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

Abstract

Pangolins form a group of scaly mammals that are trafficked at record numbers for their meat and medicinal properties. Despite their great 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 pangolin species. Robust orthologous gene-based phylogenies recovered the monophyly of the three genera of pangolins, and highlighted the existence of an undescribed species closely related to South-East Asian pangolins. Signatures of middle Miocene admixture between an extinct, possibly European, lineage and the ancestor of South-East Asian pangolins, provides new insights into the early evolutionary history of the group. Demographic trajectories and genome-wide heterozygosity estimates revealed contrasts between continental vs. island populations and species lineages, suggesting that conservation planning should consider intra-specific patterns. With the expected loss of genomic diversity from recent, extensive trafficking not yet been realized in pangolins, we recommend that populations are 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 required for conserving pangolins, including tracing their illegal trade. These include the completion of whole-genomes for pangolins through the first reference genome with long reads 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.

Evolution and conservation genetics of pangolins

“…For instance, continental populations of Chinese pangolin showed substantially larger genetic diversity than what was measured for the Taiwan population (Wang et al 2022). A similar result was found for the Indian pangolin, with the Sri Lankan population showing lower genetic diversity than other populations (Heighton et al 2023). Conversely, in the case of the Malayan pangolin, the continental population appears to have significantly lower genetic diversity than island populations (Hu et al 2020b), with the island populations showing relatively similar levels of genetic diversity (Li et al 2023).…”

“…Various efforts have been made to establish the phylogenetic relationships for extant pangolin species using different genetic markers, such as mitochondrial (mt) or nuclear markers, mitogenomes, and even whole genomes. All of the previous findings consistently support a deep divergence between African and Asian pangolins (Du Toit et al 2014;Hassanin et al 2015;Gaubert et al 2018;Gu et al 2023;Heighton et al 2023). Within African pangolins, whole-genome and mt-DNA analyses supported the classification of four species into two genera Phataginus and Smutsia (Gaubert et al 2018;Gu et al 2023;Heighton et al 2023).…”

“…More specifically, the recent discovery of a ninth pangolin species (Gu et al 2023;Heighton et al 2023;Li et al 2023) and additional newly discovery populations (Nash et al 2018;Hu et al 2020b;Wang et al 2022;Wei et al 2022;Li et al 2023) provide evidence that previous studies have underestimated the diversity of pangolins. Therefore, the integration of research from morphologists, ecologists, and geneticists could be expected to provide a more comprehensive picture of pangolin diversity as well as aid conservation efforts.…”

Genomic analysis reveals a cryptic pangolin species

“…We obtained whole-genome resequencing datasets representing 138 different individuals from all eight known pangolin species, including 20 Indian pangolins ( M. crassicaudata ), 19 Chinese pangolins ( M. pentadactyla ) ( 24 ), 20 Malayan pangolins ( M. javanica ) ( 24 ), one Philippine pangolin ( M. culionensis ) ( 25 ), 20 White-bellied pangolins ( P. tricuspis ), 20 Black-bellied pangolins ( P. tetradactyla ), 29 Giant pangolins ( S. gigantea ), and two Temminck’s pangolins ( S. temminckii ), as well as seven individuals belonging to the putative cryptic new pangolin species ( SI Appendix , Table S1 ). Ninety-eight of these datasets were newly generated in the present study.…”

“…Besides the genomic sequences from five recognized pangolin species and the cryptic new species newly generated here, the genomic sequences from the other three recognized pangolin species, including one Philippine pangolin ( 25 ), 20 Chinese pangolins ( 24 ), and 20 Malayan pangolins ( 24 ), were downloaded from the NCBI GenBank database ( SI Appendix , Table S1 ).…”