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.

Marine extinction risk shaped by trait-environment interactions over 500 million years.

Perhaps the most pressing issue in predicting biotic responses to present and future global change is understanding how environmental factors shape the relationship between ecological traits and extinction risk. The fossil record provides millions of years of insight into how extinction selectivity (i.e., differential extinction risk) is shaped by interactions between ecological traits and environmental conditions. Numerous paleontological studies have examined trait-based extinction selectivity; however, the extent to which these patterns are shaped by environmental conditions is poorly understood due to a lack of quantitative synthesis across studies. We conducted a meta-analysis of published studies on fossil marine bivalves and gastropods that span 458 million years to uncover how global environmental and geochemical changes covary with trait-based extinction selectivity. We focused on geographic range size and life habit (i.e., infaunal vs. epifaunal), two of the most important and commonly examined predictors of extinction selectivity. We used geochemical proxies related to global climate, as well as indicators of ocean acidification, to infer average global environmental conditions. Life-habit selectivity is weakly dependent on environmental conditions, with infaunal species relatively buffered from extinction during warmer climate states. In contrast, the odds of taxa with broad geographic ranges surviving an extinction (>2500 km for genera, >500 km for species) are on average three times greater than narrow-ranging taxa (estimate of odds ratio: 2.8, 95% confidence interval = 2.3-3.5), regardless of the prevailing global environmental conditions. The environmental independence of geographic range size extinction selectivity emphasizes the critical role of geographic range size in setting conservation priorities.

Direct and indirect effects of biological factors on extinction risk in fossil bivalves.

Biological factors, such as abundance and body size, may contribute directly to extinction risk and indirectly through their influence on other biological characteristics, such as geographic range size. Paleontological data can be used to explicitly test many of these hypothesized relationships, and general patterns revealed through analysis of the fossil record can help refine predictive models of extinction risk developed for extant species. Here, I use structural equation modeling to tease apart the contributions of three canonical predictors of extinction--abundance, body size, and geographic range size--to the duration of bivalve species in the early Cenozoic marine fossil record of the eastern United States. I find that geographic range size has a strong direct effect on extinction risk and that an apparent direct effect of abundance can be explained entirely by its covariation with geographic range. The influence of geographic range on extinction risk is manifest across three ecologically disparate bivalve clades. Body size also has strong direct effects on extinction risk but operates in opposing directions in different clades, and thus, it seems to be decoupled from extinction risk in bivalves as a whole. Although abundance does not directly predict extinction risk, I reveal weak indirect effects of both abundance and body size through their positive influence on geographic range size. Multivariate models that account for the pervasive covariation between biological factors and extinction are necessary for assessing causality in evolutionary processes and making informed predictions in applied conservation efforts.

Using the Fossil Record to Understand Extinction Risk and Inform Marine Conservation in a Changing World.

Understanding the long-term effects of ongoing global environmental change on marine ecosystems requires a cross-disciplinary approach. Deep-time and recent fossil records can contribute by identifying traits and environmental conditions associated with elevated extinction risk during analogous events in the geologic past and by providing baseline data that can be used to assess historical change and set management and restoration targets and benchmarks. Here, we review the ecological and environmental information available in the marine fossil record and discuss how these archives can be used to inform current extinction risk assessments as well as marine conservation strategies and decision-making at global to local scales. As we consider future research directions in deep-time and conservationpaleobiology, we emphasize the need for coproduced research that unites researchers, conservation practitioners, and policymakers with the communities for whom the impacts of climate and global change are most imminent.

Long-term differences in extinction risk among the seven forms of rarity.

Rarity is widely used to predict the vulnerability of species to extinction. Species can be rare in markedly different ways, but the relative impacts of these different forms of rarity on extinction risk are poorly known and cannot be determined through observations of species that are not yet extinct. The fossil record provides a valuable archive with which we can directly determine which aspects of rarity lead to the greatest risk. Previous palaeontological analyses confirm that rarity is associated with extinction risk, but the relative contributions of different types of rarity to extinction risk remain unknown because their impacts have never been examined simultaneously. Here, we analyse a global database of fossil marine animals spanning the past 500 million years, examining differential extinction with respect to multiple rarity types within each geological stage. We observe systematic differences in extinction risk over time among marine genera classified according to their rarity. Geographic range played a primary role in determining extinction, and habitat breadth a secondary role, whereas local abundance had little effect. These results suggest that current reductions in geographic range size will lead to pronounced increases in long-term extinction risk even if local populations are relatively large at present.

Genus age, provincial area and the taxonomic structure of marine faunas.

Species are unevenly distributed among genera within clades and regions, with most genera species-poor and few species-rich. At regional scales, this structure to taxonomic diversity is generated via speciation, extinction and geographical range dynamics. Here, we use a global database of extant marine bivalves to characterize the taxonomic structure of climate zones and provinces. Our analyses reveal a general, Zipf-Mandelbrot form to the distribution of species among genera, with faunas from similar climate zones exhibiting similar taxonomic structure. Provinces that contain older taxa and/or encompass larger areas are expected to be more species-rich. Although both median genus age and provincial area correlate with measures of taxonomic structure, these relationships are interdependent, nonlinear and driven primarily by contrasts between tropical and extra-tropical faunas. Provincial area and taxonomic structure are largely decoupled within climate zones. Counter to the expectation that genus age and species richness should positively covary, diverse and highly structured provincial faunas are dominated by young genera. The marked differences between tropical and temperate faunas suggest strong spatial variation in evolutionary rates and invasion frequencies. Such variation contradicts biogeographic models that scale taxonomic diversity to geographical area.

Geographic range velocity and its association with phylogeny and life history traits in North American woody plants.

The geographic ranges of taxa change in response to environmental conditions. Yet whether rates of range movement (biotic velocities) are phylogenetically conserved is not well known. Phylogenetic conservatism of biotic velocities could reflect similarities among related lineages in climatic tolerances and dispersal-associated traits. We assess whether late Quaternary biotic velocities were phylogenetically conserved and whether they correlate with climatic tolerances and dispersal-associated traits. We used phylogenetic regression and nonparametric correlation to evaluate associations between biotic velocities, dispersal-associated traits, and climatic tolerances for 28 woody plant genera and subgenera in North America. The velocities with which woody plant taxa shifted their core geographic range limits were positively correlated from time step to time step between 16 and 7 ka. The strength of this correlation weakened after 7 ka as the pace of climate change slowed. Dispersal-associated traits and climatic tolerances were not associated with biotic velocities. Although the biotic velocities of some genera were consistently fast and others consistently slow, biotic velocities were not phylogenetically conserved. The rapid late Quaternary range shifts of plants lacking traits that facilitate frequent long-distance dispersal has long been noted (i.e., Reid's Paradox). Our results are consistent with this paradox and show that it remains robust when phylogenetic information is taken into account. The lack of association between biotic velocities, dispersal-associated traits, and climatic tolerances may reflect several, nonmutually exclusive processes, including rare long-distance dispersal, biotic interactions, and cryptic refugia. Because late Quaternary biotic velocities were decoupled from dispersal-associated traits, trait data for genera and subgenera cannot be used to predict longer-term (millennial-scale) floristic responses to climate change.

Extinctions. Paleontological baselines for evaluating extinction risk in the modern oceans.

Marine taxa are threatened by anthropogenic impacts, but knowledge of their extinction vulnerabilities is limited. The fossil record provides rich information on past extinctions that can help predict biotic responses. We show that over 23 million years, taxonomic membership and geographic range size consistently explain a large proportion of extinction risk variation in six major taxonomic groups. We assess intrinsic risk-extinction risk predicted by paleontologically calibrated models-for modern genera in these groups. Mapping the geographic distribution of these genera identifies coastal biogeographic provinces where fauna with high intrinsic risk are strongly affected by human activity or climate change. Such regions are disproportionately in the tropics, raising the possibility that these ecosystems may be particularly vulnerable to future extinctions. Intrinsic risk provides a prehuman baseline for considering current threats to marine biodiversity.

Extinctions in ancient and modern seas.

In the coming century, life in the ocean will be confronted with a suite of environmental conditions that have no analog in human history. Thus, there is an urgent need to determine which marine species will adapt and which will go extinct. Here, we review the growing literature on marine extinctions and extinction risk in the fossil, historical, and modern records to compare the patterns, drivers, and biological correlates of marine extinctions at different times in the past. Characterized by markedly different environmental states, some past periods share common features with predicted future scenarios. We highlight how the different records can be integrated to better understand and predict the impact of current and projected future environmental changes on extinction risk in the ocean.