Jump to ContentJump to Main Navigation
Show Summary Details
In This Section

Ornis Hungarica

The Journal of MME/BirdLife Hungary

2 Issues per year

Open Access
Online
ISSN
2061-9588
See all formats and pricing
In This Section

Phylogeny, Historical Biogeography and the Evolution of Migration in Accipitrid Birds of Prey (Aves: Accipitriformes)

Jenő Nagy
  • MTA-ELTE-MTM Ecology Research Group, 1117 Budapest, Pázmány Péter sétány 1/C, Hungary
  • Email:
/ Jácint Tökölyi
  • Corresponding author
  • MTA-DE “Lendület” Behavioural Ecology Research Group, Department of Evolutionary Zoology and Human Biology, University of Debrecen, 4032 Debrecen, Egyetem tér 1., Hungary
  • Email:
Published Online: 2014-12-04 | DOI: https://doi.org/10.2478/orhu-2014-0008

Abstract

Migration plays a fundamental part in the life of most temperate bird species. The regular, large-scale seasonal movements that characterize temperate migration systems appear to have originated in parallel with the postglacial northern expansion of tropical species. Migratoriness is also influenced by a number of ecological factors, such as the ability to survive harsh winters. Hence, understanding the origins and evolution of migration requires integration of the biogeographic history and ecology of birds in a phylogenetic context. We used molecular dating and ancestral state reconstruction to infer the origins and evolutionary changes in migratory behavior and ancestral area reconstruction to investigate historical patterns of range evolution in accipitrid birds of prey (Accipitriformes). Migration evolved multiple times in birds of prey, the earliest of which occurred in true hawks (Accipitrinae), during the middle Miocene period, according to our analyses. In most cases, a tropical ancestral distribution was inferred for the non-migratory ancestors of migratory lineages. Results from directional evolutionary tests indicate that migration evolved in the tropics and then increased the rate of colonization of temperate habitats, suggesting that temperate species might be descendants of tropical ones that dispersed into these seasonal habitats. Finally, we found that diet generalization predicts migratoriness in this group.

Összefoglalás

A legtöbb mérsékelt övi madárfaj életciklusában alapvető szerepet tölt be a vonulás. A rendszeres, nagy kiterjedésű mozgások, melyek a mérsékelt övi vonulási rendszereket jellemzik, egyes feltételezések szerint a trópusi fajok poszt-glaciális, északi irányú terjeszkedésével párhuzamosan jelentek meg. Ezen felül a vonulás előfordulását számos ökológiai tényező is befolyásolhatja, mint például a környezet szezonalitásának mértéke vagy a téli túlélést befolyásoló tényezők. A vonulás eredete és evolúciója ezért csak úgy érthető meg, ha a madarak biogeográfiai történetiségét és ökológiáját filogenetikai kontextusban tanulmányozzuk. Jelen vizsgálatban a vágómadár-alakúak (Accipitriformes) vonulásának evolúcióját elemeztük komparatív módszerekkel. Első lépésben létrehoztunk egy fosszilis adatok alapján datált molekuláris törzsfát, amelyen jellegrekonstrukciót végeztünk és rekonstruáltuk a fajok ősi elterjedési területét. Az elemzéseink alapján a vonulás többször alakult ki a ragadozók esetében, legkorábban a héjaformákon (Accipitrinae) belül, vélhetően a Miocén közepén. A legtöbb esetben a vonuló leszármazási vonalak nem vonuló őseinél trópusi elterjedésre következtethetünk. A direkcionális evolúciós teszt alapján a vonulás a trópusokon jelent meg és megnövelte a mérsékelt égöv kolonizációjának rátáját. Eszerint tehát a mérsékelt övi ragadozómadár fajok vonuló trópusi fajok leszármazottainak tekinthetők, melyek az erősen szezonális, északi élőhelyek irányába terjeszkedtek. Végezetül negatív kapcsolatot találtunk a vonulás megjelenése és a táplálékspecializáció mértéke között.

Keywords: ancestral area reconstruction; annual cycle; comparative; diet specialization; diurnal birds of prey; molecular dating; seasonality

Kulcsszavak: éves ciklus; jellegrekonstrukció; komparatív; molekuláris datálás; nappali ragadozómadarak; szezonalitás; táplálékspecializáció

References

  • Alerstam, T. 1993. Bird migration. - Cambridge University Press, pp. 420 do Amaral, F. R., Sheldon, F. H., Gamauf, A., Haring, E., Riesing, M., Silveira, L. F. & Wajntal, A. 2009. Patterns and processes of diversification in a widespread and ecologically diverse avian group, the buteonine hawks (Aves, Accipitridae). - Molecular Phylogenetics and Evolution 53: 703-715. DOI: 10.1016/j.ympev.2009.07.020 [Crossref] [Web of Science]

  • Bell, C. P. 2000. Process in the evolution of bird migration and pattern in avian ecogeography. - Journal of Avian Biology 31: 258-265. DOI: 10.1034/j.160 0048X.2000.310218.x Bell, C. P. 2005. The origin and development of bird migration: comments on Rappole and Jones, and an alternative evolutionary model. - Ardea 93: 115-123. [Crossref]

  • Bell, C. P. 2011. Resource buffering and the evolution of bird migration. - Evolutionary Ecology 25: 91-106. DOI: 10.1007/s10682-010-9383-4 [Web of Science] [Crossref]

  • Berthold, P. 2001. Bird migration: a general survey. - Oxford University Press, pp. 272

  • Boyle, W. A. & Conway, C. J. 2007. Why migrate? A test of the evolutionary precursor hypothesis. - The American Naturalist 169: 344-359. DOI: 10.1086/511335 [Web of Science] [Crossref]

  • Boyle, W. A., Conway, C. J. & Bronstein, J. L. 2011. Why do some, but not all, tropical birds migrate? A comparative study of diet breadth and fruit preference. - Evolutionary Ecology 25: 219-236. DOI: 10.1007/s10682-010-9403-4 [Crossref] [Web of Science]

  • Breman, F. C., Jordaens, K., Sonet, G., Nagy, Z. T., Van Houdt, J. & Louette, M. 2013. DNA barcoReferences ding and evolutionary relationships in Accipiter Brisson, 1760 (Aves, Falconiformes: Accipitridae) with a focus on African and Eurasian representatives. - Journal of Ornithology 154: 265-287. DOI: 10.1007/s10336-012-0892-5 [Web of Science] [Crossref]

  • Brown, J. W., Rest, J. S., García-Moreno, J., Sorenson, M. D. & Mindell, D. P. 2008. Strong mitochondrial DNA support for a Cretaceous origin of modern avian lineages. - BMC Biology 6: 6. DOI: 10.1186/1741-7007-6-6 [Web of Science] [Crossref] [PubMed]

  • Bruderer, B. & Salewski, V. 2008. Evolution of bird migration in a biogeographical context. - Journal of Biogeography 35: 1951-1959. DOI: 10.1111/j.1365-2699.2008.01992.x Camacho, C. 2013. Tropical phenology in temperate regions: extended breeding season in a long-distance migrant. - The Condor 115: 830-837. DOI: 10.1525/cond.2013.120192 [Crossref]

  • Castresana, J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. - Molecular Biology and Evolution 17: 540-552.

  • Charif, D. & Lobry, J. R. 2007. SeqinR 1.0-2: A contributed package to the R project for statistical computing devoted to biological sequences retrieval and analysis. - In: Bastolla, U., Porto, M., Roman, H. E. & Vendruscolo, M. (eds.) Structural approaches to sequence evolution. - Springer, Berlin, pp. 207-232.

  • Cox, G. W. 1985. The evolution of avian migration systems between temperate and tropical regions of the New World. - The American Naturalist 126: 451-474.

  • Darriba, D., Taboada, D. L., Doallo, R. & Posada, D. 2012. jModelTest 2: more models, new heuristics and parallel computing. - Nature Methods 9: 772. DOI: 10.1038/nmeth.2109 [Web of Science] [Crossref]

  • Drummond, A. J., Ho, S. Y., Phillips, M. J. & Rambaut, A. 2006. Relaxed phylogenetics and dating with confidence. - PLoS Biology 4: e88. DOI: 10.1371/ journal.pbio.0040088 [Crossref]

  • Drummond, A. & Rambaut, A. 2007. BEAST: bayesian evolutionary analysis by sampling trees. - BMC Evolutionary Biology 7: 214. DOI: 10.1186/1471-2148-7-214 [Web of Science] [Crossref] [PubMed]

  • Dunning, J. B. 2008. CRC handbook of avian body masses. - CRC Press, Boca Raton Ericson, P. G. P., Anderson, C. L., Britton, T., Elzanowski, A., Johansson, U. S., Källersjö, M., Ohlson, J. I., Parsons, T. J., Zuccon, D. & Mayr. G. 2006. Diversification of Neoaves: integration of molecular sequence data and fossils. - Biology Letters 2: 543-547. DOI: 10.1098/rsbl.2006.0523 [Crossref]

  • Ferguson-Lees, J. & Christie, D. A. 2001. Raptors of the World. - Houghton Mifflin Company, Boston Global Raptor Information Network. 2013. Species accounts. - Downloaded from http://www.globalraptors. org.

  • Griffiths, C. S., Barrowclough, G. F., Groth, J. G. & Mertz. L. A. 2007. Phylogeny, diversity, and classification of the Accipitridae based on DNA sequences of the RAG-1 exon. - Journal of Avian Biology 38: 587-602. DOI: 10.1111/j.2007.0908-8857.03971.x [Web of Science]

  • Guindon, S. & Gascuel, O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. - Systematic Biology 52: 696-704. DOI: 10.1080/10635150390235520 [Crossref] [PubMed]

  • Gwinner, E. 1990. Bird migration: physiology and ecophysiology. - Springer-Verlag, Berlin, pp. 435

  • Hackett, S. J., Kimball, R. T., Reddy, S., Bowie, R. C. K., Braun, E. L., Braun, M. J., Chojnowski, J. L., Cox, W. A., Han, K., Harshman, J., Huddleston, C. J., Marks, B. D., Miglia, K. J., Moore, W. S., Sheldon, F. H., Steadman, D. W., Witt, C. C. & Yuri, T. 2008. A phylogenomic study of birds reveals their evolutionary history. - Science 320: 1763-1768. DOI: 10.1126/science.1157704 [Crossref] [Web of Science]

  • Hadfield, J. D. & Nakagawa, S. 2010. General quantitative genetic methods for comparative biology: phylogenies, taxonomies, and multi-trait models for continuous and categorical characters. - Journal of Evolutionary Biology 23: 494-508. DOI: 10.1111/j.1420-9101.2009.01915.x [Crossref] [Web of Science]

  • Harrison, C. J. O. & Walker, C. A. 1976. Birds of the British upper Eocene. - Zoological Journal of the Linnean Society 59: 323-351. DOI: 10.1111/ j.1096-3642.1976.tb01017.x [Crossref]

  • Helbig, A. J., Kocum, A., Seibold, I. & Braun, M. J. 2005. A multi-gene phylogeny of aquiline eagles (Aves: Accipitriformes) reveals extensive paraphyly at the genus level. - Molecular Phylogenetics and Evolution 35: 147-164. DOI: 10.1016/j. ympev.2004.10.003 [Crossref]

  • Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. O. 2012. The global diversity of birds in space and time. - Nature 491: 444-448. DOI: 10.1038/nature11631 [Web of Science] [Crossref]

  • Joseph, L., Lessa, E. P. & Christidis, L. 1999. Phylogeny and biogeography in the evolution of migration: shorebirds of the Charadrius complex. - Journal of Biogeography 26: 329-342. DOI: 10.1046/j.1365-2699.1999.00269.x [Crossref]

  • Katoh, K., Kuma, K., Toh, H. & Miyata, T. 2005. MAFFT Version 5: improvement in accuracy of multiple sequence alignment. - Nucleic Acids Research 33: 511-518. DOI: 10.1093/nar/gki198 [Crossref]

  • Kendall, C., Virani, M. Z., Kirui, P., Thomsett, S. & Githiru, M. 2012. Mechanisms of coexistence in vultures: understanding the patterns of vulture abundance at carcasses in Masai Mara National Reserve, Kenya. - The Condor 114: 523-531. [Web of Science]

  • Kondo, B. & Omland, K. E. 2007. Ancestral state reconstruction of migration: multistate analysis reveals rapid changes in New World orioles (Icterus spp.). - The Auk 124: 410-419. DOI: 10.1642/0004-8038(2007)124[410:ASROMM] 2.0.CO;2 [Web of Science] [Crossref]

  • Landis, M. J., Matzke, N. J., Moore, B. R. & Huelsenbeck, J. P. 2013. Bayesian analysis of biogeography when the number of areas is large. - Systematic Biology 62: 789-804. DOI: 10.1093/sysbio/syt040 [Crossref] [PubMed] [Web of Science]

  • Lerner, H. R. L. & Mindell, D. P. 2005. Phylogeny of eagles, old world vultures, and other Accipitridae based on nuclear and mitochondrial DNA. - Molecular Phylogenetics and Evolution 37: 327-346. DOI: 10.1016/j.ympev.2005.04.010 [Crossref]

  • Louchart, A. 2008. Emergence of long distance bird migrations: a new model integrating global climate changes. - Naturwissenschaften 95: 1109-1119. DOI: 10.1007/s00114-008-0435-3 [Crossref] [Web of Science]

  • Matzke, N. J. 2013. Probabilistic historical biogeography: new models for founder-event speciation, imperfect detection, and fossils allow improved accuracy and model-testing. - Ph.D. thesis, Department Integrative Biology and Designated Emphasis in Computational and Genomic Biology, University of California, Berkeley. Available at http://phylo. wikidot.com/local-files/biogeobears/Matzke_ PhD_FINAL_v5_w_refs.pdf.

  • Milá, B., Smith, T. B. & Wayne, R. K. 2006. Postglacial population expansion drives the evolution of long-distance migration in a songbird. - Evolution 60: 2403-2409. DOI: 10.1111/j.0014-3820.2006. tb01875.x Newton, I. 2008. The migration ecology of birds. - Academic Press, London, pp. 976 [Crossref]

  • Outlaw, D. C., Voelker, G., Milá, B. & Girman, D. J. 2003. Evolution of long-distance migration in and historical biogeography of Catharus thrushes: a molecular phylogenetic approache. - The Auk 120: 299-310. DOI: 10.1642/00048038(2003)120[0299:EOLMIA] 2.0.CO;2 [Crossref]

  • Padian, K. & Chiappe, L. M. 1998. The origin and early evolution of birds. - Biological Reviews 73: 1-42. DOI: 10.1111/j.1469-185X.1997.tb00024.x Pagel, M., Meade, A. & Barker, D. 2004. Bayesian estimation of ancestral character states on phylogenies. - Systematic Biology 53: 673-684. DOI: 10.1080/10635150490522232 [Crossref]

  • Pagel, M. & Meade, A. 2006. Bayesian analysis of correlated evolution of discrete characters by reversible- jump Markov Chain Monte Carlo. - The American Naturalist 167: 808-825. DOI: 10.1086/503444 [Crossref]

  • Paradis, E., Claude, J. & Strimmer, K. 2004. APE: analyses of phylogenetics and evolution in R language. - Bioinformatics 20: 289-290. DOI: 10.1093/bioinformatics/ btg412 [Crossref]

  • Rappole, J. H. & Jones, P. 2002. Evolution of Old and New World migration systems. - Ardea 90: 525-537.

  • R Development Core Team. 2012. R: a language and environment for statistical computing. - R Foundation for Statistical Computing, Vienna. Available at http://www. R-project.org.

  • Ree, R. H., Moore, B. R., Webb, C. O. & Donoghue, M. J. 2005. A likelihood framework for inferring the evolution of geographic range on phylogenetic trees. - Evolution 59: 2299-2311. DOI: 10.1111/ j.0014-3820.2005.tb00940.x [Crossref]

  • Ree, R. H. & Smith, S. A. 2008. Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. - Systematic Biology 57: 4-14. DOI: 10.1080/10635150701883881 [Web of Science] [Crossref]

  • Ronquist, F. 1997. Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. - Systematic Biology 46: 195-203. DOI: 10.1093/sysbio/46.1.195 [Crossref]

  • Roulin, A. & Wink, M. 2004. Predator-prey relationships and the evolution of colour polymorphism: a comparative analysis in diurnal raptors. - Biological Journal of the Linnean Society 81: 565-578. DOI: 10.1111/j.1095-8312.2004.00308.x [Crossref]

  • Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihood- based phylogenetic analyses with thousands of taxa and mixed models. - Bioinformatics 22: 2688-2690. DOI: 10.1093/bioinformatics/btl446 [Crossref]

  • Stiles, F. G. 1980. Evolutionary implications of habitat relations between permanent and winter resident landbirds in Costa Rica. - In: Keast, A. & Morton, E. S. (eds.) Migrant Birds in the Neotropics. - Smithsonian Institution Press, Washington D.C., pp. 421-435.

  • Tökölyi, J. & Barta, Z. 2011. Breeding phenology determines evolutionary transitions in migratory behaviour in finches and allies. - Oikos 120: 184-193. DOI: 10.1111/j.1600-0706.2010.18592.x [Web of Science] [Crossref]

  • Wink, M. & Sauer-Gürth, H. 2004. Phylogenetic relationships in diurnal raptors based on nucleotide sequences of mitochondrial and nuclear marker genes. - In: Motta-Junior, J. C., Bueno, A., Chancellor, R. & Meyburg, B. U. (eds.) Raptors worldwide. WWGBP, Berlin, pp. 483-498.

  • Zachos, J., Pagani, M., Sloan, L., Thomas, E. & Billups, K. 2001. Trends, rhythms, and aberrations in global climate 65 Ma to present. - Science 292: 686-693. DOI: 10.1126/science.1059412

  • Zink, R. M. 2011. The evolution of avian migration. - Biological Journal of the Linnean Society 104: 237-250. DOI: 10.1111/j.1095-8312.2011.01752.x [Web of Science] [Crossref]

About the article

Published Online: 2014-12-04

Published in Print: 2014-06-01



Citation Information: Ornis Hungarica, ISSN (Online) 2061-9588, DOI: https://doi.org/10.2478/orhu-2014-0008. Export Citation

© 2014. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. (CC BY-NC-ND 3.0)

Comments (0)

Please log in or register to comment.
Log in