Issue cover image a new study points to evolutionary causes and ecological consequences of the absence of a digestive enzyme in birds

A new article published in Physiological and Biochemical Zoology, “Opportunities lost? Evolutionary causes and ecological consequences of the absence of trehalose digestion in birds,” reveals information on the evolution of birds that demonstrates the vast consequences of seemingly simple causes. The study examined 19 different avian species, and more specifically the absence of a specific digestive enzyme in their gastrointestinal systems. The results demonstrate not only the evolutionary causes of such genetic developments, but the way the consequences can reverberate across entire ecologies.

The study focused on trehalose, a non-reducing disaccharide that serves as a nutritional energy source for a variety of vertebrates. While they can’t synthesize it themselves, many species can digest it with an intestinal enzyme named trehalase that is coded by the Treh gene. Because trehalose is often found in common food sources such as yeasts, fungi, prokaryotes and invertebrates, the ability to process and digest it gives animals that can digest it an energetic advantage. And yet intestinal trehalase activity in bird species is either very low or absent. 

The authors measured the capacity to digest trehalose in the intestinal tissue homogenates of 19 bird species, and conducted genomic surveys of 10 other vertebrate species as a comparison. They followed these studies by proteomic analysis of the digestive hydrolases of the intestinal brush border membrane (BBM) of two mammals and four bird species. They found low or no enzyme activities in birds, the absence of Treh in several bird genomes, and no enzyme protein in their BBMs. Both Treh and the enzyme were found in rats and mice. They speculated that the common ancestor of birds lost the key gene.

To test this hypothesis they included the saltwater crocodile, which shares a common ancestor with birds, and several other vertebrate species (including fishes, amphibians, mammals, and reptiles) in their genomic surveys. They found Treh in all these genomes, except in birds. In all the other vertebrate species the gene was found in a well-conserved block of genes. These observations provide an evolutionary window to detect when birds lost Treh. This gene and the gene block that contains it developed early in this planet’s life: likely before the split between sharks and rays, and bony fishes. In another study, researchers found that in mammals the loss of trehalase activity in some species was the outcome of pseudogenization of Treh when trehalose was not present in a species diet. In certain species of bats, for example, the shift from an insect-based diet to a fruit and nectar based diet is accompanied by accumulations of mutations that lead to Treh’s pseudogenization. In bats that retained an insect-based diet Treh was not pseudogenized. The studied birds, in contrast, didn’t loose Treh by pseudogenization. They simply lost the gene. The authors’ study suggests that the loss was concurrent with the evolution of rearranged and very compact avian genomes. It is likely that birds lost the ability to produce the enzyme at about the time of the evolutionary split between birds, dinosaurs, and crocodilians.

The ecological consequences of this gene disappearance leads to the forfeiture of energy potentially available to birds in common food sources such as insects, which over half of all bird species eat. Similarly, very few bird species consume trehalose-rich fungi, a fact that might be attributed, at least in part to the loss of Treh. Comparisons between them and mammals such as bats, which include species with and without functional intestinal trehalase, can help to assess whether these ecological consequences are general.