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The Evolutionary Genetics of the Estrildidae

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The Evolutionary Genetics of the Estrildidae 山階鳥研報 (J. Yamashina Inst. Ornith.),17:143-158,1985 The Evolutionary Genetics of the Estrildidae Ryozo Kakizawa* and Masayoshi Watada* Abstract By means of protein electrophoresis of 26 loci, genetic variation and differen- tiation of 42 species belonging to 17 genera in the Estrildidae were analysed . A genealogic dendrogram was constructed by the UPGMA method, using the values of the genetic distances between the species of the Estrildidae. Intra-specific genetic variation was detected in 26 out of 42 species examined. The average observed heterozygosity of all the species examined was as low as 0.098. The values of genetic differentiation calculated as genetic distance averaged 0.193 at the species level and 0.397 at the generic levels, which were somewhat higher average values than normal amongs birds. The Estrildidae could be divided into two main groups, the Estrildinae and the Lonchurinae. Unlike the current accepted classification, this method proved Amadina and Lonchura pectoralis to be an old separately differentiated group. The Estrildinae is comprised of three groups, the Estrildi, Erythruri, and Amadini, while the Lonchurinae consists of the Poephili, Lonchuri, and Heteromunii. The basic taxonomic arrangement of genera and species agreed with current classification. Within each group, the average inter-specific genetic distance was 0.304 among African Estrildi as against 0.153 for Australasian Lonchuri. This reflects the older specific differentiation of the former group relative to the latter. These results give support to the hypothetical African origin of the Estrildidae with later dispersal to Asia and Australasia. Introduction The waxbills were originally considered to be close relatives of the weaverbirds, and classified as a subfamily of the Ploceidae (Chapin 1917, Sushkin 1924, 1927). Although he also considered the waxbills to be a subfamily of the Ploceidae, Delacour (1943) emphasized a distant link between the Ploceinae and the Viduinae. Subsequently, the waxbills have been treated as a separate family (Beecher 1953, Wolters 1957). The recent taxonomic arrangement of these bird groups was established by Delacour (1943), who subdivided them into three tribes, the Estrildae or waxbills, chiefly distributed in Africa; the Erythrurae or grassfinches, occurring mainly in Australia, and the Amadinae or mannikins, occurring predominantly in south Asia. This basic arrangement was followed by Mayr et al. (1968), who recognized the Estrildae, the Poephilae, and the Lonchurae. The number of species, considered as comprising the Estrildae has remained rather stable (between 127 and 132), however the number of genera, largely differs largely from authors, 15 (Delacour 1943), 27 (Mayr et al. 1968, Goodwin 1982) to 48 (Wolters 1975-82). The taxonomy of this group of birds cannot be discussed without reference to their avicultual history. Although avian taxonomy has developed based chiefly on morphologi- cal and zoogeographic data, the classification of the Estrildidae relies much on additional knowledge obtained from caged birds. These have been for example behavioral obser- Received 9 September 1985 * Yamashina Institute for Ornithology , Konoyama, Abiko, Chiba Prefecture, 270-11, Japan. 143 144 R. Kakizawa & M. Watada vations (Morris 1954, 1958, Moyniha & Hall 1954, Goodwin 1960, 1964, Ziswiler 1965, Immelmann & Immelmann 1967), studies of the mouth markings of chicks (Mitchell 1958, Steiner 1960, Nicolai 1964, 1969, Kunkel & Kunkel 1975, Immelmann & Sossinka 1977), and research on vocalization (Hall 1962, Harrison 1962, Zann 1975). In this study, tissue and blood samples from 188 individuals of 42 species belonging to 17 genera of the Estrildidae were used for electrophoretic analysis of 26 loci in order to study genetic variation and differentiation. A genealogic dendrogram was constructed to discuss their genetic relationships and evolution. Materials and Methods Specimens of 42 species of the Estrildidae were obtained from Asada bird shop, Tokyo between May 1983 and January 1984 (see Table 1). Blood samples were treated as described by Kuroda et al. (1982) and stored at -80℃ until electrophoresis. Liver and muscles dissected from birds were homogenized and centrifuged at 17000 × g for 20 minutes at 2℃. After centrifugation the supernatant was subdivided and stored in capillary glass tubes at -80℃ until electrophoresis. Erythrocytes were used for detecting Esterase D (EsD), glucose phosphate isomerase (GPI) and hemoglobin (Hb). Blood plasma was used only for the detection of albumin (Ab). Livers were used for the detection of 12 enzymes (proteins): diaphorase (DIA), glucose oxzaloacetate transisomerase (GOT), isocitric dehydrogenase (IDH), lactate dehydrogenase (LDH), malate dehydrogenase (MDH), peptidase (PEP), 6-phosphate dehydrogenase (6PGD), phosphogluco-mutase (PGM), general protein (PT), sorbital dehydrogenase (SDH), superoxide dismutase (SOD) and xylulose reductase (XR). Mus- cle samples were used for the detection of three enzymes, glutamate dehydrogenase (GDH), α-glycerophosphate dehydrogenase (α-GPDH), and lactate dehydrogenase (LDH), and muscle specific proteins. Horizontal electrophoresis was made following Kuroda et al. (1982). Three buffer systems were used for electrophoresis. They were Amine-citrate (Kuroda et al. 1982). Tris-citrate and Poulik (Selander et al. 1971). Staining for the enzyme detection were made as described by Shaw and Prasad (1970), Selander et al. (1971), Kaplan and Beutler (1967), Hopkinson et al. (1973) and Bell et al. (1982). The nomenclatures of the loci and analyses of the data were the same as those described by Numachi et al. (1983). Results (1) Genetic variation Alleles detected at each loci, and their frequency of occurrence are shown in Table 1. The number of individuals used for each species ranged from one to ten, with genetic variation found in 26 species and one subspecies, or about half of the species examined. The species with the highest genetic variation were Amandava formosa, Ortygospiza atricollis, Poephila acuticauda, and Lonchura cuculata, all of which showed variation at five loci. The loci which showed the greatest variation within a species were; 6PGD (variation found in 16 species), ES-D (10 species and two subspecies) and PGM-2 (10 The Evolutionary Genetics of the Estrildidae 145 species and two subspecies). The proportion of polymorphic loci of the Estrildidae ranged from 0 to 0.192 and the overall mean of all species was 0.061 which slightly low for the Passeriformes. There was no difference between observed (av. 0.017) and expected (av. 0.017) values of avarage heterozygosities, and these values were also low compared with the avian mean (see Table 2). Of the 26 loci tested, intra- and inter-specific variations were not found at six loci (GOT-2, MDH-1, MDH-2, PT-1, PT-4, and SOD-2), while intra-specific variation was detected at 20 loci. The highest numbers of alleles eleven were found at both 6PGD and SDH (Table 1). Almost all species were fixed at single allele at the following 11 loci; DIA, GDH, GPI, HB, IDH-2, LDH-2, PEP, PGM-1, PT-2, and PT-3. Mayr et al's (1968) grouping of three tribes was fairy well supported by 10 loci: DIA, ESD, ƒ¿-GPD, LDH-1, PGM-2, SDH, and SOD-1. At three loci, GOT-1, IDH-1, and 6PGD, no particular tendency was found. (2) Genetic differentiation Genetic identity (I) and distance (D=-lnI) were calculated from the data given in Table 1 according to Nei's (1972) formula. The results obtained from the analyses of 26 loci showed that Lonchura malacca atricapilla and L. maja had entirely the same genetic structure; the shortest genetic distances were shown between Pytilia phoenicoptera and P. hypogrammica (0.001), Lonchura bicolor and L. fringilloides (0.002), and Lonchura striata and L. punctulata (0.003), reflecting their extremely low genetic differentiation. Of particular interest is the fact that although Lonchura m. malabarica and L. m. cantans, are typically classified as subspecies (Delacour 1943, Mayr et al. 1968), they showed a mutual genetic distance of 0.063, which corresponds to species levels of genetic differentiation. The highest value, of genetic distance, (0.688), within the Estrildidae was found between Emblema guttata and Amadina fasciata. At the species level, the mean genetic distance was 0.193, which was slightly higher than the avian mean (Avise et al. 1982). The mean genetic distance between genera within the Estrildidae was found to be 0.397. (3) Genetic relationships within the Estrildidae By means of the UPGMA procedure, a genealogic dendrogram (Fig. 1) was constructed, based on values for inter-specific distances within of the Estrildidae. This dendrogram reveals that the family is divided into two distinct groups, separated by a genetic distance of 0.441. One group fits well with the currently recognized waxbills (Estrildinae), and the other comprises the so-called mannikins (Lonchurae), and grass finches (Poephilae). Here, we recognize two subfamilies, Estrildinae and Lonchurinae. Our Estrildinae consists of three groups which includes, first Cut-throat and Red Headed Finch, second waxbills (current Estrildidae with many waxbill genera) and third-parrot finches (including Erythrura and Chloebia). The Lonchurinae also has three groups which are first-Heteromunia pectoralis, second-grass finches (Poephilae of Mayr et al. 1968 and Aidemosyne modesta) and third-mannikins (Lonchura and Padda). In the present classification, Erythrura, Chloebia and Amadina which belonged to Lonchurae in Mayr et
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