Department of Biology, Institute of Molecular Evolutionary Genetics, and Astrobiology Research Center, Pennsylvania State University
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Abstract |
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Introduction |
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Mitochondrial DNA sequence studies have instead supported a phylogenetic tree of avian orders that differs considerably from the traditional classification. Those studies of mitochondrial protein-coding genes found that the palaeognath and galloanserine birds occupy derived positions within Neognathae, whereas Passeriformes occupy the most basal position among all modern birds (Mindell et al. 1997
; Härlid, Janke, and Arnason 1998
; Härlid and Arnason 1999
; Mindell et al. 1999
). Some morphological support for a basal Passeriformes and a derived position of the galloanserine birds also has been proposed (Woodbury 1998
).
With such disparate results from mitochondrial and nuclear genes, and from morphology, it is clear that additional data are needed to better understand the early history of modern birds. Of the previous molecular studies, those with broad taxonomic sampling (Ho et al. 1976
; Prager et al. 1976
; Sibley and Ahlquist 1990
) did not address the statistical significance of their findings, and those reporting statistical significance (Mindell et al. 1997
; Härlid, Janke, and Arnason 1998
; Groth and Barrowclough 1999
; Härlid and Arnason 1999
; Mindell et al. 1999
) did not sample all avian orders. Therefore, in this study, we attempted to do both by sampling a large number of nucleotide sites in all avian orders.
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Materials and Methods |
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The analyses of cytochrome b sequences obtained from GenBank were performed using Poisson-corrected distances from sequences of the complete gene (379 amino acids) and included 70 taxa representing the following bird orders (Sibley and Ahlquist 1990
): Anseriformes (L08385), Bucerotiformes (U89190), Ciconiiformes (U74347, U74348, U74351, U74352, U83305, U83311, U83312, U83314, U83316, AF076044, AF076052, AF076054, AF076062, AF076076, AF076090, AF076094), Coliiformes (U89173, U89175), Coraciiformes (U89184, U89186, U89188), Craciformes (L08384, AF068190), Cuculiformes (U89197, U89198), Galliformes (L08377, L08381, AF013763, AF028791, AF028795, AF028798, AF028802, AF068192, AF068193, Gruiformes (U11060, U27543), Passeriformes (U15206, U25736, U25738, U77331, U77336, X74251, X74256, Y16885, AF081958, AF081959, AF082007), Piciformes (U89192, U89193), Psittaciformes (U89176, U89178, U89179), Strigiformes (U89171, U89172, U89194), Struthioniformes (U76050, U76051, U76052, U76054, U76055), Tinamiformes (U76053, U76056), Trochiliformes (U89180), Trogoniformes (U89201, U89202), and Upupiformes (U89189). To test the sensitivity of the ingroup topology to choice of outgroup, alligators (Y13113) and turtles (AF039066) were used in combination and separately as outgroup.
Jackknife Analyses
The effect of sampling different numbers of taxa (avian orders) was explored through separate jackknife analyses of the mitochondrial data set and the complete data set (nuclear and mitochondrial rRNA sequences). In each case, a fixed number of palaeognath and neognath taxa were sampled 100 times randomly, without replacement, and a neighbor-joining tree was constructed using the Kimura two-parameter and transversions-only distance. In all cases, the outgroup (alligators + turtles) was included and the tree was scored as supporting or not supporting neognath monophyly. Taxon-specific jackknife analyses were performed by substituting one of the variable (randomly chosen) neognath taxa for a galliform (Gallus/Coturnix), anseriform (Anas), or passeriform (Tyrannus) in each jackknife sample. In a separate jackknife analysis (40 iterations because of extensive computational time), a measure of phylogenetic signal (tRASA; Lyons-Weiler, Hoelzer, and Tausch 1996
) for each jackknifed data set was calculated and averaged.
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Results |
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A jackknife analysis of our data sets shows that neognath monophyly was almost always supported in small or large subsets of the complete data set and in the mitochondrial data set when 20 or more orders were sampled. However, when fewer than 20 orders were included in the mitochondrial data set, neognath monophyly was not supported in as many as one quarter of the jackknife samples (table 2
). To further explore this taxon-sampling problem, we examined those specific jackknife samples (n = 81; table 2 ) that resulted in neognath paraphyly and found that 91% (74 taxa) included a galloanserine taxon. Separate taxon-specific jackknife analyses were then performed by including a galliform, an anseriform, or a passeriform in each subset. The latter neognath order was tested because it was found to be basal among modern avian orders in recent mitochondrial studies (Mindell et al. 1997
; Härlid, Janke, and Arnason 1998
; Mindell et al. 1999
; Härlid and Arnason 1999
). As predicted from the first jackknife analysis, support for neognath monophyly was significantly lower when either a galliform or an anseriform taxon was included. However, support for neognath monophyly from the jackknife analysis using a passeriform was the same as that for randomly chosen neoavian taxa (table 2
).
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Discussion |
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These jackknife analyses also revealed increases in phylogenetic signal as taxon sampling was increased (table 2
). Given that the tree-independent measure of signal we used (Lyons-Weiler, Hoelzer, and Tausch 1996
) is known to decrease as branch length heterogeneity increases (Lyons-Weiler and Hoelzer 1997
), this result provides further support for the hypothesis that a taxon-sampling problem is involved. In such cases, long-branch attraction may result, owing to sparse taxon sampling. When sufficient taxon sampling becomes available for a diversity of genes, it will be possible to test for gene-specific effects on phylogeny.
The unrooted trees are identical for the traditional Palaeognathae-Neognathae concept and for the recently found topology (Passeriformes basal) derived from the mitochondrial concatenated protein-coding genes (Mindell et al. 1997
; Härlid and Arnason 1999
; Mindell et al. 1999
). Together with these jackknife data, this observation indicates that improper rooting can occur when using sparse taxon sampling. The unrooted tree from the cytochrome b sequences (Härlid, Janke, and Arnason 1998
) is unconventional. Nonetheless, the reanalyses of this gene with additional taxa show that a taxon-sampling problem is probably involved. These reanalyses further point to the need for optimal outgroup usage in phylogenetic studies (Lyons-Weiler, Hoelzer, and Tausch 1998
).
The group comprising the orders of neognath birds exclusive of Galloanserae was found by Sibley, Ahlquist, and Monroe (1988)
based on DNA-DNA hybridization data and named Neoaves. In that study, Turniciformes were left unplaced, but otherwise the composition of the group is identical to that found here. Sibley and Ahlquist (1990)
and Sibley and Monroe (1990)
, as well as other authors (Kurochkin 1995
; Rotthowe and Starck 1998
), later used Neoaves in reference to all neognath birds including Galloanserae. Because the taxon Neoaves has been used differently, Groth and Barrowclough (1999)
proposed a new name, "Plethornithae," for the group originally named by Sibley, Ahlquist, and Monroe (1988)
. However, definitions of taxonomic names frequently change, and this is usually not a reason to abandon a taxonomic name. Although the International Code of Zoological Nomenclature does not apply to these higher-level groupings, we follow standard taxonomic practice and use the name first applied to the group in question: Neoaves. Otherwise, we agree with Groth and Barrowclough (1999)
in retaining the names Palaeognathae and Neognathae as infraclasses of the subclass Neornithes, and in treating the two remaining taxa (Galloanserae, and, in this case, Neoaves) as cohorts (fig. 1 ).
Inferring the order of appearance of the major lineages of birds permits a better understanding of the morphology and ecology of the earliest neornithine birds. The late Cretaceous avian fossils of neornithines (Chiappe 1995
; Padian and Chiappe 1998
), aside from those of a ducklike bird and a parrot (Stidham 1998
), are mostly of marine taxa (Ciconiiformes, sensu Sibley and Ahlquist 1990
). These fossils led to the proposal that all orders of modern birds arose from a marine (shore bird) ancestor (Feduccia 1995
). In contrast, the basal lineages identified in this study (tinamous, ratites, anseriforms, galliforms, and craciforms) include almost entirely terrestrial, nonmarine, ground-dwelling, and heavy-bodied birds. If our identification of the earliest neornithines is correct and the ancestral neornithines also shared these morphological and ecological traits, then the neornithine fossil record is biased, perhaps as a result of the greater chances of fossilization of aquatic, particularly marine, taxa (Benton 1997
). Furthermore, this taphonomic bias could provide an explanation of the large gap in the neornithine fossil record as implied by molecular time estimates (Hedges et al. 1996
; Cooper and Penny 1997
; Härlid, Janke, and Arnason 1997, 1998
; Waddell et al. 1999
).
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Acknowledgements |
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Footnotes |
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1 Keywords: molecular avian phylogeny
Palaeognathae-Neognathae
Galloanserae
Neoaves
taxon sampling
fossil record bias
2 Address for correspondence and reprints: S. Blair Hedges, Department of Biology, 208 Mueller Laboratory, Pennsylvania State University, University Park, Pennsylvania 16802. E-mail: sbh1{at}psu.edu
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