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The Drosophila Serido Speciation Puzzle: Putting New Pieces Together

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The Drosophila Serido Speciation Puzzle: Putting New Pieces Together Genetica 108: 217–227, 2000. 217 © 2000 Kluwer Academic Publishers. Printed in the Netherlands. The Drosophila serido speciation puzzle: putting new pieces together Alfredo Ruiz1, Alessandra M. Cansian2, Gustavo C. S. Kuhn2, Maurilio A. R. Alves2 &Fabio M. Sene3 1Departament de Genètica i de Microbiologia, Facultat de Ciències, Universitat Autònoma de Barcelona, 08193 Bellaterra (Barcelona), Spain (Phone: 93-581-2729; Fax: 93-581-2387; E-mail: [email protected]); 2Departamento de Biologia, Faculdade de Filosofia, Ciencias e Letras de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP, 14049-900 Brazil; 3Departamento de Genética, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP, 14049-900, Brazil Accepted 3 August 2000 Key words: cactophilic Drosophila, host plant specificity, inversions, karyotype, speciation Abstract The D. serido superspecies is a complex mosaic of populations distributed over a vast part of South America and showing various degrees of genetical divergence. We have analyzed its chromosomal constitution in 16 new localities of southeastern and southern Brazil. Both the metaphase and salivary gland chromosomes show a sharp split of these populations in two groups. Four populations, fixed for inversion 2e8 and showing the type I karyotype, represent the southwestern limit of D. serido type B, which inhabits the Cerrado in central-western Brazil. The remaining populations are homozygous for 2x7, an inversion also fixed in the Caatinga populations of northeastern Brazil. However, their karyotype, in those populations analyzed, belong to a different type (V) from that of the Caatinga populations. Populations in this second group are polymorphic for five inversions on chromosome 2 plus another on chromosome 5 and show considerable interpopulation differentiation. The breakpoints of chromosome 2 inversions are described and the inversion loops of several heterokaryotypes are presented. Biogeographical information suggests that there are clear ecological differences between the two groups of populations as well as among the populations within the second group. The possible role of host plants in promoting the genetic divergence among the D. serido populations is discussed. Introduction to occur in Oceanic Islands, e.g. the Hawaiian Ar- chipelago, scenarios prone to founder effects are also In the genus Drosophila, allopatric speciation is al- possible in continental settings (Giddings, Kaneshiro most certainly the rule, although there is evidence that & Anderson, 1989). sympatry may enhance premating isolation (Coyne & The second question concerns the role that natural Orr, 1997; Powell, 1997). Two unresolved questions selection plays in the speciation process. Under the related to allopatric divergence remain. One is the size founder effect model, genetic divergence is achieved of the divergent populations. In many cases, species at least in part without the concourse of, or even seem to arise by slow genetic divergence and sub- against the effect of, natural selection, which oth- sequent reproductive isolation of geographically sep- erwise plays the preeminent role under the adaptive arated and differentially adapted races and subspecies divergence model. In the latter case, however, the (Dobzhansky, 1970). By contrast, divergence may be simple acceptance of the operation of natural selection relatively faster when a new population is established leaves us with an incomplete account of the speci- by a few original founders carrying only a small frac- ation process. Identification of the selective agents tion of the genetic variation of the parental population involved is necessary, these selective agents may be (Mayr, 1963; Carson, 1975). While this is more likely abiotic factors (such as temperature, light or humidity) 218 or biotic factors (such as predators, competitors or observation, Ruiz and Wasserman (1993) proposed to parasites). Although we may ultimately conclude that include them tentatively within D. koepferae. Tidon- each speciation event is unique in this regard, we sug- Sklorz and Sene (1995a) placed them in a dendogram gest that some ecogeographical rules of speciation in closely related to D. koepferae. Populations of D. Drosophila will eventually emerge. serido from the Cerrado in central-western Brazil are In addition to the traditional advantages of Droso- homozygous for inversion 2e8 (Tosi & Sene, 1989), phila for genetical studies, cactophilic species of the an inversion which is also fixed in its close relative D. D. repleta group (Barker & Starmer, 1982; Barker, borborema (Wasserman & Richardson, 1987). Finally, Starmer & MacIntyre, 1990) are particularly suitable the populations inhabiting the rocky fields of the Ca- to the study of speciation. One of the more intricate deia do Espinhaço, States of Bahia and Minas Gerais, and intriguing situations is found in the neotropical are also fixed for 2e8 but show a consistent morpho- Drosophila serido superspecies which belong to the logical and genetic differentiation from the rest of D. buzzatii complex of the mulleri subgroup (Wasserman, serido populations and have been described as a separ- 1992; Ruiz & Wasserman, 1993). D. serido was de- ate species under the name D. seriema (Tidon-Sklorz scribed in 1977 from flies collected in Milagres, State & Sene, 1995b; Kuhn et al., 1996). In summary, the of Bahia (Brazil) (Vilela & Sene, 1977). At that time D. serido ‘superspecies’ is split at present into two its known geographical range was restricted to north- species, D. koepferae and D. seriema, plus a num- eastern and central Brazil. Subsequent work expanded ber of insufficiently known populations which are still its range, eastwards to the Bolivian Andes and south- designated with the specific name D. serido. wards to Argentina, and revealed a complex mosaic of We report here the chromosomal constitution of D. geographically dispersed populations with various de- serido populations from 16 new localities in southeast- grees of genetical divergence (Sene, Pereira & Vilela, ern and southern Brazil, a previously unstudied area. 1982, 1988; Ruiz, Fontdevila & Wasserman, 1982; We provide ecological information on this region in- Fontdevila et al., 1988). Up to six different meta- cluding the cactus species used as host plants by D. phase karyotypes (I–VI) were found (Baimai, Sene serido, describe three new polymorphic inversions and & Pereira, 1983) and up to five distinguisable ae- reinterpret some previous cytological results. Jointly, deagus types (A–E) were described (Silva & Sene, these genetical and ecological data considerably cla- 1991). These contrasting patterns of differentiation rify the biogeography of D. serido and shed light on made with various genetic markers made the polytypic the factors promoting genetic differentiation within D. serido a ‘speciation puzzle’. this polytypic taxon. Although not causally related with the origin of reproductive isolation (Zouros, 1982; Powell, 1997), chromosomal inversions usually provide considerable Materials and methods information on patterns of geographical differentiation and gene flow as well as the origin of particular Drosophila serido adults were obtained from 16 local- species (Carson, 1987; Ruiz, Heed & Wasserman, ities (Figure 1) in the States of Minas Gerais and São 1990). D. serido was found to be highly polymorphic Paulo in southeastern Brazil and the States of Parana, for inversions, chiefly on the second chromosome Santa Catarina and Rio Grande do Sul in southern (Ruiz, Fontdevila & Wasserman, 1982; Wasserman & Brazil. All localities belong to a general ecological Richardson, 1987; Tosi & Sene, 1989). From the dis- region classified as forest although clear ecological tribution of D. serido inversions, the following pattern differences among them do exist. In most cases, flies has emerged: populations from the Caatinga in north- were collected with banana-orange baits and a nylon eastern Brazil are fixed for inversion 2x7 (Wasserman net. Whenever possible, rotting cactus stems (rots) & Richardson, 1987; Tosi & Sene, 1989). Those from were located in the field, wrapped in newspaper, and northwestern Argentina and Bolivia are fixed for in- returned to the laboratory where they were placed in version 2j9 (Ruiz, Fontdevila & Wasserman, 1982; closed glass containers. Nearly 2000 flies emerged Tosi & Sene, 1989) and have been described as a from 39 rots in the first two weeks were collected with separate species under the name of D. koepferae (Font- an insect aspirator and classified to species (Table 1). devila et al., 1988). Likewise, the populations from the Most laboratory stocks were founded with single wild eastern Chaco in Argentina are presumably fixed for females but some were established using several fe- inversion 2j9 (Tosi & Sene, 1989), and based on this males. The specific identity of all D. serido stocks was 219 Figure 1. Geographical map of central-southern Brazil showing the position of the 16 localities where Drosophila serido was collected. Key (collection codes are given in parenthesis): 1. Peixoto, MG (H27); 2. Furnas, MG (H24/H26); 3. Morro do Forno, Altinópolis, SP (H6); 4. Analândia, SP (H32); 5. Sertãozinho, SP (H34); 6. Campinas, SP (H48); 7. Rio Ligeiro, PR (D92/D93); 8. Santiago, RS (H47); 9. Guaritas, RS (H44); 10. Osório, RS (H59); 11. Tramandaí, RS (H58); 12. Arroio Teixeira (H41/H61); 13. Capão da Canoa, RS (H42/H62); 14. Araranguá, SC (H63); 15. Florianópolis, SC (H64); 16. Guaratuba Beach, SP (H49). Major morphoclimatic
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