Tempo of trophic evolution and its impact on mammalian diversification

Abstract

Mammals are characterized by the complex adaptations of their dentition, which are an indication that diet has played a critical role in their evolutionary history. Although much attention has focused on diet and the adaptations of specific taxa, the role of diet in large-scale diversification patterns remains unresolved. Contradictory hypotheses have been proposed, making prediction of the expected relationship difficult. We show that net diversification rate (the cumulative effect of speciation and extinction), differs significantly among living mammals, depending upon trophic strategy. Herbivores diversify fastest, carnivores are intermediate, and omnivores are slowest. The tempo of transitions between the trophic strategies is also highly biased: the fastest rates occur into omnivory from herbivory and carnivory and the lowest transition rates are between herbivory and carnivory. Extant herbivore and carnivore diversity arose primarily through diversification within lineages, whereas omnivore diversity evolved by transitions into the strategy. The ability to specialize and subdivide the trophic niche allowed herbivores and carnivores to evolve greater diversity than omnivores. macroevolution | ecological specialization | character evolution L iving mammals are remarkably diverse: they span eight orders of magnitude in mass, occupy a variety of habitats across the globe, and exploit subterranean, aquatic, terrestrial, arboreal, and aerial niches. Living mammals also show striking differences in diversity between lineages of similar age, from the more than 2,200 species of rodent to the single species of aardvark (1, 2). Early mammals were small, homoeothermic endotherms with tribosphenic molars. Homoeothermic endothermy enabled mammals to survive in a wider range of ambient temperatures and achieve higher sustained activity levels, but it also increased energy demands (3). These increased energetic demands necessitated adaptations or behaviors that either allowed more efficient extraction of energy from the food consumed, entailed consumption of more energy rich foods, or required an increase in the time spent foraging and eating. The tribosphenic molar, which combines shearing and crushing functions in the precisely occluding teeth, is considered to be a key innovation that promoted more effective carnivory and omnivory in early mammalian lineages (4). This type of tooth is also frequently cited as facilitating the diversification of therian mammals (4-6). The tribosphenic molar is an evolutionarily and functionally highly versatile structure (4, 7) that, in combination with heterodonty (different tooth types within the jaw), enabled mammals to evolve a disparate array of specialized dentitions and thus adapt to a broad variety of niches. Indeed, the extraordinary dental diversity of mammals-to the extent that many species can be identified by the morphology of their molars alone (8)-is a testament to the importance of diet to mammalian evolution.Although the adaptations of individual mammalian lineages to d...

The role of ecological opportunity in shaping disparate diversification trajectories in a bicontinental primate radiation

“…This suggests that the decline in speciation rate (table 1; electronic supplementary material, table S5) likely driving the temporal slowdown in lineage accumulation in Asia is associated with increased exploitation of leaves by Asian species. Although generalist herbivores have high rates of net diversification and transition to other trophic niches [82], specialist species are expected to have elevated rates of speciation and extinction owing to increased susceptibility to environmental change [83]. Unique trophic specialists can also have elevated rates of morphological evolution [84].…”

Bayesian hierarchical models suggest oldest known plant-visiting bat was omnivorous

“…The evolution of cusp morphology in response to feeding ecology makes mammalian molars indicators of diet [2,3]. Teeth are so abundant in the fossil record that a substantial portion of extinct mammals are known only from their molars [4].…”

The Geography of Ecological Niche Evolution in Mammals

“…Bats also showed low levels of functional trait distance within their own order (Figure 1), because a large number of bats share the same diet, and therefore harbour trait conservatism (i.e. the tendency for lineages to retain ancestral traits [20,21]). Closely related species can have very divergent traits, especially within Dasyuromorphia (marsupial Carnivores) or Carnivora ( Figure 1).…”