Raptor genomes reveal evolutionary signatures of predatory and nocturnal lifestyles

Abstract

1 Background: Birds of prey (raptors) are dominant apex predators in terrestrial communities, 2 with hawks (Accipitriformes) and falcons (Falconiformes) hunting by day, and owls 3 (Strigiformes) hunting by night. 4 Results: Here, we report new genomes and transcriptomes for 20 species of birds, including 16 5 species of birds of prey, and high-quality reference genomes for the Eurasian eagle-owl (Bubo 6 bubo), oriental scops-owl (Otus sunia), eastern buzzard (Buteo japonicus), and common kestrel 7 (Falco tinnunculus). Our extensive genomic analysis and comparisons with non-raptor genomes 8 identified common molecular signatures that underpin anatomical structure and sensory, muscle, 9 circulatory, and respiratory systems related to a predatory lifestyle. Compared with diurnal birds, 10 owls exhibit striking adaptations to the nocturnal environment, including functional trade-offs in 11 the sensory systems (e.g., loss of color vision genes and selection for enhancement of nocturnal 12 vision and other sensory systems) that are probably convergent with other nocturnal avian orders. 13 Additionally, we found that a suite of genes associated with vision and circadian rhythm were 14 differentially expressed between nocturnal and diurnal raptors, indicating adaptive expression 15 change during the transition to nocturnality. 16 Conclusions: Overall, raptor genomes showed genomic signatures associated with the origin and 17 maintenance of several specialized physiological and morphological features essential to be apex 18 predators.19

Genomic Evidence for Sensorial Adaptations to a Nocturnal Predatory Lifestyle in Owls

“…The overrepresented functional group linked to sensory perception includes 50 genes that evolved faster in the owl ancestor ( ω background < ω foreground < 1). We found confirmatory evidence that four of these genes ( CNGB1 , ABCA4 , PCDH15 , and BEST1 ) have evolved faster in the owl ancestor, as reported in previous studies ( Wu et al 2016 ; Cho et al 2019 ). The gene RP1 is also present in the functional network of genes showing positive selection on specific sites (list iii) and links to a function for microtubules, which might be associated with the development and maintenance of photoreceptors.…”

“…Our finding that the genes RGS9 , BEST1 , RRH , RDH8 , RPE65 , PDE6B , and ALCAM evolved faster in the ancestral branch of owls than in the background branches, partially confirm previous results for nocturnal birds and raptors ( Wu et al 2016 ; Cho et al 2019 ; Zhou et al 2019 ). These genes are functionally related to visual perception, photoreceptor activity, phototransduction cascades, regeneration of visual pigments, and retina development, and some of them have been linked to genetic diseases related to vision in humans.…”

Falcon genomics in the context of conservation, speciation, and human culture

“…The saker ( Falco cherrug ) and peregrine ( F. peregrinus ) falcon genomes were sequenced at high depth (>100) using Illumina paired‐end short reads with short and large insert libraries and achieved relatively large scaffold sizes of 4.15 and 3.89 Mb, respectively (Zhan et al, ). The common kestrel ( Falco tinnunculus ) genome was sequenced more recently using similar methods, but with a very high depth of approximately 500× and achieved a scaffold N50 of 21 Mb (Cho et al, ). Less complete and lower coverage draft genomes have also recently been produced for two additional falcon species: A gyrfalcon ( Falco rusticolus ) draft genome has been assembled with a scaffold N50 of 32.8 kb (Joseph et al, ), and a prairie falcon ( Falco mexicanus ) draft genome has been assembled with a scaffold N50 of 3.7 kb (Doyle et al, ).…”

“…However, many basic traits of falcon genomes appear less typical. The falcon genomes have more genes annotated than many other avian genomes: Combined homology and de novo transcriptomic‐based approaches suggested between 16,204 and 16,481 protein‐coding genes across the annotated falcon genomes (Cho et al, ; Doyle et al, ; Zhan et al, ). In comparison, a standardized meta‐analysis found an average of 15,101 annotated protein‐coding genes in other birds and placed the peregrine falcon in the top quartile of annotated‐gene counts for birds with 16,242 reference‐based annotations (Zhang et al, ).…”

“…The annotated genes of the peregrine falcon genome are also relatively long: Total gene‐sequence lengths, coding‐sequence lengths, exon lengths, and intergenic distances were all in the upper quartile range for bird genomes, and intron lengths are also above the median length for birds (Zhang et al, ). Despite these greater sequence lengths, repetitive and transposable DNA elements are reported to account for a smaller portion of the falcon genome than typical of birds (Cho et al, ; Zhan et al, ; Zhang et al, ). Instead, a lack of deletions might explain some of the trends toward greater sequence lengths: An analysis of genome size evolution in both birds and mammals reported the peregrine falcon as having the lowest rate of microdeletions (i.e., deletions <30 bp) of the seven birds that were compared Kapusta et al, ).…”