Whence the red panda?

The evolutionary history of the red panda (Ailurus fulgens) plays a pivotal role in the higher-level phylogeny of the "bear-like" arctoid carnivoran mammals. Characters from morphology and molecules have provided inconsistent evidence for placement of the red panda. Whereas it certainly is an arctoid, there has been major controversy about whether it should be placed with the bears (ursids), ursids plus pinnipeds (seals, sea lions, walrus), raccoons (procyonids), musteloids (raccoons plus weasels, skunks, otters, and badgers [mustelids]), or as a monotypic lineage of uncertain phylogenetic affinities. Nucleotide sequence data from three mitochondrial genes and one nuclear intron were analyzed, with more complete taxonomic sampling of relevant taxa (arctoids) than previously available in analyses of primary molecular data, to clarify the phylogenetic relationships of the red panda to other arctoid carnivorans. This study provides detailed phylogenetic analyses (both parsimony and maximum-likelihood) of primary character data for arctoid carnivorans, including bootstrap and decay indices for all arctoid nodes, and three statistical tests of alternative phylogenetic hypotheses for the placement of the red panda. Combined phylogenetic analyses reject the hypotheses that the red panda is most closely related to the bears (ursids) or to the raccoons (procyonids). Rather, evidence from nucleotide sequences strongly support placement of the red panda within a broad Musteloidea (sensu lato) clade, including three major lineages (the red panda, the skunks [mephitids], and a clearly monophyletic clade of procyonids plus mustelids [sensu stricto, excluding skunks]). Within the Musteloidea, interrelationships of the three major lineages are unclear and probably are best considered an unresolved trichotomy. These data provide compelling evidence for the relationships of the red panda and demonstrate that small taxonomic sample sizes can result in misleading or possibly erroneous (based on prior modeling, as well as conflict between the results of our analyses of less and more complete data sets) conclusions about phylogenetic relationships and taxonomy.

Flynn JJ ，Nedbal MA ，Dragoo JW ，Honeycutt RL ... -  《MOLECULAR PHYLOGENETICS AND EVOLUTION》

Molecular phylogeny of the carnivora (mammalia): assessing the impact of increased sampling on resolving enigmatic relationships.

This study analyzed 76 species of Carnivora using a concatenated sequence of 6243 bp from six genes (nuclear TR-i-I, TBG, and IRBP; mitochondrial ND2, CYTB, and 12S rRNA), representing the most comprehensive sampling yet undertaken for reconstructing the phylogeny of this clade. Maximum parsimony and Bayesian methods were remarkably congruent in topologies observed and in nodal support measures. We recovered all of the higher level carnivoran clades that had been robustly supported in previous analyses (by analyses of morphological and molecular data), including the monophyly of Caniformia, Feliformia, Arctoidea, Pinnipedia, Musteloidea, Procyonidae + Mustelidae sensu stricto, and a clade of (Hyaenidae + (Herpestidae + Malagasy carnivorans)). All of the traditional "families," with the exception of Viverridae and Mustelidae, were robustly supported as monophyletic groups. We further have determined the relative positions of the major lineages within the Caniformia, which previous studies could not resolve, including the first robust support for the phylogenetic position of marine carnivorans (Pinnipedia) within the Arctoidea (as the sister-group to musteloids [sensu lato], with ursids as their sister group). Within the pinnipeds, Odobenidae (walrus) was more closely allied with otariids (sea lions/fur seals) than with phocids ("true" seals). In addition, we recovered a monophyletic clade of skunks and stink badgers (Mephitidae) and resolved the topology of musteloid interrelationships as: Ailurus (Mephitidae (Procyonidae, Mustelidae [sensu stricto])). This pattern of interrelationships of living caniforms suggests a novel inference that large body size may have been the primitive condition for Arctoidea, with secondary size reduction evolving later in some musteloids. Within Mustelidae, Bayesian analyses are unambiguous in supporting otter monophyly (Lutrinae), and in both MP and Bayesian analyses Martes is paraphyletic with respect to Gulo and Eira, as has been observed in some previous molecular studies. Within Feliformia, we have confirmed that Nandinia is the outgroup to all other extant feliforms, and that the Malagasy Carnivora are a monophyletic clade closely allied with the mongooses (Herpestidae [sensu stricto]). Although the monophyly of each of the three major feliform clades (Viverridae sensu stricto, Felidae, and the clade of Hyaenidae + (Herpestidae + Malagasy carnivorans)) is robust in all of our analyses, the relative phylogenetic positions of these three lineages is not resolvable at present. Our analyses document the monophyly of the "social mongooses," strengthening evidence for a single origin of eusociality within the Herpestidae. For a single caniform node, the position of pinnipeds relative to Ursidae and Musteloidea, parsimony analyses of data for the entire Carnivora did not replicate the robust support observed for both parsimony and Bayesian analyses of the caniform ingroup alone. More detailed analyses and these results demonstrate that outgroup choice can have a considerable effect on the strength of support for a particular topology. Therefore, the use of exemplar taxa as proxies for entire clades with diverse evolutionary histories should be approached with caution. The Bayesian analysis likelihood functions generally were better able to reconstruct phylogenetic relationships (increased resolution and more robust support for various nodes) than parsimony analyses when incompletely sampled taxa were included. Bayesian analyses were not immune, however, to the effects of missing data; lower resolution and support in those analyses likely arise from non-overlap of gene sequence data among less well-sampled taxa. These issues are a concern for similar studies, in which different gene sequences are concatenated in an effort to increase resolving power.

Flynn JJ ，Finarelli JA ，Zehr S ，Hsu J ，Nedbal MA ... -  《SYSTEMATIC BIOLOGY》

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

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.

Sato JJ ，Wolsan M ，Minami S ，Hosoda T ，Sinaga MH ，Hiyama K ，Yamaguchi Y ，Suzuki H ... -  《-》

Phylogeny of the Carnivora (Mammalia): congruence vs incompatibility among multiple data sets.

The purpose of this study was to determine the higher-level phylogenetic relationships among Carnivora, using a conditional data combination (CDC) approach to analyzing multiple data sets. New nucleotide sequences (851 base pairs from intron I of the transthyretin gene) among 22 representatives of the 11 families of Carnivora were generated and analyzed in concert with, and comparison to, other mitochondrial and morphological character data. Conditional data combination analyses of the four independent data sets (transthyretin intron I, cytochrome b, partial 12S rRNA, and morphology) indicate that the phylogenetic results derived from each generally agree, with two exceptions. The first exception, signal heterogeneity in comparisons involving transthyretin and morphology, provides an example where phylogenetic conclusions drawn from total evidence analyses may differ from conclusions drawn from CDC analyses. The second exception demonstrates that while a CDC method may reject the null hypothesis of homogeneity for a particular partition, including that partition in combined analyses, may nevertheless provide an overall increase in phylogenetic signal, in terms of nodal support for most associations, without altering the topology derived from the combined homogeneous data partitions. Phylogenetic reconstruction among the feliform families supports a sister-group relationship between the hyaenas (Hyaenidae) and mongooses (Herpestidae) and places the African palm civet (Nandinia) as basal to all other living Feliformia. Among the caniform families, CDC analyses strongly support the previously enigmatic red panda (Ailurus) as a monotypic lineage that is sister to Musteloidea sensu stricto (mustelids plus procyonids), in addition to pinniped monophyly and a sister-group relationship between the walrus and sea lions.

Flynn JJ ，Nedbal MA 《MOLECULAR PHYLOGENETICS AND EVOLUTION》

Higher level relationships of the arctoid Carnivora based on sequence data and "total evidence".

The relationships of the lesser or red panda, Ailurus, have remained elusive even as any doubts about the identity of the giant panda as a bear have been erased. While usually classified as a member of the Procyonidae (raccoons), recent anatomical studies have suggested that the red panda may not fall in any of the arctoid carnivore families but instead may reflect an early offshoot of the lineage leading to ursids (bears) and pinnipeds (seals, sea lions, and walruses). Sequence data from the cytochrome b and 12S genes for multiple representatives of all relevant families support this hypothesis. Such a systematic position makes this threatened species particularly worthy of conservation. Sequence data alone, as well as a combined analysis of the sequence and anatomical data, strongly support a single origin of pinnipeds and their aquatic adaptations, lending some resolution to the general disagreement about familial relationships in this group. These molecular data also support canids as the basal members of this caniform clade, but are unresolved with respect to whether mustelids or procyonids constitute the sister group to the (ursid, pinniped, Ailurus) clade. There is support for the notion that skunks are a genetically divergent and possibly nonmustelid lineage.

Vrana PB ，Milinkovitch MC ，Powell JR ，Wheeler WC ... -  《MOLECULAR PHYLOGENETICS AND EVOLUTION》