Evolutionary and phylogenetic insights from a nuclear genome sequence of the extinct, giant, “subfossil” koala lemur Megaladapis edwardsi

No endemic Madagascar animal with body mass >10 kg survived a relatively recent wave of extinction on the island. From morphological and isotopic analyses of skeletal “subfossil” remains we can reconstruct some of the biology and behavioral ecology of giant lemurs (primates; up to ∼160 kg) and other extraordinary Malagasy megafauna that survived into the past millennium. Yet, much about the evolutionary biology of these now-extinct species remains unknown, along with persistent phylogenetic uncertainty in some cases. Thankfully, despite the challenges of DNA preservation in tropical and subtropical environments, technical advances have enabled the recovery of ancient DNA from some Malagasy subfossil specimens. Here, we present a nuclear genome sequence (∼2× coverage) for one of the largest extinct lemurs, the koala lemur Megaladapis edwardsi (∼85 kg). To support the testing of key phylogenetic and evolutionary hypotheses, we also generated high-coverage nuclear genomes for two extant lemurs, Eulemur rufifrons and Lepilemur mustelinus, and we aligned these sequences with previously published genomes for three other extant lemurs and 47 nonlemur vertebrates. Our phylogenetic results confirm that Megaladapis is most closely related to the extant Lemuridae (typified in our analysis by E. rufifrons) to the exclusion of L. mustelinus, which contradicts morphology-based phylogenies. Our evolutionary analyses identified significant convergent evolution between M. edwardsi and an extant folivore (a colobine monkey) and an herbivore (horse) in genes encoding proteins that function in plant toxin biodegradation and nutrient absorption. These results suggest that koala lemurs were highly adapted to a leaf-based diet, which may also explain their convergent craniodental morphology with the small-bodied folivore Lepilemur.

Digestive Adaptations of Both the Fore- and Hind-gut in a Temperate Colobine Monkey

Background: In mammal herbivores, the digestion of fiber usually occurs predominantly in either the foregut or in the hindgut. However, how both gut regions function synergistically in the digestion of fiber and other nutrients has rarely been reported in wild mammals. This requires an integrative study of host anatomy, physiology and gut microbiome. Colobine monkeys (Colobinae) are folivorous, with fiber fermentation primarily occurring in the foregut, with residual fermentation in the hindgut. For the few colobine species that live in temperate regions obtaining energy from fiber during winter is critical but the mechanisms enabling this remain unclear. Results: We studied microbial and morphological digestive adaptations of golden snub-nosed monkeys (GSMs), Rhinopithecus roxellana, a temperate forest colobine from central China. We tested for synergistic foregut and hindgut fiber digestion in a species that experiences high thermal energy demands while restricted to a fibrous, low-energy winter diet. We found that the GSM’s colon has a significantly greater volume than that of other foregut fermenting colobines, and both gut regions of GSMs are dominated by microbial taxa producing enzymes to enable active digestion of complex carbohydrates. The microbiomes of the fore- and hindgut differed significantly in composition and abundance. Although the expression of microbial gene functions for fiber digestion were higher in the foregut than in the hindgut, our microbiome analysis in conjunction with that for morphology, enzyme activity and fiber-protein digestion, suggests complementary fiber and protein metabolism in both gut regions. Conclusions: Our results support that both the GSM fore- and hindgut facilitate fiber digestion, with an enlarged colon consistent as an adaptation to accommodate high throughput of fiber-rich food during winter.

Dietary interpretation and paleoecology of herbivores from Pikermi and Samos (late Miocene of Greece)

A large sample of the Pikermi and Samos ungulates was examined by microwear analysis using a light stereomicroscope (561 extinct and 809 extant comparative specimens). The results were used to infer the dietary adaptations of individual species and to evaluate the Pikermian Biome ungulate fauna. Many of the bovids have wear consistent with mixed feeding, although a few mesodont taxa apparently enjoyed an exclusive browsing and or grazing diet. The giraffids spanned the entire dietary spectrum of browsing, mixed feeding, and grazing, but most of the three-toed horses (Hippotherium) were hypsodont grazers. The colobine monkey Mesopithecus pentelici displays microwear consistent with a mixed fruit and leaf diet most likely including some hard objects. Similar results were obtained from prior scanning electron microscopy microwear studies at 500 times magnification and from the light microscope method at 35 times magnification for the same species. Results show that diet can differ between species that have very similar gross tooth morphology. Our results also suggest that the Pikermian Biome was most likely a woodland mosaic that provided a diversity of opportunities for species that depended on browsing as well as species that ate grass. The grasses were most likely C3 grasses that would grow in shaded areas of the woodland, glades, and margins of water. The ungulate component of the Pikermi and Samos fauna was more species-rich and more diverse in diet than the ungulates observed in modern African forests, woodlands, or savannas, yet dietarily most similar to the ungulates found in woodland elements of India and to some extent of Africa. It is unlikely that the Pikermi and Samos ungulates inhabited dense forests because we find no evidence for heavy fruit browsing. Conversely, a pure savanna is unlikely because many mixed feeders are present as well as browsers. Extant woodland African species are morphologically and trophically very similar to the African savanna species. Therefore the evolution of grazing and of hypsodont morphology for Africa may have evolved within the Plio-Pleistocene woodlands of Africa. Our results show that major dietary and morphologic ungulate evolution may take place within woodlands rather than as a consequence of species moving into savannas both during the late Miocene of Pikermi and Samos and during the Pleistocene–Recent of Central Africa.