Abstract

ABSTRACTAvian keratin disorder (AKD), characterized by debilitating overgrowth of the avian beak, was first documented in black-capped chickadees (Poecile atricapillus) in Alaska. Subsequently, similar deformities have appeared in numerous species across continents. Despite the widespread distribution of this emerging pathology, the cause of AKD remains elusive. As a result, it is unknown whether suspected cases of AKD in the afflicted species are causally linked, and the impacts of this pathology at the population and community levels are difficult to evaluate. We applied unbiased, metagenomic next-generation sequencing to search for candidate pathogens in birds affected with AKD. We identified and sequenced the complete coding region of a novel picornavirus, which we are calling poecivirus. Subsequent screening of 19 AKD-affected black-capped chickadees and 9 control individuals for the presence of poecivirus revealed that 19/19 (100%) AKD-affected individuals were positive, while only 2/9 (22%) control individuals were infected with poecivirus. Two northwestern crows (Corvus caurinus) and two red-breasted nuthatches (Sitta canadensis) with AKD-consistent pathology also tested positive for poecivirus. We suggest that poecivirus is a candidate etiological agent of AKD.

Highlights

  • Avian keratin disorder (AKD), characterized by debilitating overgrowth of the avian beak, was first documented in black-capped chickadees (Poecile atricapillus) in Alaska

  • Birds suffering from this condition, termed avian keratin disorder (AKD), exhibit a variety of beak deformities that interfere with the ability to feed and preen, behaviors vital for survival [1]

  • We assembled the remaining sequences into contiguous sequences using the Trinity de novo assembler [16] and compared the assemblies to the NCBI nonredundant nucleotide and protein databases using BLAST. This search revealed 2 large contigs (3,299 nt and 4,560 nt) with similarities to avian picornaviruses (i.e., 21 to 27% pairwise nucleotide identity with pigeon mesiviruses). We manually assembled these contigs into a 7.6-kb sequence, accounting for most of the genome, including the full open reading frame (ORF), of a novel picornavirus (NCBI accession number KU977108)

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Summary

Introduction

Avian keratin disorder (AKD), characterized by debilitating overgrowth of the avian beak, was first documented in black-capped chickadees (Poecile atricapillus) in Alaska. IMPORTANCE Avian keratin disorder (AKD) is an increasingly common disease of wild birds This disease, characterized by beak overgrowth, was first described in the late 1990s and has been spreading rapidly both geographically and in terms of host species affected. We found a novel and divergent picornavirus in 19/19 AKD-affected black-capped chickadees that we examined but in only 2/9 control cases We found this virus in 4 individuals of 2 other passerine species that exhibited symptoms consistent with AKD. An epizootic of gross beak abnormalities was first documented among black-capped chickadees (BCCH [Poecile atricapillus]) in Alaska in the late 1990s (Fig. 1) [1] Birds suffering from this condition, termed avian keratin disorder (AKD), exhibit a variety of beak deformities (including elongation, crossing, and pronounced curvature) that interfere with the ability to feed and preen, behaviors vital for survival [1]. Despite the similarity of the gross pathology observed in multiple species, it remains unknown whether a common factor is responsible, in part because the cause of AKD remains elusive [4]

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