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(Woodpeckers and Allies) Author(S): John C. Avise and Charles F Malate Dehydrogenase Isozymes Provide a Phylogenetic Marker for the Piciformes (Woodpeckers and Allies) Author(s): John C. Avise and Charles F. Aquadro Source: The Auk, Vol. 104, No. 2 (Apr., 1987), pp. 324-328 Published by: University of California Press on behalf of the American Ornithologists' Union Stable URL: http://www.jstor.org/stable/4087044 Accessed: 25/11/2008 15:25 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=ucal. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit organization founded in 1995 to build trusted digital archives for scholarship. We work with the scholarly community to preserve their work and the materials they rely upon, and to build a common research platform that promotes the discovery and use of these resources. For more information about JSTOR, please contact [email protected]. University of California Press and American Ornithologists' Union are collaborating with JSTOR to digitize, preserve and extend access to The Auk. http://www.jstor.org 324 ShortCommunications [Auk, Vol. 104 ination. Captive Breeding of Diurnal Birds of Prey LAKE, P. 1975. Gamete production and the fertile 1: 3-5. period with particular reference to domesticated Fujii, S., & T. TAMURA. 1963. Location of sperms in birds. Symp. Zool. Soc. London 35: 225-244. the oviducts of the domestic fowl with special MERO, K. N., & F. X. OGASAWARA. 1970. Dimensions reference to storage of sperms in the vaginal of uterovaginal sperm-storage tubules of the gland. J. Fac. Fish. Anim. Husbandry, Hiroshima chicken and their possible significance in sperm Univ. 5: 145-163. release. Poultry Sci. 49: 1304-1308. GILBERT,A. B. 1979. Female genital organs. Pp. 237- PAL, D. 1977. Histochemistry of the utero-vaginal 360 in Form and function in birds, vol. 1 (A. S. junction with special reference to the sperm-host King and J. McLelland, Eds.). New York, Aca- glands in the oviduct of the domestic duck. Folia demic Press. Histochem. Cytochem. 15: 235-242. HATCH, S. A. 1983. Mechanism and ecological sig- VAN DRIMMELEN,G. C. 1946. "Spermnests" in the nificance of sperm storage in the Northern Ful- oviduct of the domestic hen. J. S. African Vet. mar with reference to its occurrence in other Med. Assoc. 17: 43-52. birds. Auk 100: 593-600. HOWARTH,B. 1971. Transport of spermatozoa in the Received 14 March 1986, accepted 23 September1986. reproductive tract of turkey hens. Poultry Sci. 50: 84-89. Malate Dehydrogenase Isozymes Provide a Phylogenetic Marker for the Piciformes (Woodpeckersand Allies) JOHN C. AVISE AND CHARLESF. AQUADRO' Department of Genetics, University of Georgia,Athens, Georgia30602 USA Nuclear genes encode two major forms of malate of approximately equal intensity" (Kitto and Wilson dehydrogenase (MDH; E.C. 1.1.1.37) in birds: S-MDH 1966). This distinctive S-MDH pattern was subse- (or MDH-1), which is found in the soluble fraction quently observed in a Japanese woodpecker (Kuroda of the cell cytoplasm; and M-MDH (or MDH-2), which et al. 1982: fig. 3) and in three species of North Amer- is housed in mitochondria (Karig and Wilson 1971). ican woodpeckers (Aquadro and Avise 1982). Under standard starch-gel electrophoretic condi- Phylogenetic relationships of the woodpeckers and tions, S-MDH typically migrates toward the anode allies have been the subject of intense debate (Simp- while M-MDH migrates cathodally. In terms of gen- son and Cracraft 1981, Swierczewski and Raikow 1981, eral zymogram appearance and electromorph fre- Olson 1983, Raikow and Cracraft 1983, Sibley and quencies across avian taxa, both S-MDH and M-MDH Ahlquist 1986). In most traditional taxonomic lists, are very conservative evolutionarily (Kitto and Wil- six families are included in the Piciformes: Galbuli- son 1966, Aquadro and Avise 1982, Kuroda et al. 1982). dae (jacamars), Bucconidae (puffbirds), Capitonidae In particular, S-MDH assayed in pH 7.0 gels exhib- (barbets), Indicatoridae (honeyguides), Ramphasti- ited the same common electromorph in representa- dae (toucans), and Picidae (woodpeckers). Recently, tives of 22 avian orders (Kitto and Wilson 1966). Al- this classification has been challenged on the grounds though additional S-MDH variation was detected that the assemblage may be polyphyletic (Olson 1983, under the multiple electrophoretic conditions em- Sibley and Ahlquist 1986). Raikow and Cracraft (1983), ployed by Aquadro and Avise (1982), S-MDH re- however, defended the validity of the synapomorphs mains extremely conservative in comparison with (hypothesized shared-derived traits) used to infer most other enzyme systems. monophyly of the Piciformes. Additional questions Kitto and Wilson (1966) first noticed an unusual concern the relationships of true piciform families to S-MDH zymogram pattern in three species of Pici- one another. In an effort to help resolve some of these formes. Unlike the typical avian S-MDH pattern, phylogenetic issues, we surveyed members of all the which consists of an intense major band with one or taxa listed above, plus other possible piciform allies, two much lighter anodic subbands, the Piciformes for occurrence of the distinctive and obviously de- were "exceptional in having two S-MDH subbands rived S-MDH woodpecker pattern. Frozen tissue samples (usually heart, liver, or mus- l Present address: Section of Genetics and Devel- cle) were homogenized separately in an equivalent opment, Cornell University, Ithaca, New York 14853 volume of grinding solution (0.01 M Tris, 0.001 M USA. EDTA; pH 6.8) and centrifuged at 49,000 g. Electro- April 1987] Short Communications 325 GALBULOIDEA RAMfPHASTOI DeA CAP ITONOIDEA G.Ib.lid.. B5-cid.. R.Wh-id- C.pito.dd- Indi--ird.. Fi.id- J.C 0 u fbi10d0 T.o.- B-bt.. Bygldo . W. odp.lk- Fig. 1. Representative S-MDH zymogram pat- terns in various species of "piciform" birds. From left A to right: (1) Melanerpes carolinus (Picidae); (2) Galbula ruficauda (Galbulidae); (3) Veniliornis nigriceps (Pici- PICI GAOUA dae); (4) Melanerpes carolinus (Picidae); (5) Melanerpes cruentatus(Picidae); (6) Piculus rivolii (Picidae); (7) and -IDEA PICOIDEA (8) Chelidopteratenebrosa (Bucconidae); (9) Monasa ni- . G.lb.lidre Buc-oid R.ph.tid.. C.pi-oid.. Idi .-oid.. Picid.e H- grifrons (Bucconidae); (10) Melanerpes carolinus (Pici- Jc-cr Pu ffbird: Tou-n B-rb-t yguide Woodpeckers dae); (11) Andigena cucullata (Ramphastidae); (12) Pteroglossuscastanotis (Ramphastidae); (13) Ramphastos culminatus (Ramphastidae); (14) Malacoptila semicincta (Bucconidae). The 3-band S-MDH pattern is evident in lanes 1, 3-6, and 10-13. The typical S-MDH pat- Y~~~~ tern in nonpiciform birds is pictured in fig. 1 of Aquadro and Avise (1982) and is like that in lanes 2, 7-9, and 14 above. Fig. 2. Two (among several) possible phylogenies for "piciform" birds. (A) Inferred from a traditional classification proposed by Peters (1948). (B) Proposed phoresis of supernatant extracts involved horizontal by Simpson and Cracraft (1981) and independently starch gels (12.5%), run at 75 mA for 5-7 h. The fol- by Swierczewski and Raikow (1981). The postulated lowing amine-citrate (A-C) buffer system was em- origin of the derived 3-band S-MDH zymogram is ployed routinely: electrode buffer, 0.04 M citric acid, indicated by the black rectangle. pH adjusted to 6.1 with N-(3-aminopropyl) morpho- line (purchased from Aldrich Chemicals); gel buffer, 1 to 19 dilution of electrode buffer. This system was pectoral muscle, leg muscle, heart, liver, gizzard wall, chosen because, among 12 buffers utilized previ- intestine wall, eye, and brain. There were no ob- ously, it provided the best resolution for S-MDH vious, differential tissue specificities for any S-MDH (Aquadro and Avise 1982). Nonetheless, other buffer isozymes (although all bands were darkest in the conditions yielded comparable results. MDH was muscle and heart samples). stained using the recipe of Selander et al. (1971). In the woodpecker-type S-MDH zymogram, all The avian material consisted of 29 species that rep- three bands were invariably present, and the middle resented 22 of the 74 piciform genera (30%) recog- band stained most intensely. Thus, the gel pattern nized in most current checklists. In addition, mem- gives the impression of "fixed heterozygosity" for bers of Coliiformes and several families of S-MDH, which is known to be a dimeric molecule in Coraciiformes (possible relatives of the Piciformes) birds. One plausible explanation is that woodpeckers were surveyed (Table 1). The samples originated from possess a gene duplication for S-MDH, such that the three continents: Africa, North America, and South middle band in the zymogram represents an inter- America (Table 1). locus heterodimer, flanked by the two respective in- S-MDH zymograms.-The distinctive "woodpeck- tralocus homodimeric products. Similar zymogram er-type" S-MDH electrophoresed with the amine-ci- patterns and assembly of interlocus hybrid molecules trate buffer exhibits three major bands (Fig. 1), the are known in some fishes that carry an S-MDH gene two most anodal of which apparently correspond to duplication (Bailey et al. 1970, Wheat et al. 1971). If the "two subband" zymogram pattern originally no- the S-MDH gene is also duplicated in woodpeckers, ticed by Kitto and Wilson (1966).
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