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Relationships Among the Australo-Papuan Parrots, Lorikeets, and Cockatoos (Aves: Psittaciformes): Protein Evidence ’

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Relationships Among the Australo-Papuan Parrots, Lorikeets, and Cockatoos (Aves: Psittaciformes): Protein Evidence ’ TheCondor 93:302-317 0 Thecooper ornitholcgical society 1991 RELATIONSHIPS AMONG THE AUSTRALO-PAPUAN PARROTS, LORIKEETS, AND COCKATOOS (AVES: PSITTACIFORMES): PROTEIN EVIDENCE ’ L. CHRISTIDIS Department of Ornithology,Division of Natural History, Museum of Victoria, Melbourne, Victoria, Australia 3000 R. SCHODDE Australian National Wildlif Collection,Division of Wildltfe and Ecology, CSIRO, Gunghalin, Canberra, Australia 2602 D. D. SHAWAND S. F. MAYNJB Molecular and Population GeneticsGroup, ResearchSchool of Biological Sciences, Australian National University,Canberra, ACT, Australia 2601 Abstract. Allozyme variation at 21 presumptive protein loci was examined by electro- phoresis and used to assessrelationships among Australo-Papuan parrots, lorikeets and cockatoos.Hypotheses of relationships were generated from the data by phenetic and cla- distic analyses.The results,when taken into account with other biochemical, chromosomal and morphological data, demonstrate that cockatoosform a monophyletic lineage distant from the other Australo-Papuan parrots and lorikeets. The lorikeets are also monophyletic, but are clusteredamong other parrots.A core ofAustralian broad-tailed (platycercine)parrots is defined by the rosellasand ringnecks(Platycercus, Barnardius), Bluebonnet (Northiella), Red-capped Parrot (Purpureicephalus),Swift Parrot (Lathamus) and grassparrots (Psepho- tus). New Guinean Psittacellaalso appearsto be a member of this assemblage,to which the polytelitine parrots (Alisterus-Polytelis)may be linked as well. Other “conventional” platy- cercine parrots- the Ground Parrot (Pezoporus),Budgerigar (Melopsittacus), Red-fronted Parakeet (Cyanoramphus), and Blue-winged and Bourke’s Parrots (Neophema)-are still more distant and of disparate affinity; the two latter speciesare polyphyletic among the platycercines.Of psittacineparrots, Pclectus (Eclectus) and Red-cheeked Parrots (Geofioyyus) are closely related but their links to other psittacine genera are not clear. Similarly, the relationships of the fig-parrots (Cyclopsitta),pygmy-parrots (Micropsitta), lovebirds (Aga- pornis) and ring-necked parakeets(Psittacula) are ambiguous.Biogeographical implications of these results are canvassedin the discussion. Key words: Parrots:protein electrophoresis;Psittacidae; systematics; Australo-Papuan. INTRODUCTION brush-tongued lorikeets, both of which are con- The order Psittaciformes comprises some 330- fined to the Australasian and South Pacific 350 species of parrots, lorikeets and cockatoos regions. The arine parrots, comprising the entire which occur naturally in Central and South New World complement, also appear to form a America, Australasia and the South Pacific, Af- monophyletic radiation, judged by their wide rica and southern Asia. There are two major ra- biochemical distance from other parrots (Mai- diations, one in Australasia and the other in South nardi 1962, Gysels 1964) and their severalunique America. Although the order is well-defined pigmentary, ontogenetic and copulatory traits morphologically, the primary evolutionary lin- (Smith 1975). eageswithin it are not so clear-cut (cf. Glenny Most controversy centers on the only other 1957, Sibley 1960, Brereton 1963, Boetticher large group, the Australasian seed-eating psitta- 1964, Sibley and Ahlquist 1972, Smith 1975, tine parrots. Up to eight tribes and subfamilies Homberger 1980). Two discreteassemblages have have been distinguished among them (Smith been recognized in all studies: the cockatoosand 1975, Homberger 1980) and there is consider- able dispute over their composition and rela- tionshipsto the cockatoosand lorikeets(see Smith I Received28 June 1990. Final acceptance6 No- 1975 and Table 1 this study). Towards resolving vember 1990. some of thesequestions, we employed multilocus [3021 BIOCHEMICAL SYSTEMATICS OF PARROTS 303 protein electrophoresisto examine relationships TABLE 1. Recent classifications of the genera ex- among 36 speciesof Psittaciformes, covering six amined in the present study. of the tribes recognized by Smith (1975). The survey is limited to the Australasian region, and Homberger1980 smith 1975 Peters1937 focussedon the principal loriine and psittacine Cacatuinaea Platycercinae Kakatoeinae assemblages. Cacatuini’ Psittacinae Platycercinae Psittacinae MATERIALS AND METHODS Platycercini Platycercini Protein electrophoresiswas performed on 80 in- Melopsittacus Melopsittacus Melopsittacus dividuals of 36 species(Table 2) representing 16 Neophema Neophema Neophema Psephotus Psephotus Psephotus of the 22 genera of Australo-Papuan psittacine Northiella Northiella Northiella parrots, seven of the 10 genera of lorikeets, and Purpurei- Purpurei- Purpureiceph- two of the five generaof cockatoos(Condon 1975, cephalus cephalus alus Beehler and Finch 1985), as well as one Pacific Platycercus Platycercus Platycercus species (Norfolk Island Red-fronted Parakeet, Barnardius Barnadius Barnard&s Lathamus Lathamus Cyanoramphus) and two Afro-Asian psittacine Cyanoramphus Cyanoramphus Cyanoramphus genera (Psittacula, Agapornis). Locality data for Pezoporus Pezoporus the material collected are available from the au- Psittacinae Loriinae Psittacinae thors on request. Psittaculini Psittaculini Electrophoresis was carried out on liver and Geoffroyus Geojiioyus Geofroyus breast muscle samples which had been stored in Eclectus Eclectus Eclectus Psittacella Psittacella liquid nitrogen. Separatehomogenates of the two Alisterus Alisterus Alisterus tissueswere prepared by grinding a cubic milli- Polytelis Polytelis Polytelis meter of each in 300 ~1 buffer (0.1 M Tris, 1.O Agapornis Agapornis Agapornis mM EDTA, 0.5 pi/ml 2-mercaptoethanol, 0.05 Psittacula Psittacula Psittacula mM NADP, pH 7.0). The homogenates were Loriinaeb Loriinae Loriinaeb Loriinib then spun in an Eppendorf centrifuge for 3 min incl. Lathamus and the supematant screenedfor 25 enzyme sys- Cyclopsitta tems representing 32 presumptive loci (Table 3). Not examined Loriinae not recognized Enzymes were stained according to the recipes Psittaculi- in Harris and Hopkinson (1976) except GOT rostrini (Table 3), for which the procedure of Shaw and Cyclopsitta Prasad(1970) was followed. All systemswere run Not examined Loriinae Micropsittinae in a cellulose acetate matrix on a paper support Micropsittini (Cellogel, Chemetron, Italy). Where two loci rep- Micropsitta Micropsitta resented a single enzyme, the most anodal was a Includesthe 2 8em-a listedunder Cacatuidae in Table 2. bIncludes the 7 generalisted under Lmiidae in Table 2. designated - 1, and the other - 2. Individual al- leles were given alphabetical designations in se- quence from the anode, beginning with “a.” distance-Wagner (Farris 1972, Swofford 198 1) Of the 32 loci screened,the following 10 were dendrograms were then constructed with the excluded from analysis because they could not BIOSYS- 1 program (Swofford and Selander be scored consistently across all species: GPT, 1981). The distance-Wagner dendrogram was GLUD, TPI, ACON- 1, ACON-2, EST- 1, MDH- rooted by both mid-point and out-group pro- 2, GDA, NP, and PGM-2. Variation at LDH-1 cedures, the cockatoos being used as the out- and LDH-2 could not be distinguished unam- group for psittacine and loriine lineages because biguously because of differential expression of of the morphological (Smith 1975, Homberger the polymer bands. Accordingly, their variation 1980) biochemical (Adams et al. 1984, Ovenden was scored on pattern alone and treated as a et al. 1987) and chromosomal (Christidis et al., single locus. in press)evidence that they are a distinctive sister From allelic frequencies at the 2 1 loci remain- lineage of the other Psittaciformes. ing (Table 2) Rogers’ (1972) and Nei’s (1978) A cladistic analysis was also performed by genetic distances were calculated between taxa treating the loci as charactersand their constit- (Table 4). UPGMA (Sneath and Sokal1972) and uent alleles as character states. Where loci were BIOCHEMICAL SYSTEMATICS OF PARROTS 307 TABLE 3. Enzymes examined, buffers used, and tissue distribution of each enzyme. Enzyme RUMbIg Running (E.C. No.) Abbreviation No. of loci Tissue buffer time (hr)b Aconitase ACON 2 Liver, F 3 (4.2.1.3) muscle Adenylate kinase AK 1 Muscle A 3 (2.7.4.3) Aldolase ALD 1 Muscle D 3 (4.1.2.13) Creatine kinase CK 2 Muscle A 3 (2.7.3.2) Enolase ENOL 1 Liver A 3 (4.2.1.11) Esterasec EST 2 Muscle A 1.5 (3.1.1.1) Fumerase FUM 1 Liver F 2.5 (4.2.1.2) General protei& GP 1 Muscle A 3 Glucose-phosphateisomerase GPI 1 Liver E 3 (5.3.1.9) Glutamate dehydrogenase GLUD 1 Muscle A 3 (1.4.1.3) Glutamate oxaloacetatetransaminase GOT 2 Liver F 3 (2.6.1.1) Glutamate pyruvate transaminase GPT 1 Liver F 2.5 (2.6.1.2) Glyceraldehyde-3-phosphatedehydrogenase GA3PD 1 Liver D 3 (1.2.1.12) Glycerophosphatedehydrogenase GPD 1 Liver F 3 (1.1.1.8) Guanine deaminase GDA 1 Liver C 1 (3.5.4.3) Isocitrate dehydrogenase IDH 2 Liver F 3 (1.1.1.42) Lactate dehydrogenase LDH 2 Muscle A, D 3 (1.1.1.27) Malate dehydrogenase MDH 2 Muscle A 1.5 (1.1.37) Mannose phosphate isomerase MPl 1 Muscle C 1.5 (5.3.1.8) Phosphoglucomutase PGM 2 Liver A 3 (2.7.5.1) 6-Phosphogluconatedehydrogenase 6PGD 1 Liver C 2.5 (1.1.1.44) Phosphoglyceratekinase PGK 1 Liver A 3 (2.7.23) Purine nucleosidephosphorylase NP 1 Liver F 1.5 (2.4.2.1) Pyruvate kinase PK 1 Muscle B 2 (2.7.1.40) Triose-phoshpate isomerase TPI 1 Liver D 3 (5.3.1.1) a A = 50 mM TEM, B = 15 mM TEB,,C = 50 mM TEM + NADP, D = 50 mM TEM + NAD, E = 25 mM TEB, F = 0.1 M Tris-citrate. Recipes for 1 liter of above buffers. A: 6.06 g Tns, 1.86 g Na EDTA, 0.20 g anhydrous M pH to 7.8 with Maleic acid. B: 1.82 g Ttis, 1.86 g Na EDTA, 0.20 g anbydrous M&l, pH to 8.0 with boric acid. C: as for A but add 10 mg N p DP. D: as for A but add 10 mg NAD. E: 3.06 g Tris, 1.86 g Na EDTA, 0.20 g anhydrous MgCI, pH to 8.0 with boric acid. F: 12.11 g Tris, pH to 7.8 with citric acid. b At 7 mA per 12 cm gel (except B and E buffers; 5 mA). =By method A in Han-is & Hopkinson (1976) wth 4-methyl-umbelliferyl-acetate.
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