Gene loss, adaptive evolution and the co-evolution of plumage coloration genes with opsins in birds

Borges, Rui; Khan, Imran; Johnson, Warren E.; Gilbert, M. Thomas P.; Zhang, Guojie; Jarvis, Erich D.; O’Brien, Stephen J.; Antunes, Agostinho

doi:10.1186/s12864-015-1924-3

Cited by 66 publications

(75 citation statements)

References 79 publications

(116 reference statements)

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“…As expected, gene families associated with vision were commonly contracted in the nocturnal birds (Additional file 1: Tables S34 and S35). Specifically, gene loss of the violet/ultraviolet-sensitive opsin SWS1 ( OPN1SW ) was found in all of the nocturnal bird genomes, as previously reported [4, 22]. The nocturnal birds also showed common selection signatures likely linked to their adaptation to a nocturnal environment.…”

Section: Resultssupporting

confidence: 72%

Raptor genomes reveal evolutionary signatures of predatory and nocturnal lifestyles

Cho¹,

Jun²,

Kim

et al. 2019

Preprint

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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

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Section: Resultssupporting

confidence: 72%

Raptor genomes reveal evolutionary signatures of predatory and nocturnal lifestyles

Cho¹,

Jun²,

Kim

et al. 2019

Preprint

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“…By contrast, the genes flanking c TMT , namely uxs1 and st6gal2 , were found to be conserved relative to zebrafish ( zTMT2B ) (Fig 2B) and clawed frog TMT2 (data not shown). Two types of TMT opsin genes, TMT1 and TMT2, have been observed in birds [20]. In the flycatcher and lizard genomes, the tmtop1 (TMT1) locus is situated between the st6gal1 and gpr35 loci (Fig 3B).…”

Section: Resultsmentioning

confidence: 99%

Two Opsin 3-Related Proteins in the Chicken Retina and Brain: A TMT-Type Opsin 3 Is a Blue-Light Sensor in Retinal Horizontal Cells, Hypothalamus, and Cerebellum

et al. 2016

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Opsin family genes encode G protein-coupled seven-transmembrane proteins that bind a retinaldehyde chromophore in photoreception. Here, we sought potential as yet undescribed avian retinal photoreceptors, focusing on Opsin 3 homologs in the chicken. We found two Opsin 3-related genes in the chicken genome: one corresponding to encephalopsin/panopsin (Opn3) in mammals, and the other belonging to the teleost multiple tissue opsin (TMT) 2 group. Bioluminescence imaging and G protein activation assays demonstrated that the chicken TMT opsin (cTMT) functions as a blue light sensor when forced-expressed in mammalian cultured cells. We did not detect evidence of light sensitivity for the chicken Opn3 (cOpn3). In situ hybridization demonstrated expression of cTMT in subsets of differentiating cells in the inner retina and, as development progressed, predominant localization to retinal horizontal cells (HCs). Immunohistochemistry (IHC) revealed cTMT in HCs as well as in small numbers of cells in the ganglion and inner nuclear layers of the post-hatch chicken retina. In contrast, cOpn3-IR cells were found in distinct subsets of cells in the inner nuclear layer. cTMT-IR cells were also found in subsets of cells in the hypothalamus. Finally, we found differential distribution of cOpn3 and cTMT proteins in specific cells of the cerebellum. The present results suggest that a novel TMT-type opsin 3 may function as a photoreceptor in the chicken retina and brain.

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“…These data suggest that although reducing the amount of red oil droplets may be common in dim light-adapted species, their complete loss is relatively rare, and may be indicative that penguins, owls and kiwis are among the best adapted to dim light. Indeed, among avian taxa, only owls (Bowmaker and Martin, 1978;Borges et al, 2015;Wu et al, 2016;Hanna et al, under review), penguins (Bowmaker and Martin, 1985;Li et al, 2014;Borges et al, 2015) and kiwis (Le Duc et al, 2015) show evidence of reduction in the number of cone visual pigment classes, an otherwise common pattern among vertebrates adapted to dim light (Douglas et al, 1995;Meredith et al, 2013;Jacobs, 2013;Emerling and Springer, 2014;Emerling, 2017).…”

Section: Retention Of Cyp2j19 Across Most Avian Taxamentioning

confidence: 99%

Independent pseudogenization ofCYP2J19in penguins, owls and kiwis implicates gene in red carotenoid synthesis

Emerling

2017

Preprint

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Carotenoids have important roles in bird behavior, including pigmentation for sexual signaling and improving color vision via retinal oil droplets. Yellow carotenoids are dietderived, but red carotenoids (ketocarotenoids) are typically synthesized from yellow precursors via a carotenoid ketolase. Recent research on passerines has provided evidence that a cytochrome p450 enzyme, CYP2J19, is responsible for this reaction, though it is unclear if this function is phylogenetically restricted. Here I provide evidence that CYP2J19 is the carotenoid ketolase common to Aves using the genomes of 65 birds and the retinal transcriptomes of 15 avian taxa. CYP2J19 is functionally intact and robustly transcribed in all taxa except for several species adapted to foraging in dim light conditions. Two penguins, an owl and a kiwi show evidence of genetic lesions and relaxed selection in their genomic copy of CYP2J19, and six owls show evidence of marked reduction in CYP2J19 retinal transcription compared to nine diurnal avian taxa. Notably, none of these taxa are known to use red carotenoids for sexual signaling and several species of owls and penguins represent the only birds known to completely lack red retinal oil droplets. The remaining avian taxa belong to groups known to possess red oil droplets, known or expected to deposit red carotenoids in skin and/or plumage, and/or frequently forage in bright light.The loss and reduced expression of CYP2J19 is likely an adaptation to maximize retinal sensitivity, given that oil droplets reduce the amount of light available to the retina.

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Gene loss, adaptive evolution and the co-evolution of plumage coloration genes with opsins in birds

Cited by 66 publications

References 79 publications

Raptor genomes reveal evolutionary signatures of predatory and nocturnal lifestyles

Raptor genomes reveal evolutionary signatures of predatory and nocturnal lifestyles

Two Opsin 3-Related Proteins in the Chicken Retina and Brain: A TMT-Type Opsin 3 Is a Blue-Light Sensor in Retinal Horizontal Cells, Hypothalamus, and Cerebellum

Independent pseudogenization ofCYP2J19in penguins, owls and kiwis implicates gene in red carotenoid synthesis

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