The Glycogen Synthase 2 Gene (Gys2) Displays Parallel Evolution Between Old World and New World Fruit Bats

Abstract

Frugivorous and nectarivorous bats rely largely on hepatic glycogenesis and glycogenolysis for postprandial blood glucose disposal and maintenance of glucose homeostasis during short time starvation, respectively. The glycogen synthase 2 encoded by the Gys2 gene plays a critical role in liver glycogen synthesis. To test whether the Gys2 gene has undergone adaptive evolution in bats with carbohydrate-rich diets in relation to their insect-eating sister taxa, we sequenced the coding region of the Gys2 gene in a number of bat species, including three Old World fruit bats (OWFBs) (Pteropodidae) and two New World fruit bats (NWFBs) (Phyllostomidae). Our results showed that the Gys2 coding sequences are highly conserved across all bat species we examined, and no evidence of positive selection was detected in the ancestral branches leading to OWFBs and NWFBs. Our explicit convergence test showed that posterior probabilities of convergence between several branches of OWFBs, and the NWFBs were markedly higher than that of divergence. Three parallel amino acid substitutions (Q72H, K371Q, and E666D) were detected among branches of OWFBs and NWFBs. Tests for parallel evolution showed that two parallel substitutions (Q72H and E666D) were driven by natural selection, while the K371Q was more likely to be fixed randomly. Thus, our results suggested that the Gys2 gene has undergone parallel evolution on amino acid level between OWFBs and NWFBs in relation to their carbohydrate metabolism.

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

“…In fact, in many evolutionary histories, positive selection occurs episodically and is patchily distributed within a phylogeny ( Murrell et al 2012 ) such that lineages show acceleration or deceleration of molecular adaptation with respect to the background. In cases where rapid species divergence is associated with the occurrence of adaptive substitutions over short timeframes, insufficient time may pass to allow the accrual of synonymous changes, thereby increasing the chance of detecting positive selection in short branches ( dos Reis 2015 ; Indjeian et al 2016 ; Thiltgen et al 2017 ). Therefore, given that the numbers of PSGs do not follow this pattern and, in many cases, support our hypotheses based on dietary specialization, it appears that branch length is unlikely to account for the patterns we observe.…”

Nectar-feeding bats and birds show parallel molecular adaptations in sugar metabolism enzymes

“…23 Our results from GYS2 advance previous reports of parallel substitutions between fruit-eating species. 24,25 Finally, in glossophagine bats, we found molecular adaptation in SORD, which encodes sorbitol dehydrogenase (SDH). This protein functions to clear excess dietary glucose by conversion to sorbitol and then fructose via the polyol pathway.…”

Integrative single-cell characterization of frugivory adaptations in the bat kidney and pancreas

“…Prior to our study, identifying potential molecular adaptations to frugivory was mainly restricted to molecular evolutionary analyses of specific genes and comparative genomics (3,20,21,(33)(34)(35)(36)(37)(38)(39)80). Here, we were able to use scRNA-seq to systematically identify gene expression differences in an unbiased manner.…”

“…Comparative investigations of mammalian frugivorous adaptation have been primarily performed on a gene-by-gene basis, focusing on metabolism. These include genes such as GYS1 and GYS2 (glycogenesis), NRF2 (antioxidant regulation), TAT (protein catabolism), SLC2A4 (glucose transport), and AGT (glyoxylate detoxification) (33)(34)(35)(36)(37)(38)(39). In terms of gene regulatory elements, there are a limited number of studies.…”