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

Abstract

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.

Pangolin genomes offer key insights and resources for the world’s most trafficked wild mammals

“…The PSMC curves for the two P. tricuspis lineages showed different trends; the Western Central Africa (WCA) lineage presented a stable IICR through time, while the Dahomey Gap (DG) lineage experienced a progressive decline (Figure 3b). These differences are mirrored by their genetic diversity whereby DG contains low levels of genetic diversity and high levels of inbreeding, while WCA has an opposite pattern (Figure 4, see below; Aguillon, et al 2020; Zanvo, et al 2022). Our results for the two different P. tricuspis lineages (Gaubert, et al 2016) included in this study suggest that the demographic history of the species is likely complex, lineage specific, and will require more thorough investigation (notably since the DG sample had limited sequencing depth; Table S1).…”

“…We hypothesize that the low heterozygosity of the P. tricuspis DG lineage can be related to the Dahomey Gap's bioclimatic history, which shaped a suboptimal savannah habitat intermixed with forest patches. Forest fragmentation through Holocene climatic oscillations (Salzmann and Hoelzmann 2005;Demenou, et al 2016) in conjunction with high levels of inbreeding through a steady IICR decline over the last 1 million years (Figure 3) may have resulted in a drastic decrease of effective population size and loss of heterozygosity, as noted using microsatellite data (Zanvo, et al 2022). Along with Manis culionensis (0.492%), the other lineage of P. tricuspis (WCA; 0.334%) is an outlier for high levels of heterozygosity (Figure 4), alongside common species like the wild boar (Sus scrofa) and brown bear (Ursus arctos; Table S5).…”

Vendors’ perceptions on the bushmeat trade dynamics across West Africa during the COVID-19 pandemic: lessons learned on sanitary measures and awareness campaigns

“…Significantly differentiated appreciations also prevailed as to the impact of the pandemic on the bushmeat supply chain, which was strongly reported as negatively affected in Benin -including for pangolins-compared to Côte d'Ivoire and Cameroon, where the picture was more mitigated. Benin is a small country with a bushmeat supply chain endemic to the Dahomey Gap (see Zanvo et al 2022 for an example on the pangolin trade), a narrow savannah-forest mosaic zone where sourced forests are isolated and highly fragmented (Salzmann and Hoelzmann 2005). Given this socio-geographical context, it is expected that lockdown measures restricting movements, even light, could have significantly impacted the supply chain in the country.…”

Genetic tracing of the white-bellied pangolin’s trade in western central Africa

“…We assessed temporal changes in the effective population size of WCA through an approximate-likelihood approach implemented in the R package VarEff (Nikolic & Chevalet, 2014). We followed Zanvo et al (2022) by fixing a generation time of 2 yrs and a microsatellites mutation rate of 5.10 -4 per generations (Schlotterer, 2000). We ran the analysis with three mutation models (single, geometric and two phases), using 10,000 MCMC batches (length = 1, thinned every 100 batches; JMAX = 3).…”

“…Because we could not find a deep level of genetic structure within WCA, we followed the protocol based on private allele frequency rarefaction described by Zanvo et al (2022) to trace the trade of WBP in our study area. We used the generalized rarefaction approach implemented in ADZE (Szpiech et al, 2008) to compute private allele frequencies (paf) among various combinations of populations from the 10 source populations as defined above (removing Gab).…”