Ecological factors drive natural selection pressure of avian aryl hydrocarbon receptor 1 genotypes

Abstract

The aryl hydrocarbon receptor (AHR) mediates dioxin toxicities. Several studies have suggested that two amino acid residues corresponding to the 324th and 380th positions in the ligand binding domain (LBD) of the chicken AHR1 (Ile_Ser as high sensitivity, Ile_Ala as moderate sensitivity, and Val_Ala as low sensitivity), could be an important factor determining dioxin sensitivity in avian species. Here, we analyzed the association between ecological factors and AHR1 LBD genotypes of 113 avian species. Cluster analyses showed that 2 major clusters and sub-clusters of the cluster 3 were associated with specific AHR1 genotypes depending on the food, habitat, and migration of the animal. The majority of the species with Ile_Ala type were the Passeriformes, which are omnivorous or herbivorous feeders in the terrestrial environment. The species with Val_Ala type was primarily composed of raptors and waterbirds, which have been exposed to naturally occurring dioxins. An in vitro reporter gene assay revealed that the sensitivity to a natural dioxin, 1,3,7-tribromodibenzo-p-dioxin was in the order of Ile_Ser > Ile_Ala > Val_Ala. These results suggest that ecological factors related to the exposure of natural dioxins contribute to natural selection of the avian AHR1 genotype, which consequently leads to different sensitivity to man-made dioxins.

Organochlorine Chemical Residues in Northern Cardinal (Cardinalis cardinalis) Eggs from Greater Washington, DC USA

“…However, we cannot discount the potential contribution of other unmeasured congeners or structurally similar compounds (e.g., chlorinated dioxins and furans) that may be present at very low concentrations. In addition, the consensus avian TEFs are dated, and more recent research has revealed substantial among-species differences in sensitivity to dioxinlike compounds (e.g., Farmahin et al 2012;Hwang et al 2016).…”

The evolution of UDP-glycosyl/glucuronosyltransferase 1E (UGT1E) genes in bird lineages is linked to feeding habits but UGT2 genes is not

“…Avian AhRs are divided into three genetic types: highly sensitive (Ile-324 and Ser-380), moderately sensitive (Ile-324 and Ala-380), and less sensitive to dioxin (Val-324 and Ala-380) [ 36 , 37 ]. Certain species may have more of the third genetic type because they receive elevated levels of naturally occurring dioxins through the food web in specific habitats or under specific diets [ 38 ]. The lack of any observed relationship between UGTs and habitat in this study could be because UGTs are not directly involved in dealing with toxicity from dioxin-like compounds [ 36 ].…”

Species traits predict the aryl hydrocarbon receptor 1 (AHR1) subtypes responsible for dioxin sensitivity in birds

“…Remarkably, there appears to be little correspondence between the three AHR1 LBD types and phylogeny, particularly for the high sensitivity type 1 group 9,16 . Hwang et al 9 showed that the transactivation potential of a naturally-occurring dioxin was in the order of type 1 > type 2 > type 3 and demonstrated that factors related to the exposure of birds to naturally occurring dioxins, including a species' habitat and diet, may have contributed to the natural selection of the three AHR1 LBD types in avian species during their evolution. It is therefore possible that other biological and ecological factors could have influenced the evolution of the 13 AHR1 LBD subtypes in birds, but this has not been explored.…”

“…However, the AHR is an orphan receptor, and its endogenous role is not well understood 7 . Although a variety of endogenous AHR ligands have been identified 6 , and there is evidence that exogenous factors may have influenced the evolution of the AHR 9 , the endogenous role of the AHR and the reason why it is so highly conserved are unknown 6,7 .…”

“…Our objective was to evaluate support for a broad suite of species traits that might explain variations in the 13 AHR1 LBD subtypes in birds. We collected data for the three traits examined by Hwang et al 9 (diet, habitat, and migration), and we built on their work by also collecting information for the maximum number of physiological and ecological traits for which there were sufficient data for a large number of avian species. Ultimately, we examined traits indicative of each species' developmental rate, fecundity and reproduction, levels of contaminant depuration into the egg, body size, and longevity (physiological traits), and each species' migration strategy, range, habitat type, tropic level, and degree of sociality and sexual competition (ecological traits).…”