Selection by differential survival among marine animals in the Phanerozoic.

The Gaia hypothesis posits that the Earth and its biosphere function as a single self-stabilizing system, but a key challenge is explaining how this could have arisen through Darwinian evolution. One theory is that of "selection by differential survival," in which a clade's extinction probability decreases with age as it accumulates adaptations resisting environmental disturbances. While this is hard to assess during early Earth history, we can assess whether this process operated among marine animal genera throughout the Phanerozoic. To that end, we analyzed time ranges of 36,117 extinct animal genera using fossil occurrence data from the Paleobiology Database in order to calculate marine metazoan extinction age selectivity, extinction rates, and speciation rates over the Phanerozoic. We identify four signatures of selection by differential survival: lower extinction rates among older lineages, heritability and taxonomically nested propagation of extinction resistance, reduced age selectivity during rare environmental perturbations, and differential extinction rather than speciation as the primary driver of the phenomenon. Evidence for this process at lower taxonomic levels also implies its possibility for life as a whole - indeed, the possibility of Gaia.

Asteroid break-ups and meteorite delivery to Earth the past 500 million years.

The meteoritic material falling on Earth is believed to derive from large break-up or cratering events in the asteroid belt. The flux of extraterrestrial material would then vary in accordance with the timing of such asteroid family-forming events. In order to validate this, we investigated marine sediments representing 15 time-windows in the Phanerozoic for content of micrometeoritic relict chrome-spinel grains (>32 µm). We compare these data with the timing of the 15 largest break-up events involving chrome-spinel-bearing asteroids (S- and V-types). Unexpectedly, our Phanerozoic time windows show a stable flux dominated by ordinary chondrites similar to today's flux. Only in the mid-Ordovician, in connection with the break-up of the L-chondrite parent body, do we observe an anomalous micrometeorite regime with a two to three orders-of-magnitude increase in the flux of L-chondritic chrome-spinel grains to Earth. This corresponds to a one order-of-magnitude excess in the number of impact craters in the mid-Ordovician following the L-chondrite break-up, the only resolvable peak in Phanerozoic cratering rates indicative of an asteroid shower. We argue that meteorites and small (<1-km-sized) asteroids impacting Earth mainly sample a very small region of orbital space in the asteroid belt. This selectiveness has been remarkably stable over the past 500 Ma.

The efficiency paradox: How wasteful competitors forge thrifty ecosystems.

Organic waste, an inevitable byproduct of metabolism, increases in amount as metabolic rates (per capita power) of animals and plants rise. Most of it is recycled within aerobic ecosystems, but some is lost to the system and is sequestered in the crust for millions of years. Here, I identify and resolve a previously overlooked paradox concerning the long-term loss of organic matter. In this efficiency paradox, high-powered species are inefficient in that they release copious waste, but the ecosystems they inhabit lose almost no organic matter. Systems occupied by more efficient low-powered species suffer greater losses because of less efficient recycling. Over Phanerozoic time, ecosystems have become more productive and increasingly efficient at retaining and redistributing organic matter even as opportunistic and highly competitive producers and consumers gained power and became less efficient. These patterns and trends are driven by natural selection at the level of individuals and coherent groups, which favors winners that are more powerful, active, and wasteful. The activities of these competitors collectively create conditions that are increasingly conducive to more efficient recycling and retention of organic matter in the ecosystem.

Mass extinctions alter extinction and origination dynamics with respect to body size.

Whether mass extinctions and their associated recoveries represent an intensification of background extinction and origination dynamics versus a separate macroevolutionary regime remains a central debate in evolutionary biology. The previous focus has been on extinction, but origination dynamics may be equally or more important for long-term evolutionary outcomes. The evolution of animal body size is an ideal process to test for differences in macroevolutionary regimes, as body size is easily determined, comparable across distantly related taxa and scales with organismal traits. Here, we test for shifts in selectivity between background intervals and the 'Big Five' mass extinction events using capture-mark-recapture models. Our body-size data cover 10 203 fossil marine animal genera spanning 10 Linnaean classes with occurrences ranging from Early Ordovician to Late Pleistocene (485-1 Ma). Most classes exhibit differences in both origination and extinction selectivity between background intervals and mass extinctions, with the direction of selectivity varying among classes and overall exhibiting stronger selectivity during origination after mass extinction than extinction during the mass extinction. Thus, not only do mass extinction events shift the marine biosphere into a new macroevolutionary regime, the dynamics of recovery from mass extinction also appear to play an underappreciated role in shaping the biosphere in their aftermath.

Oxygen isotope composition of the Phanerozoic ocean and a possible solution to the dolomite problem.

The 18O/16O of calcite fossils increased by ∼8‰ between the Cambrian and present. It has long been controversial whether this change reflects evolution in the δ18O of seawater, or a decrease in ocean temperatures, or greater extents of diagenesis of older strata. Here, we present measurements of the oxygen and ?clumped" isotope compositions of Phanerozoic dolomites and compare these data with published oxygen isotope studies of carbonate rocks. We show that the δ18O values of dolomites and calcite fossils of similar age overlap one another, suggesting they are controlled by similar processes. Clumped isotope measurements of Cambrian to Pleistocene dolomites imply crystallization temperatures of 15-158 °C and parent waters having δ18OVSMOW values from -2 to +12‰. These data are consistent with dolomitization through sediment/rock reaction with seawater and diagenetically modified seawater, over timescales of 100 My, and suggest that, like dolomite, temporal variations of the calcite fossil δ18O record are largely driven by diagenetic alteration. We find no evidence that Phanerozoic seawater was significantly lower in δ18O than preglacial Cenozoic seawater. Thus, the fluxes of oxygen-isotope exchange associated with weathering and hydrothermal alteration reactions have remained stable throughout the Phanerozoic, despite major tectonic, climatic and biologic perturbations. This stability implies that a long-term feedback exists between the global rates of seafloor spreading and weathering. We note that massive dolomites have crystallized in pre-Cenozoic units at temperatures >40 °C. Since Cenozoic platforms generally have not reached such conditions, their thermal immaturity could explain their paucity of dolomites.

The apparent exponential radiation of Phanerozoic land vertebrates is an artefact of spatial sampling biases.

There is no consensus about how terrestrial biodiversity was assembled through deep time, and in particular whether it has risen exponentially over the Phanerozoic. Using a database of 60 859 fossil occurrences, we show that the spatial extent of the worldwide terrestrial tetrapod fossil record itself expands exponentially through the Phanerozoic. Changes in spatial sampling explain up to 67% of the change in known fossil species counts, and these changes are decoupled from variation in habitable land area that existed through time. Spatial sampling therefore represents a real and profound sampling bias that cannot be explained as redundancy. To address this bias, we estimate terrestrial tetrapod diversity for palaeogeographical regions of approximately equal size. We find that regional-scale diversity was constrained over timespans of tens to hundreds of millions of years, and similar patterns are recovered for major subgroups, such as dinosaurs, mammals and squamates. Although the Cretaceous/Palaeogene mass extinction catalysed an abrupt two- to three-fold increase in regional diversity 66 million years ago, no further increases occurred, and recent levels of regional diversity do not exceed those of the Palaeogene. These results parallel those recovered in analyses of local community-level richness. Taken together, our findings strongly contradict past studies that suggested unbounded diversity increases at local and regional scales over the last 100 million years.

Sex and the shifting biodiversity dynamics of marine animals in deep time.

The fossil record of marine animals suggests that diversity-dependent processes exerted strong control on biodiversification: after the Ordovician Radiation, genus richness did not trend for hundreds of millions of years. However, diversity subsequently rose dramatically in the Cretaceous and Cenozoic (145 million years ago-present), indicating that limits on diversification can be overcome by ecological or evolutionary change. Here, we show that the Cretaceous-Cenozoic radiation was driven by increased diversification in animals that transfer sperm between adults during fertilization, whereas animals that broadcast sperm into the water column have not changed significantly in richness since the Late Ordovician (∼450 million years ago). We argue that the former group radiated in part because directed sperm transfer permits smaller population sizes and additional modes of prezygotic isolation, as has been argued previously for the coincident radiation of angiosperms. Directed sperm transfer tends to co-occur with many ecological traits, such as a predatory lifestyle. Ecological specialization likely operated synergistically with mode of fertilization in driving the diversification that began during the Mesozoic marine revolution. Plausibly, the ultimate driver of diversification was an increase in food availability, but its effects on the fauna were regulated by fundamental reproductive and ecological traits.

Extending the scope of Darwin's 'abominable mystery': integrative approaches to understanding angiosperm origins and species richness.

Background and aims: Angiosperms are the most species-rich group of land plants, but their origins and fast and intense diversification still require an explanation. Scope: Extending research scopes can broaden theoretical frameworks and lines of evidence that can lead to solving this 'abominable mystery'. Solutions lie in understanding evolutionary trends across taxa and throughout the Phanerozoic, and integration between hypotheses and ideas that are derived from multiple disciplines. Key Findings: Descriptions of evolutionary chronologies should integrate between molecular phylogenies, descriptive palaeontology and palaeoecology. New molecular chronologies open new avenues of research of possible Palaeozoic angiosperm ancestors and how they evolved during as many as 200Myr until the emergence of true angiosperms. The idea that 'biodiversity creates biodiversity' requires evidence from past and present ecologies, with changes in herbivory and resource availability throughout the Phanerozoic appearing to be particularly promising. Conclusions: Promoting our understanding of angiosperm origins and diversification in particular, and the evolution of biodiversity in general, requires more profound understanding of the ecological past through integrating taxonomic, temporal and ecological scopes.

Influence of sulfate reduction rates on the Phanerozoic sulfur isotope record.

Phanerozoic levels of atmospheric oxygen relate to the burial histories of organic carbon and pyrite sulfur. The sulfur cycle remains poorly constrained, however, leading to concomitant uncertainties in O2 budgets. Here we present experiments linking the magnitude of fractionations of the multiple sulfur isotopes to the rate of microbial sulfate reduction. The data demonstrate that such fractionations are controlled by the availability of electron donor (organic matter), rather than by the concentration of electron acceptor (sulfate), an environmental constraint that varies among sedimentary burial environments. By coupling these results with a sediment biogeochemical model of pyrite burial, we find a strong relationship between observed sulfur isotope fractionations over the last 200 Ma and the areal extent of shallow seafloor environments. We interpret this as a global dependency of the rate of microbial sulfate reduction on the availability of organic-rich sea-floor settings. However, fractionation during the early/mid-Paleozoic fails to correlate with shelf area. We suggest that this decoupling reflects a shallower paleoredox boundary, primarily confined to the water column in the early Phanerozoic. The transition between these two states begins during the Carboniferous and concludes approximately around the Triassic-Jurassic boundary, indicating a prolonged response to a Carboniferous rise in O2. Together, these results lay the foundation for decoupling changes in sulfate reduction rates from the global average record of pyrite burial, highlighting how the local nature of sedimentary processes affects global records. This distinction greatly refines our understanding of the S cycle and its relationship to the history of atmospheric oxygen.

Ecological interactions on macroevolutionary time scales: clams and brachiopods are more than ships that pass in the night.

Competition among organisms has ecological and evolutionary consequences. However, whether the consequences of competition are manifested and measureable on macroevolutionary time scales is equivocal. Marine bivalves and brachiopods have overlapping niches such that competition for food and space may occur. Moreover, there is a long-standing debate over whether bivalves outcompeted brachiopods evolutionarily, because brachiopod diversity declined through time while bivalve diversity increased. To answer this question, we estimate the origination and extinction dynamics of fossil marine bivalve and brachiopod genera from the Ordovician through to the Recent while simultaneously accounting for incomplete sampling. Then, using stochastic differential equations, we assess statistical relationships among diversification and sampling dynamics of brachiopods and bivalves and five paleoenvironmental proxies. None of these potential environmental drivers had any detectable influence on brachiopod or bivalve diversification. In contrast, elevated bivalve extinction rates causally increased brachiopod origination rates, suggesting that bivalves have suppressed brachiopod evolution.

Metabolic dominance of bivalves predates brachiopod diversity decline by more than 150 million years.

Brachiopods and bivalves feed in similar ways and have occupied the same environments through geological time, but brachiopods were far more diverse and abundant in the Palaeozoic whereas bivalves dominate the post-Palaeozoic, suggesting a transition in ecological dominance 250 Ma. However, diversity and abundance data alone may not adequately describe key changes in ecosystem function, such as metabolic activity. Here, we use newly compiled body size data for 6066 genera of bivalves and brachiopods to calculate metabolic rates and revisit this question from the perspective of energy use, finding that bivalves already accounted for a larger share of metabolic activity in Palaeozoic oceans. We also find that the metabolic activity of bivalves has increased by more than two orders of magnitude over this interval, whereas brachiopod metabolic activity has declined by more than 50%. Consequently, the increase in bivalve energy metabolism must have occurred via the acquisition of new food resources rather than through the displacement of brachiopods. The canonical view of a mid-Phanerozoic transition from brachiopod to bivalve dominance results from a focus on taxonomic diversity and numerical abundance as measures of ecological importance. From a metabolic perspective, the oceans have always belonged to the clams.

Accretion of "young" Phanerozoic subcontinental lithospheric mantle triggered by back-arc extension-the case of the Ivrea-Verbano Zone.

The subcontinental lithospheric mantle (SCLM) beneath Phanerozoic regions is mostly constituted by fertile lherzolites, which sharply contrast with cratonic mantle made of highly-depleted peridotites. The question of whether this chemical difference results from lower degrees of melting associated with the formation of Phanerozoic SCLM or from the refertilization of ancient depleted SCLM remains a subject of debate. Additionally, the timing and geodynamic environment of accretion of the fertile SCLM in many Phanerozoic regions are poorly constrained. We here document new geochemical and Nd-Hf isotopic data for orogenic lherzolite massifs from the Ivrea-Verbano Zone (IVZ), Southern Alps. Even though a few Proterozoic Re depletion ages are locally preserved in these mantle bodies, our data reveal that the IVZ lherzolitic massifs were "recently" accreted to the SCLM in the Upper Devonian (ca. 370 Ma) during Pangea amalgamation, with a petrochemical evolution characterized by low-degree (~ 5-12%) depletion and nearly contemporaneous pervasive to focused melt migration. The lithospheric accretion putatively took place through asthenospheric upwelling triggered by Variscan intra-continental extension in a back-arc setting related to the subduction of the Rheic Ocean. We thus conclude that the fertile sections of Phanerozoic SCLM can be accreted during "recent" events of back-arc continental extension, even where Os isotopes preserve memories of melting events in much older times.

The Phanerozoic climate.

We review the long-term climate variations during the last 540 million years (Phanerozoic Eon). We begin with a short summary of the relevant geological and geochemical datasets available for the reconstruction of long-term climate variations. We then explore the main drivers of climate that appear to explain a large fraction of these climatic oscillations. The first is the long-term trend in atmospheric CO2 due to geological processes, while the second is the atmospheric ionization due to the changing galactic environment. Other drivers, such as albedo and geographic effects, are of secondary importance. In this review, we pay particular attention to problems that may affect the measurements of temperature obtained from oxygen isotopes, such as the long-term changes in the concentration of δ18 O seawater.

A persistent influence of supernovae on biodiversity over the Phanerozoic.

It is an open question what has constrained macroevolutionary changes in marine animal diversity on the time scale of the Phanerozoic. Here, we will show that supernovae appear to have significantly influenced the biodiversity of life. After normalizing diversity curves of major animal marine genera by the changes in the area of shallow marine margins, a close correlation between supernovae frequency and biodiversity is obtained. The interpretation is that supernovae influence Earth's climate, which controls the ocean and atmospheric circulation of nutrients. With this, supernovae influence ocean bioproductivity and are speculated to affect genera-level diversity. The implication is a surprisingly influential role of stellar processes on evolution.

Reduced strength and increased variability of extinction selectivity during mass extinctions.

Two of the traits most often observed to correlate with extinction risk in marine animals are geographical range and body size. However, the relative effects of these two traits on extinction risk have not been investigated systematically for either background times or during mass extinctions. To close this knowledge gap, we measure and compare extinction selectivity of geographical range and body size of genera within five classes of benthic marine animals across the Phanerozoic using capture-mark-recapture models. During background intervals, narrow geographical range is strongly associated with greater extinction probability, whereas smaller body size is more weakly associated with greater extinction probability. During mass extinctions, the association between geographical range and extinction probability is reduced in every class and fully eliminated in some, whereas the association between body size and extinction probability varies in strength and direction across classes. While geographical range is universally the stronger predictor of survival during background intervals, variation among classes during mass extinction suggests a fundamental shift in extinction processes during these global catastrophes.

Was the Late Ordovician mass extinction truly exceptional?

The Late Ordovician mass extinction event is the oldest of the five great extinction events in the fossil record. It has long been regarded as an outlier among mass extinctions, primarily due to its association with a cooling climate. However, recent temporally better resolved fossil biodiversity estimates complicate this view, providing growing evidence for a prolonged but punctuated biodiversity decline modulated by changes in atmospheric composition, ocean chemistry, and viable habitat area. This evolving view invokes extinction drivers similar to those that occurred during other major extinctions; some are even factors in the current human-induced biodiversity crisis. Even this very ancient and, at first glance, exceptional event conveys important lessons about the intensifying 'sixth mass extinction'.

Dataset of Phanerozoic continental climate and Köppen-Geiger climate classes.

This article describes a suite of global climate model output files that provide continental climatic conditions (monthly temperatures, precipitation, evaporation, precipitation minus evaporation balance, runoff) together with the calculated Köppen-Geiger climate classes and topography, for 28 evenly spaced time slices through the Phanerozoic (Cambrian to Quaternary, 540 Ma to 0 Ma). Climatic variables were simulated with the Fast Ocean Atmosphere Model (FOAM), using a recent set of open-access continental reconstructions with paleotopography and recent atmospheric CO2 and solar luminosity estimates. FOAM is a general circulation model frequently used in paleoclimate studies, especially in the Palaeozoic. Köppen-Geiger climate classes were calculated based on simulated temperature and precipitation fields using Wong Hearing et al.'s [1] implementation of Peel et al.'s [2] updated classification. This dataset provides a unique window onto changing continental climate throughout the Phanerozoic that accounts for the simultaneous evolution of paleogeography (continental configuration and topography), atmospheric composition and greenhouse gas forcing, and solar luminosity.

Phanerozoic parasitism and marine metazoan diversity: dilution versus amplification.

Growing evidence suggests that biodiversity mediates parasite prevalence. We have compiled the first global database on occurrences and prevalence of marine parasitism throughout the Phanerozoic and assess the relationship with biodiversity to test if there is support for amplification or dilution of parasitism at the macroevolutionary scale. Median prevalence values by era are 5% for the Paleozoic, 4% for the Mesozoic, and a significant increase to 10% for the Cenozoic. We calculated period-level shareholder quorum sub-sampled (SQS) estimates of mean sampled diversity, three-timer (3T) origination rates, and 3T extinction rates for the most abundant host clades in the Paleobiology Database to compare to both occurrences of parasitism and the more informative parasite prevalence values. Generalized linear models (GLMs) of parasite occurrences and SQS diversity measures support both the amplification (all taxa pooled, crinoids and blastoids, and molluscs) and dilution hypotheses (arthropods, cnidarians, and bivalves). GLMs of prevalence and SQS diversity measures support the amplification hypothesis (all taxa pooled and molluscs). Though likely scale-dependent, parasitism has increased through the Phanerozoic and clear patterns primarily support the amplification of parasitism with biodiversity in the history of life. This article is part of the theme issue 'Infectious disease macroecology: parasite diversity and dynamics across the globe'.

Assessing canalisation of intraspecific variation on a macroevolutionary scale: the case of crinoid arms through the Phanerozoic.

Clades that represent a new 'Bauplan' have been hypothesised to exhibit more variability than more derived clades. Accordingly, there is an expectation of greater variation around the time of the origin of a clade than later in its evolutionary history. This 'canalisation' has been tested in terms of morphological disparity (interspecific variation), whereas intraspecific variation in macroevolution is rarely studied. We analysed extensive data of brachial counts in crinoid populations from the Ordovician to the Recent to test for canalisation in morphological intraspecific variation. Our results show no support for the canalisation hypothesis through the Phanerozoic. This lack of pattern is maintained even when considering crinoid subclades separately. Our study is an example of the lack of universality in such macroevolutionary patterns both in terms of organisms and in terms of modules within them. It is also an example on the challenges and limitations of palaeontological studies of macroevolutionary processes.

Continental igneous rock composition: A major control of past global chemical weathering.

The composition of igneous rocks in the continental crust has changed throughout Earth's history. However, the impact of these compositional variations on chemical weathering, and by extension on seawater and atmosphere evolution, is largely unknown. We use the strontium isotope ratio in seawater [(87Sr/86Sr)seawater] as a proxy for chemical weathering, and we test the sensitivity of (87Sr/86Sr)seawater variations to the strontium isotopic composition (87Sr/86Sr) in igneous rocks generated through time. We demonstrate that the 87Sr/86Sr ratio in igneous rocks is correlated to the epsilon hafnium (εHf) of their hosted zircon grains, and we use the detrital zircon record to reconstruct the evolution of the 87Sr/86Sr ratio in zircon-bearing igneous rocks. The reconstructed 87Sr/86Sr variations in igneous rocks are strongly correlated with the (87Sr/86Sr)seawater variations over the last 1000 million years, suggesting a direct control of the isotopic composition of silicic magmatism on (87Sr/86Sr)seawater variations. The correlation decreases during several time periods, likely reflecting changes in the chemical weathering rate associated with paleogeographic, climatic, or tectonic events. We argue that for most of the last 1000 million years, the (87Sr/86Sr)seawater variations are responding to changes in the isotopic composition of silicic magmatism rather than to changes in the global chemical weathering rate. We conclude that the (87Sr/86Sr)seawater variations are of limited utility to reconstruct changes in the global chemical weathering rate in deep times.