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

Borges R, Khan I, Johnson WE, Gilbert MT, Zhang G, Jarvis ED, O'Brien SJ, Antunes A - BMC Genomics (2015)

Bottom Line: At the intra-avian level we observed some unique adaptive patterns.These patterns in the barn owl and penguins were convergent with adaptive strategies in nocturnal and aquatic mammals, respectively.We conclude that birds have evolved diverse opsin adaptations through gene loss, adaptive selection and coevolution with plumage coloration, and that differentiated selective patterns at the species level suggest novel photic pressures to influence evolutionary patterns of more-recent lineages.

View Article: PubMed Central - PubMed

Affiliation: CIIMAR/CIMAR, Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Rua dos Bragas, 177, 4050-123, Porto, Portugal. ruiborges23@gmail.com.

ABSTRACT

Background: The wide range of complex photic systems observed in birds exemplifies one of their key evolutionary adaptions, a well-developed visual system. However, genomic approaches have yet to be used to disentangle the evolutionary mechanisms that govern evolution of avian visual systems.

Results: We performed comparative genomic analyses across 48 avian genomes that span extant bird phylogenetic diversity to assess evolutionary changes in the 17 representatives of the opsin gene family and five plumage coloration genes. Our analyses suggest modern birds have maintained a repertoire of up to 15 opsins. Synteny analyses indicate that PARA and PARIE pineal opsins were lost, probably in conjunction with the degeneration of the parietal organ. Eleven of the 15 avian opsins evolved in a non-neutral pattern, confirming the adaptive importance of vision in birds. Visual conopsins sw1, sw2 and lw evolved under negative selection, while the dim-light RH1 photopigment diversified. The evolutionary patterns of sw1 and of violet/ultraviolet sensitivity in birds suggest that avian ancestors had violet-sensitive vision. Additionally, we demonstrate an adaptive association between the RH2 opsin and the MC1R plumage color gene, suggesting that plumage coloration has been photic mediated. At the intra-avian level we observed some unique adaptive patterns. For example, barn owl showed early signs of pseudogenization in RH2, perhaps in response to nocturnal behavior, and penguins had amino acid deletions in RH2 sites responsible for the red shift and retinal binding. These patterns in the barn owl and penguins were convergent with adaptive strategies in nocturnal and aquatic mammals, respectively.

Conclusions: We conclude that birds have evolved diverse opsin adaptations through gene loss, adaptive selection and coevolution with plumage coloration, and that differentiated selective patterns at the species level suggest novel photic pressures to influence evolutionary patterns of more-recent lineages.

No MeSH data available.


Related in: MedlinePlus

The presence/absence patterns of avian opsins. Green circles indicate the presence of a complete gene sequence; yellow circles represent a partial gene sequence; red cross indicates that no sequences were found by t-blastn searches. For the visual opsins, the species highlighted with a yellow line have a tetrachromatic visual system. The bird phylogeny and the mean divergence times were based on Jarvis et. al (2014) [17]. The high coverage genomes (≥80X) are indicated in bold. Numbers identify each species: 1. Merops nubicus, 2. Picoides pubescens, 3. Buceros rhinoceros, 4. Apaloderma vittatum, 5. Leptosomus discolor, 6. Colius striatus, 7. Tyto alba, 8. Haliaeetus leucocephalus, 9. Haliaeetus albicilla, 10. Cathartes aura, 11. Taeniopygia guttata, 12. Geospiza fortis, 13. Corvus brachyrhynchos, 14. Manacus vitellinus, 15. Acanthisitta chloris, 16. Nestor notabilis, 17. Melopsittacus undulatus, 18. Falco peregrinus, 19. Cariama cristata, 20. Pelecanus crispus, 21. Egretta garzetta, 22. Nipponia nippon, 23. Phalacrocorax carbo, 24. Aptenodytes forsteri, 25. Pygoscelis adeliae, 26. Fulmarus glacialis, 27. Gavia stellata, 28. Eurypyga helias, 29. Phaethon lepturus, 30. Balearica regulorum, 31. Charadrius vociferus, 32. Opisthocomus hoazin, 33. Calypte anna, 34. Chaetura pelagica, 35. Antrostomus carolinensis, 36. Chlamydotis macqueenii, 37. Tauraco erythrolophus, 38. Cuculus canorus, 39. Mesitornis unicolor, 40. Pterocles gutturalis, 41. Columba livia, 42. Podiceps cristatus, 43. Phoenicopterus ruber, 44. Meleagris gallopavo, 45. Gallus gallus, 46. Anas platyrhynchos, 47. Struthio camelus and 48. Tinamus major
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Fig1: The presence/absence patterns of avian opsins. Green circles indicate the presence of a complete gene sequence; yellow circles represent a partial gene sequence; red cross indicates that no sequences were found by t-blastn searches. For the visual opsins, the species highlighted with a yellow line have a tetrachromatic visual system. The bird phylogeny and the mean divergence times were based on Jarvis et. al (2014) [17]. The high coverage genomes (≥80X) are indicated in bold. Numbers identify each species: 1. Merops nubicus, 2. Picoides pubescens, 3. Buceros rhinoceros, 4. Apaloderma vittatum, 5. Leptosomus discolor, 6. Colius striatus, 7. Tyto alba, 8. Haliaeetus leucocephalus, 9. Haliaeetus albicilla, 10. Cathartes aura, 11. Taeniopygia guttata, 12. Geospiza fortis, 13. Corvus brachyrhynchos, 14. Manacus vitellinus, 15. Acanthisitta chloris, 16. Nestor notabilis, 17. Melopsittacus undulatus, 18. Falco peregrinus, 19. Cariama cristata, 20. Pelecanus crispus, 21. Egretta garzetta, 22. Nipponia nippon, 23. Phalacrocorax carbo, 24. Aptenodytes forsteri, 25. Pygoscelis adeliae, 26. Fulmarus glacialis, 27. Gavia stellata, 28. Eurypyga helias, 29. Phaethon lepturus, 30. Balearica regulorum, 31. Charadrius vociferus, 32. Opisthocomus hoazin, 33. Calypte anna, 34. Chaetura pelagica, 35. Antrostomus carolinensis, 36. Chlamydotis macqueenii, 37. Tauraco erythrolophus, 38. Cuculus canorus, 39. Mesitornis unicolor, 40. Pterocles gutturalis, 41. Columba livia, 42. Podiceps cristatus, 43. Phoenicopterus ruber, 44. Meleagris gallopavo, 45. Gallus gallus, 46. Anas platyrhynchos, 47. Struthio camelus and 48. Tinamus major

Mentions: We retrieved sequences of opsin genes through t-blastn searches in 48 bird genomes [17] using the well annotated chicken (Gallus gallus) and zebra finch (Taeniopygia guttata) opsin gene sequences as queries. We found most opsins assumed to be present in tetrapoda genomes: RH1, RH2, OPN1lw, OPN1sw1, OPN1sw2, OPN4m, OPN4x, OPN3, RGR, RRH, OPN5, PIN and VA (Fig. 1). We also identified for the first time the two different types of teleost multiple tissue opsin genes in birds (designated as TMT and TMT2). We could not find the parietopsin and parapinopsin pineal opsins (PARA and PARIE) in any of the 48 studied genomes (blast searches conducted on the raw read sequences; Fig. 1). Syntenic analyses of other genes around where PARA and PARIE pineal genes were expected suggest that they were lost in birds and mammals (Fig. 2); only non-avian reptiles have the PARIE and PARA genes. These results suggest that birds have a repertoire of 15 opsin representatives, and that PARIE and PARA were independently lost in both birds and mammals.Fig. 1


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

Borges R, Khan I, Johnson WE, Gilbert MT, Zhang G, Jarvis ED, O'Brien SJ, Antunes A - BMC Genomics (2015)

The presence/absence patterns of avian opsins. Green circles indicate the presence of a complete gene sequence; yellow circles represent a partial gene sequence; red cross indicates that no sequences were found by t-blastn searches. For the visual opsins, the species highlighted with a yellow line have a tetrachromatic visual system. The bird phylogeny and the mean divergence times were based on Jarvis et. al (2014) [17]. The high coverage genomes (≥80X) are indicated in bold. Numbers identify each species: 1. Merops nubicus, 2. Picoides pubescens, 3. Buceros rhinoceros, 4. Apaloderma vittatum, 5. Leptosomus discolor, 6. Colius striatus, 7. Tyto alba, 8. Haliaeetus leucocephalus, 9. Haliaeetus albicilla, 10. Cathartes aura, 11. Taeniopygia guttata, 12. Geospiza fortis, 13. Corvus brachyrhynchos, 14. Manacus vitellinus, 15. Acanthisitta chloris, 16. Nestor notabilis, 17. Melopsittacus undulatus, 18. Falco peregrinus, 19. Cariama cristata, 20. Pelecanus crispus, 21. Egretta garzetta, 22. Nipponia nippon, 23. Phalacrocorax carbo, 24. Aptenodytes forsteri, 25. Pygoscelis adeliae, 26. Fulmarus glacialis, 27. Gavia stellata, 28. Eurypyga helias, 29. Phaethon lepturus, 30. Balearica regulorum, 31. Charadrius vociferus, 32. Opisthocomus hoazin, 33. Calypte anna, 34. Chaetura pelagica, 35. Antrostomus carolinensis, 36. Chlamydotis macqueenii, 37. Tauraco erythrolophus, 38. Cuculus canorus, 39. Mesitornis unicolor, 40. Pterocles gutturalis, 41. Columba livia, 42. Podiceps cristatus, 43. Phoenicopterus ruber, 44. Meleagris gallopavo, 45. Gallus gallus, 46. Anas platyrhynchos, 47. Struthio camelus and 48. Tinamus major
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4595237&req=5

Fig1: The presence/absence patterns of avian opsins. Green circles indicate the presence of a complete gene sequence; yellow circles represent a partial gene sequence; red cross indicates that no sequences were found by t-blastn searches. For the visual opsins, the species highlighted with a yellow line have a tetrachromatic visual system. The bird phylogeny and the mean divergence times were based on Jarvis et. al (2014) [17]. The high coverage genomes (≥80X) are indicated in bold. Numbers identify each species: 1. Merops nubicus, 2. Picoides pubescens, 3. Buceros rhinoceros, 4. Apaloderma vittatum, 5. Leptosomus discolor, 6. Colius striatus, 7. Tyto alba, 8. Haliaeetus leucocephalus, 9. Haliaeetus albicilla, 10. Cathartes aura, 11. Taeniopygia guttata, 12. Geospiza fortis, 13. Corvus brachyrhynchos, 14. Manacus vitellinus, 15. Acanthisitta chloris, 16. Nestor notabilis, 17. Melopsittacus undulatus, 18. Falco peregrinus, 19. Cariama cristata, 20. Pelecanus crispus, 21. Egretta garzetta, 22. Nipponia nippon, 23. Phalacrocorax carbo, 24. Aptenodytes forsteri, 25. Pygoscelis adeliae, 26. Fulmarus glacialis, 27. Gavia stellata, 28. Eurypyga helias, 29. Phaethon lepturus, 30. Balearica regulorum, 31. Charadrius vociferus, 32. Opisthocomus hoazin, 33. Calypte anna, 34. Chaetura pelagica, 35. Antrostomus carolinensis, 36. Chlamydotis macqueenii, 37. Tauraco erythrolophus, 38. Cuculus canorus, 39. Mesitornis unicolor, 40. Pterocles gutturalis, 41. Columba livia, 42. Podiceps cristatus, 43. Phoenicopterus ruber, 44. Meleagris gallopavo, 45. Gallus gallus, 46. Anas platyrhynchos, 47. Struthio camelus and 48. Tinamus major
Mentions: We retrieved sequences of opsin genes through t-blastn searches in 48 bird genomes [17] using the well annotated chicken (Gallus gallus) and zebra finch (Taeniopygia guttata) opsin gene sequences as queries. We found most opsins assumed to be present in tetrapoda genomes: RH1, RH2, OPN1lw, OPN1sw1, OPN1sw2, OPN4m, OPN4x, OPN3, RGR, RRH, OPN5, PIN and VA (Fig. 1). We also identified for the first time the two different types of teleost multiple tissue opsin genes in birds (designated as TMT and TMT2). We could not find the parietopsin and parapinopsin pineal opsins (PARA and PARIE) in any of the 48 studied genomes (blast searches conducted on the raw read sequences; Fig. 1). Syntenic analyses of other genes around where PARA and PARIE pineal genes were expected suggest that they were lost in birds and mammals (Fig. 2); only non-avian reptiles have the PARIE and PARA genes. These results suggest that birds have a repertoire of 15 opsin representatives, and that PARIE and PARA were independently lost in both birds and mammals.Fig. 1

Bottom Line: At the intra-avian level we observed some unique adaptive patterns.These patterns in the barn owl and penguins were convergent with adaptive strategies in nocturnal and aquatic mammals, respectively.We conclude that birds have evolved diverse opsin adaptations through gene loss, adaptive selection and coevolution with plumage coloration, and that differentiated selective patterns at the species level suggest novel photic pressures to influence evolutionary patterns of more-recent lineages.

View Article: PubMed Central - PubMed

Affiliation: CIIMAR/CIMAR, Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Rua dos Bragas, 177, 4050-123, Porto, Portugal. ruiborges23@gmail.com.

ABSTRACT

Background: The wide range of complex photic systems observed in birds exemplifies one of their key evolutionary adaptions, a well-developed visual system. However, genomic approaches have yet to be used to disentangle the evolutionary mechanisms that govern evolution of avian visual systems.

Results: We performed comparative genomic analyses across 48 avian genomes that span extant bird phylogenetic diversity to assess evolutionary changes in the 17 representatives of the opsin gene family and five plumage coloration genes. Our analyses suggest modern birds have maintained a repertoire of up to 15 opsins. Synteny analyses indicate that PARA and PARIE pineal opsins were lost, probably in conjunction with the degeneration of the parietal organ. Eleven of the 15 avian opsins evolved in a non-neutral pattern, confirming the adaptive importance of vision in birds. Visual conopsins sw1, sw2 and lw evolved under negative selection, while the dim-light RH1 photopigment diversified. The evolutionary patterns of sw1 and of violet/ultraviolet sensitivity in birds suggest that avian ancestors had violet-sensitive vision. Additionally, we demonstrate an adaptive association between the RH2 opsin and the MC1R plumage color gene, suggesting that plumage coloration has been photic mediated. At the intra-avian level we observed some unique adaptive patterns. For example, barn owl showed early signs of pseudogenization in RH2, perhaps in response to nocturnal behavior, and penguins had amino acid deletions in RH2 sites responsible for the red shift and retinal binding. These patterns in the barn owl and penguins were convergent with adaptive strategies in nocturnal and aquatic mammals, respectively.

Conclusions: We conclude that birds have evolved diverse opsin adaptations through gene loss, adaptive selection and coevolution with plumage coloration, and that differentiated selective patterns at the species level suggest novel photic pressures to influence evolutionary patterns of more-recent lineages.

No MeSH data available.


Related in: MedlinePlus