Patterns of maximum body size evolution in Cenozoic land mammals: eco-evolutionary processes and abiotic forcing.

There is accumulating evidence that macroevolutionary patterns of mammal evolution during the Cenozoic follow similar trajectories on different continents. This would suggest that such patterns are strongly determined by global abiotic factors, such as climate, or by basic eco-evolutionary processes such as filling of niches by specialization. The similarity of pattern would be expected to extend to the history of individual clades. Here, we investigate the temporal distribution of maximum size observed within individual orders globally and on separate continents. While the maximum size of individual orders of large land mammals show differences and comprise several families, the times at which orders reach their maximum size over time show strong congruence, peaking in the Middle Eocene, the Oligocene and the Plio-Pleistocene. The Eocene peak occurs when global temperature and land mammal diversity are high and is best explained as a result of niche expansion rather than abiotic forcing. Since the Eocene, there is a significant correlation between maximum size frequency and global temperature proxy. The Oligocene peak is not statistically significant and may in part be due to sampling issues. The peak in the Plio-Pleistocene occurs when global temperature and land mammal diversity are low, it is statistically the most robust one and it is best explained by global cooling. We conclude that the macroevolutionary patterns observed are a result of the interplay between eco-evolutionary processes and abiotic forcing.

Effects of allometry, productivity and lifestyle on rates and limits of body size evolution.

Body size affects nearly all aspects of organismal biology, so it is important to understand the constraints and dynamics of body size evolution. Despite empirical work on the macroevolution and macroecology of minimum and maximum size, there is little general quantitative theory on rates and limits of body size evolution. We present a general theory that integrates individual productivity, the lifestyle component of the slow-fast life-history continuum, and the allometric scaling of generation time to predict a clade's evolutionary rate and asymptotic maximum body size, and the shape of macroevolutionary trajectories during diversifying phases of size evolution. We evaluate this theory using data on the evolution of clade maximum body sizes in mammals during the Cenozoic. As predicted, clade evolutionary rates and asymptotic maximum sizes are larger in more productive clades (e.g. baleen whales), which represent the fast end of the slow-fast lifestyle continuum, and smaller in less productive clades (e.g. primates). The allometric scaling exponent for generation time fundamentally alters the shape of evolutionary trajectories, so allometric effects should be accounted for in models of phenotypic evolution and interpretations of macroevolutionary body size patterns. This work highlights the intimate interplay between the macroecological and macroevolutionary dynamics underlying the generation and maintenance of morphological diversity.

The maximum rate of mammal evolution.

How fast can a mammal evolve from the size of a mouse to the size of an elephant? Achieving such a large transformation calls for major biological reorganization. Thus, the speed at which this occurs has important implications for extensive faunal changes, including adaptive radiations and recovery from mass extinctions. To quantify the pace of large-scale evolution we developed a metric, clade maximum rate, which represents the maximum evolutionary rate of a trait within a clade. We applied this metric to body mass evolution in mammals over the last 70 million years, during which multiple large evolutionary transitions occurred in oceans and on continents and islands. Our computations suggest that it took a minimum of 1.6, 5.1, and 10 million generations for terrestrial mammal mass to increase 100-, and 1,000-, and 5,000-fold, respectively. Values for whales were down to half the length (i.e., 1.1, 3, and 5 million generations), perhaps due to the reduced mechanical constraints of living in an aquatic environment. When differences in generation time are considered, we find an exponential increase in maximum mammal body mass during the 35 million years following the Cretaceous-Paleogene (K-Pg) extinction event. Our results also indicate a basic asymmetry in macroevolution: very large decreases (such as extreme insular dwarfism) can happen at more than 10 times the rate of increases. Our findings allow more rigorous comparisons of microevolutionary and macroevolutionary patterns and processes.

The evolution of maximum body size of terrestrial mammals.

The extinction of dinosaurs at the Cretaceous/Paleogene (K/Pg) boundary was the seminal event that opened the door for the subsequent diversification of terrestrial mammals. Our compilation of maximum body size at the ordinal level by sub-epoch shows a near-exponential increase after the K/Pg. On each continent, the maximum size of mammals leveled off after 40 million years ago and thereafter remained approximately constant. There was remarkable congruence in the rate, trajectory, and upper limit across continents, orders, and trophic guilds, despite differences in geological and climatic history, turnover of lineages, and ecological variation. Our analysis suggests that although the primary driver for the evolution of giant mammals was diversification to fill ecological niches, environmental temperature and land area may have ultimately constrained the maximum size achieved.

Lower extinction risk in sleep-or-hide mammals.

An ever larger proportion of Earth's biota is affected by the current accelerating environmental change. The mismatches between organisms and their environments are now increasing in both magnitude and frequency, resulting in lowered fitness and hence the decline of populations. Under this scenario, species with behavioral and/or physiological traits that provide them shelter from the environment are predicted to be less vulnerable to population declines than species that are always exposed to the elements. Here, we coded 4,536 living mammal species for sleep-or-hide (SLOH) behavior, including hibernation, torpor, and the use of burrows, among other related traits. We demonstrate that species that exhibit SLOH behavior are underrepresented in high-risk International Union for Conservation of Nature Red List categories. We found that SLOH behavior contributes to lowering extinction risk even after we accounted for other factors that directly or indirectly buffer species against extinction, such as larger geographic ranges and smaller body sizes. This result is robust to analyses using phylogenetically independent contrasts. Sleep-or-hide behavior, made possible by a related suite of physiological adaptations, allows mammals to function at lower metabolic rates and/or buffer them from changing physical elements. Mammals with SLOH behavior have a greater propensity to survive in the current extinction crisis and probably also in past crises because of reduced exposure to environmental stress.

Higher origination and extinction rates in larger mammals.

Do large mammals evolve faster than small mammals or vice versa? Because the answer to this question contributes to our understanding of how life-history affects long-term and large-scale evolutionary patterns, and how microevolutionary rates scale-up to macroevolutionary rates, it has received much attention. A satisfactory or consistent answer to this question is lacking, however. Here, we take a fresh look at this problem using a large fossil dataset of mammals from the Neogene of the Old World (NOW). Controlling for sampling biases, calculating per capita origination and extinction rates of boundary-crossers and estimating survival probabilities using capture-mark-recapture (CMR) methods, we found the recurring pattern that large mammal genera and species have higher origination and extinction rates, and therefore shorter durations. This pattern is surprising in the light of molecular studies, which show that smaller animals, with their shorter generation times and higher metabolic rates, have greater absolute rates of evolution. However, higher molecular rates do not necessarily translate to higher taxon rates because both the biotic and physical environments interact with phenotypic variation, in part fueled by mutations, to affect origination and extinction rates. To explain the observed pattern, we propose that the ability to evolve and maintain behavior such as hibernation, torpor and burrowing, collectively termed "sleep-or-hide" (SLOH) behavior, serves as a means of environmental buffering during expected and unexpected environmental change. SLOH behavior is more common in some small mammals, and, as a result, SLOH small mammals contribute to higher average survivorship and lower origination probabilities among small mammals.