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Dietary Diversification and Specialization in Neotropical Bats Facilitated by Early Molecular Evolution.

ABSTRACT: Dietary adaptation is a major feature of phenotypic and ecological diversification, yet the genetic basis of dietary shifts is poorly understood. Among mammals, Neotropical leaf-nosed bats (family Phyllostomidae) show unmatched diversity in diet; from a putative insectivorous ancestor, phyllostomids have radiated to specialize on diverse food sources including blood, nectar, and fruit. To assess whether dietary diversification in this group was accompanied by molecular adaptations for changing metabolic demands, we sequenced 89 transcriptomes across 58 species and combined these with published data to compare ∼13,000 protein coding genes across 66 species. We tested for positive selection on focal lineages, including those inferred to have undergone dietary shifts. Unexpectedly, we found a broad signature of positive selection in the ancestral phyllostomid branch, spanning genes implicated in the metabolism of all major macronutrients, yet few positively selected genes at the inferred switch to plantivory. Branches corresponding to blood- and nectar-based diets showed selection in loci underpinning nitrogenous waste excretion and glycolysis, respectively. Intriguingly, patterns of selection in metabolism genes were mirrored by those in loci implicated in craniofacial remodeling, a trait previously linked to phyllostomid dietary specialization. Finally, we show that the null model of the widely-used branch-site test is likely to be misspecified, with the implication that the test is too conservative and probably under-reports true cases of positive selection. Our findings point to a complex picture of adaptive radiation, in which the evolution of new dietary specializations has been facilitated by early adaptations combined with the generation of new genetic variation.

SUBMITTER: Potter JHT

PROVIDER: S-EPMC8382914 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:As the most species-rich class of tetrapod vertebrates, Aves possesses diverse feeding habits, with multiple origins of insectivory, carnivory, frugivory, nectarivory, granivory and omnivory. Since digestive enzymes mediate and limit energy and nutrient uptake, we hypothesized that genes encoding digestive enzymes have undergone adaptive evolution in birds. To test this general hypothesis, we identified 16 digestive enzyme genes (including seven carbohydrase genes (hepatic amy, pancreatic amy, salivary amy, agl, g6pc, gaa and gck), three lipase genes (cyp7a1, lipf and pnlip), two protease genes (ctrc and pgc), two lysozyme genes (lyz and lyg) and two chitinase genes (chia and chit1)) from the available genomes of 48 bird species. Among these 16 genes, three (salivary amy, lipf and chit1) were not found in all 48 avian genomes, which was further supported by our synteny analysis. Of the remaining 13 genes, eight were single-copy and five (chia, gaa, lyz, lyg and pgc) were multi-copy. Moreover, the multi-copy genes gaa, lyg and pgc were predicted to exhibit functional divergence among copies. Positively selected sites were detected in all of the analyzed digestive enzyme genes, except agl, g6pc, gaa and gck, suggesting that different diets may have favored differences in catalytic capacities of these enzymes. Furthermore, the analysis also revealed that the pancreatic amylase gene and one of the lipase genes (cyp7a1) have higher ω (the ratio of nonsynonymous to the synonymous substitution rates) values in species consuming a larger amount of seeds and meat, respectively, indicating an intense selection. In addition, the gck carbohydrase gene in species consuming a smaller amount of seeds, fruits or nectar, and a lipase gene (pnlip) in species consuming less meat were found to be under relaxed selection. Thus, gene loss, gene duplication, functional divergence, positive selection and relaxed selection have collectively shaped the evolution of digestive enzymes in birds, and the evolutionary flexibility of these enzymes may have facilitated their dietary diversification.

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Dietary Diversification and Specialization in Neotropical Bats Facilitated by Early Molecular Evolution.

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