Malate Dehydrogenase Isozymes Provide a Phylogenetic Marker For

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Malate Dehydrogenase Isozymes Provide a Phylogenetic Marker For 324 ShortCommunications [Auk,Vol. 104 ination. CaptiveBreeding of Diurnal Birdsof Prey LAKE,P. 1975. Gamete production and the fertile 1: 3-5. period with particular reference to domesticated FuJII,S., & T. TAMURA.1963. Locationof spermsin birds. Symp. Zool. Soc. London 35: 225-244. the oviducts of the domesticfowl with special MERO, K. N., • F. X. OGASAWARA. 1970. Dimensions reference to storageof spermsin the vaginal of uterovaginal sperm-storagetubules of the gland. J. Fac.Fish. Anim. Husbandry,Hiroshima chicken and their possiblesignificance in sperm Univ. 5: 145-163. release. Poultry Sci. 49: 1304-1308. GILBERT,A.B. 1979. Femalegenital organs.Pp. 237- PAL, D. 1977. Histochemistry of the utero-vaginal 360 in Form and function in birds, vol. I (A. S. junction with specialreference to the sperm-host King and J. McLelland, Eds.). New York, Aca- glandsin the oviduct of the domesticduck. Folia demic Press. Histochem.Cytochem. 15: 235-242. HATCH,S. A. 1983. Mechanismand ecologicalsig- VAN DRIMMELEN,G. C. 1946. "Spermnests" in the nificanceof sperm storagein 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. Transportof spermatozoain the Received14 March 1986, accepted23 September1986. reproductive tract of turkey hens. Poultry Sci. 50: 84-89. Malate DehydrogenaseIsozymes Provide a PhylogeneticMarker for the Piciformes(Woodpeckers and Allies) JOHN C. AVISEAND CHARLESF. AQUADRO• Departmentof Genetics,University of Georgia,Athens, Georgia 30602 USA Nuclear genesencode two major forms of malate of approximatelyequal 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 observedin a Japanesewoodpecker (Kuroda of the cell cytoplasm;and M-MDH (or MDH-2), which et al. 1982:fig. 3) and in three speciesof North Amer- is housedin mitochondria(Karig and Wilson 1971). ican woodpeckers(Aquadro and Avise 1982). Under standard starch-gel electrophoretic condi- Phylogeneticrelationships of the woodpeckersand tions, S-MDH typically migrates toward the anode allieshave been the subjectof intensedebate (Simp- while M-MDH migratescathodally. In termsof gen- son and Cracraft 1981, Swierczewski and Raikow 1981, eral zymogram appearance and electromorph fre- Olson 1983, Raikow and Cracraft 1983, Sibley and quenciesacross avian taxa, both S-MDH and M-MDH Ahlquist 1986). In most traditional taxonomic lists, are very conservativeevolutionarily (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 assayedin pH 7.0 gels exhib- (barbers),Indicatoridae (honeyguides),Ramphasti- ited the same common electromorphin representa- dae (toucans),and Picidae (woodpeckers).Recently, tives of 22 avian orders (Kitto and Wilson 1966). Al- this classificationhas been challengedon the grounds though additional S-MDH variation was detected that the assemblagemay be polyphyletic(Olson 1983, under the multiple electrophoreticconditions em- Sibleyand Ahlquist 1986).Raikow and Cracraft(1983), ployed by Aquadro and Avise (1982), S-MDH re- however, defendedthe 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 concernthe relationshipsof true piciform families to S-MDH zymogram pattern in three speciesof Pici- one another.In an effort to help resolvesome of these formes. Unlike the typical avian S-MDH pattern, phylogeneticissues, we surveyedmembers of all the which consistsof an intense major band with one or taxa listed above, plus other possiblepiciform allies, two much lighter anodic subbands,the Piciformes for occurrenceof the distinctiveand obviously de- were "exceptionalin having two S-MDH subbands rived S-MDH woodpecker pattern. Frozen tissuesamples (usually heart, liver, or mus- • Present address: Section of Genetics and Devel- cle) were homogenized separatelyin 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- •,pril 1987] ShortCommunications 325 r+ Fig. I. Representative S-MDH zymogram pat- ternsin variousspecies of "piciforrn" birds. From left to right: (I) Melanerpescarolinus (Picidae); (2) Galbula ruficauda(Galbulidae); (3) Veniliornisnigriceps (Pici- dae); (4) Melanerpescarolinus (Picidae); (5) Melanerpes cruentatus(Picidae); (6) Piculusrivolii (Picidae); (7) and (8) Chelidopteratenebrosa (Bucconidae); (9) Monasani- grifrons(Bucconidae); (10) Melanerpescarolinus (Pici- dae); (11) Andigena cucullata (Ramphastidae); (12) Pteroglossuscastanotis (Ramphastidae); (13) Ramphastos culminatus(Ramphastidae); (14) Malacoptilasemicincta (Bucconidae).The 3-band S-MDH pattern is evident in lanes I, 3-6, and 10-13. The typical S-MDH pat- tern in nonpiciforrn birds is pictured in fig. I of Aquadro and Avise (1982) and is like that in lanes 2, 7-9, and 14 above. Fig. 2. Two (amongseveral) possible phylogenies for "piciform"birds. (A) Inferred from a traditional classificationproposed by Peters(1948). (B) Proposed phoresisof supernatantextracts involved horizontal by Simpsonand Cracraft(1981) and independently starchgels (12.5%),run at 75 mA for 5-7 h. The fol- by Swierczewskiand 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: electrodebuffer, 0.04 M citric acid, indicated by the black rectangle. pH adjustedto 6.1 with N-(3-aminopropyl) morpho- line (purchasedfrom Aldrich Chemicals);gel buffer, I to 19 dilution of electrode buffer. This systemwas pectoralmuscle, leg muscle,heart, liver, gizzardwall, 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 tissuespecificities 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 muscleand heart samples). stained using the recipe of Selander et al. (1971). In the woodpecker-type S-MDH zymogram, all The avian material consistedof 29 speciesthat rep- three bandswere invariably present,and the middle resented 22 of the 74 piciforrn 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 Coraciiforrnes(possible relatives of the Piciforrnes) birds. One plausibleexplanation is that woodpeckers were surveyed(Table I). The samplesoriginated from possessa gene duplication for S-MDH, such that the three continents: Africa, North America, and South middle band in the zymogram representsan inter- America (Table I). locusheterodimer, flanked by the two respectivein- S-MDH zymograms.--Thedistinctive "woodpeck- iralocus homodimeric products. Similar zymogram er-type" S-MDH electrophoresedwith the arnine-ci- patternsand assemblyof interlocushybrid molecules trate buffer exhibits three major bands (Fig. I), the are known in somefishes that carry an S-MDH gene two most anodal of which apparently correspondto 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). This pattern is individuals detectably heterozygousat either locus readily distinguishablefrom the usual S-MDH pat- shouldexhibit a 6-bandzymogram (three homo- and tern in other birds, which on A-C gels consistsof a three heterodimers).Unfortunately, despiteassay of single intense band, with occasional,much lighter more than I00 piciform specimens(Table I), we did surrounding bands observableupon heavy staining not detect any heterozygotes.This may not be sur- (Fig. 1). prising, however, because S-MDH is essentially In both the Downy Woodpecker(Picoides pubescens) monomorphic in most avian species (Aquadro and and Northern Flicker (Colapiesauratus), we assayed Avise 1982). 326 ShortCommunications [Auk, Vol. 104 T^BI•E1. Woodpeckersand possiblenonpasseriform allies assayedfor presencevs. absenceof the unique S-MDH isozymepattern. Unique "woodpecker" S-MDH Taxon n Continent of collection zymogram? Piciformes Picidae (woodpeckers) Colaptesauratus • 3 North America Yes Dryocopuspileatus 1 North America Yes Melanerpescarolinus 34 North America Yes Melanerpeserythrocephalus 7 North America Yes Melanerpesformicivorus 11 North America Yes Picoidespubescens 21 North America Yes Picoides scalaris 5 North America Yes Picoides villosus 5 North America Yes Sphyrapicusvarius 2 North America Yes Melanerpescruentatus 1 South America Yes Piculus rivolii 1 South America Yes Veniliornisnigriceps 1 South America Yes Veniliornispasserinus 1 South America Yes Campetheraabingoni 1 Africa Yes Dendropicosfuscescens 1 Africa Yes Indicatoridae(honeyguides) Indicator minor 2 Africa Yes Capitonidae (barbers) Lybiustorquatus b 1 Africa Yes Trachyphonusvaillantii 3 Africa Yes Tricholaema leucomelas 1 Africa Yes Rhamphastidae(toucans) Andigenacucullata 1 South America Yes
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