David Jablonski

LARVAL ECOLOGY OF MARINE BENTHIC INVERTEBRATES: PALEOBIOLOGICAL IMPLICATIONS

1. Modes of larval development play important roles in the ecology, biogeography, and evolution of marine benthic organisms. Studies of the larval ecology of fossil organisms can contribute greatly to our understanding of such roles by allowing us to race effects on evolutionary time scales.

Background and Mass Extinctions: The Alternation of Macroevolutionary Regimes

Comparison of evolutionary patterns among Late Cretaceous marine bivalves and gastropods during times of normal, background levels of extinction and during the end-Cretaceous mass extinction indicates that mass extinctions are neither an intensification of background patterns nor an entirely random culling of the biota. During background times, traits such as planktotrophic larval development, broad geographic range of constituent species, and high species richness enhanced survivorship of species and genera. In contrast, during the, end-Cretaceous and other mass extinctions these factors were ineffectual, but broad geographic deployment of an entire lineage, regardless of the ranges of its constituent species, enhanced survivorship. Large-scale evolutionary patterns are evidently shaped by the alternation of these two macroevolutionary regimes, with rare but important mass extinctions driving shifts in the composition of the biota that have little relation to success during the background regime. Lineages or adaptations can be lost during mass extinctions for reasons unrelated to their survival values for organisms or species during background times, and long-term success would require the chance occurrence within a single lineage of sets of traits conducive to survivorship under both regimes.

Effects of sampling standardization on estimates of Phanerozoic marine diversification.

Global diversity curves reflect more than just the number of taxa that have existed through time: they also mirror variation in the nature of the fossil record and the way the record is reported. These sampling effects are best quantified by assembling and analyzing large numbers of locality-specific biotic inventories. Here, we introduce a new database of this kind for the Phanerozoic fossil record of marine invertebrates. We apply four substantially distinct analytical methods that estimate taxonomic diversity by quantifying and correcting for variation through time in the number and nature of inventories. Variation introduced by the use of two dramatically different counting protocols also is explored. We present sampling-standardized diversity estimates for two long intervals that sum to 300 Myr (Middle Ordovician-Carboniferous; Late Jurassic-Paleogene). Our new curves differ considerably from traditional, synoptic curves. For example, some of them imply unexpectedly low late Cretaceous and early Tertiary diversity levels. However, such factors as the current emphasis in the database on North America and Europe still obscure our view of the global history of marine biodiversity. These limitations will be addressed as the database and methods are refined.

Heritability at the Species Level: Analysis of Geographic Ranges of Cretaceous Mollusks

Geographic range has been regarded as a property of species rather than of individuals and thus as a potential factor in macroevolutionary processes. Species durations in Late Cretaceous mollusks exhibit statistically significant positive relationships with geographic range, and the attainment of a typical frequency distribution of geographic ranges in the cohort of species that originated just before the end-Cretaceous extinction indicates that species duration is the dependent variable. The strong relation between geographic ranges in pairs of closely related species indicates that the trait is, in effect, heritable at the species level. The significant heritabilities strengthen claims for processes of evolution by species-level selection, and for differential survivorship of organismic-level traits owing to extinction and origination processes operating at higher levels.

The dynamics of evolutionary stasis

Abstract The fossil record displays remarkable stasis in many species over long time periods, yet studies of extant populations often reveal rapid phenotypic evolution and genetic differentiation among populations. Recent advances in our understanding of the fossil record and in population genetics and evolutionary ecology point to the complex geographic structure of species being fundamental to resolution of how taxa can commonly exhibit both short-term evolutionary dynamics and long-term stasis.

Onshore-offshore patterns in the evolution of phanerozoic shelf communities.

Cluster analysis of Cambrian-Ordovician marine benthic communities and community-trophic analysis of Late Cretaceous shelf faunas indicate that major ecological innovations appeared in nearshore environments and then expanded outward across the shelf at the expense of older community types. This onshoreinnovation, offshore-archaic evolutionary pattern is surprising in light of the generally, higher species turnover rates of offshore clades. This pattern probably results from differential extinction rates of onshore as compared to offshore clades, or from differential origination rates of new ecological associations or evolutionary novelties in nearshore environments.

Mass extinctions and macroevolution

Abstract Mass extinctions are important to macroevolution not only because they involve a sharp increase in extinction intensity over “background” levels, but also because they bring a change in extinction selectivity, and these quantitative and qualitative shifts set the stage for evolutionary recoveries. The set of extinction intensities for all stratigraphic stages appears to fall into a single right-skewed distribution, but this apparent continuity may derive from failure to factor out the well-known secular trend in background extinction: high early Paleozoic rates fill in the gap between later background extinction and the major mass extinctions. In any case, the failure of many organism-, species-, and clade-level traits to predict survivorship during mass extinctions is a more important challenge to the extrapolationist premise that all macroevolutionary processes are simply smooth extensions of microevolution. Although a variety of factors have been found to correlate with taxon survivorship for particular extinction events, the most pervasive effect involves geographic range at the clade level, an emergent property independent of the range sizes of constituent species. Such differential extinction would impose “nonconstructive selectivity,” in which survivorship is unrelated to many organismic traits but is not strictly random. It also implies that correlations among taxon attributes may obscure causation, and even the focal level of selection, in the survival of a trait or clade, for example when widespread taxa within a major group tend to have particular body sizes, trophic habits, or metabolic rates. Survivorship patterns will also be sensitive to the inexact correlations of taxonomic, morphological, and functional diversity, to phylogenetically nonrandom extinction, and to the topology of evolutionary trees. Evolutionary recoveries may be as important as the extinction events themselves in shaping the long-term trajectories of individual clades and permitting once-marginal groups to diversify, but we know little about sorting processes during recovery intervals. However, both empirical extrapolationism (where outcomes can be predicted from observation of pre- or post-extinction patterns) and theoretical extrapolationism (where mechanisms reside exclusively at the level of organisms within populations) evidently fail during mass extinctions and their evolutionary aftermath. This does not mean that conventional natural selection was inoperative during mass extinctions, but that many features that promoted survivorship during background times were superseded as predictive factors by higher-level attributes. Many intriguing issues remain, including the generality of survivorship rules across extinction events; the potential for gradational changes in selectivity patterns with extinction intensity or the volatility of target clades; the heritability of clade-level traits; the macroevolutionary consequences of the inexact correlations between taxonomic, morphological, and functional diversity; the factors governing the dynamics and outcome of recoveries; and the spatial fabric of extinctions and recoveries. The detection of general survivorship rules—including the disappearance of many patterns evident during background times—demonstrates that studies of mass extinctions and recovery can contribute substantially to evolutionary theory.

Patterns and Processes in the History of Life

Paleontology can be a rich source of theory and data on evolutionary and ecological processes at more inclusive hierarchical levels and greater time scales than those available to the neontologist. Although the generation-by-generation record of ancient populations and communities is obscured by inconstancy of sedimentation and bioturbation, the record of lager-scale patterns of intraand interspecific morphological change (and stasis) can be analyzed with confidence when sampling schemes and the questions being asked allow for the discontinuous nature of the rock record and the difficulty of precise time correlation among localities. These considerations permit the analysis of such diverse problems as the evolutionary consequences of different genetic population structures (e.g., fragmented vs. panmictic) or genetical systems (e.g., sexual vs. asexual); the intrinsic and extrinsic factors giving rise to a bias towards stasis or gradualism within the species of a given group; and the origin, persistence, and cohesiveness of different ecological communities and community types. The rich morphological data of paleontology (generally only hardparts, although some extraordinary localities provide a far more complete record) yield insights into the pattern of occupation of morpho space through geological time and into the ways in which differential speciation and extinction generate evolutionary trends in groups dominated by morphological stasis. The smooth extrapolation of microevolutionary processes evidently also fails to explain the evolutionary consequences of mass extinction events, which are more frequent, more disruptive, and more important as 8 D. Jablonski et al. agents of faunal replacement than previously thought. In its direct study of inclusive levels and long time intervals and of the large and rare events that only repeat sufficiently often in the fulness of geological time, paleontology yields a wealth of phenomena not accessible to neon to logy and promises a fruitful union with micro evolution and ecology for a more comprehensive theory of organic change and stability.

Paleoenvironmental patterns in the evolution of post-Paleozoic benthic marine invertebrates

The ecological context of large-scale evolutionary patterns has been neglected. Several workers have recently reported a bathymetric bias in the evolution of benthic marine communities, such that nearshore assemblages tend to contain advanced taxa and community structures and offshore assemblages contain more archaic features. A clade-by-clade analysis is the most powerful approach for assessing the generality of the pattern and testing hypotheses on underlying mechanisms. We develop a paleoenvironmental framework for constructing time-environment histories for higher taxa that should be of general comparative utility, based on five environmental categories recognized by physical sedimentary and biostratinomic criteria. The robustness of negative data (absence of a given taxon from a particular time and environment) is evaluated using taphonomic control groupshigher taxa with ecological, morphological, and mineralogical properties similar to those of the group under study. Within this framework we have constructed three detailed time-environment histories from the primary literature, for the crinoid Order Isocrinida (based on 99 early Triassic-Recent occurrences), the bryozoan Order Cheilostomata (67 late Jurassic-late Eocene occurrences), and the bivalve Superfamily Tellinacea (70 late Triassic-Miocene occurrences). These three time-environment diagrams as well as numerous anecdotal reports suggest that the onshore-offshore trends previously reported for communities are actually underlain by individualistic clade histories that only appear to act in concert when viewed on a coarse time scale. For these three particular higher taxa differences in rates and timing of movement through environments also falsify causal hypotheses that invoke sea-level fluctuations or mass extinctions. We outline remaining viable hypotheses for driving mechanisms and suggest further tests; at present the data are consistent with a broad array of intrinsic biological mechanisms. These pervasive shifts through time of environmental preferences severely undermine approaches to paleoenvironmental reconstruction based on interpreting fossil content in the light of present-day faunal distributions. Production of detailed timeenvironment histories for additional higher taxa will permit paleoenvironmental analyses based on overlapping environmental range zones, in which particular co-occurrences are diagnostic of different habitats at different times.

Biotic Interactions and Macroevolution: Extensions and Mismatches Across Scales and Levels

Abstract Clade dynamics in the fossil record broadly fit expectations from the operation of competition, predation, and mutualism, but data from both modern and ancient systems suggest mismatches across scales and levels. Indirect effects, as when antagonistic or mutualistic interactions restrict geographic range and thereby elevate extinction risk, are probably widespread and may flow in both directions, as when species- or organismic-level factors increase extinction risk or speciation probabilities. Apparent contradictions across scales and levels have been neglected, including (1) the individualistic geographic shifts of species on centennial and millennial timescales versus evidence for fine-tuned coevolutionary relationships; (2) the extensive and dynamic networks of interactions faced by most species versus the evolution of costly enemy-specific defenses and finely attuned mutualisms; and (3) the macroevolutionary lags often seen between the origin and the diversification of a clade or an evolutionary novelty versus the rapid microevolution of advantageous phenotypes and the invasibility of most communities. Resolution of these and other cross-level tensions presumably hinges on how organismic interactions impinge on genetic population structures, geographic ranges, and the persistence of incipient species, but generalizations are not yet possible. Paleontological and neontological data are both incomplete and so the most powerful response to these problems will require novel integrative approaches. Promising research areas include more realistic approaches to modeling and empirical analysis of large-scale diversity dynamics of ostensibly competing clades; spatial and phylogenetic dissections of clades involved in escalatory dynamics (where prey respond evolutionarily to a broad and shifting array of enemies); analyses of the short- versus long-term consequences of mutualistic symbioses; and fuller use of abundant natural experiments on the evolutionary impacts of ecosystem engineers.