Duplication and parallel evolution of the pancreatic ribonuclease gene (RNASE1) in folivorous non-colobine primates, the howler monkeys (Alouatta spp.)

Mareike C Janiak,Todd R Disotell,Andrew S Burrell,Joseph D Orkin

doi:10.1038/s41598-019-56941-7

Abstract

In foregut-fermenting mammals (e.g., colobine monkeys, artiodactyl ruminants) the enzymes pancreatic ribonuclease (RNASE1) and lysozyme C (LYZ), originally involved in immune defense, have evolved new digestive functions. Howler monkeys are folivorous non-colobine primates that lack the multi-chambered stomachs of colobines and instead digest leaves using fermentation in the caeco-colic region. We present data on the RNASE1 and LYZ genes of four species of howler monkey (Alouatta spp.). We find that howler monkey LYZ is conserved and does not share the substitutions found in colobine and cow sequences, whereas RNASE1 was duplicated in the common ancestor of A. palliata, A. seniculus, A. sara, and A. pigra. While the parent gene (RNASE1) is conserved, the daughter gene (RNASE1B) has multiple amino acid substitutions that are parallel to those found in RNASE1B genes of colobines. The duplicated RNase in Alouatta has biochemical changes similar to those in colobines, suggesting a novel, possibly digestive function. These findings suggest that pancreatic ribonuclease has, in parallel, evolved a new role for digesting the products of microbial fermentation in both foregut- and hindgut-fermenting folivorous primates. This may be a vital digestive enzyme adaptation allowing howler monkeys to survive on leaves during periods of low fruit availability.

Highlights

In foregut-fermenting mammals the enzymes pancreatic ribonuclease (RNASE1) and lysozyme C (LYZ), originally involved in immune defense, have evolved new digestive functions
While colobines and cows have a number of parallel amino acid changes, these substitutions are not found in howler monkey lysozyme C (Fig. 1)
The branch-site model did not support the hypothesis that any sites along the howler monkey RNASE1B genes are under positive selection, as the alternative model did not have a significantly better fit than the null model (ΔLRT = 3.41, p = 0.065; Table 1)

Summary

Introduction

In foregut-fermenting mammals (e.g., colobine monkeys, artiodactyl ruminants) the enzymes pancreatic ribonuclease (RNASE1) and lysozyme C (LYZ), originally involved in immune defense, have evolved new digestive functions. The duplicated RNase in Alouatta has biochemical changes similar to those in colobines, suggesting a novel, possibly digestive function These findings suggest that pancreatic ribonuclease has, in parallel, evolved a new role for digesting the products of microbial fermentation in both foregutand hindgut-fermenting folivorous primates. This may be a vital digestive enzyme adaptation allowing howler monkeys to survive on leaves during periods of low fruit availability. The plant material is broken down by symbiotic bacteria found in the host’s gut This process releases volatile fatty acids, which are absorbed[22] but the bacteria themselves are digested by the host and are an important source of nitrogen[22,23]. Endogenous digestive enzymes are a crucial component of an animal’s digestive system and include important dietary adaptations[24], such as the enzymes lysozyme and pancreatic ribonuclease

Methods

Results

Discussion

Conclusion