Transcriptomic analysis identifies genes and pathways related to myrmecophagy in the Malayan pangolin (Manis javanica)

Abstract

The Malayan pangolin (Manis javanica) is an unusual, scale-covered, toothless mammal that specializes in myrmecophagy. Due to their threatened status and continuing decline in the wild, concerted efforts have been made to conserve and rescue this species in captivity in China. Maintaining this species in captivity is a significant challenge, partly because little is known of the molecular mechanisms of its digestive system. Here, the first large-scale sequencing analyses of the salivary gland, liver and small intestine transcriptomes of an adult M. javanica genome were performed, and the results were compared with published liver transcriptome profiles for a pregnant M. javanica female. A total of 24,452 transcripts were obtained, among which 22,538 were annotated on the basis of seven databases. In addition, 3,373 new genes were predicted, of which 1,459 were annotated. Several pathways were found to be involved in myrmecophagy, including olfactory transduction, amino sugar and nucleotide sugar metabolism, lipid metabolism, and terpenoid and polyketide metabolism pathways. Many of the annotated transcripts were involved in digestive functions: 997 transcripts were related to sensory perception, 129 were related to digestive enzyme gene families, and 199 were related to molecular transporters. One transcript for an acidic mammalian chitinase was found in the annotated data, and this might be closely related to the unique digestive function of pangolins. These pathways and transcripts are involved in specialization processes related to myrmecophagy (a form of insectivory) and carbohydrate, protein and lipid digestive pathways, probably reflecting adaptations to myrmecophagy. Our study is the first to investigate the molecular mechanisms underlying myrmecophagy in M. javanica, and we hope that our results may play a role in the conservation of this species.

The brain of the tree pangolin (Manis tricuspis). II. The olfactory system

“…Thus, in the tree pangolin, which has approximately 940 MOB glomeruli, the number of odorants to which the tree pangolin should respond using its MOB would be approximately 470. This is well below the total number of 942 olfactory receptor genes found in the Malay pangolin (Ma et al, ), indicating that around the same number of olfactory receptor genes have become pseudogenes. However, in the human the ratio is approximately 350 cohorts to approximately 5,500 glomeruli (~1:16), in the mouse approximately 1,100 cohorts to approximately 3,700 glomeruli (~1:3), and in the honey bee approximately 170 cohorts to approximately 170 glomeruli (~1:1) (Sinakevitch et al, ), making such a simplistic calculation untenable for the pangolin as this ratio is unknown.…”

“…While there are roughly 1,000 olfactory receptor genes in the mammalian genome, in many species a large proportion of these genes have become pseudogenes (Olender, Lancet, & Nebert, ). Ma et al, () have reported a total of 942 olfactory receptor genes in the Malayan pangolin, but the number of these genes that have become pseudogenes is not known. As discussed above, it is likely that any olfactory receptor genes belonging to the V2R family are pseudogenes, thus reducing the potential number of active odorant receptor genes in pangolins.…”

“…Given the nocturnal, selective, myrmecophagous, habits of the pangolins, the potential for olfactory specialization to enhance foraging is a reasonable working hypothesis. Recent genomic analyses of the Malayan ( Manis javanica ) and Chinese ( M. pentadactyla ) pangolins indicated that the olfactory receptor gene families are significantly expanded (Choo et al, ), with 969 genes associated with olfactory transduction in M. javanica , 942 of which appear to be olfactory receptors (Ma et al, ), supporting the notion that there may be neural specializations related to this sensory system in pangolins.…”

Chitinase genes ( CHIA s) provide genomic footprints of a post-Cretaceous dietary radiation in placental mammals

“…Because of the surprisingly minimal number of CHIA s in the genomes of the highly insectivorous pangolins (table S1), possibly due to a historical contingency (table S5), we tested whether the immune chitinase gene CHIT1 is expressed in the GI tract alongside CHIA5 . In NCBI, we BLASTed (megablast) the assembled Manis javanica CHIA5 and the coding sequence of an M. javanica CHIT1 gene model (XM_017667770.1) against an M. javanica salivary gland RNA library (table S3) ( 50 ).…”

A socio-economic survey of pangolin hunting in Assam, Northeast India

“…Mahmood et al 2015, low density (e.g. Mahmood et al 2014Mahmood et al , 2018 and specialised niche requirements (Ma et al 2017)] are also taken into account, the international trade of pangolins is now recognised as the most significant impediment for their conservation (Zhang et al 2017).…”