Kyle J. Shaney

The Burmese python genome reveals the molecular basis for extreme adaptation in snakes

Significance The molecular basis of morphological and physiological adaptations in snakes is largely unknown. Here, we study these phenotypes using the genome of the Burmese python (Python molurus bivittatus), a model for extreme phenotypic plasticity and metabolic adaptation. We discovered massive rapid changes in gene expression that coordinate major changes in organ size and function after feeding. Many significantly responsive genes are associated with metabolism, development, and mammalian diseases. A striking number of genes experienced positive selection in ancestral snakes. Such genes were related to metabolism, development, lungs, eyes, heart, kidney, and skeletal structure—all highly modified features in snakes. Snake phenotypic novelty seems to be driven by the system-wide coordination of protein adaptation, gene expression, and changes in genome structure. Snakes possess many extreme morphological and physiological adaptations. Identification of the molecular basis of these traits can provide novel understanding for vertebrate biology and medicine. Here, we study snake biology using the genome sequence of the Burmese python (Python molurus bivittatus), a model of extreme physiological and metabolic adaptation. We compare the python and king cobra genomes along with genomic samples from other snakes and perform transcriptome analysis to gain insights into the extreme phenotypes of the python. We discovered rapid and massive transcriptional responses in multiple organ systems that occur on feeding and coordinate major changes in organ size and function. Intriguingly, the homologs of these genes in humans are associated with metabolism, development, and pathology. We also found that many snake metabolic genes have undergone positive selection, which together with the rapid evolution of mitochondrial proteins, provides evidence for extensive adaptive redesign of snake metabolic pathways. Additional evidence for molecular adaptation and gene family expansions and contractions is associated with major physiological and phenotypic adaptations in snakes; genes involved are related to cell cycle, development, lungs, eyes, heart, intestine, and skeletal structure, including GRB2-associated binding protein 1, SSH, WNT16, and bone morphogenetic protein 7. Finally, changes in repetitive DNA content, guanine-cytosine isochore structure, and nucleotide substitution rates indicate major shifts in the structure and evolution of snake genomes compared with other amniotes. Phenotypic and physiological novelty in snakes seems to be driven by system-wide coordination of protein adaptation, gene expression, and changes in the structure of the genome.

Conservation challenges regarding species status assessments in biogeographically complex regions: examples from overexploited reptiles of Indonesia

IUCN Red List assessments are important for conservation and management initiatives. However, status assessments are often challenging because of poor sampling between biogeographical regions. Researchers sometimes assess poorly known species, which can have unforeseen ramifications, including the trade of rare and cryptic species under common species names. Here, we address this issue in relation to economically important reptile species in Indonesia. We reviewed examples of single species categorized as Least Concern for which the assessments probably encompassed multiple closely related species. We also examined Red List assessments that utilized species distribution modelling techniques, and identified biogeography as a major barrier to using such methods. To test how biogeography may affect status assessments we used our own model lizard system from Indonesia, taking an integrative phylogeographical approach to quantify status assessments under contrasting scenarios. We show that failure to account for biogeographical breaks leads to significant variation in Red List status. Our model system fluctuates from Least Concern to Endangered, depending upon whether biogeographical boundaries are considered in taxonomic evaluations. We identify Sauria (lizards) and Serpentes (snakes) as major lineages requiring taxonomic and conservation attention in Indonesia. We also make the following recommendations: (1) Indonesias trade quotas should further subdivide management zones to account for gaps in taxonomic evaluations; (2) genetic sampling should be considered a high priority during wildlife exportation processes from poorly studied geographical areas; and (3) continuation of thorough biological inventory is critical for conservation initiatives across heterogeneous mountain and island landscapes.

Coalescent species delimitation of a Sumatran parachuting frog

We conduct species delimitation of the widespread parachuting frog species Rhacophorus catamitus using samples from across the island of Sumatra, Indonesia. We use mitochondrial, genomic and morphological data, and find that R. catamitus is composed of three lineages corresponding to northern, central and southern lineages. Mitochondrial and genomic data show admixture or incomplete lineage sorting between the central and southern lineages, but deep divergence from the northern lineage. Coalescent species delimitation supports a three species model for this complex, and we recommend that the northern lineage be described as a new species. Our study highlights the power of coalescent species delimitation in an integrative framework for identifying unrecognised diversity in understudied tropical species complexes. We also emphasise the evolutionary importance of northern Sumatra, a region that harboured montane refugia during Pliocene–Pleistocene climate change, but has also been heavily affected by volcanic activity.

Endemic Dragons of Sumatra's Volcanoes: New Species of Dendragama (Squamata: Agamidae) and Status of Salea rosaceum Thominot

Abstract: We discovered new populations of Dendragama at the northern and southern ends of Sumatra. High genetic distances and concordance of multiple, apparently independent diagnostic characters support our descriptions of these two populations as new species. We define new characters of the sublabial, tympanic, dorsal crest, and dorsolateral crest scales. The three species of Dendragama undergo remarkable color change in response to time of day and stress. Females lay 2–4 ovoid eggs, reach sexual maturity at about 60 mm snout–vent length, and likely produce multiple clutches each year. We remove Salea rosaceum Thominot from the synonymy of Dendragama boulengeri and argue that the unique holotype of S. rosaceum is a specimen of Pseudocalotes tympanistriga with incorrect locality information.

Taxonomic Status of the Sumatran Pitviper Trimeresurus (Popeia) toba David, Petri, Vogel & Doria, 2009 (Squamata: Viperidae) and Other Sunda Shelf Species of the Subgenus Popeia

Abstract The pitviper Trimeresurus (Popeia) toba was described on the basis of slight morphological differences between six specimens collected in northern Sumatra and the other recognized species of Trimeresurus (Popeia) from the Sunda Shelf. In January 2014, we collected two additional specimens of T. (P.) toba from Sumatra and located a third unexamined specimen at the Museum Zoologicum Bogoriense. We compared molecular and morphological data generated from these specimens with existing data for T. (P.) toba and the other Sunda Shelf Trimeresurus (Popeia). Our findings indicate that T. (P.) toba is indistinguishable from T. (P.) barati, the other species that occurs on Sumatra. Additionally, with the exception of T. (P.) nebularis, all currently recognized species of Trimeresurus (Popeia) from the Sunda Shelf are minimally divergent and the morphological characters used to diagnose the individual species broadly overlap. For these reasons, we conclude that all should be considered a single species, T. (P.) sabahi. Abstrak Ular bandotan toba, Trimeresurus (Popeia) toba telah dideskripsikan berdasarkan perbedaan kecil pada morfologi antara enam spesimen dari Sumatera Utara dan spesies lain yang dikenali sebagai Trimeresurus (Popeia) dari Paparan Sunda. Pada bulan Januari 2014, kami mengumpulkan dua spesimen tambahan T. (P.) toba, dan satu spesimen ketiga yang belum diperiksa di Museum Zoologicum Bogoriense. Kami membandingkan data molekuler dan morfologi yang dihasilkan dari spesimen-spesimen baru terhadap data yang ada dari Trimeresurus (Popeia) Paparan Sunda lainnya. Temuan kami menunjukkan bahwa T. (P.) toba tidak dapat dibedakan terhadap T. (P.) barati, spesies lain yang diketahui dari Sumatera. Selain itu, dengan pengecualian pada T. (P.) nebularis, saat ini semua spesies Trimeresurus (Popeia) dari Paparan Sunda berbeda sedikit dan karakter morfologi yang digunakan untuk menentukan individu spesies secara luas tumpang tindih. Untuk alasan ini, kami menyimpulkan bahwa semuanya harus dianggap merupakan spesies tunggal, T. (P.) sabahi.

A suite of potentially amplifiable microsatellite loci for ten reptiles of conservation concern from Africa and Asia

Here we document the addition of thousands of potentially amplifiable microsatellite loci (PALs) and associated primer sequences for public use. We conducted whole-genome shotgun sequencing to obtain ultra-low coverage, random genomic sampling from ten African and Asian squamate reptile species (representing ten genera). We used unique genomic processing methods and generated PALs for the following species: Acrochordus granulatus, Ahaetulla prasina, Cerberus rhynchops, Gonocephalus kuhlii, Ophiophagus hannah, Python bivittatus, Tribolonotus gracilis, Trimeresurus sabahi (Popeia sabahi), Uromastyx geryi and Varanus exanthematicus. All taxa included, as well as other related taxa not included in our study, are exploited heavily by the international skin and pet trades, yet researchers and conservation agencies currently lack substantial genetic resources for guiding conservation and management. Using stringent filtering methods, we generated between 467 and 8641 PALs for each of the ten species (52,164 PALs total), yielding a rich database of microsatellite loci and amplification primers for these taxa. In addition to the ten species targeted in our study, microsatellite markers provided in this database can likely be applied to a variety of closely related taxa that are also of conservation and commercial interest.

Sumatra's Endemic Crested Dragons (Agamidae: Lophocalotes): A New Species from the Bukit Barisan Range, Comments on Lophocalotes ludekingi, and Ecology

Abstract With the use of a concordance and a mitochondrial tree–morphological character congruence approach, we show that recently discovered populations of Lophocalotes represent a new species. Like its only known congener, the new species occurs only on Sumatra in montane forests above 1000 m. The new species differs from L. ludekingi in having more gulars, ventrals, and subdigital lamellae; in having males with a lower nuchal crest not supported by an arched flap of skin and white gular markings; and in having females with cream buccal epithelia. These agamids are slow-moving, arboreal, generalist predators and lay 2–6 eggs, multiple times per year. Lophocalotes exhibits pronounced sexual dimorphism. Interestingly, coloration of the buccal epithelium is sexually dichromatic in the new species. The recently described nematode Spinicauda sumatrana infected most hosts in our sample, and parasite load increased with snout-to-vent length. Lophocalotes is closely related to Dendragama and Pseudocalotes and shares two derived characters with Pseudocophotis sumatrana: a prehensile tail and reduced keels on the subdigital lamellae.

Impacts of anthropogenic pressures on the contemporary biogeography of threatened crocodilians in Indonesia

The Greater Sunda region of South-east Asia supports a rich diversity of economically and ecologically important species. However, human pressures are reshaping contemporary biogeography across the region. Megafaunal distributional patterns have been particularly affected because of deforestation, poaching and human–wildlife conflict. Crocodilians are at the centre of these conflicts in Indonesia and yet remain poorly studied across much of the archipelago. We conducted population surveys of salt-water crocodiles Crocodylus porosus and false gharials Tomistoma schlegelii in Sumatra, and examined whether crocodile abundance and distribution are correlated with variations in human disturbance, fishing pressure, and habitat type. We then used these data to model remaining suitable habitat for T. schlegelii across South-east Asia. We found that abundance of T. schlegelii and C. porosus was correlated with distance from human settlements, and fish-trapping pressure. We recorded the presence of T. schlegelii in a river system in which it was previously unknown, thus expanding the known range of the species. We also found that the predicted remaining suitable habitat for T. schlegelii in Indonesia is largely limited to areas of low human activity. From these empirical and modelling approaches we propose several key conservation priorities: (1) eliminate the use of fish traps in remaining patches of T. schlegelii habitat, (2) prioritize crocodile population surveys in remaining suitable habitat, particularly in remote areas, (3) consider T. schlegelii to be potentially Endangered locally in Sumatra, and (4) expand existing reserves around the Lower Kampar River and Berbak National Park/Sembilang National Park areas of Sumatra.