Zoological Department, Museum of Natural History, Vienna, Austria;
Institute of Medical Biology, University of Vienna, Austria
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Abstract |
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Introduction |
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The two largest families of birds of prey are the Accipitridae and the Falconidae. The accipitrids, known colloquially as hawks, kites, harriers, vultures, and eagles, are rather similar in their basic morphological structures, although they show great diversity in size, shape, flying ability, ecology, and predatory habits. The falconids resemble the accipitrids in some characteristics, such as a powerful hooked bill, a fleshy cere straddling the bill, heavy bony brow ridges, and a crop (to store freshly eaten food). The differences between the two families have been summarized by Olsen (1995)
in a survey of 25 anatomical and behavioral traits.
According to traditional morphological classifications (e.g., Brown and Amadon 1968
; Storer 1971
; Stresemann and Amadon 1979
; Cracraft 1981
), Accipitridae and Falconidae belong to the order Falconiformes. However, based on detailed morphological studies of several families, Jollie (1976, 1977)
concluded that falconids and accipitrids are not closely related. According to his interpretation, the order Falconiformes is polyphyletic, especially with respect to the inclusion of New World vultures (Cathartidae); that view is supported by studies of several behavioral traits (König 1982
) and, more recently, by molecular analyses (e.g., Sibley and Ahlquist 1990
; Seibold and Helbig 1995
; Wink et al. 1998
). Sibley and Ahlquist (1990)
estimated the overall genomic similarity by DNA-DNA hybridization and proposed a new classification of birds in which the New World vultures appear as close relatives of the storks (Ciconiidae). In their classification, the falconiform taxa are placed within an expanded order Ciconiiformes, in which they include the infraorders Falconides (including Falconidae and Accipitridae) and Ciconiides (including the family Ciconiidae with the subfamilies Cathartinae and Ciconiinae). Sequence analyses of the cytochrome b gene (cyt b) (Avise, Nelson, and Sibley 1994
; Seibold and Helbig 1995
; Wink et al. 1998
) support this taxonomic position for New World vultures, but the relationships of the Ciconiidae with respect to Accipitridae and Cathartidae have not been resolved unambiguously. So far, no other genetic markers (mitochondrial or nuclear) have been employed to elucidate the phylogenetic relationships of these families.
Analyses of complete mitochondrial (mt) genomes provide not only sequence data for phylogenetic studies, but also information about structural genomic rearrangements which may serve as additional markers. Sequencing of the first complete vertebrate mt genomes suggested that gene content and gene order are highly conserved, but subsequent sequence data have demonstrated that the gene order in vertebrates is not uniform (for review, see Quinn 1997
). A major rearrangement within the mt genome of chickens and other galliform birds has been described by Desjardins and Morais (1990)
. It comprises the cyt b gene, the NADH dehydrogenase subunit 6 gene (nd6), and several tRNA genes. Subsequently, this particular gene order has been found in several other avian species, suggesting that this rearrangement could have occurred at the base of the avian branch and thus might be shared by all recent bird species. However, the hypothesis of a universal gene order characteristic for all birds was refuted by the discovery of yet another rearrangement of the mt genes in Falco peregrinus, as well as in birds of four additional orders (Mindell, Sorenson, and Dimcheff 1998
). In an investigation of 137 species, representing 13 orders, Mindell, Sorenson, and Dimcheff (1998)
hypothesize that this novel arrangement, which includes the control region (CR) and surrounding sections, must have originated independently four times in avian evolution. In addition to the CR, these species possess a second noncoding (nc) region, probably generated through a duplication process. The same arrangement was recently detected in warblers of the genus Phylloscopus (Bensch and Härlid 2000
). Partial sequence analysis of the B. buteo mt genome (Haring et al. 1999
) revealed the existence of a noncoding section corresponding to the nc region of F. peregrinus, which was designated a pseudo control region (
CR). Although the position of the functional CR in B. buteo was not determined, this finding suggested that F. peregrinus and B. buteo might share the same gene order.
In this paper, we report the complete sequence of the mt genome of B. buteo. For sequence comparisons, we used the previously published complete mt genomes of nine other bird species, along with that of Alligator mississippiensis as an outgroup, to address the following questions: (1) Do Falconidae and Accipitridae share the same rearrangement within their mt genomes? (2) What are the phylogenetic positions of the genera Buteo, Ciconia, and Falco within the avian tree? (3) Are subsections as useful as complete mt genomes for resolving phylogenies? (Up to now, the majority of avian molecular phylogenies have been based on sequence data of the mitochondrial cyt b gene.) (4) What is the degree of divergence between Buteo and Falco, and can it be related to other splits in the phylogeny of birds to estimate their approximate divergence time?
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Materials and Methods |
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PCR Amplification
PCR was carried out with an Eppendorf Thermocycler in a volume of 25 µl containing 1 unit Dynazyme DNA polymerase (Finnzymes OY), 1 µM of each primer, 0.2 mM of each dNTP, and 50200 ng template DNA. The solutions were heated to 95°C (2 min) and then put through 30 reaction cycles: 95°C (10 s), annealing temperature (10 s), and 72°C (1 min/1 kb expected length), followed by a final extension at 72°C (10 min). Primers used for PCR amplification are listed in table 1
. The 11 PCR fragments that were subsequently cloned and sequenced are depicted in figure 1
. These overlapping fragments cover the whole mt genome of B. buteo except the region comprising a part of the nd6 gene, tRNAGlu, CR, tRNAPhe, and a part of the 12S rRNA gene (primer pair nd6-1+/12S-1-) determined in a previous study from the same individual of B. buteo (GenBank accession number AF202186). The 11 fragments sequenced in the present study were obtained using the following primer combinations (fig. 1
): 12S3+/16S3- (910 bp), 12S-2+/16S-2- (1,410 bp), 16S-1+/nd2-2- (2,372 bp), nd2-1+/cox2-1- (2,913 bp), cox2-3+/atp6-2- (1,397 bp), atp6-1+/nd4-4- (1,430 bp), nd3-1+/nd4-5- (1,534 bp), nd4-3+/nd5-2- (1,047 bp), nd5-3+/cytb-2- (1,747 bp), cytb-3+/cytb-4- (899 bp), cytb-1+/nd6-3- (2,071 bp).
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Sequence Analysis
Alignments of DNA and amino acid sequences were produced with the program CLUSTAL X (Thompson et al. 1997
) and improved manually. Distance-based (the neighbor-joining [NJ] algorithm; Saitou and Nei 1987
) and maximum-parsimony (MP) methods were used to infer the phylogenetic relationships. All dendrograms were calculated with the software package PAUP (test version 4.0b3a; Swofford 1998
) using a heuristic search with the tree bisection-reconnection (TBR) algorithm and a random-taxon-addition sequence. Gaps were treated as "missing," and all characters were weighted equally. The robustness of trees was tested with bootstrap analysis (100 replications). Relative-rate tests were performed with the program Phyltest (Kumar 1996
), which provides the two-cluster test of Takezaki, Rzhetsky, and Nei (1995)
. In this test, the constancy of substitution rates is examined for two lineages with a given outgroup lineage. The program allows inclusion of multiple sequences in each of the lineages. If La and Lb are the averages of observed numbers of substitutions per site from the common ancestor of clusters A and B, then La = Lb is the null hypothesis under rate constancy (
= La - Lb = 0). Because the variance of
can be estimated, the deviation of
from 0 can be tested by a two-tailed normal deviate test. For the tests, new alignments including only the sequences used were created, and Kimura (1980)
two-parameter distances were used for the calculations.
DNA Sequences
For phylogenetic comparisons, the complete mt genome sequences of the following avian species were retrieved from GenBank: Gallus gallus f. dom., NC001323 (Desjardins and Morais 1990
); Struthio camelus, Y12025 (Härlid, Janke, and Arnason 1997
); Rhea americana, NC000846 (Härlid, Janke, and Arnason 1998
); Vidua chalybeata, NC000880; Aythya americana, AF090337; Falco peregrinus, NC000878; Smithornis sharpei, NC000879 (Mindell, Sorenson, and Dimcheff 1998
; Mindell et al. 1999
); Corvus frugilegus, NC002069 (Härlid and Arnason 1999
); Ciconia ciconia, AB026818 (Yamamotu, unpublished). The sequence of Alligator mississippiensis, Y13113 (Janke and Arnason 1997
), was used as an outgroup for the rooting of phylogenetic trees.
Designation of Sequences
Although the sequences of the various avian mt genomes used in this study are derived from defined taxonomic entities (species/subspecies), e.g., B. b. buteo, the phylogenetic reconstructions were made at the genus level or at even higher taxonomic levels. Therefore, for the sake of brevity, we refer to the taxa only by their genus names in the text. In the tables and figures, the following abbreviations are used: All, A. mississippiensis; Ayt, A. americana; But, B. buteo; Cic, C. ciconia; Cor, C. frugilegus; Fal, F. peregrinus; Gal, G. gallus; Rhe, R. americana; Smi, S. sharpei; Str, S. camelus; Vid, V. chalybeata.
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Results |
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Phylogenetic Analyses
The phylogenetic analysis was carried out using the coding regions of Buteo and the nine bird species listed above and Alligator. Each gene was aligned separately after excluding nonmatching positions at the length-variable 3' ends. Although the Alligator sequence was considerably diverged from the avian sequences, a reasonable alignment could be achieved. In a distance matrix (not shown) calculated from the concatenated coding sequences (15,742 bp), the distances (HKY85; Hasegawa, Kisgino, and Yano 1985
) between all ingroup taxa and Alligator, respectively, are rather homogenous, indicating no major differences in substitution rates. The distances among ingroup taxa range from 18.1% to 27.2%. The distance between Buteo and Falco (21.3%) is on the same order of magnitude as that between the two struthioniform species Rhea and Struthio (19.6%) and between the two galloanserine species Gallus and Aythya (22.3%). Concerning the phylogenetic relationships of Buteo, it is remarkable that with 11 out of 14 genes compared, Buteo appears more closely related to Ciconia than to Falco (table 7
), an affiliation that does not conform with classical taxonomy. The divergence of the total coding sequence is more extensive between Buteo and Falco than between Buteo and Ciconia (
2 = 34.86, df = 1, P < 0.001).
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An MP dendrogram based on the complete coding sequence (15,742 bp) is depicted in figure 3 . Three species pairs are supported by high bootstrap values: Gallus/Aythya, Rhea/Struthio, and Corvus/Vidua. In the cluster of the three ciconiiform species, Buteo and Falco appear as sister taxa, although with weak bootstrap support. The passeriform split is at the base of the tree, yet Passeriformes do not form a monophyletic group, since Smithornis branches off as the most basal bird taxon. The corresponding NJ dendrogram (not shown) resembles the MP dendrogram with two exceptions: Buteo clusters with Ciconia (bootstrap value = 97), and Smithornis is not the sister group to all other ingroup taxa. Instead, there is a trichotomy of the three lineages (Smithornis/CorvusVidua/remaining avian taxa). In both the MP and the NJ dendrograms, the passeriform taxa are placed at the base of the birds, and the two pairs Gallus/Aythya and Rhea/Struthio are grouped as one clade that is the sister group of the cluster Buteo/Falco/Ciconia. Dendrograms were also calculated from deduced protein sequences and from DNA sequences using transversions only (data not shown). However, in general, better resolution and stronger bootstrap support were obtained with DNA sequences that included all substitutions, so those were used for subsequent phylogenetic analysis.
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Discussion |
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Relationships Among Buteo, Falco, and Ciconia
Although we included all avian mt genomes available, our main interest in this study was the group Buteo/Falco/Ciconia. Nevertheless, despite the huge amount of DNA sequence, the relationships within this triad were not clearly resolved. Whereas in the distance-based dendrogram of the complete coding sequence Buteo clusters with Ciconia, the MP analysis yielded the expected group Buteo/Falco. Saturation effects are not the only explanation for the poor resolution, because the topology of the rest of the tree (with the exception of the position of Smithornis) seems to be unambiguous. It is more likely that unequal substitution rates among Buteo, Falco, and Ciconia are the reason for the conflicting topologies. Another possibility might be that the radiation of the lineages leading to Buteo, Falco, and Ciconia occurred within a relatively short time frame. The fossil evidence for the first appearance of the three lineages is rather vague: the earliest storklike fossil, Palaeoepphippiorhynchus, stems from the early Oligocene (3726 MYA) of Fayum, Egypt (Olson 1985
). The oldest accipitrid fossils are also from early Oligocene deposits in France. These are thought to be Buteo-like (Newton and Olsen 1990
), but according to Feduccia (1996)
, these remains are in need of revision. Falconids have been reported from 55 MYA (del Hoyo, Elliott, and Sargatal 1994
) and 48 MYA (Peters 1991
), respectively, but from fragmentary fossils. The first well-documented falconids, however, were described from the Eo-Oligocene in France and England (Peters 1991
). Therefore, from the fossil record, it is not possible to decide which of the three lineages split first. With respect to anatomical traits, storks differ from accipitrids and falconids mainly in numerous characteristics of skeletal bone structure, skull formation, and the arrangement of some muscles (Rea 1983
). One exceptional behavioral trait which storks share with cathartids, but not with accipitrids and falconids, is that storks keep cool by squirting their legs with urine. Although the distance-based algorithms favor a topology with Buteo and Ciconia as sister taxa, a closer relationship between Buteo and Falco is suggested by the following arguments: In the CR, the most variable part of the mt genome, sequence similarity is stronger between Buteo and Falco (71.4%, 691 bp; uncorrected, gaps
5 excluded) than between either of them and Ciconia (Buteo/Ciconia: 66.8%; Falco/Ciconia: 69.0%, 691 bp; uncorrected, gaps
5 excluded). Furthermore, Buteo and Falco share, in contrast to Ciconia, the same derived rearrangement of the CR. Thus, the topology of the ciconiiform clade in the MP dendrogram is not only in accordance with the classical taxonomic view, but is also corroborated by structural features of the mt genome.
Usefulness of Markers
Investigations of mt genes of various vertebrates by Russo, Takezaki, and Nei (1996)
indicated that amino acid sequences were more informative than nucleotide sequences for reconstructing reliable trees. Our results do not conform with this, since resolution, as well as bootstrap support, decreases when amino acid sequences are used. Moreover, nd5, cyt b, and nd4 do not appear to be the most appropriate genes in our analyses. Nevertheless, the two studies differ with respect to taxonomic level: Russo, Takezaki, and Nei (1996)
analyzed vertebrate phylogeny, whereas we focused on avian evolution only. Moreover, we also included RNA sequences for our comparisons.
With respect to usefulness of marker genes, the results of our MP analyses of nucleotide sequences can be interpreted as follows: In general, dendrograms derived from single mt genes have low resolution and bootstrap support for expected species pairs. Whereas most genes support the species pairs Corvus/Vidua and Rhea/Struthio, the clades Gallus/Aythya and Buteo/Falco are found in the 16S and tRNA trees only. Therefore, none of the protein-coding genes can be recommended as reliable markers for phylogenetic studies at this taxonomic level. Among the concatenated protein-coding sequences, cox(13) (although only half as long) appears better than nd(16). Concatenated rRNAs plus tRNAs (4,350 bp) resolve all four expected species pairs and are thus as good as the complete coding sequence (15,742 bp). In a dendrogram calculated from the complete coding sequence except nd5 and 12S, the two genes supporting the Buteo/Ciconia clustering, the bootstrap value of the Buteo/Falco clade rose to 92, while the rest of the tree remained unchanged. A tree based on only 16S and tRNAs yielded high bootstrap support in the Buteo/Falco/Ciconia cluster but lower values for the other nodes. To summarize, the concatenated RNA genes (rRNAs, tRNAs) appear to be the favorable combination, although bootstrap support is lower than that for the total sequence.
Basal Relationships and Dating of Splits
The phylogeny presented in this study, which is based on MP analyses of mt genomes, is in accordance with several other studies based on whole mt genomes (Härlid, Janke, and Arnason 1997, 1998
; Härlid and Arnason 1999
; Mindell et al. 1999
; Waddell et al. 1999
) and nuclear sequences (Stapel et al. 1984
; Caspers et al. 1997
). It is also compatible with the results of Griffiths (1994)
, based on syringeal morphology. In comparison to the dendrogram of Mindell et al. (1999)
, three additional taxa were included in the present study: Buteo, Ciconia, and Corvus. Whereas in the maximum-likelihood tree of Mindell et al. (1999)
Falco clusters with Smithornis, in our trees Smithornis never clusters with ciconiiform species. Instead, the Ciconiiformes appear as a stable monophyletic group that is the sister group of the clade Galloanserinae/Ratitae. The Passeriformes split at the base of the avian tree, although in some of the dendrograms they do not appear to be a monophyletic group. Instead, Smithornis (a representative of the suboscines, which are considered the most basal passeriform group) splits off as the most basal lineage of the dendrogram. Our mt-based phylogeny contradicts those derived from other studies of mt as well as nuclear genes, in which ratites appear at the base of the avian tree (Groth and Barrowclough 1999
; van Tuinen, Sibley, and Hedges 2000
). This incongruity is not necessarily due to marker selection (nuclear/mitochondrial). One reason for it might be that the studies differ in taxon composition. For example, in the dendrogram presented by Groth and Barrowclough (1999)
based on the nuclear gene RAG-1, no ciconiiform and no suboscine species are represented. On the other hand, sequences of the mt genomes of birds included in the RAG-1 study (cranes, loons, penguins, hemipodes, shorebirds, rollers) have not been published so far. Another reason for the incongruity might be the different lengths of the marker sequences (e.g., 3-kb RAG vs. 15,742-bp mt genes). In our MP dendrogram, the branches of the passeriform taxa appear shorter. This may be due either to the fact that the Alligator sequence is not a suitable outgroup to root the tree or to a slower substitution rate in the Passeriformes. Thus, we cannot rule out the possibility that the basal position of Passeriformes might be caused by long-branch attraction of the ciconiiform and galloanserine clusters. Altogether, a reasonable comparison between nuclear and mt-derived phylogenies will be possible only when (1) representatives of more avian groups (with both mt and nuclear genes) have been analyzed and (2) more nuclear sequence data (different genes) are available.
Unfortunately, the fossil record allows neither corroboration nor falsification of our data concerning the position of passeriformes. When the reports about the first appearances of avian groups are compared, no clear conclusions about the succession of splits or divergence times of the various lineages can be drawn. For example, according to Feduccia (1996
, p. 166), the oldest fossils of Ratitae are from the Paleocene (6553 MYA), and according to Houde and Haubold (1987)
, the oldest ostrich fossils are from the early Eocene (5337 MYA), the epoch from which the oldest putative passeriform fossils (Boles 1995
) as well as falconids (see above) are also dated. As the oldest neognathous fossils are from the Mesozoic (Olson 1992), there is at least no support from the fossil record for the hypothesis that the Paleognathae represent the most basal lineage.
Faced with the incomplete fossil record for birds of prey, the dating of divergences has to rely on a molecular approach. The following molecular datings are available. For the Rhea/Gallus split, Härlid, Janke, and Arnason (1997)
calculated 8090 MYA, and Waddel et al. (1999)
calculated 92 MYA. For the divergence of Aythya/Gallus, 68 MYA has been estimated (Waddel et al.1999
). According to our HKY85 distances (22.3% for Aythya/Gallus, 23.7% for Galloanserinae/Struthioniformes), these two splits should be closer. From the two different reference points, the divergence of Buteo/Falco (21.3%) can be estimated to have occurred in the late Cretaceous, either at 7283 MYA or at 65 MYA.
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Supplementary Material |
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Acknowledgements |
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Footnotes |
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1 Keywords: Buteo buteo
mitochondrial genome
avian phylogeny
gene order
control and pseudo control regions
2 Address for correspondence and reprints: Elisabeth Haring, 1. Zoological Department, Museum of Natural History Vienna, Burgring 7, A-1014 Vienna, Austria. elisabeth.haring{at}nhm-wien.ac.at
.
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