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The Chromosomal Phylogeny of Owls (Strigiformes) and New Karyotypes of Seven Species W

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The Chromosomal Phylogeny of Owls (Strigiformes) and New Karyotypes of Seven Species W _??_1993 The Japan Mendel Society Cytologia 58: 403-416 , 1993 The Chromosomal Phylogeny of Owls (Strigiformes) and New Karyotypes of Seven Species W. E.R. Rebholz1*, L.E. M. De Boer2, M . Sasaki3, R.H. R. Belterman1, and C. Nishida-Umehara4 1Stichting Koninklijke Rotterdamse Diergaarde , P. O.Box 532, 3000AM Rotterdam, TheNetherlands 2National Foundati onfor Research inZoological Gardens, P. O. Box 20164, Amsterdam,TheNetherlands 3Sasaki Institute , 2-2,Kanda-Surugadai, Chiyoda-ku, Tokyo 101, Japan 4 ChromosomeResearch Unit, Hokkaido University, Sapporo 060, Japan Accepted July 15, 1993 The order of Strigiformes (owls) consists of 134 species in 25 genera (Burton 1973). After decades of study taxonomic and phylogenetic relationships of this order are still a matter of discussion (Sibley and Ahlquist 1972: review). Phylogenetics of owls have been studied using egg-white protein data (Sibley and Ahlquist 1972), morphological data (Cracraft 1981), karyotypical data (Belterman and De Boer 1984, Schmutz and Moker 1991), DNA-DNA hybridization data (Sibley et al. 1988) and allozyme data (Randi et al. 1991). Unfortunately, these studies do not result in a uniform phylogeny, because they contradict each other in several aspects. Cracraft (1981) is the only one who put all owls (Tyto and Phodilius inclusive) in the family Strigidae, which he believes to be part of the order Falconiformes. All other recent publications believe the Strigiformes and Falconiformes to be separate orders. Two publica tions put all owls in the suborder Strigi (comprising two families: Tytonidae and Strigidae) and combine this suborder with the suborders Aegotheli and Caprimulgi in the order Strigiformes (Sibley et al. 1988, Randi et al. 1991), which is closely related to the Musophagidae and distantly related to the Falconidae. Some authors put all owls in one family (Sibley and Ahlquist 1972), others make a distinction between Tytonidae and Strigidae (Belterman and De Boer 1984, Sibley et al. 1988, Randi et al. 1991). From this information it is clear that it is still too early to arrive at a uniform phylogeny. The karyotypes of 26 species from 15 genera have been studied and recorded in the literature, but few subspecies and individuals per species are studied. Consequently, much about intraspecific variation or differences between subspecies is unknown. Different karyo types have been found within some single species of which enough individuals were studied, of which Asio otus, Pulsatrix perspicillata and Tyto alba are some examples. Some published karyotypes or karyotype dscriptions are of questionable quality and those species need to be reexamined. Most karyotypes have been published separately without comparing them with other owl karyotypes. Belterman and De Boer (1984) and Schmutz and Moker (1991) published reviews on the karyological phylogeny of owls. We try to establish a phylogenetic tree based on karyotypes studied to date and this should make it easier for other researchers to see where their results fit in. It could be helpful if future publications on karyology would refer to the phylogenetic tree published in this paper, to increase understanding about phylogeny of this order. It is convenient to use Bubo virginianus as reference for the ancestral Strigidae type because G-banded and C-banded karyotypes have been published (Biederman et al. 1980). * Current address: Department of Chemical Pathology University of Cape Town, Cape Town, South Africa. 404 W. E. R. Rebholz et al. Cytologia 58 Materials and methods Blood samples used in this study were from Asio otus (2 males), Athene noctua (1 female), Bubo lacteus (1 male), Ketupa blakistoni (1 female), Ketupa ketupa (1 female), Otus scops (1 female), Pulsatrix perspicillata (1 male, 2 females), Speotyto cunicularia (2 males), Strix hylophila (1 male), Strix leptogrammica (1 male, 1 female), Strix nebulosa (2 males, 1 female), and Tyto alba (1 male, 2 females). Lymphocyte cultures were carried out as described by Belterman and De Boer (1984). C-banding was done as described by Sumner (1972). Chromosomes were stained with Orcein or Giemsa. Observations In karyotypes presented here a uniform system of chromosome numbering is used unless shown otherwise. This means that homologous chromosomes in different species have identical numbers, but homologies are based on Orcein stained macrochromosomes only. Pairs numbe red 5/7 indicate supposed fusion products of ancestral chromosomes 5 and 7. Microchromo somes are acrocentric or telocentric and the difference is often cryptic. The original chromo some numbering can be found in Belterman and De Boer (1984). The supposed ancestral Strigidae karyotype is deduced from comparison with other avian orders (Belterman and De Boer 1984) and the fact that four different genera all have an identical type seems to justify this. Karyotypes of the ancestral Strigidae type species consist of an acrocentric pair 1, acrocentric pairs 2 and 3 of comparable size, a submetacentric pair 4 half the size of pair 1, an acrocentric pair 5, one or two metacentric Z-chromosomes about the size of pair 4 and about 60 to 70 telocentric microchromosomes. W-chromosomes vary in size and form, but are smaller than Z-chromosomes. This supposed ancestral type is represented in the phylogenetic tree by 11 species studied so far: Asio flammeus (Sasaki et al. 1981, Biederman in Shields 1982, Bian et al. 1988, Bian and Li 1989: 2n=82), Bubo lacteus (this report Fig. 1: 2n= 80-84), Bubo poensis (Belterman unpublished data), Bubo virginianus (Krishan et al. 1965, Biederman et al. 1980: 2n=82), Ketupa blakistoni (Sasaki et al. 1981, this report Fig. 2: 2n= 82), Ketupa ketupa (Sasaki et al. 1981, this report Fig. 4: 2n=82), Ketupa zeylonensis (Belterman and De Boer 1984, Roy 1990: 2n=78-80), Nyctea scandiaca (Sasaki et al. 1981, Fig. 1. Karyotype of a male Bubo lacteus (2n=80-84) with Z-chromosomes which are chosen tentatively, because only males were studied. 1993 The Chromosomal Phylogeny of Owls 405 Fig. 2. Karyotype of a female Ketupa blakistoni (2n=82) . Fig. 3. A C-banded karyotype of a female Ketupa blakistoni (2n=82), with additional C-band material in pair 2. Fig. 4. Karyotype of a female Ketupa ketupa (2n=82). Belterman and De Boer 1984: 2n=82), Otus leucotis (Belterman and De Boer 1984: 2n=70 or higher), Otus bakkamoena (Sasaki et al. 1981: 2n=82, Bhunya and Mohanty 1987, Roy et al. 1987, Bian et al. 1988, Bian and Li 1989, Roy 1990: 2n=78), and Otus scops (This report Fig. 5: 2n=74-84). In the karyotype of O. scops the W-chromosome could not be identified 406 W. E. R. Rebholz et al. Cytologia 58 Fi.g 5. Karyotype of a female Otus scops (2n=74-84) in which the W-chromosome could not be identified amongst other microchromosomes. amongst other microchromosomes. Schmutz and Moker (1991) argue that Asio otus also belongs to this group, but since there are three different types of this species, we did not include it in this group yet. K. blakistoni (Sasaki et al. 1981, this report Fig. 2: 2n=82) shows a somewhat different karyotype from others in that pair 2 is similar in length to pair 1, which is due to an extra large block of C-band material in pair 2 (Fig. 3). The five species of the genus Strix studied so far, S. aluco (Renzoni and Vegni-Talluri 1966, Hammar 1970: 2n=80), S. hylophila (Fig. 6: 2n=80), S. leptogrammica (Sasaki et al. 1981, this report Fig. 8: 2n=82?), S. nebulosa (Biederman in Shields 1982, this report Fig. 10: 2n= 80) and S. uralensis (Takagi and Sasaki 1974, Sasaki et al. 1981: 2n=82), are all very similar, having a characteristic fusion pair 5/7. Ciccaba woodfordii (Belterman and De Boer 1984: 2n= 82) also belongs to this group. Z-chromosomes and W-chromosomes vary in this group: the ancestral metacentric Z is found in S. aluco, S. leptogrammica and S. uralensis, a submetacentric Z, the same size as the ancestral one in S. nebulosa, a large metacentric Z in size between pairs 1 and 2 in S. hylophila and C. woodfordii. Z-chromosomes in the karyotype of S. hylophila (Fig. Fig. 6. Karyotype of a male Strix hylophila (2n=80) having fusion pair 5/7 as a characteristic element. The unusually large Z-chromosomes are chosen after comparison with other Strix-species. 1993 Th e Chromosomal Phylogeny of Owls 407 Fig. 7. A C-banded karyotype of a male Strix hylophila showing that all centromeres a re extremely C-band positive. Fig. 8. Karyotype of a female Strix leptogrammica (2n=82?) having fusion pair 5/7 as a characteristic element. 6), which are unusually large for owls, are chosen after comparison with other Strix species. W-chromosomes vary from metacentric (S. leptogrammica, S. uralensis japonica) and sub metacentric (S. nebulosa, S. uralensis hondoensis) to telocentric (S. aluco). The size of W-chromosomes is also variable between these species, with S. aluco having the smallest W-chromosome and S. uralensis japonica having the largest W-chromosome. The W chromosomes of S. leptogrammica, S. nebulosa, which are of the same size, are a little bit smaller than those of S. uralensis hondoensis. It should be noticed that the two subspecies of S. uralensis have different W-chromosomes. Now that several females per (sub)species have been studied, it seems evident that W-chromosomes do not vary in size within a subspecies. A C-banded karyotype of a male S. hylophila (Fig. 7) shows that all centromeres are extremely C-band positive. The additional C-band material found in the long arms of the Z-chromosomes could possibly be responsible for their exceptional size. A C-banded karyotype of a females. leptogrammica (Fig. 9) shows that all macrochromosomes and nearly all microchromosomes are C-band positive.
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