Adaptive evolution toward larger size in mammals

Abstract

The notion that large body size confers some intrinsic advantage to biological species has been debated for centuries. Using a phylogenetic statistical approach that allows the rate of body size evolution to vary across a phylogeny, we find a long-term directional bias toward increasing size in the mammals. This pattern holds separately in 10 of 11 orders for which sufficient data are available and arises from a tendency for accelerated rates of evolution to produce increases, but not decreases, in size. On a branch-bybranch basis, increases in body size have been more than twice as likely as decreases, yielding what amounts to millions and millions of years of rapid and repeated increases in size away from the small ancestral mammal. These results are the first evidence, to our knowledge, from extant species that are compatible with Cope's rule: the pattern of body size increase through time observed in the mammalian fossil record. We show that this pattern is unlikely to be explained by several nonadaptive mechanisms for increasing size and most likely represents repeated responses to new selective circumstances. By demonstrating that it is possible to uncover ancient evolutionary trends from a combination of a phylogeny and appropriate statistical models, we illustrate how data from extant species can complement paleontological accounts of evolutionary history, opening up new avenues of investigation for both. macroevolution | adaptive evolution | evolutionary trends | Cope's rule | ancestral state reconstruction T he idea that large size confers some intrinsic advantage has lingered in the psyche of biologists for centuries. Researchers have proposed that bigger body sizes can increase tolerance to environmental extremes (1), reduce mortality (2), and enhance predation success (3), among other advantages. In support of these conjectures, analyses from a range of different taxonomic groups demonstrate that larger individuals within populations have significantly enhanced survival, fecundity, and mating success (4, 5). If these advantages are general and have played out over long time scales, they could explain the existence of Cope's rule (6): a broad trend toward increasing size through time (4, 5, 7).Mammals evolved from a relatively small common ancestor over 165 Ma (8-10) and went on to form one of the largest and most successful vertebrate radiations in Earth's history. Mammals vary greatly in size, spanning almost eight orders of magnitude. This variation implies that some groups have experienced much greater evolutionary change in size from the ancestral form than others. Indeed, the mammalian fossil record provides the clearest evidence in support of Cope's rule over long evolutionary time scales (6,11,12).Despite the paleontological support, evidence for Cope's rule remains elusive from studies of extant data alone (13-15), including studies of the mammals (16). A possible reason for the discrepancy between paleontological and extant data might be that conventional comparative methods for studying tr...

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