Relationships of Birds – Molecules versus Morphology

Abstract

Molecules and morphology frequently point to different phylogenies of modern birds, hence making birds unique models to study reasons for such conflicts. Molecules generally make a less biased tool for phylogenetic inference, but evolutionary interpretation of a phylogeny requires knowledge from both morphology and fossils. In the past decade, considerable progress has been made in reconciling molecular and morphological phylogenies, the examples of which are discussed here. Despite this progress and a wealth of new data now available, key features of the avian phylogenetic tree remain unresolved. This pattern more likely reflects the short time interval during which the majority of modern bird lineages diversified. Much improved insight about the early evolution of modern birds more likely will come from (1) genomic data, provided that biases at this scale are understood and (2) well‐preserved fossils that represent the stem of distinct bird lineages. At present, such data are too incomplete to resolve most key nodes in the diversification of modern birds.

Key Concepts:

  • Phylogenies represent the best interpretation of the evolutionary history of a chosen taxon set.

  • At increasing taxonomic level, both DNA sequence‐based and morphological variation are expected to increase.

  • DNA sequence variation at neutral markers is produced and enhanced by the process of random mutation; therefore, it is a function of time.

  • Morphological variation is enhanced by selection for certain phenotypes; therefore, it is a function of the environment.

  • Evolutionary convergence is less likely at the molecular level than at the morphological level.

  • If underlying changes at the molecular/morphological level are modelled appropriately (e.g. alignment, substitution bias and character weighting), reconstruction of phylogeny from either molecular or morphological data should yield the same result.

  • Rampant phylogenetic conflict at the ordinal level in modern birds can be explained by ordinal diversification taking place over a short time interval. During this interval, morphological key innovations were quickly selected for, but augmentation of molecular differences was small.

  • Phylogenetic conflict in modern birds is exacerbated by lack of molecular resolution, imperfect taxonomic sampling, uncertainty about extent of morphological homoplasy and paucity of well‐preserved fossils plesiomorphic for clades Palaeognathae, Neognathae and Neoaves.

Keywords: molecules; morphology; birds; evolution; convergence

Figure 1.

Current molecular understanding of the phylogenetic relationships among modern birds. Molecules and morphology agree in separating ratites and tinamous from all other birds, whereas placing gamefowl and waterfowl basal within the latter group. Consensus further exists in placing swifts with hummingbirds (and not with swallows) and suboscines (represented by New World flycatcher) with oscine perching birds (represented by robin and swallow). In addition to the universally recognised cases of morphological convergence between swifts and swallows and penguins and auks, molecules have revealed several other instances of convergent evolution. This result implies that organismal change can proceed at a much faster pace than previously recognised. Examples of convergent evolution shown here include hoatzin versus gamefowl, frigatebirds versus pelicans, loons versus grebes and flamingos versus storks and waterfowl. Note that current consensus among molecular studies is strong, except for the lineages labelled Turacos to Pigeons. For these, three hypotheses have emerged: (1) Metaves (sensu Fain and Houde, ; Hackett et al., ); (2) Cuckoos to Tropicbirds, sensu Ericson et al., : excluding beta‐fibrinogen intron 7; and (3) Turacos–Strisores, McCormack et al., : 416 loci completely sampled.

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References

Assis LCS and de Carvalho MR (2010) Key innovations: further remarks on the importance of morphology in elucidating systematic relationships and adaptive radiations. Evolutionary Biology 37: 247–254.

Barker FK, Cibois A, Schikler P, Feinstein J and Cracraft J (2004) Phylogeny and diversification of the largest avian radiation. Proceedings of the National Academy of Sciences of the USA 101: 11040–11045.

Bourdon E, Bouya B and Iarochene M (2005) Earliest African neornithine bird: A new species of Prophaethontidae (Aves) from the Paleocene of Morocco. Journal of Vertebrate Paleontology 25: 157–170.

Brown JW and van Tuinen M (2011) Evolving perceptions on the antiquity of the modern avian tree. In: Dyke K (ed.) Living Dinosaurs: The Evolutionary History of Modern Birds, vol. 12, pp 306–324. Chichester, UK: John Wiley and sons.

Clarke JA, Ksepka DT, Stucchi M et al. (2007) Paleogene equatorial penguins challenge the proposed relationship between biogeography, diversity, and Cenozoic climate change. Proceedings of the National Academy of Sciences of the USA 104: 11545–11550.

Cooper A, Lalueza‐Fox C, Anderson S et al. (2001) Complete mitochondrial genome sequences of two extinct moas clarify ratite evolution. Nature 409: 704–707.

Cracraft J (1988) The major clades of birds. In: Benton MJ (ed.) The Phylogeny and Classification of the Tetrapods, pp 339–361. Oxford: Clarendon Press.

Cracraft J, Barker FK, Braun M et al. (2004) Phylogenetic relationships among modern birds: (Neornithes) towards an avian tree of life. In: Cracraft J and Donoghue M (eds) Assembling the Tree of Life, pp 468–489. New York: Oxford University Press.

Doolittle RF (1994) Convergent evolution: the need to be explicit. Trends in Biochemical Sciences 19: 15–18.

Ericson PGP, Anderson CL, Britton T et al. (2006) Diversification of Neoaves: integration of molecular sequence data and fossils. Biology Letters 2: 543–547.

Fain MG and Houde P (2004) Parallel radiations in the primary clades of birds. Evolution 58: 2558–2573.

Feduccia A (1996) The Origin and Evolution of Birds. New Haven and London: Yale University Press.

Hackett SJ, Kimball RT, Reddy S et al. (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320: 1763–1768.

Haddrath O and Baker AJ (2001) Complete mitochondrial DNA genome sequences of extinct birds: ratite phylogenetics and the vicariance biogeography hypothesis. Proceedings of the Royal Society London B: Biological Sciences 268: 939–945.

Harshman J, Braun EL, Braun MJ et al. (2008) Phylogenomic evidence for multiple losses of flight in ratite birds. Proceedings of the National Academy of Sciences of the USA 105: 13462–13467.

Hedges SB and Kumar S (eds) (2009) The Timetree of Life. NY: Oxford University Press.

Hedges SB and Maxson LR (1996) Molecules and morphology in amniote phylogeny. Molecular Phylogenetics and Evolution 6: 312–314.

Hedges SB and Sibley CG (1994) Molecules vs. morphology in avian evolution: the case of the ‘pelecaniform’ bird. Proceedings of the National Academy of Sciences of the USA 91: 9861–9865.

Hedges SB, Simmons MD, van Dijk MAM et al. (1995) Phylogenetic relationships of the hoatzin, an enigmatic South American bird. Proceedings of the National Academy of Sciences of the USA 92: 11662–11665.

Hughes JM and Baker AJ (1999) Phylogenetic relationships of the enigmatic hoatzin (Opisthocomus hoazin) resolved using mitochondrial and nuclear gene sequences. Molecular Biology and Evolution 16: 1300–1307.

Johansson US, Parsons TJ, Irestedt M and Ericson PGP (2001) Clades within the ‘higher land birds’, evaluated by nuclear DNA sequences. Journal of Zoological Systematics and Evolutionary Research 39: 37–51.

Johnston P (2011) New morphological evidence supports congruent phylogenies and Gondwana vicariance for palaeognathous birds. Zoological Journal of the Linnean Society 163: 959–982.

Livezey BC and Zusi RL (2007) Higher‐order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy: II – Analysis and discussion. Zoological Journal of the Linnean Society 149: 1–94.

Mayr G (2004) Morphological evidence for sister group relationship between flamingos (Aves: Phoenicopteridae) and grebes (Podicipedidae). Zoological Journal of the Linnean Society 140: 157–169.

Mayr G (2008a) Avian higher‐level phylogeny: well‐supported clades and what we can learn from a phylogenetic analysis of 2954 morphological characters. Journal of Zoological Systematics and Evolutionary Research 46: 63–72.

Mayr G (2008b) The higher‐level phylogeny of birds – when morphology, molecules, and fossils coincide. Oryctos 7: 67–73.

Mayr G (2010) Parrot interrelationships – morphology and the new molecular phylogenies. Emu 110: 348–357.

Mayr G (2011a) Metaves, Mirandornithes, Strisores, and other novelties – a critical review of the higher‐level phylogeny of neornithine birds. Journal of Zoological Systematics and Evolutionary Research 49: 58–76.

Mayr G (2011b) The phylogeny of charadriiform birds (shorebirds and allies) – reassessing the conflict between morphology and molecules. Zoological Journal of the Linnean Society 161: 916–934.

McCormack JE, Harvey MG, Faircloth BC et al. (2013) A phylogeny of birds based on over 1,500 loci collected by target enrichment and high‐throughput sequencing. PLoS One 8: e54848.

Phillips MJ, Gibb GC, Crimp EA and Penny D (2009) Tinamous and moa flock together: mitochondrial genome sequence analysis reveal independent losses of flight among ratites. Systematic Biology 59: 1–18.

Sibley CG and Ahlquist J (1990) Phylogeny and Classification of Birds. New Haven, CT: Yale University Press.

Smith JV, Braun EA, and Kimball RT (2013) Ratite nonmonophyly: independent evidence from 40 novel loci. Systematic Biology 62: 35–49.

Smith ND (2010) Phylogenetic analysis of Pelecaniformes (Aves) based on osteological data: implications for waterbird phylogeny and fossil calibration studies. PLoS One 5: e13354.

Suh A, Paus M, Kiefmann M et al. (2011) Mesozoic retroposons reveal parrots as the closest living relatives of passerine birds. Nature Communications 2: 443.

van Tuinen M, Butvill DB, Kirsch JAW and Hedges SB (2001) Convergence and divergence in the evolution of aquatic birds. Proceedings of the Royal Society London B: Biological Sciences 268: 1–6.

van Tuinen M and Hedges SB (2001) Calibration of avian molecular clocks. Molecular Biology and Evolution 18: 206–213.

van Tuinen M, Stidham TA and Hadly EA (2006) Tempo and mode of modern birds inferred from large‐scale taxonomic sampling. Historical Biology 18: 209–225.

Wetmore A (1960) A classification for the birds of the world. Smithsonian Miscellaneous Collections 139: 1–37.

Wiens JJ (2000) Phylogenetic Analysis of Morphological Data. Washington, DC: Smithsonian Institution Press.

Further Reading

Cooper A and Penny D (1997) Mass survival of birds across the K–T boundary: molecular evidence. Science 275: 1109–1113.

Dyke GJ and van Tuinen M (2004) The evolutionary radiation of modern birds (Neornithes): reconciling molecules, morphology and the fossil record. Zoological Journal of the Linnean Society 141: 153–178.

Groth JG and Barrowclough GF (1999) Basal divergences in birds and the phylogenetic utility of the nuclear RAG‐1 gene. Molecular Phylogenetics and Evolution 12: 115–123.

Hedges SB, Parker PH, Sibley CG and Kumar S (1996) Continental breakup and the ordinal diversification of birds and mammals. Nature 381: 226–229.

Ho CY‐K, Prager E, Wilson AC, Osuga DT and Feeney RE (1976) Penguin evolution: comparisons demonstrate phylogenetic relationship to flying aquatic birds. Journal of Molecular Evolution 8: 271–282.

Irestedt M, Johansson US, Parsons TJ and Ericson PGP (2001) Phylogeny of major lineages of suboscines (Passeriformes) analysed by nuclear DNA sequence data. Journal of Avian Biology 32: 15–25.

Mindell DP (1997) Avian Molecular Evolution and Systematics. San Diego, CA: Academic Press.

Sheldon FH and Bledsoe AH (1993) Avian molecular systematics, 1970s to 1990s. Annual Review of Ecology and Systematics 24: 243–278.

Storer RW (1971) Adaptive radiation in birds. In: Farner DS and King JR (eds) Avian Biology, pp 149–188. New York: Academic Press.

van Tuinen M, Paton T, Haddrath O and Baker AJ (2003) “Big Bang” for Tertiary birds? A reply. Trends in Ecology and Evolution 18: 442–443.

van Tuinen M, Sibley CG and Hedges SB (2000) The early history of modern birds inferred from DNA sequence of mitochondrial and nuclear ribosomal genes. Molecular Biology and Evolution 17: 451–457.

Wilson AC, Carlson SS and White TJ (1977) Biochemical evolution. Annual Review of Biochemistry 46: 573–639.

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Torres, Christopher, and van Tuinen, Marcel(Sep 2013) Relationships of Birds – Molecules versus Morphology. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0003357.pub3]