Trehalase Gene as a Molecular Signature of Dietary Diversification in Mammals

Abstract

Diet is a key factor in determining and structuring animal diversity and adaptive radiations. The mammalian fossil record preserves phenotypic evidence of many dietary shifts, whereas genetic changes followed by dietary diversification in mammals remain largely unknown. To test whether living mammals preserve molecular evidence of dietary shifts, we examined the trehalase gene (Treh), which encodes an enzyme capable of digesting trehalose from insect blood, in bats and other mammals with diverse diets. Bats represent the largest dietary radiation among all mammalian orders, with independent origins of frugivory, nectarivory, carnivory, omnivory, and even sanguivory in an otherwise insectivorous clade. We found that Treh has been inactivated in unrelated bat lineages that independently radiated into noninsectivorous niches. Consistently, purifying selection has been markedly relaxed in noninsectivorous bats compared with their insectivorous relatives. Enzymatic assays of intestinal trehalase in bats suggest that trehalase activity tends to be lost or markedly reduced in noninsectivorous bats compared with their insectivorous relatives. Furthermore, our survey of Treh in 119 mammal species, which represent a deeper evolutionary timeframe, additionally identified a number of other independent losses of Treh in noninsectivorous species, recapitulating the evolutionary pattern that we found in bats. These results document a molecular record of dietary diversification in mammals, and suggest that such molecular signatures of dietary shifts would help us understand both historical and modern changes of animal diets.

Long-read sequencing reveals rapid evolution of immunity- and cancer-related genes in bats

“…Trehalase encodes for an enzyme crucial for digestion of trehalose, the primary sugar in insect blood 91 . Trehalase can be duplicated in insects 92 but was found to be a single-copy gene in bats and other mammals 22 . We found evidence for independent deletions of the trehalase gene linked to dietary specialization in noctilionid bat genomes ( Figure 5).…”

“…The insect-eating Pteronotus mesoamericanus and the omnivorous Phyllostomus discolor have each maintained a functional trehalase gene as well as the neighboring pseudogene. The majority of phyllostomids sequenced to date do not have a functional trehalase gene 22,23 , suggesting multiple independent loss events. Such losses of the trehalase gene are linked to dietary shifts across mammals 22 .…”

“…The majority of phyllostomids sequenced to date do not have a functional trehalase gene 22,23 , suggesting multiple independent loss events. Such losses of the trehalase gene are linked to dietary shifts across mammals 22 . These gene losses can occur via small deactivating mutations or larger structural variations such as deletions.…”

“…Although little is known about bat-specific genetic mechanisms of cancer resistance, previous studies have implicated genetic modifications in telomere maintenance genes 19 , tumor suppressors (including TP53 and BRCA2) and DNA damage checkpoint-DNA repair pathway genes 15 as well as growth hormone 20 . Other studies of bats have detected gene losses and positive selection associated with dietary specializations 17,[21][22][23] and echolocation 24,25 .…”

Molecular adaptation and convergent evolution of frugivory in Old World and neotropical fruit bats

“…Among all mammalian orders, Chiroptera (bats) has the widest variety of diets, which include insects and other arthropods, mammals, birds, reptiles, amphibians, fish, blood, carrion, fruit, flowers, nectar, pollen and foliage (Altringham, 1996). Based on palaeontological and phylogenetic analyses, ancestral bats are inferred to have been insectivorous (Gunnell & Simmons, 2005;Jiao et al, 2019;Simmons, Seymour, Habersetzer, & Gunnell, 2008), whereas modern bats show independent origins of frugivory, nectarivory, carnivory and omnivory that are unparalleled in other mammalian clades (Neuweiler, 2000). Although approximately 70% of all bats are insectivorous, two lineages that first diverged around 64 million years ago (Teeling et al, 2005) have independently evolved obligate frugivory.…”