The giant panda genome codes for all necessary enzymes associated with a carnivorous digestive system but lacks genes for enzymes needed to digest cellulose, the principal component of their bamboo diet. It has been posited that this iconic species must therefore possess microbial symbionts capable of metabolizing cellulose, but these symbionts have remained undetected. Here we examined 5,522 prokaryotic ribosomal RNA gene sequences in wild and captive giant panda fecal samples. We found lower species richness of the panda microbiome than of mammalian microbiomes for herbivores and nonherbivorous carnivores. We detected 13 operational taxonomic units closely related to Clostridium groups I and XIVa, both of which contain taxa known to digest cellulose. Seven of these 13 operational taxonomic units were unique to pandas compared with other mammals. Metagenomic analysis using ∼37-Mbp contig sequences from gut microbes recovered putative genes coding two cellulose-digesting enzymes and one hemicellulose-digesting enzyme, cellulase, β-glucosidase, and xylan 1,4-β-xylosidase, in Clostridium group I. Comparing glycoside hydrolase profiles of pandas with those of herbivores and omnivores, we found a moderate abundance of oligosaccharide-degrading enzymes for pandas (36%), close to that for humans (37%), and the lowest abundance of cellulases and endohemicellulases (2%), which may reflect low digestibility of cellulose and hemicellulose in the panda's unique bamboo diet. The presence of putative cellulose-digesting microbes, in combination with adaptations related to feeding, physiology, and morphology, show that giant pandas have evolved a number of traits to overcome the anatomical and physiological challenge of digesting a diet high in fibrous matter.
The panda lineage dates back to the late Miocene and ultimately leads to only one extant species, the giant panda (Ailuropoda melanoleuca). Although global climate change and anthropogenic disturbances are recognized to shape animal population demography their contribution to panda population dynamics remains largely unknown. We sequenced the whole genomes of 34 pandas at an average 4.7-fold coverage and used this data set together with the previously deep-sequenced panda genome to reconstruct a continuous demographic history of pandas from their origin to the present. We identify two population expansions, two bottlenecks and two divergences. Evidence indicated that, whereas global changes in climate were the primary drivers of population fluctuation for millions of years, human activities likely underlie recent population divergence and serious decline. We identified three distinct panda populations that show genetic adaptation to their environments. However, in all three populations, anthropogenic activities have negatively affected pandas for 3,000 years.
The giant panda (Ailuropoda melanoleuca) is currently threatened by habitat loss, fragmentation, and human persecution. Its dietary specialization, habitat isolation, and reproductive constraints have led to a perception that this is a species at an "evolutionary dead end," destined for deterministic extinction in the modern world. Here we examine this perception by a comprehensive investigation of its genetic diversity, population structure, and demographic history across its geographic range. We present analysis of 655 base pairs of mitochondrial (mt) control region (CR) DNA and 10 microsatellite loci for samples from its 5 extant mountain populations (Qinling, Minshan, Qionglai, Liangshan, and Lesser Xiangling). Surprisingly, extant populations display average to high levels of CR and microsatellite diversity compared with other bear species. Genetic differentiation among populations was significant in most cases but was markedly higher between Qinling and the other mountain ranges, suggesting, minimally, that the Qinling population should comprise a separate management unit for conservation purposes. Recent demographic inference using microsatellite markers demonstrated a clear genetic signature for population decline starting several thousands years ago or even further back in the past, and being accelerated and enhanced by the expansion of human populations. Importantly, these data suggest that the panda is not a species at an evolutionary "dead end," but in common with other large carnivores, has suffered demographically at the hands of human pressure. Conservation strategies should therefore focus on the restoration and protection of wild habitat and the maintenance of the currently substantial regional genetic diversity, through active management of disconnected populations.
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