarity may provide the most robust measure of our current biodiversity crisis relative to those past, and new insights into the dynamics of mass extinction.

Oxygen, temperature and the deep-marine stenothermal cradle of Ediacaran evolution.

Ediacaran fossils document the early evolution of complex megascopic life, contemporaneous with geochemical evidence for widespread marine anoxia. These data suggest early animals experienced frequent hypoxia. Research has thus focused on the concentration of molecular oxygen (O2) required by early animals, while also considering the impacts of climate. One model, the Cold Cradle hypothesis, proposed the Ediacaran biota originated in cold, shallow-water environments owing to increased O2 solubility. First, we demonstrate using principles of gas exchange that temperature does have a critical role in governing the bioavailability of O2-but in cooler water the supply of O2 is actually lower. Second, the fossil record suggests the Ediacara biota initially occur approximately 571 Ma in deep-water facies, before appearing in shelf environments approximately 555 Ma. We propose an ecophysiological underpinning for this pattern. By combining oceanographic data with new respirometry experiments we show that in the shallow mixed layer where seasonal temperatures fluctuate widely, thermal and partial pressure ( pO2) effects are highly synergistic. The result is that temperature change away from species-specific optima impairs tolerance to low pO2. We hypothesize that deep and particularly stenothermal (narrow temperature range) environments in the Ediacaran ocean were a physiological refuge from the synergistic effects of temperature and low pO2.

Parsing parallel evolution: ecological divergence and differential gene expression in the adaptive radiations of thick-lipped Midas cichlid fishes from Nicaragua.

The study of parallel evolution facilitates the discovery of common rules of diversification. Here, we examine the repeated evolution of thick lips in Midas cichlid fishes (the Amphilophus citrinellus species complex)-from two Great Lakes and two crater lakes in Nicaragua-to assess whether similar changes in ecology, phenotypic trophic traits and gene expression accompany parallel trait evolution. Using next-generation sequencing technology, we characterize transcriptome-wide differential gene expression in the lips of wild-caught sympatric thick- and thin-lipped cichlids from all four instances of repeated thick-lip evolution. Six genes (apolipoprotein D, myelin-associated glycoprotein precursor, four-and-a-half LIM domain protein 2, calpain-9, GTPase IMAP family member 8-like and one hypothetical protein) are significantly underexpressed in the thick-lipped morph across all four lakes. However, other aspects of lips' gene expression in sympatric morphs differ in a lake-specific pattern, including the magnitude of differentially expressed genes (97-510). Generally, fewer genes are differentially expressed among morphs in the younger crater lakes than in those from the older Great Lakes. Body shape, lower pharyngeal jaw size and shape, and stable isotopes (δ(13)C and δ(15)N) differ between all sympatric morphs, with the greatest differentiation in the Great Lake Nicaragua. Some ecological traits evolve in parallel (those related to foraging ecology; e.g. lip size, body and head shape) but others, somewhat surprisingly, do not (those related to diet and food processing; e.g. jaw size and shape, stable isotopes). Taken together, this case of parallelism among thick- and thin-lipped cichlids shows a mosaic pattern of parallel and nonparallel evolution.

Intermediate water circulation drives distribution of Pliocene Oxygen Minimum Zones.

Oxygen minimum zones (OMZs) play a critical role in global biogeochemical cycling and act as barriers to dispersal for marine organisms. OMZs are currently expanding and intensifying with climate change, however past distributions of OMZs are relatively unknown. Here we present evidence for widespread pelagic OMZs during the Pliocene (5.3-2.6 Ma), the most recent epoch with atmospheric CO2 analogous to modern (~400-450 ppm). The global distribution of OMZ-affiliated planktic foraminifer, Globorotaloides hexagonus, and Earth System and Species Distribution Models show that the Indian Ocean, Eastern Equatorial Pacific, eastern South Pacific, and eastern North Atlantic all supported OMZs in the Pliocene, as today. By contrast, low-oxygen waters were reduced in the North Pacific and expanded in the North Atlantic in the Pliocene. This spatially explicit perspective reveals that a warmer world can support both regionally expanded and contracted OMZs, with intermediate water circulation as a key driver.

North Atlantic surface ocean warming and salinization in response to middle Eocene greenhouse warming.

Quantitative reconstructions of hydrological change during ancient greenhouse warming events provide valuable insight into warmer-than-modern hydrological cycles but are limited by paleoclimate proxy uncertainties. We present sea surface temperature (SST) records and seawater oxygen isotope (δ18Osw) estimates for the Middle Eocene Climatic Optimum (MECO), using coupled carbonate clumped isotope (Δ47) and oxygen isotope (δ18Oc) data of well-preserved planktonic foraminifera from the North Atlantic Newfoundland Drifts. These indicate a transient ~3°C warming across the MECO, with absolute temperatures generally in accordance with trace element (Mg/Ca)-based SSTs but lower than biomarker-based SSTs for the same interval. We find a transient ~0.5‰ shift toward higher δ18Osw, which implies increased salinity in the North Atlantic subtropical gyre and potentially a poleward expansion of its northern boundary in response to greenhouse warming. These observations provide constraints on dynamic ocean response to warming events, which are consistent with theory and model simulations predicting an enhanced hydrological cycle under global warming.

Evidence for abrupt speciation in a classic case of gradual evolution.

In contrast with speciation in terrestrial organisms, marine plankton frequently display gradual morphological change without lineage division (e.g., phyletic gradualism or gradual evolution), which has raised the possibility that a different mode of evolution dominates within pelagic environments. Here, we reexamine a classic case of putative gradual evolution within the Globorotalia plesiotumida-G. tumida lineage of planktonic foraminifera, and find both compelling evidence for the existence of a third cryptic species during the speciation event and the abrupt evolution of the descendant G. tumida. The third morphotype, not recognized in previous analyses, differs in shape and coiling direction from its ancestor, G. plesiotumida. This species dominates the globorotaliid population for 414,000 years just before the appearance of G. tumida. The first population of the descendant, G. tumida, evolves abruptly within a 44,000-year interval. A combination of morphological data and biostratigraphic evidence suggests that G. tumida evolved by cladogenesis. Our findings provide an unexpected twist on one of the best-documented cases of within-lineage phyletic gradualism and, in doing so, revisit the limitations and promise of the study of speciation in the fossil record.

Photosymbiont associations persisted in planktic foraminifera during early Eocene hyperthermals at Shatsky Rise (Pacific Ocean).

Understanding the sensitivity of species-level responses to long-term warming will become increasingly important as we look towards a warmer future. Here, we examine photosymbiont associations in planktic foraminifera at Shatsky Rise (ODP Site 1209, Pacific Ocean) across periods of global warming of differing magnitude and duration. We compare published data from the Paleocene-Eocene Thermal Maximum (PETM; ~55.9 Ma) with data from the less intense Eocene Thermal Maximum 2 (ETM2; ~54.0 Ma), and H2 events (~53.9 Ma). We use a positive relationship between test size and carbon isotope value (size-δ13C) in foraminifera shells as a proxy for photosymbiosis in Morozovella subbotinae and Acarinina soldadoensis, and find no change in photosymbiont associations during the less intense warming events, in contrast with PETM records indicating a shift in symbiosis in A. soldadoensis (but not M. subbotinae). Declines in abundance and differing preservation potential of the asymbiotic species Subbotina roesnaesensis along with sediment mixing likely account for diminished differences in δ13C between symbiotic and asymbiotic species from the PETM and ETM2. We therefore conclude that photosymbiont associations were maintained in both A. soldadoensis and M. subbotinae across ETM2 and H2. Our findings support one or both of the hypotheses that 1) changing symbiotic associations in response to warming during the PETM allowed A. soldadoensis and perhaps other acarininids to thrive through subsequent hyperthermals or 2) some critical environmental threshold value was not reached in these less intense hyperthermals.

Paleozoic ammonoid ecomorphometrics test ecospace availability as a driver of morphological diversification.

The early burst model suggests that disparity rises rapidly to fill empty ecospace following clade origination or in the aftermath of a mass extinction. Early bursts are considered common features of fossil data, but neontological studies have struggled to identify them. Furthermore, tests have proven difficult because factors besides ecology can drive changes in morphology. Here, we document the ecomorphometric evolution of the extinct Ammonoidea at 1-million-year resolution, from their origination in the Early Devonian (Emsian) to the Early Triassic (Induan), over ~156 million years. This time interval encompasses six global extinction events, including two of the Big Five, and incorporates multiple ammonoid radiations. However, we find no evidence for early bursts of ecomorphological disparity. This contradicts arguments that the temporal scope, or traits measured in genomic data, conceal evidence of early bursts. Rather, early bursts may be less prevalent in fossil data than is often assumed.

The evolution of complex life and the stabilization of the Earth system.

The half-billion-year history of animal evolution is characterized by decreasing rates of background extinction. Earth's increasing habitability for animals could result from several processes: (i) a decrease in the intensity of interactions among species that lead to extinctions; (ii) a decrease in the prevalence or intensity of geological triggers such as flood basalt eruptions and bolide impacts; (iii) a decrease in the sensitivity of animals to environmental disturbance; or (iv) an increase in the strength of stabilizing feedbacks within the climate system and biogeochemical cycles. There is no evidence that the prevalence or intensity of interactions among species or geological extinction triggers have decreased over time. There is, however, evidence from palaeontology, geochemistry and comparative physiology that animals have become more resilient to an environmental change and that the evolution of complex life has, on the whole, strengthened stabilizing feedbacks in the climate system. The differential success of certain phyla and classes appears to result, at least in part, from the anatomical solutions to the evolution of macroscopic size that were arrived at largely during Ediacaran and Cambrian time. Larger-bodied animals, enabled by increased anatomical complexity, were increasingly able to mix the marine sediment and water columns, thus promoting stability in biogeochemical cycles. In addition, body plans that also facilitated ecological differentiation have tended to be associated with lower rates of extinction. In this sense, Cambrian solutions to Cambrian problems have had a lasting impact on the trajectory of complex life and, in turn, fundamental properties of the Earth system.

Extensive morphological variability in asexually produced planktic foraminifera.

Marine protists are integral to the structure and function of pelagic ecosystems and marine carbon cycling, with rhizarian biomass alone accounting for more than half of all mesozooplankton in the oligotrophic oceans. Yet, understanding how their environment shapes diversity within species and across taxa is limited by a paucity of observations of heritability and life history. Here, we present observations of asexual reproduction, morphologic plasticity, and ontogeny in the planktic foraminifer Neogloboquadrina pachyderma in laboratory culture. Our results demonstrate that planktic foraminifera reproduce both sexually and asexually and demonstrate extensive phenotypic plasticity in response to nonheritable factors. These two processes fundamentally explain the rapid spatial and temporal response of even imperceptibly low populations of planktic foraminifera to optimal conditions and the diversity and ubiquity of these species across the range of environmental conditions that occur in the ocean.

Eggshell geochemistry reveals ancestral metabolic thermoregulation in Dinosauria.

Studying the origin of avian thermoregulation is complicated by a lack of reliable methods for measuring body temperatures in extinct dinosaurs. Evidence from bone histology and stableisotopes often relies on uncertain assumptions about the relationship between growth rate and body temperature, or the isotopic composition (δ18O) of body water. Clumped isotope (Δ47) paleothermometry, based on binding of 13C to 18O, provides a more robust tool, but has yet to be applied across a broad phylogenetic range of dinosaurs while accounting for paleoenvironmental conditions. Applying this method to well-preserved fossil eggshells demonstrates that the three major clades of dinosaurs, Ornithischia, Sauropodomorpha, and Theropoda, were characterized by warm body temperatures. Dwarf titanosaurs may have exhibited similar body temperatures to larger sauropods, although this conclusion isprovisional, given current uncertainties in taxonomic assignment of dwarf titanosaur eggshell. Our results nevertheless reveal that metabolically controlled thermoregulation was the ancestral condition for Dinosauria.