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Enzymatic and Quantitative Variation in European and African Populations of Drosophila Simulans

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Enzymatic and Quantitative Variation in European and African Populations of Drosophila Simulans Heredity 54 (1985) 209-217 The Genetical Society of Great Britain Received 3 September 1984 Enzymatic and quantitative variation in European and African populations of Drosophila simulans P. Hyytia, Laboratoire de Biologie et Génétique Evolutives CNRS, 91 190 Gif sur Yvette, France; P. Capy, * Departmentof Biology, McMaster University, J. R. David and Hamilton, Ontario Canada L8S 4K1. *R. S. Singh Allozyme polymorphism at 15 loci of D. simulans was studied in 7 natural populations from Europe, North and tropical Africa. Morphological traits were studied in nine European and eleven Afrotropical strains. Within a population, the biochemical polymorphisms of Drosophila simulans and its sibling Drosophila melanogaster are not very different, although D. simulans has a lower heterozygosity. Between-populations genetic differentiation is however much lower in D. simulans than in D. melanogaster. Several loci of D. simulans do exhibit latitudinal trends but these are relatively weak. For morphological traits, both species show an increase of size with latitude, but geographic variation is again less pronounced in D. simulans. Both species are native to tropical Africa and have colonised the rest of the world. During this process, D. simulans has undergone much less geographic differentiation than has D. melanogaster, so that the ecological success of the two species is not correlated with similarities in their genetic properties. INTflODUCTION 1978; Stalker, 1980; Knibb et a!., 1981), allozyme variation (Kojima eta!., 1970; Band, 1975; Mettler Amongabout 2500 species known in the et a!., 1977 Triantaphyllidis et a!., 1980; 1982; drosophilid family (Wheeler, 1981), only 21 have Oakeshott et a!., 1981a, b; David, 1982; Singh et a subcosmopolitan status, in that they exist in at a!., 1982; Capy et a!., 1983; Anderson and Oake- least three non-adjacent biogeographic realms shott, 1984),.biometrical traits (Teissier, 1956; Tan- (David and Tsacas, 1981). All these species occupy tawy and Mallah, 1960; David et a!., 1976; 1977; their present geographic range as a result of Capy et a!., 1983) and physiological traits (David involuntary transport by man. Among the 21 and Bocquet, 1975; Allemand and David, 1976; species, the sibling D. melanogaster and D. David et a!., 1977; Cohet et a!., 1980; Parsons, simulans are especially interesting since they are l980b, C;Bouletreau-Merleet a!., 1982). Several the only two which possess large populations in authors argue that this extensive genetic differenti- both tropical and temperate conditions (David and ation is one cause of the demographic success of Tsacas, 1981). Many studies of the ecology, D. melanogaster under a variety of ecological con- ecophysiology and genetics of these domestic ditions. species have attempted to understand their popula- D. simulans is closely related -toD. tion dynamics, ecology and other reasons of which melanogaster and shows comparable ecological may underlie their demographic success (e.g., Par- success. We might hence expect a comparable sons, 1975; l980a; 1983; Parsons and Stanley, genetic differentiation among its populations. 1981). However, although D. simulans is far less studied Populations of D. melanogaster, are genetically it already appears that, for a variety of traits, it is highly differentiated, for chromosomal poly- less variable than D. melanogaster. For example, morphism (Ashburner and Lemeunier, 1976; natural populations are monomorphic for their Watanabe and Watanabe, 1977; Voelker et a!., chromosome structures (Ashburner and 210 P. HYYTIA, P. CAPY, J. R. DAVID AND R. S. SINGH Lemeunier, 1976); the species does not exhibit a systems in eich species. Moreover, we have also latitudinal dine for ethanol tolerance (David and indicated when alleles with identical mobilities Bocquet, 1975); its protein polymorphism, studied were observed in the two species. with 2-dimensional electrophoresis, is lower than Biometrical analysis was performed on 9 in D. melanogaster (Onishi et a!., 1982). Surpris- French and 11 Afrotropical strains. Each strain ingly few studies have been devoted to allozyme was founded by several (in most cases more than polymorphism in D. simulans (O'Brien and 10) females and kept in the laboratory as a mass Maclntyre, 1969; Berger, 1970; Triantaphyllidis, culture in bottles. Larvae were grown at 25°C at 1973; Steiner et a!., 1976; Triantaphyllidis et a!., low density on a killed yeast medium and for each 1980;Salam eta!., 1981; 1982; Cabrera eta!., 1982; strain, six different traits were measured on 30 Onishi eta!., 1982; Anderson and Oakeshott, 1984) different adults. These traits were fresh adult and most of these concern temperate popula- weight (taken a few hours after emergence), wing tions. and thorax lengths, sternopleural and abdominal D. melanogaster and D. simu!ans are now chaetae numbers and ovariole number in females known to be native to tropical Africa (Tsacas and (see David, 1979 for more details). Viability and Lachaise, 1974; David and Tsacas, 1981) and in duration of development were also measured for D. melanogaster, there is extensive genetic diver- each strain, starting from a sample of 300 eggs (see gence between the ancestral, Afrotropical popula- David et a!., 1976, for techniques). tions and the European ones. Here we compare the allozyme polymorphism of seven natural popu- lations of D. simulans from Europe, North and RESULTS tropical Africa (mainland and islands). Differences in metric characters are often easier to detect than Al/ozyme frequencies are differences in gene frequencies (e.g., Lewontin, Five of the 15 loci studied: ADH (alcohol dehy- 1984) and are generally thought to be more directly drogenase), FU (fumarase), HK-3 (hexokinase 3), subject to natural selection than are allozymes ME (malic enzyme) and 6-PGD (6 phosphoglu- (Kimura, 1983). Our analysis has hence been conate dehydrogenase) were monomorphic in all extended to include morphological comparisons populations. between French and Afrotropical populations of The most polymorphic loci (table 1) as shown D. simulans and D. me!anogaster. by average expected heterozygosities (table 2) are EST-C (esterase-C), EST-6 (esterase 6), ACPH (acidphosphatase), PGM (phospho-gluco- MATERIALSAND METHODS mutase), XDH (xanthinedehydrogenase), ALDOX (aldehydeoxidase) and HK-l Wildliving females were used to initiate isofemale (hexokinase 1). These results generally confirm lines. Two adult flies were electrophoresed from what was already found by previous authors with each line after a few generations (from I to 10) of the exception of HK- I (Kojima ci a!., 1970; Onishi laboratory culture. The populations sampled were cia!.,1982 and Cabrera ci a!., 1982) which was from Villeurbanne, France (20 lines), Antibes, previously found to be polymorphic (2 alleles) only France (23 lines), Athens, Greece (25 lines), Nas- at low heterozygosity (0.019) in a single Spanish rallah, Tunisia (42 lines), Brazzaville, Congo (39 population. ADH is generally monomorphic in D. lines), Mahé, Seychelles islands (23 lines) and simu!ans and we failed to find any rare alleles, Tananarive, Madagascar (26 lines). although such alleles have been reported from Methods of starch gel electrophoresis were other parts of the world: such as Texas (Kojima adapted from Shaw and Prasad (1970) and Ayala eta!., 1970); Hawaii (Steiner et al., 1976) and Spain cia!.,(1972), and 15 different gene-enzyme loci (Cabrera et a! 1982). a-GPDH is monomorphic were studied in each population. Alleles were in most Drosophila species (Lakovaara and characterised by their migration distance on the Keranen, 1980), although rare alleles in D. gel, the most common one receiving the arbitrary simulans, are known from Texas (Kojima et a!., value of 1 00. Expected heterozygosity was calcu- 1970), Hawaii (Steiner et a!., 1976) and Greece lated (assuming Hardy—Weinberg equilibrium) for (Triantaphyllidis ci a!., 1980). each locus and populations. Few enzyme loci are Table 3 shows that, in most populations, about mapped in D. simu!ans, However, in all cases, an half of the 15 loci sampled were polymorphic with homology could be established with an already a mean of 2 alleles per locus and an average identified locus of D. melanogasier and we have heterozygosity of 16 per cent. Differences between used the same nomenclature for describing enzyme populations are generally small, although more GEOGRAPHIC VARIATION IN D. SIMULANS 211 Table 1Frequency of alleles in populations of Drosophila simulans. Alleles marked *exhibitthe same mobility as alleles found in D. melanogaster France Villeurb. Antib. GreeceTunisiaCongo Seychelles Madagascar Average Locus and Allele 457°N 436°N 38°N 35°6N 4°2S 38°S l87S ACPH: acid phosphatase 095 0300 0200 0250 0131 0087 0130 0039 0l50 100 0700 0800 0729 0851 0873 0870 0913 0829 106 . • 0021 0018 0040 • 0048 0021 Het. 0420 0320 0406 0258 0229 0226 0163 0288±0096 ALDOX: aldehyde oxidase l•00 0744 0767 0910 0792 0967 l•000 0962 0880 103 0256 0233 0090 0208 0033 • 0038 0l20 Het. 0381 0357 0164 0329 0064 0 0073 0195±0158 EST-C: Esterase C 087 . • 0010 0001 089 . .. • 0010 0001 093 0138 0267 02l7 0274 0058 0239 0049 0175 096 0338 0289 0l52 0360 0026 0l41 0l86 0207 100 0475 0256 0522 0183 0377 0500 0363 0364 102 0025 O'l67 0087 017l 0507 0109 0324 0226 104 0025 0022 0022 0012 0032 0011 0059 0026 Het. 0640 0751 0649 0732 0596 0661 0723 0679±0057 EST-6 esterase 6 087 . • 0182 0207 0060 093 • 0067 • • 0020 • 0020 0014 0.96* 0350 0244 0292 0429 0442 0329 0340 0362 1.00* 0650 0689 0667 0544 0357 0427 0530 0537 103 .. • 0042 0018 • 0037 0090 0024 104 . .. .. • 0020 0003 Het. 0455 0462 0468 0509 0644 0665 0595 0542±0090 a-GPDH: o-Glycerophos- phate deydrogenase 095 . 0 0 0013 . 0003 1.00* 1000 1000 1000 1000 0987 1000 1000 0997 Het. 0 0 0 0 0025 0 0 0004±0009 HK-l: hexokinase I 097 .. 0020 . 0036 0100 0173 0045 l.00* 0971 0964 0970 0963 0869 0837 0808 0915 103 0029 0036 0010 0037 0095 0063 0019 0040 Het.
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