Chromosome-length genome assemblies and cytogenomic analyses of pangolins reveal remarkable chromosome counts and plasticity.

We report the first chromosome-length genome assemblies for three species in the mammalian order Pholidota: the white-bellied, Chinese, and Sunda pangolins. Surprisingly, we observe extraordinary karyotypic plasticity within this order and, in female white-bellied pangolins, the largest number of chromosomes reported in a Laurasiatherian mammal: 2n = 114. We perform the first karyotype analysis of an African pangolin and report a Y-autosome fusion in white-bellied pangolins, resulting in 2n = 113 for males. We employ a novel strategy to confirm the fusion and identify the autosome involved by finding the pseudoautosomal region (PAR) in the female genome assembly and analyzing the 3D contact frequency between PAR sequences and the rest of the genome in male and female white-bellied pangolins. Analyses of genetic variability show that white-bellied pangolins have intermediate levels of genome-wide heterozygosity relative to Chinese and Sunda pangolins, consistent with two moderate declines of historical effective population size. Our results reveal a remarkable feature of pangolin genome biology and highlight the need for further studies of these unique and endangered mammals.

Vertebrate Scavengers Control Abundance of Diarrhea-causing Bacteria in Tropical Plantations.

Scavenging is a common phenomenon, particularly amongst carnivorous vertebrates. By consuming carrion, vertebrate scavengers reduce resource availability for both pathogenic bacteria and their insect vectors. We investigated the ability of wild vertebrate scavengers to control agents of human diarrheal diseases (specifically Salmonella spp. and Shiga toxin-producing Escherichia coli [STEC]) in oil palm plantations in Sabah (East Malaysia), and the existence of spillover effect whereby additional vertebrate scavengers from adjacent forest patches result in greater disease control in plantation sections near these forest edges. Experimental carcasses were removed by common scavengers (Varanus salvator, Canis lupus familiaris, and Viverra tangalunga) at different time points, and this determined the length of time that the carcasses persisted in the environment. The amount of pathogenic bacteria on the surfaces of filth flies collected above the experimental carcasses was positively correlated to the duration of carcass persistence, and reduction in pathogenic bacterial abundances was largely due to carcass consumption by these vertebrate scavengers. Instead of a predicted positive spillover effect (greater scavenger activity near forest edges, hence reduced pathogen abundance), we detected a weak inverse spillover effect in which STEC counts were marginally higher in plantation sections near forest patches, and human hunting along the forest-plantation boundaries could explain this. We propose that making oil palm plantations scavenger-friendly could yield great human health benefits for the millions of workers employed in this rapidly-expanding industry, without drastically changing current management practices.

Genomic analysis reveals hidden biodiversity within colugos, the sister group to primates.

Colugos are among the most poorly studied mammals despite their centrality to resolving supraordinal primate relationships. Two described species of these gliding mammals are the sole living members of the order Dermoptera, distributed throughout Southeast Asia. We generated a draft genome sequence for a Sunda colugo and a Philippine colugo reference alignment, and used these to identify colugo-specific genetic changes that were enriched in sensory and musculoskeletal-related genes that likely underlie their nocturnal and gliding adaptations. Phylogenomic analysis and catalogs of rare genomic changes overwhelmingly support the contested hypothesis that colugos are the sister group to primates (Primatomorpha), to the exclusion of treeshrews. We captured ~140 kb of orthologous sequence data from colugo museum specimens sampled across their range and identified large genetic differences between many geographically isolated populations that may result in a >300% increase in the number of recognized colugo species. Our results identify conservation units to mitigate future losses of this enigmatic mammalian order.

Selective­logging and oil palm: multitaxon impacts, biodiversity indicators, and trade­offs for conservation planning.

Strong global demand for tropical timber and agricultural products has driven large-scale logging and subsequent conversion of tropical forests. Given that the majority of tropical landscapes have been or will likely be logged, the protection of biodiversity within tropical forests thus depends on whether species can persist in these economically exploited lands, and if species cannot persist, whether we can protect enough primary forest from logging and conversion. However, our knowledge of the impact of logging and conversion on biodiversity is limited to a few taxa, often sampled in different locations with complex land-use histories, hampering attempts to plan cost-effective conservation strategies and to draw conclusions across taxa. Spanning a land-use gradient of primary forest, once- and twice-logged forests, and oil palm plantations, we used traditional sampling and DNA metabarcoding to compile an extensive data set in Sabah, Malaysian Borneo for nine vertebrate and invertebrate taxa to quantify the biological impacts of logging and oil palm, develop cost-effective methods of protecting biodiversity, and examine whether there is congruence in response among taxa. Logged forests retained high species richness, including, on average, 70% of species found in primary forest. In contrast, conversion to oil palm dramatically reduces species richness, with significantly fewer primary-forest species than found on logged forest transects for seven taxa. Using a systematic conservation planning analysis, we show that efficient protection of primary-forest species is achieved with land portfolios that include a large proportion of logged-forest plots. Protecting logged forests is thus a cost-effective method of protecting an ecologically and taxonomically diverse range of species, particularly when conservation budgets are limited. Six indicator groups (birds, leaf-litter ants, beetles, aerial hymenopterans, flies, and true bugs) proved to be consistently good predictors of the response of the other taxa to logging and oil palm. Our results confidently establish the high conservation value of logged forests and the low value of oil palm. Cross-taxon congruence in responses to disturbance also suggests that the practice of focusing on key indicator taxa yields important information of general biodiversity in studies of logging and oil palm.

Expression and Evolution of Short Wavelength Sensitive Opsins in Colugos: A Nocturnal Lineage That Informs Debate on Primate Origins.

A nocturnal activity pattern is central to almost all hypotheses on the adaptive origins of primates. This enduring view has been challenged in recent years on the basis of variation in the opsin genes of nocturnal primates. A correspondence between the opsin genes and activity patterns of species in Euarchonta-the superordinal group that includes the orders Primates, Dermoptera (colugos), and Scandentia (treeshrews)-could prove instructive, yet the basic biology of the dermopteran visual system is practically unknown. Here we show that the eye of the Sunda colugo (Galeopterus variegatus) lacks a tapetum lucidum and has an avascular retina, and we report on the expression and spectral sensitivity of cone photopigments. We found that Sunda colugos have intact short wavelength sensitive (S-) and long wavelength sensitive (L-) opsin genes, and that both opsins are expressed in cone photoreceptors of the retina. The inferred peak spectral sensitivities are 451 and 562 nm, respectively. In line with adaptation to nocturnal vision, cone densities are low. Surprisingly, a majority of S-cones coexpress some L-opsin. We also show that the ratio of rates of nonsynonymous to synonymous substitutions of exon 1 of the S-opsin gene is indicative of purifying selection. Taken together, our results suggest that natural selection has favored a functional S-opsin in a nocturnal lineage for at least 45 million years. Accordingly, a nocturnal activity pattern remains the most likely ancestral character state of euprimates.

Gliding saves time but not energy in Malayan colugos.

Gliding is thought to be an economical form of locomotion. However, few data on the climbing and gliding of free-ranging gliding mammals are available. This study employed an animal-borne three-dimensional acceleration data-logging system to collect continuous data on the climbing and gliding of free-ranging Malayan colugos, Galeopterus variegatus. We combined these movement data with empirical estimates of the metabolic costs to move horizontally or vertically to test this long-standing hypothesis by determining whether the metabolic cost to climb to sufficient height to glide a given distance was less than the cost to move an equivalent distance horizontally through the canopy. On average, colugos climb a short distance to initiate glides. However, due to the high energetic cost of climbing, gliding is more energetically costly to move a given horizontal distance than would be predicted for an animal travelling the same distance through the canopy. Furthermore, because colugos spend a small fraction of their time engaged in locomotor activity, the high costs have little effect on their overall energy budget. As a result, the energetic economy hypothesis for the origins of gliding is not supported. It is likely that other ecologically relevant factors have played a greater role in the origins of gliding in colugos and other mammals.

Take-off and landing kinetics of a free-ranging gliding mammal, the Malayan colugo (Galeopterus variegatus).

Arboreal animals negotiate a highly three-dimensional world that is discontinuous on many spatial scales. As the scale of substrate discontinuity increases, many arboreal animals rely on leaping or gliding locomotion between distant supports. In order to successfully move through their habitat, gliding animals must actively modulate both propulsive and aerodynamic forces. Here we examined the take-off and landing kinetics of a free-ranging gliding mammal, the Malayan colugo (Galeopterus variegatus) using a custom-designed three-dimensional accelerometry system. We found that colugos increase the propulsive impulse to affect longer glides. However, we also found that landing forces are negatively associated with glide distance. Landing forces decrease rapidly as glide distance increases from the shortest glides, then level off, suggesting that the ability to reorient the aerodynamic forces prior to landing is an important mechanism to reduce velocity and thus landing forces. This ability to substantially alter the aerodynamic forces acting on the patagial wing in order to reorient the body is a key to the transition between leaping and gliding and allows gliding mammals to travel long distances between trees with reduced risk of injury. Longer glides may increase the access to distributed resources and reduce the exposure to predators in the canopy or on the forest floor.

The hog-badger is not an edentate: systematics and evolution of the genus Arctonyx (Mammalia: Mustelidae).

Hog-badgers (mustelid carnivorans classified in the genus Arctonyx) are distributed throughout East and Southeast Asia, including much of China, the eastern Indian Subcontinent, Indochina and the large continental Asian island of Sumatra. Arctonyx is usually regarded as monotypic, comprising the single species A. collaris F. Cuvier, 1825, but taxonomic boundaries in the genus have never been revised on the basis of sizeable series from throughout this geographical range. Based on a review of most available specimens in world museums, we recognize three distinctive species within the genus, based on craniometric analyses, qualitative craniodental features, external comparisons, and geographical and ecological considerations. Arctonyx albogularis (Blyth, 1853) is a shaggy-coated, medium-sized badger widely distributed in temperate Asia, from Tibet and the Himalayan region to eastern and southern China. Arctonyx collaris F. Cuvier, 1825, is an extremely large, shorter-haired badger, distributed throughout Southeast Asia, from eastern India to Myanmar, Thailand, Vietnam, Cambodia and Laos. The world's largest extant badger, A. collaris co-occurs with A. albogularis in eastern India and probably in southern China, and fossil comparisons indicate that its geographical range may have extended into central China in the middle Pleistocene. The disjunctly distributed species Arctonyx hoevenii (Hubrecht, 1891), originally described within the order 'Edentata' by a remarkable misunderstanding, is the smallest and darkest member of the genus and is endemic to the Barisan mountain chain of Sumatra. Apart from A. hoevenii, no other Arctonyx occurs on the Sunda Shelf below peninsular Thailand. The natural history of each species of Arctonyx, so far as is known, is briefly reviewed. No claim to original US Government works.