j Raptor Res. 27(4):196-202 ¸ 1993 The Raptor ResearchFoundation, Inc.

CHROMOSOMES OF FIVE NORTH AMERICAN BUTEONINE HAWKS

SHEILAM. SCHMUTZ,JANE S. MOKER AND TRACEYD. THUE Departmentof Animal and PoultryScience, University of Saskatchewan, Saskatoon,SK, Canada S7N OWO

ABSTRACT.--Fivespecies of buteoninehawks were karyotypedfor the first time, includingthe Swainson's Hawk (Buteoswainsoni), Gray Hawk (B. nitidus),Ferruginous Hawk (B. regalis),Harris' Hawk (Parabu- teo unicinctus),and Broad-winged Hawk (B. platypterus).All five specieshave 68 chromosomes.The karyotypesof the first four speciesappear to be very similar to each other and to other buteosreported previouslyin the literature, differing in the shapeof only one chromosome.The Broad-wingedHawk karyotypediffers in the morphologyof severalchromosomes.

Cromosomasde cincoespecies norteamericanas de halconesdel g•nero Buteo RESUMEN.--Porprimera vez han sido examinadosy caracterizadoslos cariotiposde cincohalcones del g6neroButeo (Aguililla Migratoria Mayor Buteoswainsoni, Aguililla Gris B. nitidus,Aguililla Real B. regalis,Aguililla Rojinegra Parabuteounicinctus, y Aguililla Migratoria Menor B. platypterus).Todas las cinco especiestienen 68 cromosomas.Parece ser que los cariotipos de halconesde las cuatro primeras especies(B. swainsoni,B. nitidus,B. regalis,y Parabuteounicinctus) son muy similaresentre ellos,asl como lo soncon los de otroshalcones de esteg6nero ya referidosen literaturaanterior. l•stos se diferencian s61opor la forma de s61oun cromosoma,mientras que el Aguililla Migratoria Menor difiere por la morfologlade varioscromosomas. [Traducci6n de Eudoxio Paredes-Ruiz]

Chromosomeanalysis has been used to studyphy- pus; Bulatova 1977), the RoadsideHawk (B. mag- logeneticrelationships in severalspecies, such as nirostris;de Lucca 1983), and the White-tailed Hawk falcons (Schmutz and Oliphant 1987) and owls (B. albicaudatus;de Lucca 1985). (Schmutz and Moker 1991). In our view, cytoge- neticsis well suitedto cladisticanalysis because the MATERIALS AND METHODS phylogeniesare basedon centricfusions (Robert- The blood sample from the Ferruginous Hawk was sonian translocations)and inversions(White 1973, collectedin Alberta, Canada. Bloodsamples from the Har- Hsu 1979), bothof whichalso impair fertility (Ther- ris' and four Gray Hawks were collectedin Arizona. The man 1980, Diedrichet al. 1983, Lippman-Hand and bloodsamples from the Swainson'sHawk and the Broad- winged Hawk were collectedfrom birds in captivityfor Vekemans1983), part of the classicaldefinition of rehabilitation at the Western College of Veterinary Med- speciesseparation. icine after injury near Saskatoon,Saskatchewan, Canada. In an ongoingattempt to collectcytogenetic data Lymphocytecultures were establishedfrom 0.5 ml of on raptorsfor this purpose,we havekaryotyped five whole blood and chromosomesprepared as describedby speciesof buteoninehawks not previouslyreported. Schmutzand Oliphant (1987). Karyotypeswere basedon the bestmetaphase(s) obtained on completecells. Several The five speciesof hawksare the Swainson'sHawk cells were photographedand the chromosomesarranged (Buteoswainsoni), Gray Hawk (B. nitidus),Ferru- Comparativestudies of karyotypesnot done in our own ginousHawk (B. regalis),Harris' Hawk (Parabuteo lab are basedupon figuresin the original publishedpapers unicinctus),and Broad-wingedHawk (B. platyp- when availableor photocopiesthrough interlibrary loan. terus). Prior to our study,five other species of buteoshad RESULTS beenkaryotyped. These were the CommonBuzzard Although most bird specieshave a large number (B. buteo;Renzoni and Vegni-Talluri 1966, De Boer of microchromosomesand few macrochromosomes, 1976), the Red-tailed Hawk (B. jamaicensis;Shoff- the hawksand eaglesare atypicalin that few of their ner 1974, Pape and Ogasawara 1978, Stock and chromosomes could be called microchromosomes. The Worthen 1980), the Rough-leggedHawk (B. lago- Swainson'sHawk (Fig. 1), Gray Hawk (Fig. 2),

196 DECEMBER 1993 BUTEO CHROMOSOMES 197

Figure 1. The karyotypeof a male Swainson'sHawk (Buteoswainsoni) with an arrow marking chromosome7, the variable chromosomewhich is metacentricin this species.

FerruginousHawk (Fig. 3), and Harris' Hawk (Fig. The Broad-winged hawk differed from the other 4) each had 68 chromosomesincluding one large four hawks we studied although the total number metacentricpair (the sex chromosomes),five large remained 68 (Fig. 5). The largest pair was again submetacentricpairs, six medium-sizedmetacentric metacentricand we presume it to be the sex chro- pairs, eight small metacentricpairs, and 13 small mosomepair. However, therewere only 16 submeta- acrocentricpairs, and one pair which was variable centric or metacentricpairs in total as opposedto in morphology.This variable chromosomewas ei- 20-21 pairs. ther a large submetacentricor large acrocentric.It We subdivided the buteonine hawks into two ma- was the seventhlargest by size and therefore we jor groups based on the different morphologiesof refer to it as chromosome7. Traditionally chro- chromosome7 (Fig. 6) and placedB. platypterusin mosomesare groupedby centromereposition and a third separate group since chromosomes16-20 then secondarilyby size.We havedecided to arrange differed.Although the karyotypeof the Gray Hawk the chromosomesfor easeof comparisonamong the (Fig. 2) doesnot have an obviousacrocentric chro- species,in the traditional order for the $wainson's mosome7, it is the clearest karyotype overall and Hawk and Common Buzzard but with chromosome thereforewe choseto publish it. Other karyotypes 7 out of its traditional place for the other species. we studied clearly indicate that chromosome7 is Other authors, such as Stock and Worthen (1980) acrocentricin this species.Less clear, is the mor- who have publishedonly a singlespecies karyotype, phologyof chromosome20 which also appears ac- place this chromosomewith the other acrocentrics rocentricin this photograph(Fig. 2). so it would be number 21 in their karyotype. We attemptedto include the other buteo species 198 SGHMUTZ ET AL. VOL. 27, NO. 4

Figure 2. The karyotypeof a male Gray Hawk (Buteonitidus) with an arrow markingchromosome 7, the variable chromosomewhich is acrocentricin this species.

Figure 3. The karyotypeof a femaleFerruginous Hawk (Buteoregalis) with an arrow markingchromosome 7, the variable chromosomewhich is acrocentricin this species. z w

Figure 4. The karyotype of a female Harris' Hawk (Parabuteounicinctus) with an arrow marking chromosome7, the variable chromosomewhich is acrocentricin this species.

z z

Figure 5. The karyotypeof a female Broad-wingedHawk (B. platypterus).The karyotypeis arrangedto emphasize that chromosomes16-20 in the middle row are acrocentricin this speciesas opposedto metacentricin the other buteos. 200 SCHMUTZET AL. VOL. 27, NO. 4

I 2 3 4 5 6 Buteo regalis Buteo nitidus 7 8 9 10 11 12 Buteo jamaicensis X X X x x x Buteo iagopus 13 14 15 16 17 18 19 Buteo aibicaudatus n n nn n n Buteo magnirostris 21 22 23 24 25 26 27 Parabuteo unicinctus

28 29 30 31 32 33

I 2 3 4 5 6 Buteo swainsoni 7 8 • •0 • •2 Buteobuteo • • X X X x • • x 13 14 15 16 17 18 19

21 22 23 24 25 26 27

29 30 31 32 33

1 2 $ 4 5 & z X X Xx x x x Buteo platypterus 7 8 9 10 11 12 13; 14 tl n n n n 16 17 18 19 20

21 22 25 24 25 26, 27

28 29 30 31 32 33 Figure6. A cladogramillustrating therelationships among the buteonine hawks studied todate and computer drawn idiogramsof thethree karyotypes observed, upon which the phylogeny is based.

studiedpreviously, although the copiesof the kar- tailed Hawk (B. albicaudatus;de Lucca 1985) match yotypesthat we usedmake our interpretationten- the buteoswe did very closely.However, a minute tative.The karyotypesof theCommon Buzzard ( B. metacentricwas described(De Boer 1976, Stockand buteo;De Boer 1976), the Red-tailedHawk (B. Worthen 1980) which we cannotverify or dispute maicensis;Stock and Worthen 1980), and the White- sincethe small chromosomesin our karyotypes are DECEMBER 1993 BUTEO CHROMOSOMES 201 not elongatedenough to determinethis. We worked mosomesto demonstratespecific translocations and with poorphotocopies of karyotypesof the Rough- inversionsin mammals (Ward et al. 1991). Avian leggedHawk (B. lagopus;Bulatova 1977) and the karyotypesare much more difficultto obtain than RoadsideHawk (B. magnirostris;de Lucca 1983) mammaliankaryotypes, primarily due to the lower andcan only say that thetop two rows(Fig. 6) agree numbersof dividing cells stimulatedby mitogens in general with the karyotypesof the buteoswe (Prus and Schmutz 1987). Low numbersof dividing studied. cells therefore make chromosomebanding difficult sincemost techniqueswork well on only a small DISCUSSION proportion of these cells. Although chromosome Four speciesof buteoninehawks studiedhere for banding is necessaryto determinewith precision the first time have one of the sametwo karyotypes. which chromosomes are involved in translocations, This similarity supportsthe closetaxonomic rela- bandingis not necessaryto identify the presenceor tionshipBrown and Amadon (1968) suggestedamong absenceof translocations,which is the key to phy- thesespecies. Further differentiationamong subfam- logeneticcomparisons. ilies would need to be basedon other typesof data, In addition to a poor responseto mitogens,cy- suchas DNA sequencedata which is currentlyunder togeneticstudies of birds have been further ham- investigationby Bob Sheehy(pers. comm.). peredbecause fresh blood samples or growingfeath- The difference in morphologyof chromosome ers, capableof further cell divisionin culture, are number 7 is likely due to an inversion,in this case required for analysis.Many rare and endangered a pericentricinversion, one of the two cytogenetic birds exist in remote areas. Field collection of sam- changesthat typicallyoccur during evolution(Hsu plesfrom wild caughtbirds is occasionallypossible 1979). We are unableto saywhich is the "ancestral" but the logisticsof air transport to an appropriate shapeof chromosome7 and thereforeour cladogram lab within 24 hr is frequentlyimpossible. Despite is "unrooted" and shows the two main branches as suchdifficulties, chromosome analysis can providea deriving at an equal point in time (Fig. 6). useful tool in taxonomic studies and we encourage The Harris' Hawk is placedin the genus?ara- raptorbiologists to collaboratein suchstudies. buteoas opposedto Buteo;however, its karyotype ACKNOWLEDGMENTS would not distinguishit from mostof the other Buteo We thank JosefK. Schmutz,Bob Sheehy,and Collette speciesstudied to date.This suggeststhat the Harris' Wheler for collectingthe bloodsamples which madethis Hawk is indeed a close relative of the buteos. study possible.We acknowledgefunding from the Sas- In contrastthe karyotype of the Broad-winged katchewanAgricultural Development Fund and the Na- Hawk showsfive chromosomes,numbers 16-20, that tional Scienceand EngineeringResearch Council which differ in morphologyfrom the restof the buteos(Fig. supportsour laboratory. 5). This would suggestthat it is the most divergent LITERATURE CITED in the subfamily.It is more closelyrelated to the Swainsoh's Hawk and Common Buzzard than the BROWN,n. AND D. AMADON. 1968. Eagles, hawks and falcons of the world. McGraw Hill, New York, NY other buteos,based on the morphologyof chromo- U.S.A. some7 (Fig. 6). BULATOVA,N.S. 1977. Chromosomestructure and evo- In contrastto the similarity foundamong the bu- lution in birds. NAUKA Publishing House, Novosi- teos,the nine speciesof falconsstudied to dateexhibit birsk, Russia. four differentkaryotypes in the genus(Schmutz and DE BOER,L.E.M. 1976. The somatic chromosomecom- Oliphant 1987, Longmireet al. 1988). The primary plementsof 16 speciesof Falconiformes(Aves) and the cytogeneticdifferences among the falconsare cen- karyoloõicalrelationships of the order.Genetica 46:77- tric fusionsor translocationsas opposedto inver- 113. sions, with the Merlin (Falco columbarius)having BE LUCCA, E.J. 1983. Somatic chromosomesof Falco sparveriusand Buteornagnirostris (Falconiformes: Aves). the greatestnumber of chromosomes(Longmire et Nucleus. 26:48-56. al. 1988) and therefore being the most diverged, 1985. Kar¾otypeand nucleolusorganizing followedby the PeregrineFalcon (F. peregrinus)and regionsin somaticchromosomes of the White-tailed Prairie Falcon(F. mexicanus;Schmutz and Oliphant Hawk Buteoalbicaudatus (Falconiformes: Aves). 1987). roblos 42:7-13. Cytogeneticistsfrequently use banding of chro- DIEDRICH, U., I. HANSMANN,D. JANKE,O. OPITZ AND 202 SGHMUTZ ET AL. VOL. 27, NO. 4

H.-D. PROBECK. 1983. Chromosome anomalies in SCHMUTZ,S.M. ANDJ.S. MOKER. 1991. A cytogenetic 136 coupleswith a historyof recurrentabortions. Hum. comparisonof someNorth American owl species.Ge- Genet. 65:48-52. nome 34:714-717. Hsu, T.C. 1979. Human and mammalian cytogenetics --AND L.W. OLIPHANT.1987. A chromosomestudy an historicalperspective. Springer-Verlag, New York, of the Peregrine,Prairie, and Gyrfalconswith impli- NY U.S.A. cationsfor hybrids.J. Hered. 78:388-390. LIPPMAN-HAND,A. ANDM. VEKEMANS. 1983. Balanced SHOFFNER,R.N. 1974. Chromosomesof birds. Pages translocationsamong couples with two or more spon- 223-287 in H. Busch (ED.), The cell nucleus. Aca- taneousabortions: are malesand femalesequally likely demic Press, New York, NY U.S.A. to be carriers? Hum. Genet. 63:252-257. STOCK,A.D. ^ND G.L. WORTHEN. 1980. Identification LONGMIRE, J.L., A.K. LEWIS, N.C. BROWN, J.M. of the sex chromosomesof the Red-tailed Hawk (Buteo BUCKINGHAM, L.M. CLARK, M.D. JONES, L.J. jamaicensis)by C- and G-banding. RaptorRes. 14:65- MEINCKE,J. MEYNE, R.L. RATLIFF,F.A. RAY, R.P. 68. WAGNER AND R.K. MOYZIS. 1988. Isolation and mo- THERMAN, E. 1980. Human chromosomesstructure, lecular characterizationof a highly polymorphiccen- behavior, effects. Springer-Verlag, New York, NY tromerictandem repeat in the family Falconidae.Gen- U.S.A. omics 2:14-24. WARD,O.J., A.S. GRAPHODATSKY,D.H. WURSTER-HILL, PAPE,K.L. AND F.X. OGASAWARA.1978. Studies on the V.R. EREMINA,J.P. PARKAND (•. YU. 1991. Cy- karyotypeof the Red-tailedHawk. RaptorRes. 12:28- togeneticsof beavers:a case study of speciationby 34. monobrachial centtic fusion. Genome 34:324-328. PRUS,S.E. AND S.M. SCHMUTZ. 1987. Comparative ef- WHITE, M.J.D. 1973. Animal cytologyand evolution. ficiencyand accuracyof surgicaland cytogenetic sexing CambridgeUniv. Press,Cambridge, U.K. in psittacines.Avian Dis. 31:420-424. RENZONI, A. AND M. VEGNI-TALLURI. 1966. The kar- yogramsof someFalconiformes and Strigiformes. Chromosoma 20:133-150. Received25 April 1993; accepted30 August 1993