Evolution of Acidic Mammalian Chitinase Genes (CHIA) Is Related to Body Mass and Insectivory in Primates

Abstract

Insects are an important food resource for many primates, but the chitinous exoskeletons of arthropods have long been considered to be indigestible by the digestive enzymes of most mammals. However, recently mice and insectivorous bats were found to produce the enzyme acidic mammalian chitinase (AMCase) to digest insect exoskeletons. Here, we report on the gene CHIA and its paralogs, which encode AMCase, in a comparative sample of nonhuman primates. Our results show that early primates likely had three CHIA genes, suggesting that insects were an important component of the ancestral primate diet. With some exceptions, most extant primate species retain only one functional CHIA paralog. The exceptions include two colobine species, in which all CHIA genes have premature stop codons, and several New World monkey species that retain two functional genes. The most insectivorous species in our sample also have the largest number of functional CHIA genes. Tupaia chinensis and Otolemur garnettii retain three functional CHIA paralogs, while Tarsius syrichta has a total of five, two of which may be duplications specific to the tarsier lineage. Selection analyses indicate that CHIA genes are under more intense selection in species with higher insect consumption, as well as in smaller-bodied species (<500 g), providing molecular support for Kay's Threshold, a well-established component of primatological theory which proposes that only small primates can be primarily insectivorous. These findings suggest that primates, like mice and insectivorous bats, may use the enzyme AMCase to digest the chitin in insect exoskeletons, providing potentially significant nutritional benefits.

Seasonality of the gut microbiota of free-ranging white-faced capuchins in a tropical dry forest

“…CBM50 has been reported to bind to the N-acetylglucosamine (GlcNac) present in chitin [76] and previously shown to function in chitin degradation [77]. Our result-that a dominant module in the capuchin gut microbiota was CBM50-is consistent with the hypothesis that the bacterial microbiome has an important role in digestion of invertebrate exoskeletons, thus augmenting capacities of the host genome for acquiring energy and nutrition from this essential component of their diet [78]. However, given that CBM50 is also involved in polysaccharide digestion and in the breakdown of peptidoglycans, this result warrants further investigation.…”

The gut microbiome and metabolome of saddleback tamarins (Leontocebus weddelli): Insights into the foraging ecology of a small‐bodied primate

“…The data presented show little evidence that the saddleback tamarin gut microbiome significantly contributes to invertebrate exoskeleton digestion, despite the predicted abundance of chitin degrading genes. Thus, insect digestion capabilities may be mainly encoded by the tamarin genome, particularly by acidic mammalian chitinases, whose functional genes are higher in abundance in most insect‐feeding and smaller‐bodied primates (Janiak, Chaney, & Tosi, ). In addition, acidic mammalian chitinases are present in the stomach of several species of insectivorous bats and primates, and play a critical role in chitin breakdown (Paoletti, Norberto, Damini, & Musumeci, ; Strobel, Roswag, Becker, Trenczek, & Encarnação, ).…”

Insects as food and feed, a new emerging agricultural sector: a review

“…Recent evidence suggest that 1.8 million years ago insects in Tanzania were a major food source (Heriot-Watt University, 2018). Primates used the enzyme acidic mammalian chitinase to digest the chitin in insect exoskeletons, which have long been considered indigestible (Janiak et al, 2018). There is a general gradient pattern in reduction of edible insects with increased latitude (Lesnik, 2017), probably because in tropical regions insects are more abundant and easy to harvest (Van Huis, 2018).…”