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, Cote 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 (Cote 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 dernieres annees, les volumes de pangolins africains alimentant le commerce illegal d'especes sauvages ont augmente de facon spectaculaire. Nous avons mene une etude de genetique de la conservation sur l'espece africaine la plus braconnee, le pangolin a ventre blanc (PVB; Phataginus tricuspis), a travers trois pays d'Afrique de l'Ouest incluant la Guinee, la Cote d'Ivoire et le Ghana. Notre etude combinant le sequencage de l'ADN mitochondrial et le genotypage par microsatellites est la premiere a reveler un patron generalise d'admixture entre deux des six lignees mitochondriales precedemment delimitees au sein du PVB. Nous mettons en evidence une signature d'isolement par la distance mais un manque de structuration genetique des populations, soutenant l'idee que le PVB a des capacites de dispersion jusque-la sous-estimees. Les niveaux de diversite genetique observes dans les lignees d'Afrique de l'Ouest (WAfr et Gha) sont faibles par rapport a ceux observes en Afrique Centrale, confirmant la pauperisation genetique des populations de PVB en Afrique de l'Ouest. Nous avons observe un declin de 85 a 98% de la taille efficace de la population ouest-africaine entre 3200 et 400 ans, les estimations actuelles (520-590) se situant a l'extremite inferieure des seuils minimums de viabilite. Les marqueurs microsatellites utilises sont suffisamment puissants pour differencier les individus et identifier les doublons d'echantillons, confirmant l'utilite de ces marqueurs pour tracer le commerce des pangolins. Nos estimations de diversite genetique ont confirme que Yopougon, le principal marche de viande de brousse d'Abidjan (Cote d'Ivoire), etait alimente par un vaste reseau commercial, comme le confirment les vendeurs signalant 10 sources differentes situees a 62-459 km du marche. Nous concluons que les PVB presents dans le bloc forestier de Haute Guinee devraient etre consideres comme une seule unite de gestion a fort interet de conservation, etant soumis a une erosion de sa diversite genetique, un declin drastique de la taille efficace de sa population et un approvisionnement a grande echelle des marches urbains de viande de brousse. Compte tenu du schema d'admixture genetique detecte chez les PVB d'Afrique de l'Ouest, nous preconisons une strategie multi-locus pour tracer le commerce international de l'espece. Our work derives from an unprecedented, exhaustive genetic survey of the pangolin trade in three countries from West Africa (Guinea, Cote d'Ivoire, and Ghana). Our study combining mitochondrial DNA sequencing and microsatellite genotyping is the first to reveal a global pattern of admixture between two of the six mitochondrial lineages previously delimited within the white-bellied pangolin (WBP).image