Dynamic evolution of olfactory receptor genes in the Turkey Vulture and Black Vulture

Abstract

Olfactory receptors (ORs), the largest vertebrate multigene family, exhibit wide copy number variation among taxa, ranging from ∼100 to 4000. The ecological importance of smell has been suggested to positively correlate with OR gene number, though debate exists on whether the number of total ORs, functional ORs, or the percentage of pseudogenes matters most. While olfaction has been poorly studied in most birds, Turkey Vultures (Cathartes aura) demonstrate keen olfactory ability, capable of foraging using smell alone. In contrast, Black Vultures (Coragyps atratus) have been thought to primarily use vision to locate food. Comparison of the OR genes in these two New World vultures presents an opportunity to examine the dynamics of OR evolution in related avian species that may differ in olfactory abilities. Using a PCR and cloning approach with degenerate primers, we sampled the OR subgenome in Turkey and Black Vultures, as well as Red-tailed Hawks (Buteo jamaicensis) and the distantly related Chicken (Gallus gallus), neither of which are thought to use olfaction extensively. Our results indicate that Turkey Vultures have many more OR genes than Red-tailed Hawks or chickens. Surprisingly, Black Vultures had an intermediate number of OR genes. The number of OR genes we estimated in the Turkey Vulture was much greater than previously reported in studies that used short-read sequencing. Additionally, we found that OR genes from New World vultures and Red-tailed Hawks form clades that were distinct from the clade that included most chicken OR genes, indicating that chickens share few OR orthologs with New World vultures or hawks. As previously observed in other animal groups, pseudogenes appeared throughout all clades and their percentage varied among taxa. These findings suggest the OR gene family is highly dynamic, changing rapidly over evolutionary time, and that taxa may have distinct suites of ORs in their genomes.