Relaxed Evolution in the Tyrosine Aminotransferase Gene Tat in Old World Fruit Bats (Chiroptera: Pteropodidae)

Abstract

Frugivorous and nectarivorous bats fuel their metabolism mostly by using carbohydrates and allocate the restricted amounts of ingested proteins mainly for anabolic protein syntheses rather than for catabolic energy production. Thus, it is possible that genes involved in protein (amino acid) catabolism may have undergone relaxed evolution in these fruit- and nectar-eating bats. The tyrosine aminotransferase (TAT, encoded by the Tat gene) is the rate-limiting enzyme in the tyrosine catabolic pathway. To test whether the Tat gene has undergone relaxed evolution in the fruit- and nectar-eating bats, we obtained the Tat coding region from 20 bat species including four Old World fruit bats (Pteropodidae) and two New World fruit bats (Phyllostomidae). Phylogenetic reconstructions revealed a gene tree in which all echolocating bats (including the New World fruit bats) formed a monophyletic group. The phylogenetic conflict appears to stem from accelerated TAT protein sequence evolution in the Old World fruit bats. Our molecular evolutionary analyses confirmed a change in the selection pressure acting on Tat, which was likely caused by a relaxation of the evolutionary constraints on the Tat gene in the Old World fruit bats. Hepatic TAT activity assays showed that TAT activities in species of the Old World fruit bats are significantly lower than those of insectivorous bats and omnivorous mice, which was not caused by a change in TAT protein levels in the liver. Our study provides unambiguous evidence that the Tat gene has undergone relaxed evolution in the Old World fruit bats in response to changes in their metabolism due to the evolution of their special diet.

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

“…Certainly, the evolution of frugivory is considered one of the major ecological release points in the radiation of the Neotropical leaf-nosed bats, as a major burst of lineage diversification occurs after this point ( Rojas et al 2011 ; Rojas et al 2012 ; Rojas et al 2018 ). Indeed, the subfamily Stenodermatinae is often considered an adaptive radiation in its own right, showing unique selective signatures which differentiate it from the other frugivorous subfamilies Carolliinae and Rhinophyllinae ( Dumont et al 2012 ; Shi and Rabosky 2015 ; Rojas et al 2016 ).…”

Molecular Evolution of the Nuclear Factor (Erythroid-Derived 2)-Like 2 Gene Nrf2 in Old World Fruit Bats (Chiroptera: Pteropodidae)

“…Third, sequence changes may have occurred in the regulatory region of the Nrf2 gene in New World fruit bats instead of the coding regions. It is noteworthy that several other recent molecular evolution studies on diet-related genes in bats have also found similar evolutionary discrepancies between Old and New World fruit bats [ 60 – 63 ]. For example, PCK1, which plays an important role in glucose homeostasis during fasting, also has specific amino acid changes in the Old World fruit bats but not in New World fruit bats [ 62 ].…”

“…For example, PCK1, which plays an important role in glucose homeostasis during fasting, also has specific amino acid changes in the Old World fruit bats but not in New World fruit bats [ 62 ]. The tat gene, which encodes tyrosine aminotransferase (TAT) that is involved in amino acid metabolism, has undergone relaxed evolution in Old World fruit bats but not in New World fruit bats [ 63 ]. Since our results were obtained from a single New World fruit bat of the family Phyllostomidae, more sampling of New World fruit bats is needed to further confirm this finding.…”

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.…”