Open Access
How to translate text using browser tools
1 December 2009 Molecular Phylogeny of Owls (Strigiformes) Inferred from DNA Sequences of the Mitochondrial Cytochrome b and the Nuclear RAG-1 gene
Michael Wink, Abdel-Aziz El-Sayed, Hedi Sauer-Gürth, Javier Gonzalez
Author Affiliations +
Abstract

For 97 owl taxa from 15 of the larger genera (some monotyplc taxa are not represented) a molecular phylogeny was Inferred from a combined dataset of nucleotide sequences of mitochondrial cytochrome b and nuclear RAG-1 genes. The molecular phylogeny can be used to create a taxonomic framework, which agrees with cladistics. Strigiformes are divided Into two families: Tytonldae and Strigidae. The Tytonldae are subdivided into the subfamilies Tytoninae (with Tyto) and Phodilinae (with Phodilus). The Strigidae cluster in three subfamilies: Striginae, Surniinae and Ninoxinae (with the genera Ninox, and possibly the monotypic Uroglaux and Sceloglaux). The Surniinae are subdivided in three tribes Surnini (with Surnia, Glaucidium and Taenloglaux), Athenini (with Athene) and Aegolini (with Aegolius). The Striginae are subdivided into six tribes: Bubonini (with Bubo including the former Nyctea, Ketupa and Scotopelia), Strigini (with Strix and Jubula), Pulsatrigini (with Pulsatrix and Lophostrix), Megascopini (with Megascops and Psiloscops), Otini (with Otus and Mimizuku) and Asionini (with Asio, Ptilopsis and possibly the monotypic Nesaslo and Pseudoscops).

INTRODUCTION

The avian order Strigiformes represents a fascinating group of nocturnal raptor with a complex biology (Bock & McEvey 1969, Eck & Busse 1973, Mikkola 1983, Amadon & Bull 1988, Burton 1992, del Hoyo et al. 1999, König et al. 1999, König & Weick 2008). In order to occupy the ecological niche of a nocturnal raptor, owls had to evolve several adaptations. Besides specialized hunting strategies, owls developed a sophisticated acoustical communication system. Morphology is often cryptic and invariant in many owl species but the distinctive calls, which are inherited and not learned, are of considerable taxonomic value (Hekstra 1982, König 1991a,b, 1994a,b). If phylogenetic relationships were reconstructed on the basis of the morphological characteristics alone, wrong conclusions might be drawn since some of these characteristics may be convergent traits that are not related to the underlying phylogeny.

The Strigiformes are subdivided into two families (Sibley & Monroe 1990, del Hoyo et al. 1999, Weick 2006): Tytonidae and Strigidae. Whereas the Tytonidae consist of two subfamilies and two genera (and no further substructure), the Strigidae have a much more complex structure being split in three subfamilies which are further subdivided in six tribes:

  • subfamily Striginae with tribes Otini, Bubonini and Strigini,

  • subfamily Asioninae,

  • subfamily Surniinae with tribes Surnini, Aegolini and Ninoxini.

We have chosen the mitochondrial (mt) cytochrome b gene to study the finer details of speciation and phylogeny of owls (Wink & Heidrich 1999, 2000, Wink et al. 2004, 2008). We have enlarged our cytochrome b data base and have additionally sequenced the nuclear (nc) RAG-1 gene for all groups that were critical in order to get better support for the deeper branches. Basically, the ncDNA data support the results obtained from mtDNA (Wink & Heidrich 1999, Wink et al. 2004, 2008). Our present dataset has a good coverage for most genera. The missing genera belong to monotypic ones, so that a general picture on the phylogeny of owls becomes possible with this analysis.

METHODS

The cytochrome b and RAG-1 genes were amplified by PCR (primer sequences in Groth & Barrowclough 1999, Wink 2000). First, sequences were obtained by using AlfExpress (Amersham Pharmacia Biotech) or ABI 3100 (Applied Biosystems). Since 2003, sequences were determined using the DYEnamic ET Terminator Cycle Sequencing Kit (Amersham Pharmacia Biotech). Sephadex™ G-50 columns (Amersham Biosciences) and Multiscreen filter plates (Millipore Corporation) were used for sequencing purification products. Sequences were analyzed by capillary electrophoresis using a MegaBACE™ 1000 sequencer (Molecular Dynamics Inc., Amersham Pharmacia). Sequences of 900–1000 base pairs (bp) for cytochrome b and 953 bp for RAG-1 have been deposited in GenBank (Appendix 1).

The sequences were aligned by BioEdit version 7.0.5 (Hall 2004). Basic statistics, variable and parsimony informative sites, and p-distances were calculated with MEGA version 4.0 (Tamura et al. 2007). Molecular phylogenies were constructed using maximum likelihood (ML) in PAUP* v. 4.0b10a (Swofford 2002) and Bayesian inference (BI) in MPI-MrBayes version 3.1.2. (Ronquist & Huelsenbeck 2003, Altekar et al. 2004). Phylogenetic analyses were performed for both genes separately and concatenated (cytb + RAG-1) as well. We explored the model of sequence evolution that fits the data best with Modeltest version 3.7 (Posada & Crandall 1998). The best model was then used with the ML analyses. Robustness of nodes was assessed by 1000 bootstrap replicates using the program GARLI version 0.951 (Zwickl 2006). For BI analyses, two independent runs of 8 000 000 generations each were performed along with four Markov chains. The evolutionary model selected for BI analysis was the GTR + Γ + I. Trees were sampled every 500 generations and the first 4000 samples were discarded as ‘burn-in’. Two partitions (cytb and RAG-1) were considered in BI analysis in the combined dataset.

For most species we have determined the cytochrome b at least from two individuals, so that the sequences used in this analysis are unequivocal and reliable (Heidrich 1998, Wink & Heidrich 1999, Wink et al. 2008). When a significant haplotype differentiation was absent the molecular analysis were conducted with a single sequence (cytb + RAG-1) per taxon.

Three outgroup species were selected to root the owl tree: Mountain Owlet-nightjar Aegotheles albertisi, the Greater White-fronted Goose Anser albifrons and the chicken Gallus gallus. The sequences for these taxa were available from GenBank.

RESULTS AND DISCUSSION

ML and BI trees were inferred from a combined dataset (cytb + RAG-1) of 97 sequences (Fig. 1), which resolves even the deeper nodes. Most of the clades are supported by high bootstrap and posterior probability values allowing a re-evaluation of the traditional owl systematics in terms of families, subfamilies, tribes and genera.

Relationships within the family Tytonidae

The genetic data support the view of a monophyletic family Tytonidae which consists of two monophyletic subfamilies: Tytoninae and Phodilinae (Fig. 1).

Although several taxa in the Tyto complex have been recognized as distinct species already (Sibley & Monroe 1990, König et al. 1999, Weick 2006, König & Weick 2008), several others within T. alba, T. delicatula, T. novaehollandiae, T. longimembris, T. tenebricosa and T. furcata are considered to be subspecies. Some of them, especially some island taxa, may apparently represent distinct and endemic species. According to König & Weick (2008) and Weick (2006) 25 species are recognized.

The Australian region is settled by two different lineages of the genus Tyto: (1) T. novaehollandiae, T. castanops, T. multipuncta, T. longimembris and T. tenebricosa and (2) T. delicatula (including the more derived T. d. sumbaensis — from Sumba Islands — which probably merits species status).

The Eurasian Barn Owl Tyto alba has been divided into several subspecies, of which a number have already been converted into true and distinct species. Whereas the subspecies T. alba and T. guttata can hardly be distinguished genetically, T. erlangeri (from the eastern Mediterranean) and T. affinis (from Africa) form distinct but not highly diverged lineages within the T. alba complex. Tyto soumagnei from Madagascar is a sister to T. alba and T. furcata, which together share ancestry with the T. delicatula group from Australasia (Wink et al. 2008).

Relationships within the subfamily Striginae

Within the Striginae in its traditional circumscription, three tribes are recognised (Weick 2006): Strigini (with Strix, Jubula, Lophostrix and Pulsatrix), Bubonini (with the genera Bubo, Nyctea, Ketupa and Scotopelia) and Otini (with the genera Otus, Megascops, Macabra, Pyrroglaux, Gymnoglaux, Psiloscops, Ptilopsis and Mimizuku).

TRIBE STRIGINI

Presently, 18 species are recognised in the genus Strix (Weick 2006). Tawny and Wood Owls (genus Strix) always form a monophyletic clade (94% bootstrap support, see Fig. 1) and cluster as a sister group to the Bubo complex (tribe Bubonini) with a 73% of bootstrap proportion.

The New World species S. rufipes and S. varia form a monophyletic clade and cluster as a sister to the Old World species, which diverged from a common ancestor 5–6 Myr ago (Wink & Heidrich 1999). Future studies, which should include several of the numerous New World species, will show whether this assumption holds true for all New World species.

Three species are recognized in the Central and South American genus Pulsatrix, of which we have studied P. perspicillata and P. koeniswaldiana. The phylogenetic position of Pulsatrix cannot be resolved with certainty even with the concatenated dataset (cytb + RAG-1): in ML analyses (Fig. 1) it clusters between Strix and Megascops, but nodes are not supported by high bootstrap values. It is therefore questionable whether Pulsatrix is a true member of the tribe Strigini.

Lophostrix and Jubula are both monotypic genera: Jubula lettii occurs in West and Central Africa while Lophostrix cristata in Central and South America. Only a short DNA sequence of cytb has been submitted to GenBank, which corresponds to L. cristata. A preliminary DNA analysis would place it as a sister to Pulsatrix (Wink et al. 2008). Whether both taxa belong to the tribe Strigini cannot be answered with certainty at present. It is more likely that Lophostrix and Pulsatrix form their own tribe, the Pulsatrigini.

TRIBE BUBONINI

Members of the tribe Bubonini form a monophyletic clade in all the phylogenetic reconstructions (with 99–100% of bootstrap support). About 19 species are recognised in the genus Bubo (Weick 2006). Bubo ascalaphus, which occurs in North West Africa and the Near East, has been treated as a distinct species (Sibley & Monroe 1990). In our analysis, B. bubo and B. ascalaphus differ by an uncorrected p-distance of 3.5%. Also B. b. interpositus, which is morphologically distinct from B. bubo and thrives in the desert from Israel, is also genetically distinct (p-distance of 2.8%, Wink & Heidrich 1999); it clusters as a sister to Bubo ascalaphus. Since a sequence divergence of more than 2% is indicative of species level, it could be justified to treat both taxa, Bubo ascalaphus and Bubo interpositus, as distinct species or at least B. interpositus as a subspecies of B. ascalaphus.

The Snowy Owl (Bubo scandiacus, formerly Nyctea scandiaca) shares definite common ancestry with the genus Bubo (Fig. 1), especially with the New World species B. virginianus. The separation from a common ancestor took place more than 4 Myr ago (Wink & Heidrich 1999). Nyctea represents a monotypic genus but unambiguously clusters within the Bubo complex, which would make the genus Bubo paraphyletic. Since paraphyletic taxa should be avoided in systematics, the taxonomic consequences would be to lump Nyctea with Bubo and call the species Bubo scandiacus. This change has been accepted already by most authorities, except Weick (2006).

A similar paraphyly as in Nyctea can be seen in Ketupa, of which three species (K. zeylonensis, K. flavipes and K. ketupu) have been described from Southeast Asia. Ketupa zeylonensis and K. ketupu cluster as close relatives to the Asian Bubo species, such as B. nipalensis (Fig. 1). Also the general appearance of Ketupa is similar to that of Bubo; because of genetic relationships (p-distance of 9–10%) we agree with Amadon & Bull (1988) to merge Ketupa in Bubo. Also this change has been accepted by now by most authorities (König & Weick 2008).

Three species have been described in African Fishing Owls of the genus Scotopelia. So far, we could only compare the cytb sequence of a single individual from S. peli with other members of the tribe Bubonini. According to this analysis (Wink et al. 2008), Scotopelia unequivocally clusters together with Bubo vossleri, B. nipalensis and B. sumatranus (Wink et al. 2008). Such a position would make the genus Bubo paraphyletic. In order to overcome the problem, the simplest way would be to merge Scotopelia in Bubo, as suggested for Nyctea and Ketupa.

TRIBE OTINI

The combined dataset (cytb + RAG-1) unambiguously shows that members of the tribe Otini cluster in at least three different monophyletic lineages, indicating that the genus Otus and the tribe Otini are paraphyletic or polyphyletic in their former circumscriptions (Wink & Heidrich 1999); a systematic revision of the genus Otus and the tribe Otini was a logical consequence.

The Screech Owls of the New World represent a distinct group, which is separated from Old World members of Otus by genetic distances of 12–16% (equivalent to 6–8 Myr, Wink & Heidrich 1999). Within the Screech Owl complex, which has its radiation centre in South and Central America, several species have been recognized on account of different acoustic repertoires (König 1994a). Sequence data could corroborate these findings (Heidrich et al. 1995 a), stressing the importance of vocalization for speciation and taxonomy.

Figure 1.

ML bootstrap phylogram of the generic relationships in owls based on a combined dataset of cytb and RAG-1 sequences. ML bootstrap values/BI posterior probability values indicated for each node. The tree is separated in two parts in order to make it readable.

f01a_581.eps

Continued

f01b_581.eps

The American taxa have been either placed in the genus Megascops (with 25 species) or Psiloscops. The Flammulated Owl Otus flammeolus differs in vocalisation and genetics (Fig. 1) from Megascops, therefore a monotypic genus Psiloscops (Coues 1899), which clusters as a sister group to Megascops, appears to be adequate (Penhallurick 2002, Weick 2006, König & Weick 2008). Megascops albogularis has been placed in the subgenus Macabra (Weick 2006); however, the phylogenetic data do not support such a monotypic subgenus (Wink et al., 2008).

Several Old World Scops Owls (44 species) have been described (overview in Sibley & Monroe 1990, Weick 2006) of which 10 have been included here as representatives for this group. As can be seen from Fig. 1 these Scops Owls fall into a common clade, which is very distinct from the New World Megascops/Psiloscops complex. Using 12S mt rDNA sequences, Mindell et al. (1997) showed that O. mirus, O. mindorensis and Mimizuku gurneyi cluster together with O. megalotis and O. longicornis. Since we studied also the latter two species, we can conclude that Mimizuku gurneyi is a likely member of the Old World Otus group. Since Mimizuku clusters within this group it is doubtful whether this monotypic genus is valid.

The African White-faced Owl (formerly Otus leucotis) differs both morphologically and genetically from the other Old World Otus species (Wink & Heidrich 1999) and has therefore been placed in the genus Ptilopsis. In Africa two taxa occur, P. leucotis in West, Central and East Africa and P. granti in southern Africa. In all reconstructions (Fig. 1) Ptilopsis figures as a sister group to the genus Asio.

Pyrroglaux and Gymnoglaux represent monotypic genera. Pyrroglaux podarginus has been described from Palau Islands and Gymnoglaux lawrencii from Cuba. DNA analyses are required to see whether both taxa represent monotypic genera and with which other genus they share ancestry.

Concluding, it seems obvious that the different monophyletic clades of the former Otus complex should also be revised taxonomically, i.e., by creating the genera Otus, Megascops, Psiloscops and Ptilopsis, which has been done by several authorities already (Penhallurick 2002, König & Weick 2008). As can be seen from Fig. 1, the former tribe Otini is paraphyletic and interrupted by the Asionini. In order to create a cladistically coherent system, we need to split the former tribe Otini in the tribes Otini, Megascopini and Asionini (taking care of Ptilopsis).

Relationships within the subfamily Asioninae

Three genera have been placed in the subfamily Asioninae, Asio and the monotypic Pseudoscops and Nesasio. Within Asio, seven species are distinguished (Weick 2006).

Asio otus, A. clamator, A. capensis and A. flammeus always fall into the same clade (Fig. 1); the genetic distances imply a divergence time of more than 5 Myr. Asio always clusters as a sister to Ptilopsis (Fig. 1). The combined dataset provides strong evidence (94% bootstrap support) that Asioninae does not form a distinct subfamily, but clusters within the Striginae (independent of the tree building methods used). Thus, we suggest merging Asioninae with Striginae in order to avoid paraphyletic groups. The rank of a tribe Asionini containing the genera Asio and Ptilopsis would be adequate.

Pseudoscops grammicus occurs in Jamaica, Nesasio solomonensis on the Solomon Archipelago, Bougainville, Choiseul and Santa Isabel. Without DNA evidence it is difficult to say whether they deserve the status of monotypic taxa and which affiliation they have (probably tribe Asionini).

Relationships within the subfamily Surniinae

The subfamily Surniinae in the traditional circumscription (Weick 2006) is formally subdivided in three tribes: Surniini (with the genera Surnia, Glaucidium, Taenioglaux, Xenoglaux, Micrathene and Athene), Aegolini (Aegolius), Ninoxini (Ninox, Uroglaux and Sceloglaux).

TRIBE SURNIINI

Pygmy Owls (32 species) of the former genus Glaucidium occur in the Old and New World. Whereas their plumage is very similar in most instances (a fact which makes their taxonomy so difficult), they can be distinguished by a unique repertoire of vocalizations (König 1994b). Recent taxonomical classifications based on differing acoustic signals (König 1994b) have been corroborated with DNA sequence data (Heidrich et al. 1995b). Fig. 1 clearly shows that Old and New World species cluster in separate monophyletic clades, which share common ancestry but have diverged more than 7–8 Myr ago (Wink & Heidrich 1999).

In the Pygmy Owls of the Old World two clades are apparent: G. passerinum, G. tephronotum and G. perlatum cluster as a sister to the New World species. Members of the subgenus Taenioglaux Kaup 1848, which differ in morphology from members of the genus Glaucidium s.str., are represented in our cytb dataset by G. capense and G. cuculoides (Wink et al. 2008). Apparently both species cluster in a more distant, separate clade and form a sister group to Surnia/Glaucidium s.str. A split of this subgroup into the genus Taenioglaux (see König & Weick 2008) is thus supported by molecular evidence.

The Northern Hawk Owl Surnia ulula of northern Eurasia and North America shares common ancestry and forms a monophyletic group (96% bootstrap support) with the Glaucidium s. str. complex (Fig. 1).

Three species have been recognized in the genus Athene, i.e. A. noctua (Eurasia), A. brama (southeast Asia) and A. blewitti (India). Within A. noctua several distinct lineages become visible (similar to the situation in the American Glaucidium complex) that indicate a high degree of geographic differentiation. So far we have detected three genetic lineages, which are supported by high bootstrap values; genetic differences (p-distance) between these groups account for 5–6%, exceeding the 2% which is typical for ‘good’ species in owls. Little Owls from Israel, Cyprus and Turkey have been recognised as A. n. lilith. On a genetic level, A. n. lilith is clearly separated from Little Owls of central and western Europe, representing the subspecies A. n. noctua and A. n. vidalii, but share ancestry with A. n. indigena from southeast Europe (Wink et al. 2008). Because of the significant genetic distances, it would be plausible to recognise A. lilith as a distinct species (König et al. 2008). Also A. n. plumipes from Mongolia and China shows a distinct genetic lineage (Fig. 1), probably indicating species status; we suggest recognising this taxon as A. plumipes.

The former Speotyto cunicularia represents the genus Athene in the New World and this species has sometimes been considered as a member of the genus Athene. Because DNA—DNA hybridization suggested significant differences (Sibley & Monroe 1990), a separation into a monotypic genus appeared justified. However, according to the sequence data, it is clear that Speotyto and Athene share common ancestry (divergence approximately 6 Myr ago) and that they form a monophyletic group. Because of similarities in morphology, general outlook and in behaviour, we suggested to merge Speotyto back into Athene (Wink & Heidrich 1999). Most authorities have accepted this suggestion (König et al. 1999, König & Weick 2008).

The genetic analyses of A. noctua and A. cunicularia are still incomplete. Because of the phylogeographic variation detected in both taxon complexes, a more detailed study, which would cover the whole distribution range, will certainly reveal a more complex pattern with several distinct species and subspecies.

The Athene complex clusters as a sister to Glaucidium/Taenioglaux/Surnia in all reconstructions, independent of the methods used for tree reconstruction (Fig. 1). This clade corresponds to the tribe Surniini. From a cladistic point of view, such a tribe would agree with basic rules. On the other hand, the subfamily Striginae needs to be subdivided into several smaller tribes, which would make a tribe Surniini rather large. In order to create tribes of more even shape it would also be possible to recognise a distinct tribe Athenini as a sister to Surniini, the latter containing the genera Glaucidium, Taenioglaux and Surnia.

TRIBE AEGOLINI

Owls in the genus Aegolius can be found as a third major monophyletic group (Fig. 1) (tribe Aegolini) besides the tribe Surniini with Glaucidium, Surnia and Athene. The North American A. acadicus diverges with 12.9% (p-distance) from A. funereus, implicating a divergence time of more than 6 Myr (Wink & Heidrich 1999). Two geographically separated subspecies, A. a. acadicus and A. a. brooksi can be recognized (p-distance of 0.7%). The South American A. harrisii is more closely related to the North American A. acadius than to A. funereus (Fig. 1), suggesting a common ancestor for the New World species.

The tribes Aegolini and Surniini share common ancestry with a high bootstrap proportion (100%); this group excludes the tribe Ninoxini (Fig. 1).

TRIBE NINOXINI

The genus Ninox comprises 25 species with Australasian distribution. According to the general appearance they could be related to the Glaucidium/Athene complex and formally they were recognised as the tribe Ninoxini within the subfamily Surniinae. In our phylogenetic analyses, Ninox clusters basal within Strigidae (Fig. 1) indicating that the subfamily Surniinae is paraphyletic. As a consequence, the tribe Ninoxini should be excluded from the Surniinae and possibly form a subfamily of its own, the Ninoxinae (with the genera Ninox, Uroglaux and Sceloglaux).

Recently, a new owl was discovered on Sumba Island, which was assumed to be a member of the genus Otus. DNA analysis revealed unequivocally that it is a member of the genus Ninox. It was described as Ninox sumbaiensis (Olsen et al. 2002).

Two monotypic genera have been included in the tribe Surniini, Xenoglaux loweryi from northern Peru and Micrathene whitneyi from southwestern North America. Preliminary DNA sequence data only exist for M. whitneyi, which would place it outside the tribe Surniini (Wink et al. 2008) but close to the subfamily Surniinae. Uroglaux dimorpha (north-western New Guinea) and Scelogalux albifacies (New Zealand) have been included in the tribe Ninoxini, which would make sense in view of distribution and general appearance. DNA samples are needed to see whether their status as monotypic genera and their affiliation can be maintained.

Phylogenetic position of owls as compared to diurnal raptors and nightjars

Linné (1758) placed owls, vultures, eagles and falcons together as an order Accipitres. In 1827 owls were separated from diurnal raptors as a distinct order by L'Herminier; Nitsch (1840) already recognized the differences between Tytonidae and Strigidae. This view was supported by Fürbringer (1888) and Gadow (1892), who also stressed a close relationship between Strigiformes and Caprimulgiformes, a view maintained by Mayr & Amadon (1951). However, Cracraft (1981) using a cladistic approach, concluded a closer relationship between owls and falcons. Sibley & Ahlquist's (1990) study using DNA-DNA hybridisation implied that Caprimulgiformes, rather than falcons, are the nearest neighbour to the owls. However, mtDNA sequences do not support a Strigiformes/Caprimulgiformes clade (Wink and Heidrich 1999).

Figure 2.

Phylogeny of birds (simplified after Ericson et al. 2006 and Hacket et al. 2008).

f02_581.eps

Table 1.

Summary of a systematic classification of owls rigorously based on monophyletic groups.

t01_581.gif

Recently, a large dataset of five nuclear genes (Fain & Houde 2004, Ericson et al. 2006) has provided good evidence that Caprimulgiformes are part of the Metaves, whereas owls are members of the Coronaves. Within the Coronaves, owls are found in a clade with diurnal raptors except falcons, the latter clustering as a sister to parrots and song birds (Fig. 2).

Morphological and anatomical similarities between owls and nightjars, which were the basis for the hypothesis of a closer relationships to owls, are probably influenced by convergence (as implied already by Bock & McEvey 1969, Mikkola 1983, Feduccia 1996), cannot be supported by gene sequence data.

Conclusions

About 120 taxa of the Strigidae and 23 taxa of Tytonidae have been studied so far in our laboratory (Wink et al. 2008) and phylogenetic analyses based on cytochrome b and nuclear markers (RAG-1) provide insight into the evolution of owls. Phylogenetic analyses suggest a few changes in overall owl systematics to generate monophyletic taxa, as has been discussed in this paper (summarized in Table 1). Sequence data of mt and ncDNA provide a powerful tool (besides morphology, anatomy, behaviour and bioacoustics) to elucidate and reconstruct the evolutionary past and speciation in owls.

ACKNOWLEDGEMENTS

We thank W. Bednarek, G. Ehlers, O. Hatzofe, R. Krahe, D. Reynolds, A. Kemp, C. Fentzloff, W. Grummt, C. König, J. YomTov, D. Ristow, E. Thaler, B. Etheridge, J. Perry-Jones, C. White, J. Olsen, J. Penhallurick, H.-H. Witt, the Owl Trust and U. Schneppat for providing blood or tissues of owls. The study of owl phylogenetics has been performed in close collaboration with C. König (Stuttgart) and J. Penhallurick (Canberra) whom we would like to thank for his help and encouragement. Professor Dr. H. Bock (Managing Director of IWR) and S. Friedel kindly provided access to the parallel computing facilities at the Interdisciplinary Center for Scientific Computing (IWR, Heidelberg University).

REFERENCES

1.

G. Altekar , S. Dwarkadas , J.P. Huelsenbeck & F. Ronquist 2004. Parallel Metropolis-coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics 20: 407–415. Google Scholar

2.

D. Amadon & J. Bull 1988. Hawks and owls of the world. Proc. W. Found. Vertebr. Zool. 3: 297–357. Google Scholar

3.

W.J. Bock & A. McEvey 1969. The radius and relationships of owls. Wilson Bull. 81: 55–68. Google Scholar

4.

J.A. Burton 1992. Owls of the world, their evolution, structure and ecology. Peter Lowe, London. Google Scholar

5.

J. Cracraft 1981. Towards a phylogenetic classification of recent birds of the world (class Aves). Auk 98: 681–714. Google Scholar

6.

J. del Hoyo , A. Elliott & J. Sargatal (eds) 1999. Handbook of the birds of the world, Vol. 5. Barn-owls to Hummingbirds. Lynx Edicions, Barcelona. Google Scholar

7.

S. Eck & H. Busse 1973. Eulen. Ziemsem Verlag, Wittenberg-Lutherstadt. Google Scholar

8.

P.G.P. Ericson , C.L. Anderson , T. Britton , A. Elzanowski , U. Johansson , M. Källersjö , J.I. Ohlson , T.J. Parsons , D. Zuccon & G. Mayr 2006. Diversification of neoaves: integration of molecular sequence data and fossils. Biol. Lett. 2: 543–547. Google Scholar

9.

M.G. Fain & P. Houde 2004. Parallel radiations in the primary clades of birds. Evolution 58: 2558–2573. Google Scholar

10.

A. Feduccia 1996. The origins and evolution of birds. Yale Univ. Press, New Haven. Google Scholar

11.

M. Fürbringer 1888. Untersuchungen zur Morphologie und Systematik der Vögel. Amsterdam. Google Scholar

12.

H. Gadow 1892. On the classification of birds. Proc. Zool. Soc. London 1892: 229–256. Google Scholar

13.

J.G. Groth & G.F. Barrowclough 1999. Basal divergences in birds and the phylogenetic utility of the nuclear RAG-1 gene. Mol. Phylogenet. Evol. 12: 115–23. Google Scholar

14.

S.J. Hackett , R.T. Kimball , S. Reddy , R.C.K. Bowie , E.L. Braun , M.J. Braun et al. 2008. A phylogenomic study od birds reveals their evolutionary history. Science 320: 1763–1768. Google Scholar

15.

T. Hall 2004 BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41: 95–98. Google Scholar

16.

P. Heidrich 1998. Untersuchungen zur molekularen Phylogenie ausgewählter Vogelgruppen anhand von DNA-Sequenzen des mitochondriellen Cytochrom b-Gens. PhD Thesis, Heidelberg University. Google Scholar

17.

P. Heidrich , C. König & M. Wink 1995a. Molecular phylogeny of the South American Screech Owls of the Otus atricapillus complex (Aves, Strigidae) inferred from nucleotide sequences of the mitochondrial cytochrome b gene. Z. Naturforsch. 50c: 294–302. Google Scholar

18.

P.C. Heidrich , C. König & M. Wink 1995b. Bioakustik, Taxonomie und molekulare Systematik amerikanischer Sperlingskäuze (Strigidae: Glaucidium spp.). Stuttgarter Beiträge Naturkunde A 534: 1–47. Google Scholar

19.

G.P. Hekstra 1982. Description of twenty-four new subspecies of American Otus (Aves, Strigidae). Bull. Zool. Mus. Amsterdam 9: 49–63. Google Scholar

20.

C. König 1991a. Taxonomische und ökologische Untersuchungen an Kreischeulen (Otus spp.) des südlichen Südamerika. J. Ornithol. 132: 209–214. Google Scholar

21.

C. König 1991b. Zur Taxonomie und Ökologie der Sperlingskäuze (Glaucidium spp.) des Andenraumes. Ökol. Vögel 13: 15–76. Google Scholar

22.

C. König 1994a. Lautäußerungen als interspezifische Isolations-mechanismen bei Eulen der Gattung Otus (Aves: Strigidae) aus dem südlichen Südamerika. Beitr. Naturkde. Ser. A. Google Scholar

23.

C. König 1994b. Biological patterns in owl taxonomy, with emphasis on bioacoustical studies on neotropical pygmy (Glaucidium) and screech owls (Otus). In: B.-U. Meyburg & R.D. Chancellor (eds) Raptor conservation today. Pica Press, pp. 1–19. Google Scholar

24.

C. König , W. Weick & J. Becking 1999. Owls. A guide to the owls of the World. Pica Press, Sussex. Google Scholar

25.

C. König & W. Weick 2008. Owls. A guide to the owls of the World. Second edition. Christopher Helm, London. Google Scholar

26.

E. Mayr & D. Amadon 1951. A classification of recent birds. Americ. Mus. Novit. 1496. Google Scholar

27.

H. Mikkola 1983. Owls of Europe. T. & A.D. Poyser, Calton. Google Scholar

28.

D.P. Mindell , M.D. Sorenson , C.J. Huddleston , J. Miranda , A. Knight , S.J. Sawchuk & T. Yuri 1997. Phylogenetic relationships among and within select avian orders based on mitochondrial DNA. In: D.P. Mindell (ed.) Avian molecular evolution and systematic. Academic Press, San Diego, pp. 213–247. Google Scholar

29.

C.L. Nitsch 1840. System der Pterylographie. E. Anton, Halle. Google Scholar

30.

J. Olsen , M. Wink , H. Sauer-Gürth & S. Trost 2002. A new Ninox owl from Sumba, Indonesia. Emu 102: 223–232. Google Scholar

31.

J.M. Penhallurick 2002. The taxonomy and conservation status of the owls of the world: a review. In: I. Newton , R. Kavanagh , J. Olsen & I. Taylor (eds) Ecology and conservation of Owls. CSIRO Publishing, Australia, pp. 343–354. Google Scholar

32.

D. Posada & K.A. Crandall 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818. Google Scholar

33.

G.A. Proudfoot , R.L. Honeycutt & R.D. Slack 2006. Mitochondrial DNA variation and phylogeography of the Ferruginous Pygmy-Owl (Glaucidium brasilianum). Conserv. Genet. 7: 1–12. Google Scholar

34.

F. Ronquist & J.P. Huelsenbeck 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. Google Scholar

35.

C.G. Sibley & J.E. Ahlquist 1990. Phylogeny and classification of birds. Yale Univ. Press, New Haven. Google Scholar

36.

C.G. Sibley & B.L. Monroe 1990. Distribution and taxonomy of birds of the World. Yale University Press, New Haven, London. Google Scholar

37.

D.L. Swofford 2002. PAUP-Phylogenetic analysis using parsimony. Version 4.0b10. Google Scholar

38.

K. Tamura , J. Dudley , M. Nei & S. Kumar 2007. MEGA 4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596–1599. Google Scholar

39.

F. Weick 2006. Owls (Strigiformes). Annotated and illustrated checklist. Springer. Google Scholar

40.

M. Wink 2000. Advances in DNA studies of diurnal and nocturnal raptors. In: R.D. Chancellor & B.-U. Meyburg (eds) Raptors at risk. WWGBP/Hancock House, London, pp. 831–844. Google Scholar

41.

M. Wink & P. Heidrich 1999. Molecular evolution and systematics of owls (Strigiformes). In: C. König , F. Weick & J.H. Becking (eds) Owls of the world. Pica Press, Kent, pp. 39–57. Google Scholar

42.

M. Wink & P. Heidrich 2000. Molecular systematics of owls (Strigiformes) based on DNA sequences of the mitochondrial cytochrome b gene. In: R.D. Chancellor & B.-U. Meyburg (eds) Raptors at Risk, 819–828. WWGBP/Hancock House, London. Google Scholar

43.

M. Wink , P. Heidrich , H. Sauer-Gürth , A.-A. El-Sayed & J.M. Gonzalez 2008. Molecular phylogeny and systematics of owls (Strigiformes). In: C. König & F. Weick (eds) Owls of the world, Second edition. Christopher Helm, London, pp. 42–63. Google Scholar

44.

M. Wink , H. Sauer-Gürth & M. Fuchs 2004. Phylogenetic relationships in owls based on nucleotide sequences of mitochondrial and nuclear marker genes. In: R.D. Chancelor & B.-U. Meyburg (eds) Raptors Worldwide. WWGBP, Berlin, pp. 517–526. Google Scholar

45.

D.J. Zwickl 2006. Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD dissertation, University of Texas, Austin. Google Scholar

Appendices

SAMENVATTING

Op grond van moleculair onderzoek is de onderlinge verwantschap van 97 uilensoorten vastgesteld. Dergelijke gegevens zijn tegenwoordig een belangrijke basis voor de naamgeving en ordening van soorten. De orde van de Uilen is opgesplitst in de families Tytonidae en Strigidae. De Tytonidae zijn onderverdeeld in de onderfamilies Tytoninae (met het geslacht Tyto) en Phodilinae (met Phodilus). De Strigidae zijn onderverdeeld in de onderfamilies Striginae, Surniinae en Ninoxinae (met het geslacht Ninox, en mogelijk de monotypische Uroglaux and Sceloglaux). De Surniinae zijn onderverdeeld in de takken Surnini (met Surnia, Glaucidium en Taenioglaux), Athenini (met Athene) en Aegolini (met Aegolius). De Striginae zijn onderverdeeld in de takken Bubonini (met Bubo waaronder de vroeger geheten Nyctea, Ketupa en Scotopelia), Strigini (met Strix en Jubula), Pulsatrigini (met Pubatrix en Lophostrix), Megascopini (met Megascops en Psiloscops), Otini (met Otus en Mimizuku) en Asionini (met Asio, Ptilopsis en mogelijk de monotypische Nesasio en Pseudoscops).

Appendix 1

Appendix 1.

Origin, collection codes and accession numbers of owl taxa investigated in this study. Taxa are in alphabetical order.

tA01_581.gif
Michael Wink, Abdel-Aziz El-Sayed, Hedi Sauer-Gürth, and Javier Gonzalez "Molecular Phylogeny of Owls (Strigiformes) Inferred from DNA Sequences of the Mitochondrial Cytochrome b and the Nuclear RAG-1 gene," Ardea 97(4), 581-591, (1 December 2009). https://doi.org/10.5253/078.097.0425
Published: 1 December 2009
KEYWORDS
cladistics
cytochrome b
phylogeny
RAG-1
Strigidae
Strigiformes
Tytonidae
Back to Top