Conservation genetics of the white-bellied pangolin in West Africa: A story of lineage admixture, declining demography, and wide sourcing by urban bushmeat markets.

During the last 40 years, the volumes of African pangolins feeding the illegal wildlife trade have dramatically increased. We conducted a conservation genetics survey of the most traded African species, the white bellied pangolin (WBP; Phataginus tricuspis), across three West African countries including Guinea, Côte d'Ivoire, and Ghana. Our study combining mitochondrial DNA sequencing and microsatellite genotyping is the first to reveal a wide pattern of admixture between two of the six mitochondrial lineages as previously delimited within WBP. We found a signature of isolation by distance but a lack of population genetic structuring, supporting the idea that WBP may have underestimated dispersal abilities. Levels of genetic diversity were low in West African lineages (WAfr and Gha) compared to Central Africa, reinforcing the picture of genetic pauperization shared by West African WBP. We observed a 85%-98% decline in the effective population size of WBP occurring c. 3200 to 400 ya, with current numbers (520-590) at the lower end of the conservative thresholds for minimum viable population size. The microsatellite markers were powerful enough to differentiate between individuals and identify replicated samples, confirming the utility of this approach in tracing the pangolin trade. Genetic diversity estimates confirmed that Yopougon, the main bushmeat market from Abidjan (Côte d'Ivoire), was fed by a large trade network as confirmed by vendors reporting 10 different sources situated 62-459 km away from the market. We conclude that WBP distributed in the Upper Guinean Block should be considered a single management unit of high conservation concern, as impacted by genetic diversity erosion, drastic decline in effective population size, and wide range sourcing for feeding urban bushmeat markets. Given the genetic admixture pattern detected within WBP from West Africa, we advocate for a multi-locus strategy to trace the international trade of the species.

Au cours des 40 dernières années, les volumes de pangolins africains alimentant le commerce illégal d'espèces sauvages ont augmenté de façon spectaculaire. Nous avons mené une étude de génétique de la conservation sur l'espèce africaine la plus braconnée, le pangolin à ventre blanc (PVB; Phataginus tricuspis), à travers trois pays d'Afrique de l'Ouest incluant la Guinée, la Côte d'Ivoire et le Ghana. Notre étude combinant le séquençage de l'ADN mitochondrial et le génotypage par microsatellites est la première à révéler un patron généralisé d'admixture entre deux des six lignées mitochondriales précédemment délimitées au sein du PVB. Nous mettons en évidence une signature d'isolement par la distance mais un manque de structuration génétique des populations, soutenant l'idée que le PVB a des capacités de dispersion jusque­là sous­estimées. Les niveaux de diversité génétique observés dans les lignées d'Afrique de l'Ouest (WAfr et Gha) sont faibles par rapport à ceux observés en Afrique Centrale, confirmant la paupérisation génétique des populations de PVB en Afrique de l'Ouest. Nous avons observé un déclin de 85 à 98% de la taille efficace de la population ouest­africaine entre 3200 et 400 ans, les estimations actuelles (520­590) se situant à l'extrémité inférieure des seuils minimums de viabilité. Les marqueurs microsatellites utilisés sont suffisamment puissants pour différencier les individus et identifier les doublons d'échantillons, confirmant l'utilité de ces marqueurs pour tracer le commerce des pangolins. Nos estimations de diversité génétique ont confirmé que Yopougon, le principal marché de viande de brousse d'Abidjan (Côte d'Ivoire), était alimenté par un vaste réseau commercial, comme le confirment les vendeurs signalant 10 sources différentes situées à 62­459 km du marché. Nous concluons que les PVB présents dans le bloc forestier de Haute Guinée devraient être considérés comme une seule unité de gestion à fort intérêt de conservation, étant soumis à une érosion de sa diversité génétique, un déclin drastique de la taille efficace de sa population et un approvisionnement à grande échelle des marchés urbains de viande de brousse. Compte tenu du schéma d'admixture génétique détecté chez les PVB d'Afrique de l'Ouest, nous préconisons une stratégie multi­locus pour tracer le commerce international de l'espèce.

African bushpigs exhibit porous species boundaries and appeared in Madagascar concurrently with human arrival.

Several African mammals exhibit a phylogeographic pattern where closely related taxa are split between West/Central and East/Southern Africa, but their evolutionary relationships and histories remain controversial. Bushpigs (Potamochoerus larvatus) and red river hogs (P. porcus) are recognised as separate species due to morphological distinctions, a perceived lack of interbreeding at contact, and putatively old divergence times, but historically, they were considered conspecific. Moreover, the presence of Malagasy bushpigs as the sole large terrestrial mammal shared with the African mainland raises intriguing questions about its origin and arrival in Madagascar. Analyses of 67 whole genomes revealed a genetic continuum between the two species, with putative signatures of historical gene flow, variable FST values, and a recent divergence time (<500,000 years). Thus, our study challenges key arguments for splitting Potamochoerus into two species and suggests their speciation might be incomplete. Our findings also indicate that Malagasy bushpigs diverged from southern African populations and underwent a limited bottleneck 1000-5000 years ago, concurrent with human arrival in Madagascar. These results shed light on the evolutionary history of an iconic and widespread African mammal and provide insight into the longstanding biogeographic puzzle surrounding the bushpig's presence in Madagascar.

Pangolin Genomes Offer Key Insights and Resources for the World's Most Trafficked Wild Mammals.

Pangolins form a group of scaly mammals that are trafficked at record numbers for their meat and purported medicinal properties. Despite their conservation concern, knowledge of their evolution is limited by a paucity of genomic data. We aim to produce exhaustive genomic resources that include 3,238 orthologous genes and whole-genome polymorphisms to assess the evolution of all eight extant pangolin species. Robust orthologous gene-based phylogenies recovered the monophyly of the three genera and highlighted the existence of an undescribed species closely related to Southeast Asian pangolins. Signatures of middle Miocene admixture between an extinct, possibly European, lineage and the ancestor of Southeast Asian pangolins, provide new insights into the early evolutionary history of the group. Demographic trajectories and genome-wide heterozygosity estimates revealed contrasts between continental versus island populations and species lineages, suggesting that conservation planning should consider intraspecific patterns. With the expected loss of genomic diversity from recent, extensive trafficking not yet realized in pangolins, we recommend that populations be genetically surveyed to anticipate any deleterious impact of the illegal trade. Finally, we produce a complete set of genomic resources that will be integral for future conservation management and forensic endeavors for pangolins, including tracing their illegal trade. These comprise the completion of whole-genomes for pangolins through the hybrid assembly of the first reference genome for the giant pangolin (Smutsia gigantea) and new draft genomes (∼43x-77x) for four additional species, as well as a database of orthologous genes with over 3.4 million polymorphic sites.

Genomic analysis reveals a cryptic pangolin species.

Eight extant species of pangolins are currently recognized. Recent studies found that two mitochondrial haplotypes identified in confiscations in Hong Kong could not be assigned to any known pangolin species, implying the existence of a species. Here, we report that two additional mitochondrial haplotypes identified in independent confiscations from Yunnan align with the putative species haplotypes supporting the existence of this mysterious species/population. To verify the new species scenario we performed a comprehensive analysis of scale characteristics and 138 whole genomes representing all recognized pangolin species and the cryptic new species, 98 of which were generated here. Our morphometric results clearly attributed this cryptic species to Asian pangolins (Manis sp.) and the genomic data provide robust and compelling evidence that it is a pangolin species distinct from those recognized previously, which separated from the Philippine pangolin and Malayan pangolin over 5 Mya. Our study provides a solid genomic basis for its formal recognition as the ninth pangolin species or the fifth Asian one, supporting a new taxonomic classification of pangolins. The effects of glacial climate changes and recent anthropogenic activities driven by illegal trade are inferred to have caused its population decline with the genomic signatures showing low genetic diversity, a high level of inbreeding, and high genetic load. Our finding greatly expands current knowledge of pangolin diversity and evolution and has vital implications for conservation efforts to prevent the extinction of this enigmatic and endangered species from the wild.

Examining the international bushmeat traffic in Belgium: A threat to conservation and public health.

The carriage of bushmeat into the European Union is an infringement of EU Animal Health and Wildlife Trade legislation and poses a threat to biodiversity and public health. To explore the nature and scale of the international bushmeat trade, seized leaking luggage and passengers arriving at Brussels Zaventem airport from sub-Saharan Africa between 2017 and 2018 were searched for "meat" (bushmeat and livestock) by border control authorities. Visual identification, radiography and genetic analysis were applied to derive information from seized specimens, including at least ten CITES-listed species. We estimate that an average of 3.9 t of bushmeat is smuggled monthly through Brussels. The average consignment of meat seized per passenger was 2.8 kg and 4 kg of bushmeat or domestic livestock meat, respectively. The international trafficking of bushmeat is evidently active, yet penalties are rarely enforced; hence we provide suggestions to simplify law enforcement procedures.

Is social media the new wet market? Social media platforms facilitate the online sale of bushmeat in West Africa.

Social media provides a platform for wildlife crime syndicates to access a global consumer-driven market. Whilst studies have uncovered the online trade in wildlife, the availability of wild meat (bushmeat) has not been assessed. To investigate the sale of wild meat online, we analysed 563 posts published between 2018 and 2022 from six West African Facebook pages selected using predetermined search criteria. Across 1511 images and 18 videos, we visually identified 25 bushmeat species-level taxa including mammals (six Rodentia, five Artiodactyla, three Carnivora, two Pholidota, one Primate, two Lagomorpha, one Hyracoidea), birds (three Galliformes) and reptiles (two Squamata), predominately advertised as smoked (63%) or fresh (30%) whole carcasses or portions. Among the species identified, 16% feature a status of concern on the International Union for Conservation of Nature (IUCN) Red List (Near Threatened to Endangered), 16% are listed on the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES; Appendix I and II) and 24% are either fully or partially protected by local legislation. Images were commonly used as propaganda rather than to display inventory, where additional taxa protected from game hunting in West Africa, such as hornbill, were exclusively listed in captions. The advertisement of these protected and vulnerable species on the surface web indicates weak local and international legislative enforcement. Comparatively, when the same search criteria were applied to the deep web browser Tor no results were generated, reinforcing the idea that bushmeat vendors have no need to hide their activities online. Despite local and international trade restrictions, the taxa advertised feature similarities with bushmeat seizures reported in Europe, alluding to the interconnectedness of the trade facilitated by social media. We conclude that enhanced policy enforcement is essential to combat the online sale of bushmeat and mitigate the potential biodiversity and public health impacts.

The antique genetic plight of the Mediterranean monk seal (Monachus monachus).

Disentangling the impact of Late Quaternary climate change from human activities can have crucial implications on the conservation of endangered species. We investigated the population genetics and demography of the Mediterranean monk seal (Monachus monachus), one of the world's most endangered marine mammals, through an unprecedented dataset encompassing historical (extinct) and extant populations from the eastern North Atlantic to the entire Mediterranean Basin. We show that Cabo Blanco (Western Sahara/Mauritania), Madeira, Western Mediterranean (historical range) and Eastern Mediterranean regions segregate into four populations. This structure is probably the consequence of recent drift, combined with long-term isolation by distance (R2 = 0.7), resulting from prevailing short-distance (less than 500 km) and infrequent long-distance dispersal (less than 1500 km). All populations (Madeira especially), show high levels of inbreeding and low levels of genetic diversity, seemingly declining since historical time, but surprisingly not being impacted by the 1997 massive die-off in Cabo Blanco. Approximate Bayesian Computation analyses support scenarios combining local extinctions and a major effective population size decline in all populations during Antiquity. Our results suggest that the early densification of human populations around the Mediterranean Basin coupled with the development of seafaring techniques were the main drivers of the decline of Mediterranean monk seals.

Warthog Genomes Resolve an Evolutionary Conundrum and Reveal Introgression of Disease Resistance Genes.

African wild pigs have a contentious evolutionary and biogeographic history. Until recently, desert warthog (Phacochoerus aethiopicus) and common warthog (P. africanus) were considered a single species. Molecular evidence surprisingly suggested they diverged at least 4.4 million years ago, and possibly outside of Africa. We sequenced the first whole-genomes of four desert warthogs and 35 common warthogs from throughout their range. We show that these two species diverged much later than previously estimated, 400,000-1,700,000 years ago depending on assumptions of gene flow. This brings it into agreement with the paleontological record. We found that the common warthog originated in western Africa and subsequently colonized eastern and southern Africa. During this range expansion, the common warthog interbred with the desert warthog, presumably in eastern Africa, underlining this region's importance in African biogeography. We found that immune system-related genes may have adaptively introgressed into common warthogs, indicating that resistance to novel diseases was one of the most potent drivers of evolution as common warthogs expanded their range. Hence, we solve some of the key controversies surrounding warthog evolution and reveal a complex evolutionary history involving range expansion, introgression, and adaptation to new diseases.

Can DNA help trace the local trade of pangolins? Conservation genetics of white-bellied pangolins from the Dahomey Gap (West Africa).

BACKGROUND: African pangolins are currently experiencing unprecedented levels of harvesting, feeding both local demands and the illegal international trade. So far, the lack of knowledge on the population genetics of African pangolins has hampered any attempts at assessing their demographic status and tracing their trade at the local scale. We conducted a pioneer study on the genetic tracing of the African pangolin trade in the Dahomey Gap (DG). We sequenced and genotyped 189 white-bellied pangolins from 18 forests and 12 wildlife markets using one mitochondrial fragment and 20 microsatellite loci. RESULTS: Tree-based assignment procedure showed that the pangolin trade is endemic to the DG region, as it was strictly fed by the the Dahomey Gap lineage (DGL). DGL populations were characterized by low levels of genetic diversity, an overall absence of equilibrium, important inbreeding levels, and lack of geographic structure. We identified a 92-98% decline in DGL effective population size 200-500 ya-concomitant with major political transformations along the 'Slave Coast'-leading to contemporaneous estimates being inferior to minimum viable population size (< 500). Genetic tracing suggested that wildlife markets from the DG sourced pangolins through the entire DGL range. Our loci provided the necessary power to distinguish among all the genotyped pangolins, tracing the dispatch of a same individual on the markets and within local communities. We developed an approach combining rarefaction analysis of private allele frequencies with cross-validation of observed data that traced five traded pangolins to their forest origin, c. 200-300 km away from the markets. CONCLUSIONS: Although the genetic toolkit that we designed from traditional markers can prove helpful to trace the illegal trade in pangolins, our tracing ability was limited by the lack of population structure within the DGL. Given the deleterious combination of genetic, demographic, and trade-related factors affecting DGL populations, the conservation status of white-bellied pangolins in the DG should be urgently re-evaluated.

Ancient divergence of Indian and Tibetan wolves revealed by recombination-aware phylogenomics.

The grey wolf (Canis lupus) expanded its range across Holarctic regions during the late Pleistocene. Consequently, most grey wolves share recent (<100,000 years ago) maternal origins corresponding to a widespread Holarctic clade. However, two deeply divergent (200,000-700,000 years ago) mitochondrial clades are restricted, respectively, to the Indian subcontinent and the Tibetan Plateau, where remaining wolves are endangered. No genome-wide analysis had previously included wolves corresponding to the mitochondrial Indian clade or attempted to parse gene flow and phylogeny. We sequenced four Indian and two Tibetan wolves and included 31 additional canid genomes to resolve the phylogenomic history of grey wolves. Genomic analyses revealed Indian and Tibetan wolves to be distinct from each other and from broadly distributed wolf populations corresponding to the mitochondrial Holarctic clade. Despite gene flow, which was reflected disproportionately in high-recombination regions of the genome, analyses revealed Indian and Tibetan wolves to be basal to Holarctic grey wolves, in agreement with the mitochondrial phylogeny. In contrast to mitochondrial DNA, however, genomic findings suggest the possibility that the Indian wolf could be basal to the Tibetan wolf, a discordance potentially reflecting selection on the mitochondrial genome. Together, these findings imply that southern regions of Asia have been important centers for grey wolf evolution and that Indian and Tibetan wolves represent evolutionary significant units (ESUs). Further study is needed to assess whether these ESUs warrant recognition as distinct species. This question is especially urgent regarding the Indian wolf, which represents one of the world's most endangered wolf populations.

Preservative chemicals as a new health risk related to traditional medicine markets in western Africa.

Health risks associated to the use of tropical wildlife have so far been envisioned through the lens of zoonotic pathogens spread by the bushmeat trade, putting aside the equally vibrant network of traditional medicine markets (TMMs). We collected information on the preservative techniques used for animal body parts from TMMs in Benin through a semi-structured questionnaire addressed to 45 sellers. We show that a recent shift from traditional preservative techniques using harmless treatments towards modern techniques -involving the recurrent use of hazardous chemicals (such as Sniper)- is likely to pose a serious health risk to practitioners and consumers of animal parts from TMMs in Benin. We conclude that the non-regulation of the TMM activities represents a critical risk to both biodiversity conservation and human health in western Africa.

The role and impact of Zootaxa in mammalogy in its first 20 years.

Zootaxa came as a new and innovative publication medium for taxonomy, amidst a scenario of devaluation of this important biological science. After 20 years, it has ascertained itself as one of the main journals in animal taxonomy. However, the contribution of the journal to the taxonomy of Mammalia (mammals), one of the most studied groups of animals with a long-standing, dedicated spectrum of specialized journals (mammalogy), could have been expected as minor. All the current and former editors of the Mammalia section of Zootaxa analyzed the relative contribution of the journal to the description of new species of mammals since 2001. We also analyzed the contribution of Zootaxa by taxon, geographic origin of taxa, and geographic origin of first authors. The taxonomic methodology of authors in species description is described as well as the temporal trends in publications and publication subjects. We highlight the editors' picks and eventually, the challenges for the future. We found that Zootaxa has had a significant contribution to mammalogy, being the second journal (the first being Journal of Mammalogy) in terms of number of new species described (76; 10.6% of the new mammalian species described between 2001 and 2020). The majority of the new species were described following an integrative taxonomic approach with at least two sources of data (86%). The analysis of published taxa, their geographic origin, and the country of origin of first authors shows a wide coverage and exhaustive representation, except for the species from the Nearctic. We conclude that Zootaxa has likely responded to a repressed demand for an additional taxonomic journal in mammalogy, with as possible appeals the absence of publication fees and an established publication speed. With 246 articles published in the past 20 years, the Mammalia section of Zootaxa embraces a large spectrum of systematic subjects going beyond alpha taxonomy. The challenges for the future are to encourage publications of authors from the African continent, still poorly represented, and from the palaeontology community, as the journal has been open to palaeontology since its early days.

Ethnozoological and commercial drivers of the pangolin trade in Benin.

BACKGROUND: Pangolins are trafficked in unsustainable volumes to feed both local and global trade networks for their meat and the medicinal properties of their derivatives, including scales. We focus on a West African country (Benin) to assess the medicinal and spiritual values of pangolins among different ethnic groups and identify the cohort of buyers involved in the pangolin trade and related economic values along the chain, notably from local diasporas. METHODS: We organised 54 focus groups in villages surrounding occurrence habitats of pangolins across Benin and conducted 35 individual interviews with vendors from five major traditional medicine markets (TMMs). Our questionnaire addressed the different uses of pangolins, the commercial value of pangolin items, the categories of clients and the related selling prices. RESULTS: Pangolin meat was strictly consumed as food. Scales, head, bones, tongue, blood, heart and xiphisternum were the items used by local communities as part of medicinal (65% of the focus groups) and spiritual (37%) practices. Scales were the most frequently used item (use value index = 1.56). A total of 42 medicinal and spiritual uses, covering 15 International Classification of Diseases (ICD) categories, were recorded among ethnic groups. The ICD and spiritual categories-based analyses of similarity showed a partial overlapping of ethnozoological knowledge across Benin, although knowledge was significantly influenced by ethnicity and geographic location. The pricing of pangolins both varied with the category of stakeholders (local communities vs. stakeholders of TMMs) and clients (local and West African clients vs. Chinese community) and the type of items sold. The Chinese community was reported to only buy pangolins alive, and average selling prices were 3-8 times higher than those to West African clients. CONCLUSIONS: Our results confirm that pangolins in Africa are valuable and versatile resources for consumption and medicinal / spiritual practices. The pangolin trade in Benin is based on an endogenous and complex network of actors that now appears influenced by the specific, high-valued demand from the Chinese diaspora. Further investigations are required to assess the growing impact of the Chinese demand on the African wildlife trade.

Dire wolves were the last of an ancient New World canid lineage.

Dire wolves are considered to be one of the most common and widespread large carnivores in Pleistocene America1, yet relatively little is known about their evolution or extinction. Here, to reconstruct the evolutionary history of dire wolves, we sequenced five genomes from sub-fossil remains dating from 13,000 to more than 50,000 years ago. Our results indicate that although they were similar morphologically to the extant grey wolf, dire wolves were a highly divergent lineage that split from living canids around 5.7 million years ago. In contrast to numerous examples of hybridization across Canidae2,3, there is no evidence for gene flow between dire wolves and either North American grey wolves or coyotes. This suggests that dire wolves evolved in isolation from the Pleistocene ancestors of these species. Our results also support an early New World origin of dire wolves, while the ancestors of grey wolves, coyotes and dholes evolved in Eurasia and colonized North America only relatively recently.

Development and characterization of 20 polymorphic microsatellite markers for the white-bellied pangolin Phataginus tricuspis (Mammalia, Pholidota).

Pangolins, or scaly anteaters, have recently been flagshiped as one of the most illegally traded mammals, and as a corollary, as potential intermediate hosts at the origin of the COVID-19 pandemic. In order to improve the traceability of their trade, we developed 20 polymorphic microsatellite loci for the white-bellied pangolin (Phataginus tricuspis), the species most frequently found on African bushmeat markets. We genotyped 24 white-bellied pangolins from the Douala market, Cameroon, originating from the Ebo forest c. 75 km north-east of Douala. The number of alleles per locus ranged from 4 to 12 (mean = 6.95), and mean observed and expected heterozygosities were 0.592 (0.208-0.875) and 0.671 (0.469-0.836), respectively. Genetic diversity was higher than that cross-estimated from microsatellite loci developed for other species of pangolins. Two loci deviated from Hardy-Weinberg equilibrium and two loci showed linkage disequilibrium. Genetic variance (PCoA) was increased with the addition of 13 pangolins of unknown origin, possibly suggesting that the Douala market is fed from differentiated source populations of white-bellied pangolins. Each of the 37 individuals had a unique multilocus genotype. The unbiased probability of identity (uPI) and the probability of identity among siblings (PIsibs) were both very low (uPI = 8.443 e-21; PIsibs = 1.011 e-07). Only five microsatellite loci were needed to reach the conservative value of PIsibs < 0.01, overall indicating a powerful discriminating power of our combined loci. These 20 newly developed microsatellite loci might prove useful in tracing the local-to-global trade of the white-bellied pangolin, and will hopefully contribute to the DNA-assisted implementation of future conservation strategies at reasonable costs.

Interspecific Gene Flow Shaped the Evolution of the Genus Canis.

The evolutionary history of the wolf-like canids of the genus Canis has been heavily debated, especially regarding the number of distinct species and their relationships at the population and species level [1-6]. We assembled a dataset of 48 resequenced genomes spanning all members of the genus Canis except the black-backed and side-striped jackals, encompassing the global diversity of seven extant canid lineages. This includes eight new genomes, including the first resequenced Ethiopian wolf (Canis simensis), one dhole (Cuon alpinus), two East African hunting dogs (Lycaon pictus), two Eurasian golden jackals (Canis aureus), and two Middle Eastern gray wolves (Canis lupus). The relationships between the Ethiopian wolf, African golden wolf, and golden jackal were resolved. We highlight the role of interspecific hybridization in the evolution of this charismatic group. Specifically, we find gene flow between the ancestors of the dhole and African hunting dog and admixture between the gray wolf, coyote (Canis latrans), golden jackal, and African golden wolf. Additionally, we report gene flow from gray and Ethiopian wolves to the African golden wolf, suggesting that the African golden wolf originated through hybridization between these species. Finally, we hypothesize that coyotes and gray wolves carry genetic material derived from a "ghost" basal canid lineage.

Whole-Genome Sequencing of African Dogs Provides Insights into Adaptations against Tropical Parasites.

Natural selection in domestic dogs is of great interest in evolutionary biology since dogs have migrated to every inhabited continent of the world alongside humans, and adapted to diverse environments. Here, we explored their demographic history and genetic basis of adaptation to the tropical African environment using whole genome analyses of 19 African indigenous dogs from Nigeria. Demographic analysis suggests that the ancestors of these dogs migrated into Africa from Eurasia 14,000 years ago and underwent a severe founder effect before population expansion. Admixture analysis further reveals that African dog genomes contain about 1.88-3.50% introgression from African golden wolves (Canis anthus). Population genetic analysis identifies 50 positively selected genes linked with immunity, angiogenesis, ultraviolet protection, as well as insulin secretion and sensitivity that may contribute to adaptation to tropical conditions. One of the positively selected genes, adhesion G protein-coupled receptor E1 (ADGRE1), has also been found to be association with severe malaria resistance in African human populations. Functional assessments showed that ADGRE1 provides protective host defense against Plasmodium infections. This result, together with the fact that the inflammatory response to canine babesiosis is similar to complicated falciparum malaria in humans, support the dogs as a model for the study of malaria control and treatment.

The Complete Phylogeny of Pangolins: Scaling Up Resources for the Molecular Tracing of the Most Trafficked Mammals on Earth.

Pangolins, considered the most-trafficked mammals on Earth, are rapidly heading to extinction. Eight extant species of these African and Asian scale-bodied anteaters are commonly recognized, but their evolutionary relationships remain largely unexplored. Here, we present the most comprehensive phylogenetic assessment of pangolins, based on genetic variation of complete mitogenomes and 9 nuclear genes. We confirm deep divergence among Asian and African pangolins occurring not later than the Oligocene-Miocene boundary ca. 23 million years ago (Ma) (95% HPD = 18.7-27.2), limited fossil evidence suggesting dispersals from Europe. We recognize 3 genera including Manis (Asian pangolins), Smutsia (large African pangolins), and Phataginus (small African pangolins), which first diversified in the Middle-Upper Miocene (9.8-13.3 Ma) through a period of gradual cooling coinciding with a worldwide taxonomic diversification among mammals. Based on large mitogenomic distances among the 3 genera (18.3-22.8%) and numerous (18) morphological traits unique to Phataginus, we propose the subfamily Phatagininae subfam. nov. to designate small African pangolins. In contrast with the morphological-based literature, our results establish that the thick-tailed pangolin (Manis crassicaudata) is sister-species of the Sunda (Manis javanica) and Palawan (Manis culionensis) pangolins. Mitogenomic phylogenetic delineations supported additional pangolin species subdivisions (n = 13), including 6 African common pangolin (Phataginus tricuspis) lineages, but these patterns were not fully supported by our multi-locus approach. Finally, we identified more than 5000 informative mitogenomic sites and diagnostic variation from 5 nuclear genes among all species and lineages of pangolins, providing an important resource for further research and for effectively tracing the worldwide pangolin trade.