Abstract
Third-generation (long-read-based) sequencing technologies are reshaping our understanding of genome structure and function. One of the most persistent challenges in genome biology has been confidently reconstructing radiations of complex gene families. Olfactory receptors (ORs) represent just such a gene family with upward of thousands of receptors in some mammalian taxa. Whereas in birds olfaction was historically an overlooked sensory modality, new studies have revealed an important role for smell. Chromosome-level assemblies for birds allow a new opportunity to characterize patterns of OR diversity among major bird lineages. Previous studies of short-read-based (second-generation) genome assemblies have associated OR gene family size with avian ecology, but such conclusions could be premature especially when new assembly methods reshape our understanding of avian OR evolution. Here we provide a fundamental characterization of OR repertoires in five recent genome assemblies, including the most recent assembly of golden-collared manakin (Manacus vitellinus). We find that short read-based assemblies systematically undercount the avian-specific gamma-c OR subfamily, a subfamily that comprises over 65% of avian OR diversity. Therefore, in contrast to previous studies, we find a high diversity of gamma-c ORs across the avian tree of life. Building on these findings, ongoing sequencing efforts and improved genome assemblies will clarify the relationship between OR diversity and avian ecology.
Highlights
Our understanding of avian sensory biology has progressed substantially in recent years
Our results show that Illumina short-read–based approaches were not successful in accurately characterizing the gamma-c Olfactory receptors (ORs) subfamily
In all five of the assemblies sequenced with long reads, we found that gamma-c ORs constituted at least 66% of the OR subgenome, and, on average, there were 148 gamma-c loci per species
Summary
Our understanding of avian sensory biology has progressed substantially in recent years. Misconceptions about bird olfaction date back nearly 200 years, when John James Audubon falsely concluded that turkey vultures (Cathartes aura) could not smell carrion (Audubon 1826). Darwin performed behavioral experiments on Andean condors (Vultur gryphus) to conclude that they could not smell meat (Darwin 1891). An examination of olfactory bulb size across a diversity of bird species concluded that birds could not have anything more than a rudimentary sense of smell (Hill 1905). In response to these conclusions, bird olfaction remained relatively unexplored until behavioral studies showed odor recognition in pigeons (Michelsen 1959). There have been a wealth of morphological and behavioral studies testing for olfaction in both captive and wild birds (Bang and Cobb 1968; Hagelin 2007; Gwinner and Berger 2008; Nevitt et al 2008; Krause et al 2012; Van Huynh and Rice 2019)
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