Morphological volatility precedes ecological innovation in early echinoderms.

Origins of higher taxonomic groups entail dramatic and nearly simultaneous changes in morphology and ecological function, limiting our ability to disentangle the drivers of evolutionary diversification. Here we phylogenetically compare the anatomy and life habits of Cambrian-Ordovician echinoderms to test which facet better facilitates future success. Rates of morphological evolution are faster and involve more volatile trait changes, allowing morphological disparity to accrue faster and earlier in the Cambrian. However, persistent life-habit evolution throughout the early Palaeozoic, combined with iterative functional convergence within adaptive strategies, results in major expansion of ecospace and functional diversity. The interactions between tempo, divergence and convergence demonstrate not only that anatomical novelty precedes ecological success, but also that ecological innovation is constrained, even during a phylum's origin.

Hierarchical complexity and the size limits of life.

Over the past 3.8 billion years, the maximum size of life has increased by approximately 18 orders of magnitude. Much of this increase is associated with two major evolutionary innovations: the evolution of eukaryotes from prokaryotic cells approximately 1.9 billion years ago (Ga), and multicellular life diversifying from unicellular ancestors approximately 0.6 Ga. However, the quantitative relationship between organismal size and structural complexity remains poorly documented. We assessed this relationship using a comprehensive dataset that includes organismal size and level of biological complexity for 11 172 extant genera. We find that the distributions of sizes within complexity levels are unimodal, whereas the aggregate distribution is multimodal. Moreover, both the mean size and the range of size occupied increases with each additional level of complexity. Increases in size range are non-symmetric: the maximum organismal size increases more than the minimum. The majority of the observed increase in organismal size over the history of life on the Earth is accounted for by two discrete jumps in complexity rather than evolutionary trends within levels of complexity. Our results provide quantitative support for an evolutionary expansion away from a minimal size constraint and suggest a fundamental rescaling of the constraints on minimal and maximal size as biological complexity increases.

Modelling the ecological-functional diversification of marine Metazoa on geological time scales.

The ecological traits and functional capabilities of marine animals have changed significantly since their origin in the late Precambrian. These changes can be analysed quantitatively using multi-dimensional parameter spaces in which the ecological lifestyles of species are represented by particular combinations of parameter values. Here, we present models that describe the filling of this multi-dimensional 'ecospace' by ecological lifestyles during metazoan diversification. These models reflect varying assumptions about the processes that drove ecological diversification; they contrast diffusive expansion with driven expansion and niche conservatism with niche partitioning. Some models highlight the importance of interactions among organisms (ecosystem engineering and predator-prey escalation) in promoting new lifestyles or eliminating existing ones. These models reflect processes that were not mutually exclusive; rigorous analyses will continue to reveal their applicability to episodes in metazoan history.

The multidimensionality of the niche reveals functional diversity changes in benthic marine biotas across geological time.

Despite growing attention on the influence of functional diversity changes on ecosystem functioning, a palaeoecological perspective on the long-term dynamic of functional diversity, including mass extinction crises, is still lacking. Here, using a novel multidimensional functional framework and comprehensive null-models, we compare the functional structure of Cambrian, Silurian and modern benthic marine biotas. We demonstrate that, after controlling for increases in taxonomic diversity, functional richness increased incrementally between each time interval with benthic taxa filling progressively more functional space, combined with a significant functional dissimilarity between periods. The modern benthic biota functionally overlaps with fossil biotas but some modern taxa, especially large predators, have new trait combinations that may allow more functions to be performed. From a methodological perspective, these results illustrate the benefits of using multidimensional instead of lower dimensional functional frameworks when studying changes in functional diversity over space and time.

The evolutionary consequences of oxygenic photosynthesis: a body size perspective.

The high concentration of molecular oxygen in Earth's atmosphere is arguably the most conspicuous and geologically important signature of life. Earth's early atmosphere lacked oxygen; accumulation began after the evolution of oxygenic photosynthesis in cyanobacteria around 3.0-2.5 billion years ago (Gya). Concentrations of oxygen have since varied, first reaching near-modern values ~600 million years ago (Mya). These fluctuations have been hypothesized to constrain many biological patterns, among them the evolution of body size. Here, we review the state of knowledge relating oxygen availability to body size. Laboratory studies increasingly illuminate the mechanisms by which organisms can adapt physiologically to the variation in oxygen availability, but the extent to which these findings can be extrapolated to evolutionary timescales remains poorly understood. Experiments confirm that animal size is limited by experimental hypoxia, but show that plant vegetative growth is enhanced due to reduced photorespiration at lower O(2):CO(2). Field studies of size distributions across extant higher taxa and individual species in the modern provide qualitative support for a correlation between animal and protist size and oxygen availability, but few allow prediction of maximum or mean size from oxygen concentrations in unstudied regions. There is qualitative support for a link between oxygen availability and body size from the fossil record of protists and animals, but there have been few quantitative analyses confirming or refuting this impression. As oxygen transport limits the thickness or volume-to-surface area ratio-rather than mass or volume-predictions of maximum possible size cannot be constructed simply from metabolic rate and oxygen availability. Thus, it remains difficult to confirm that the largest representatives of fossil or living taxa are limited by oxygen transport rather than other factors. Despite the challenges of integrating findings from experiments on model organisms, comparative observations across living species, and fossil specimens spanning millions to billions of years, numerous tractable avenues of research could greatly improve quantitative constraints on the role of oxygen in the macroevolutionary history of organismal size.

Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity.

The maximum size of organisms has increased enormously since the initial appearance of life >3.5 billion years ago (Gya), but the pattern and timing of this size increase is poorly known. Consequently, controls underlying the size spectrum of the global biota have been difficult to evaluate. Our period-level compilation of the largest known fossil organisms demonstrates that maximum size increased by 16 orders of magnitude since life first appeared in the fossil record. The great majority of the increase is accounted for by 2 discrete steps of approximately equal magnitude: the first in the middle of the Paleoproterozoic Era (approximately 1.9 Gya) and the second during the late Neoproterozoic and early Paleozoic eras (0.6-0.45 Gya). Each size step required a major innovation in organismal complexity--first the eukaryotic cell and later eukaryotic multicellularity. These size steps coincide with, or slightly postdate, increases in the concentration of atmospheric oxygen, suggesting latent evolutionary potential was realized soon after environmental limitations were removed.

Scale-dependence of Cope's rule in body size evolution of Paleozoic brachiopods.

The average body size of brachiopods from a single habitat type increased gradually by more than two orders of magnitude during their initial Cambrian-Devonian radiation. This increase occurred nearly in parallel across all major brachiopod clades (classes and orders) and is consistent with Cope's rule: the tendency for size to increase over geological time. The increase is not observed within small, constituent clades (represented here by families), which underwent random, unbiased size changes. This scale-dependence is caused by the preferential origination of new families possessing initially larger body sizes. However, this increased family body size does not confer advantages in terms of greater geological duration or genus richness over families possessing smaller body sizes. We suggest that the combination of size-biased origination of families and parallel size increases among major, more inclusive brachiopod clades from a single habitat type is best explained by long-term, secular environmental changes during the Paleozoic that provided opportunities for body size increases associated with major morphological evolution.