Hologenomic insights into mammalian adaptations to myrmecophagy

Abstract

Highly specialized myrmecophagy (ant- and termite-eating) has independently evolved multiple times in species of various mammalian orders and represents a textbook example of phenotypic evolutionary convergence. We explored the mechanisms involved in this unique dietary adaptation and convergence through multi-omic analyses, including analyses of host genomes and transcriptomes, as well as gut metagenomes, in combination with validating assays of key enzymes’ activities, in the species of three mammalian orders (anteaters, echidnas and pangolins of the orders Xenarthra, Monotremata and Pholidota, respectively) and their relatives. We demonstrate the complex and diverse interactions between hosts and their symbiotic microbiota that provided adaptive solutions for nutritional and detoxification challenges associated with high levels of protein and lipid metabolisms, trehalose degradation, and toxic substance detoxification. Interestingly, we also reveal their spatially complementary cooperation involved in degradation of ants’ and termites’ chitin exoskeletons. This study contributes new insights into the dietary evolution of mammals and the mechanisms involved in the coordination of physiological functions by animal hosts and their gut commensals.

Transcriptomic data reveal divergent paths of chitinase evolution underlying dietary convergence in anteaters and pangolins

“…More specifically, CHIA5 was found expressed at particularly high levels in the stomach and salivary glands. These results are in line with previous proteomic studies that have also identified CHIA5 as a digestive enzyme (Zhang et al 2019), which has been confirmed to be highly expressed by RT-qPCR in the specialized oxyntic glands stomach (Ma et al 2018a;Cheng et al 2022), reflecting a key adaptation of the Malayan pangolin to its strictly myrmecophagous diet. By contrast, in the southern tamandua (T. tetradactyla) only CHIA5 is pseudogenized (Emerling et al 2018;Cheng et al 2022).…”

“…These results are in line with previous proteomic studies that have also identified CHIA5 as a digestive enzyme (Zhang et al 2019), which has been confirmed to be highly expressed by RT-qPCR in the specialized oxyntic glands stomach (Ma et al 2018a;Cheng et al 2022), reflecting a key adaptation of the Malayan pangolin to its strictly myrmecophagous diet. By contrast, in the southern tamandua (T. tetradactyla) only CHIA5 is pseudogenized (Emerling et al 2018;Cheng et al 2022). Although CHIA1 and CHIA2 are functional, they did not appear to be expressed in the organs of the digestive tract of the southern tamandua individual sampled here (Fig.…”

“…Our differential expression comparison of the distinct chitinase paralogs across different organs further highlighted the importance of CHIA5 for Malayan pangolin digestion physiology by confirming its ubiquitous expression in all major digestive tissue types (tongue, salivary glands, stomach, pancreas, liver, and large and small intestines) (Ma et al 2017;Ma et al 2019;Cheng et al 2022;and Fig. 4).…”

“…A first metagenomic study of the fecal microbiome of the Malayan pangolin (M. javanica) previously identified a number of gut bacterial taxa containing chitinase genes capable of degrading chitin (Ma et al 2018b). A more recent study has confirmed the chitin degradation potential of the Malayan pangolin gut microbiome and proposed that chitin is digested in this species by a combination of endogenous chitinolytic enzymes produced by oxyntic glands in the stomach and bacterial chitinases secreted in the colon (Cheng et al 2022). Moreover, metagenomic data of fecal samples from captive giant anteater (M. tridactyla) individuals have revealed a chitin degradation potential in their gut microbiome (Cheng et al 2022).…”

“…It has long been shown that chitinase enzymes are present in the digestive tract of mammals and vertebrates more broadly (Jeuniaux 1961; Jeuniaux 1966; Jeuniaux 1971; Jeuniaux and Cornelius 1997). More recent studies have indeed shown that chitinase genes are present in the mammalian genome and may play an important digestive function in insectivorous species (Bussink et al 2007; Emerling et al 2018; Janiak et al 2018; Wang et al 2020; Cheng et al 2022). Elevated levels of digestive enzyme gene expression have notably been observed in placental mammal salivary glands.…”