Anthropogenic disruptions to longstanding patterns of trophic-size structure in vertebrates.

Diet and body mass are inextricably linked in vertebrates: while herbivores and carnivores have converged on much larger sizes, invertivores and omnivores are, on average, much smaller, leading to a roughly U-shaped relationship between body size and trophic guild. Although this U-shaped trophic-size structure is well documented in extant terrestrial mammals, whether this pattern manifests across diverse vertebrate clades and biomes is unknown. Moreover, emergence of the U-shape over geological time and future persistence are unknown. Here we compiled a comprehensive dataset of diet and body size spanning several vertebrate classes and show that the U-shaped pattern is taxonomically and biogeographically universal in modern vertebrate groups, except for marine mammals and seabirds. We further found that, for terrestrial mammals, this U-shape emerged by the Palaeocene and has thus persisted for at least 66 million years. Yet disruption of this fundamental trophic-size structure in mammals appears likely in the next century, based on projected extinctions. Actions to prevent declines in the largest animals will sustain the functioning of Earth's wild ecosystems and biomass energy distributions that have persisted through deep time.

Ecological Filtering and Exaptation in the Evolution of Marine Snakes.

AbstractConvergent evolution is often attributed to adaptation of form to function, but it can also result from ecological filtering, exaptation, or nonaptation. Testing among these possibilities is critical to understanding how and why morphological similarities emerge independently in multiple lineages. To address this challenge, we combined multiple preexisting phylogenetic methods to jointly estimate the habitats and morphologies of lineages within a phylogeny. We applied this approach to the invasions of snakes into the marine realm. We utilized a data set for 1,243 extant snake species consisting of newly compiled biome occupancy information and preexisting data on reproductive strategy, body mass, and environmental temperature and elevation. We find evidence for marine clades arising from a variety of aquatic and terrestrial habitats. Furthermore, there is strong evidence of ecological filtering for nonmarine ancestors that were already viviparous, had slightly larger-than-average body sizes, and lived in environments with higher-than-average temperatures and lower-than-average elevations. In aggregate, similarities among independent lineages of marine snakes result from a combination of exaptation and strong ecological filtering. Strong barriers to entry of new habitats appear to be more important than common adaptations following invasions for producing similarities among independent lineages invading a shared, novel habitat.

Metabolic tradeoffs control biodiversity gradients through geological time.

The latitudinal gradient of increasing marine biodiversity from the poles to the tropics is one of the most conspicuous biological patterns in modern oceans.1-3 Low-latitude regions of the global ocean are often hotspots of animal biodiversity, yet they are set to be most critically affected by anthropogenic climate change.4 As ocean temperatures rise and deoxygenation proceeds in the coming centuries, the volume of aerobically viable habitat is predicted to decrease in these zones.5,6 In contrast to the slightly asymmetrical modern latitudinal biodiversity gradient,7 compilations of fossil occurrences indicate peaks in biodiversity may have existed much further away from the equator in the past, with transitions between climate states hypothesized to explain this trend.8-13 We combine a new compilation of fossil mollusc occurrences, paleotemperature proxies, and biogeographic data to reveal a non-monotonic relationship between temperature and diversity in the paleontological record over the last 145 million years. We derive a metabolic model that integrates the kinetic effects of temperature on biodiversity14 with the recently described Metabolic Index that calculates aerobic habitat availability based on the effect of temperature on hypoxia sensitivity.5,15,16 Although factors such as coastal habitat area and homeothermy are important,17,18 we find strong congruence between our metabolic model and our fossil and paleotemperature meta-analysis. We therefore suggest that the effects of ocean temperature on the aerobic scope of marine ectotherms is a primary driver of migrating biodiversity peaks through geologic time and will likely play a role in the restructuring of biodiversity under projected future climate scenarios.

Physiological constraints on body size distributions in Crocodyliformes.

At least 26 species of crocodylian populate the globe today, but this richness represents a minute fraction of the diversity and disparity of Crocodyliformes. Fossil forms are far more varied, spanning from erect, fully terrestrial species to flippered, fully marine species. To quantify the influence of a marine habitat on the directionality, rate, and variance of evolution of body size in Crocodyliformes and thereby identify underlying selective pressures, we compiled a database of body sizes for 264 fossil and modern species of crocodyliform covering terrestrial, semi-aquatic, and marine habitats. We find increases in body size coupled with increases in strength of selection and decreases in variance following invasions of marine habitats but not of semiaquatic habitats. A model combining constraints from thermoregulation and lung capacity provides a physiological explanation for the larger minimum and average sizes of marine species. It appears that constraints on maximum size are shared across Crocodyliformes, perhaps through factors such as the allometric scaling of feeding rate versus basal metabolism with body size. These findings suggest that broad-scale patterns of body size evolution and the shapes of body size distributions within higher taxa are often determined more by physiological constraints than by ecological interactions or environmental fluctuations.

Energetic tradeoffs control the size distribution of aquatic mammals.

Four extant lineages of mammals have invaded and diversified in the water: Sirenia, Cetacea, Pinnipedia, and Lutrinae. Most of these aquatic clades are larger bodied, on average, than their closest land-dwelling relatives, but the extent to which potential ecological, biomechanical, and physiological controls contributed to this pattern remains untested quantitatively. Here, we use previously published data on the body masses of 3,859 living and 2,999 fossil mammal species to examine the evolutionary trajectories of body size in aquatic mammals through both comparative phylogenetic analysis and examination of the fossil record. Both methods indicate that the evolution of an aquatic lifestyle is driving three of the four extant aquatic mammal clades toward a size attractor at ∼500 kg. The existence of this body size attractor and the relatively rapid selection toward, and limited deviation from, this attractor rule out most hypothesized drivers of size increase. These three independent body size increases and a shared aquatic optimum size are consistent with control by differences in the scaling of energetic intake and cost functions with body size between the terrestrial and aquatic realms. Under this energetic model, thermoregulatory costs constrain minimum size, whereas limitations on feeding efficiency constrain maximum size. The optimum size occurs at an intermediate value where thermoregulatory costs are low but feeding efficiency remains high. Rather than being released from size pressures, water-dwelling mammals are driven and confined to larger body sizes by the strict energetic demands of the aquatic medium.

Melanin concentration gradients in modern and fossil feathers.

In birds and feathered non-avian dinosaurs, within-feather pigmentation patterns range from discrete spots and stripes to more subtle patterns, but the latter remain largely unstudied. A ∼55 million year old fossil contour feather with a dark distal tip grading into a lighter base was recovered from the Fur Formation in Denmark. SEM and synchrotron-based trace metal mapping confirmed that this gradient was caused by differential concentration of melanin. To assess the potential ecological and phylogenetic prevalence of this pattern, we evaluated 321 modern samples from 18 orders within Aves. We observed that the pattern was found most frequently in distantly related groups that share aquatic ecologies (e.g. waterfowl Anseriformes, penguins Sphenisciformes), suggesting a potential adaptive function with ancient origins.