Evolution of diet in extant marsupials: emergent patterns from a broad phylogenetic perspective

Abstract

Extant marsupials are highly diverse, both morphologically and ecologically. As a key ecological factor, diet has been studied in marsupials at the species level. However, a general lack of phylogenetic integration has resulted in macroevolutionary patterns of diet remaining largely unexplored in the group. We review dietary information for extant marsupials and present the results of an evolutionary analysis in an explicit phylogenetic framework. We compiled dietary data from diverse sources, coding characters in four dietary schemes. We reconstructed ancestral states of predominant diet and dietary shifts during marsupial evolution, by using a published, dated phylogeny that includes 193 extant species representing 97% of genera. The ancestral diet was predominant insectivory. Most frequent transitions occurred towards carnivory, since the late Eocene. By contrast, the shift towards browse herbivory occurred only once, in Australasia, in Diprotodontia, as early as the Palaeocene. The browse herbivorous ancestor gave rise to several other herbivore strategies, as well as to the predominant mycophagy that evolved in Potoroidae. In the Americas, only one extant marsupial clade evolved predominant herbivory (frugivory in Caluromyinae). We found omnivory to be a derived dietary strategy that occurred in both American and Australasian lineages. Temporal and geographic patterns of marsupial dietary diversification appear to be dependent on major palaeoclimatic events and on concurrent diversification of other (placental) clades. The higher frequency of transitions from an insectivorous ancestor towards carnivory might be related to the minor anatomical, physiological and molecular changes required by a transition within an animalivory (protein-based) dietary gradient, in contrast with major changes required by shifts towards herbivory (carbohydrate-based diet). The contrasting evolutionary patterns of diet between marsupials in the Americas and Australasia may be explained, at least partially, by the radically different faunas with which marsupials from each region interacted during their parallel evolutionary history.