Deciphering and dating the red panda's ancestry and early adaptive radiation of Musteloidea

Abstract

Few species have been of more disputed affinities than the red or lesser panda (Ailurus fulgens), an endangered endemic Southeast Asian vegetarian member of the placental mammalian order Carnivora. This peculiar carnivoran has mostly been classified with raccoons (Procyonidae) or bears (Ursidae), grouped with the giant panda (Ailuropoda melanoleuca) in their own family, or considered a separate lineage of equivocal ancestry. Recent molecular studies have indicated a close affinity of the red panda to a clade of procyonids and mustelids (weasels, otters, martens, badgers, and allies), but have failed to unambiguously resolve the position of this species relative to mephitids (skunks and stink badgers). We examined the relationship of the red panda to other extant species of the carnivoran suborder Caniformia using a set of concatenated approximately 5.5-kb sequences from protein-coding exons of five nuclear genes. Bayesian, maximum likelihood, and parsimony phylogenetic analyses strongly supported the red panda as the closest living relative of a clade containing Procyonidae and Mustelidae to the exclusion of Mephitidae. These three families together with the red panda (which is classified here as a single extant species of a distinct family, Ailuridae) compose the superfamily Musteloidea, a clade strongly supported by all our phylogenetic analyses as sister to the monophyletic Pinnipedia (seals, sea lions, walruses). The approximately unbiased, Kishino-Hasegawa, and Templeton topology tests rejected (P<0.05) each of all possible alternative hypotheses about the relationships among the red panda and mephitids, procyonids, and mustelids. We also estimated divergence times for the red panda's lineage and ones of other caniform taxa, as well as the ages of the first appearance datums for the crown and total clades of musteloids and the total clades of the red panda, mephitids, procyonids, and mustelids. Bayesian relaxed molecular-clock analysis using combined information from all sampled genes yielded a approximately 42-Myr timescale to caniform evolution and provided evidence of five periods of increased diversification. The red panda's lineage and those of other extant musteloid families are estimated to have diverged during a 3-Myr interval from the mid-Early Oligocene to near the Early/Late Oligocene boundary. We present fossil evidence that extends the early adaptive radiation of the total clade of musteloids to the Eocene-Oligocene transition and also suggests Asia as a center of this radiation.