The Journal of Heredity 2001:92(5)
© 2001 The American Genetic Association 92:382-391
Gametic Associations Between Inversion and Allozyme Polymorphisms in Drosophila buzzatii
From GIBE, Departamento de Ciencias Biológicas, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Universitaria Pab. II. (1428) Buenos Aires, Argentina.
Address correspondence to Esteban Hasson at the address above or e-mail: ehasson{at}bg.fcen.uba.ar.
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Abstract |
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Gametic disequilibria between second chromosome polymorphic arrangements and seven linked allozyme loci were estimated in seven populations of Drosophila buzzatii from Argentina. Significant and consistent associations across populations were detected for Est-1, Est-2, Aldox, and Xdh. Phenograms based on Nei's genetic distance showed that chromosomes carrying the 2ST arrangement were more similar to each other, irrespective of the population from which they were extracted, than to chromosomes carrying the derived 2J and 2JZ3.Restriction of recombination in heterokaryotypes seems to be the best explanation for the significant linkage disequilibria between inversions and the loci located inside the rearranged segments, for example, Est-1 and Aldox, or close to the break points, for example, Est-2. However, epistatic interactions between Xdh, which is outside the inversions and not near the break points, and loci tightly linked to the inversions, is the most likely explanation for the association between Xdh and chromosomal arrangements. Some of the associations detected in endemic Argentinean populations are coincident with data obtained in colonizing populations of the Old World and Australia. Thus historical processes that took place in the original area of the species' distribution can account for these linkage disequilibria in colonized populations of D. buzzatii.
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Introduction |
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The origin and maintenance of inversion polymorphisms in the genus Drosophila has captured the interest of evolutionary biologists (reviewed in Krimbas and Powell 1992; Powell 1997). According to the hypothesis that new arrangements arise from unique inversion events, that is, chromosomes sharing a certain arrangement have a monophyletic origin, a new inversion captures a particular combination of alleles of the loci located inside the inverted segment. After the origin of a new inversion, the genes within any copy of a specific arrangement should be identical, but this identity decays in subsequent generations due to genetic exchange with other arrangements by double crossovers, gene conversion, and new mutations. Thus nonrandom associations of alleles at different loci with the inversion can be considered as the signature of young inversions (Krimbas and Powell 1992; Powell 1997). However, the recovery of variability in the population of chromosomes carrying the new arrangement occurs at a very slow rate since recombination in heterokaryotypes is greatly reduced (Hedrick 1978). Further, the rate of decay of linkage disequilibrium can be even lower if natural selection favors certain combinations of alleles of the loci captured by the inversion (Powell 1997), while genetic drift can also generate nonrandom associations (Hedrick 2000).
Several investigations have provided evidence for the adaptive role of the inversion polymorphisms in the cactophilic Drosophila buzzatii. This has involved studies in experimental populations maintained on media prepared with tissues of different host plants (Ruiz and Fontdevila 1985; Fernandez Iriarte and Hasson 2000), observations of latitudinal clines (Hasson et al. 1995; Knibb et al. 1987; Rodríguez et al. 2000), and fitness components analysis in natural populations (Barbadilla et al. 1994; Fanara et al. 1996; Hasson et al. 1991; Rodríguez et al. 1999; Ruiz et al. 1986). The effects of inversions on fitness are thought to be caused by associations between arrangements and particular alleles that influence the traits (Powell 1997).
Similarly various studies have suggested the adaptive significance of variation at allozyme loci linked to second-chromosome inversions in D. buzzatii. For instance, allele frequency variation at the loci Est-1, Est-2, and Aldox in nature seems to constitute an adaptive response to temporal and spatial environmental changes (Barker and East 1980; Barker et al. 1986a; Mulley et al. 1979; Sokal et al. 1987), and thermal shocks (Watt 1981). Moreover, Est-2 was suggested to be involved in differential attraction to and oviposition preference for yeasts (Barker et al. 1981, 1986b) and cactus species (Fernandez Iriarte 1999). However, Est-1, Est-2, and Aldox have been shown to be in strong gametic disequilibrium with inversions in natural populations of Australia (Knibb et al. 1987) and Spain (Betrán et al. 1995; Quezada-Díaz 1993), suggesting that the adaptive effects of inversions and linked allozyme loci may not be independent. On the one hand, allozyme loci could be the primary target of selection acting on the inversion polymorphism, or in other words, gene selection might be involved in the maintenance of the chromosomal polymorphism (Wasserman 1982). On the other hand, variation at allozyme loci could be the result of hitchhiking with the adaptive inversion polymorphism. In this case genetic variation is maintained through chromosomal selection and hitchhiking (Wasserman 1982).
However, since populations studied in previous surveys (Betrán et al. 1995; Knibb and Barker 1988) are the result of colonization events, several evolutionary factors such as historical processes and/or genetic drift due to founder events may also account for the associations, aside from the simplest explanation based on the reduction of recombination in heterokaryotypes due to the position of the studied loci within the inverted segments. Thus data of gametic associations in populations of the original area of distribution in the Argentinean Chaco are needed in order to test between these alternative hypotheses and to unveil the evolutionary history of the inversion polymorphism of D. buzzatii.
Samples of gametes or haplotypes are necessary if our purpose is the accurate estimation of linkage disequilibrium. However, sampling gametes from natural populations is a difficult task, and estimations of linkage disequilibrium may often be biased due to departures from Hardy-Weinberg expectations, since estimations are often obtained from genotypic data (Weir 1996). The genus Drosophila is exceptional in this sense, since the absence of recombination in males allows us to obtain flies homozygous for entire wild chromosomes, and thus haplotypic data including information for several linked loci associated with polymorphic arrangements (Dobzhansky et al. 1977).
The objective of this article is the investigation of gametic associations between allozyme loci and inversion arrangements on the second chromosome in populations from different phytogeographic regions of Argentina in order to compare the estimates of linkage disequilibrium with those reported in colonized populations of Australia (Knibb et al. 1987) and Spain (Betrán et al. 1995).
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Materials and Methods |
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Seven natural populations belonging to the Chaco Phytogeographic Dominion (Cabrera 1976) were sampled for the present study: Chumbicha, La Sébila, and Río Hondo in Western Chaco; Berna and Tirol in Eastern Chaco; and Otamendi and Arroyo Escobar in the Pampa (for a detailed description of the localities see Rodríguez et al. 2000). Samples of adult flies from Arroyo Escobar, Chumbicha, La Sébila, and Río Hondo were obtained in the autumn of 1995, those from Berna and Tirol in spring 1995, and Otamendi in spring 1996.
Flies were collected by net sweeping on fermenting banana baits. Males were individually crossed (Figure 1) with virgin females of a laboratory stock carrying balancer second chromosomes and the dominant mutations Antennapedia (Antp) and Delta 5 (
5) (for a description of the stocks see Barker 1994). After 48 h males were frozen at -70°C and vials with progeny were maintained until the emergence of adults. One Antennapedia male (heterozygous for a wild second chromosome) from each F1 progeny was backcrossed with virgin females of the laboratory balancer stock and frozen at -70°C 48 h later. The chromosomal arrangement transmitted by each wild male to their corresponding F1 sons was ascertained with a probability greater than 95% by means of the cytological analysis of five F2 third instar larvae.
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The genotypes at seven allozyme loci were obtained by means of the electrophoretic analysis of wild males (see below). The F1 males of each parental cross that fathered the F2 larvae used for the cytological analysis were also electrophoresed, allowing the detection of null alleles.
Salivary gland chromosome preparations were obtained following the methodology described in Fontdevila et al. (1981). Electrophoretic methods followed Barker et al. (1986a), Barker and Mulley (1976), and Sánchez (1986). The loci assayed were esterase-1 (Est-1), esterase-2 (Est-2), aldehyde oxidase (Aldox), xanthine dehydrogenase (Xdh), peptidase-1 (Pep-1), peptidase-2 (Pep-2), and leucine-amino peptidase (Lap). All loci are located on the second chromosome, Est-1 and Aldox inside the segment rearranged by inversions J and Z3, whereas Est-2 is just beyond the proximal breakpoint of inversion J but included in inversion Z3. In the standard arrangement (2ST), Aldox maps between Est-1 and Est-2 (Schafer et al. 1993). Pep-2 (Betrán et al. 1995), Lap (Schafer et al. 1993) and Xdh (Ranz et al. 1977) are outside the rearranged segments, whereas the position of Pep-1 with respect to the inversion system is unknown.
Gametic disequilibrium is defined as the difference between observed haplotype frequencies and those expected under random association between alleles at two loci. For two loci (A and B) with two alleles (u and v), gametic disequilibrium can be measured by means of the D coefficient (Lewontin and Kojima 1960) such that
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The null hypothesis (H0: Duv = 0), that is, alleles are not in gametic disequilibrium, can be tested using the expression
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However, D can have different ranges of variation for different pairs of loci and for the same pairs of loci in different populations. Thus in order to compare departures from linkage equilibrium between different loci and/or between different populations for the same pairs of loci, standardized coefficients are required.Lewontin (1974) defined the normalized coefficient:
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Since our experimental design allowed the estimation of allele frequencies for the seven loci within each of the arrangements segregating in the populations sampled, we estimated the degree of genetic similarity using Nei's coefficient of genetic distance (Nei 1978) between arrangements within populations.
Allele frequencies and coefficients of gametic disequilibrium were calculated using the program Arlequin (Excoffier et al. 1992). UPGMA phenograms based on Nei's genetic distances were obtained using the program GDA (Genetic Data Analysis) (Lewis and Zaykin 1998).
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Results |
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Five populations—Chumbicha, La Sebila, Río Hondo, Arroyo Escobar, and Otamendi—were polymorphic for arrangements 2ST, 2J, and 2JZ3, while in Berna and Tirol, only 2ST and 2J were present in polymorphic frequencies (Table 1). Allele frequencies of all electrophoretic loci in the seven populations studied are given in Table 2, along with conditional allele frequencies, that is, allozyme frequencies within each inversion arrangement in each population.
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Coefficients of linkage disequilibrium (D' and D) between allozyme loci and chromosomal arrangements estimated in each population are presented in Table 3. We detected significant associations between Est-1, Est-2, Aldox, Xdh, and inversion arrangements (Table 3). Further, some alleles of these loci not only showed cases of individually significant linkage disequilibria with chromosomal arrangements, but also, when not significant, the direction was the same for each population, with the exception of Est-2. For example, taking into account the most common alleles of these loci, Est-1a, Aldoxb, and Xdhc tended to be more associated with 2ST, whereas Est-1b, Aldoxa, and Xdhb were predominantly in 2J. Examination of conditional allele frequencies of these loci within each of the second chromosome arrangements illustrate the nature of the disequilibria (Table 2). In addition, a small number of D and D' values between the other loci assayed, Pep-1, Lap, and Pep-2, and inversions were significant in some of the populations but did not show any consistent trend (data not shown).
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Strong and significant associations between four of the loci assayed and inversions were also detected in the global sample (Est-1: XT2 = 46.46, df = 4, P = .000; Est-2: XT2 = 69.0, df = 8, P = .000; Aldox: XT2 = 25.1, df = 6, P = .000; and Xdh: XT2 = 32.65, df = 6, P = .000). Furthermore, associations that were significant in individual populations and consistent across populations are reflected in D and D' values estimated in the global sample (Table 4). Likewise, it is important to note that the pattern of gametic disequilibria between loci tightly linked to inversions, Est-1 and Aldox and surprisingly Xdh showed overall concordant trends in the derived arrangements 2J and 2JZ3 that were opposite to those observed in 2ST. We indirectly tested these trends by means of an F-statistics analysis and observed that differentiation among populations within arrangements was only significant for Est-2 (FST = 0.146, P < .05 statistical significance determined according to jackknife estimates of the 95% confidence interval) but not for the other loci.
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The observation of significant and consistent associations in the different populations and in the complete dataset suggests that the genetic content of chromosomes with a given gene order tended to be more similar to each other than to other arrangements, irrespective of the population. This pattern of similarity can be described as follows: average genetic distance between chromosomes carrying the same arrangement and sampled from different localities was smaller, ranging from 0.02 for 2JZ3 to 0.04 for 2ST, than between arrangements, with the exception of the comparison 2J versus 2JZ3 that were more similar to each other than to 2ST (Table 5). This pattern was more evident when genetic distances were calculated using the loci located inside the rearranged segments, namely Est-1 and Aldox. Chromosomes carrying the most recently derived arrangement, 2JZ3 showed the lowest intra-arrangement average genetic distance (Table 5 and Figure 2). Two main clusters can be observed in the tree constructed with the complete dataset, one including mostly 2ST chromosomes, and the other 2J and 2JZ3 (Figure 2a). In addition, all chromosomes sampled in the population of Arroyo Escobar diverged from the rest at higher genetic distances independent of the arrangement considered (Figure 2a). Similarly the phenogram based on Est-1 and Aldox showed two more clearly defined clusters, one including 2ST chromosomes and the other derived arrangements. Again Arroyo Escobar chromosomes (2STAE, 2JAE, and 2JZ3AE) clustered according to the arrangement and were the more divergent within their corresponding group (Figure 2b).
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Discussion |
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Comparisons of allele frequencies at seven allozyme loci among inversion arrangements showed that second chromosomes carrying the same gene order tended to be genetically more similar than chromosomes with different arrangements, irrespective of the population from which chromosomes were sampled. Furthermore, the lowest genetic similarity was observed between the ancestral 2ST and the derived arrangements 2J and 2JZ3. This pattern of similarities is concordant with the chromosomal phylogeny of D. buzzatii (Ruiz and Wasserman 1993), despite the remarkable genetic differentiation among the populations studied (Rodríguez et al. 2000). Thus our present results allow us to accept the monophyletic origin of the inversions, assuming that the very few exceptions detected in the phenograms can be attributed to recombination between arrangements (see below).
The restriction of recombination in inversion heterozygotes is probably the best explanation for the genetic differentiation between ancestral and derived arrangements. Thus the persistence of gametic disequilibria between inversions and loci tightly linked to the rearranged segments, namely Est-1, Aldox, and Est-2, might be indicating that the inversion polymorphism is relatively young. However, a recent report of levels of nucleotide variation in regions spanning the break points of inversion 2J showed the presence of 22 fixed differences in 2J when compared to 2ST (Cáceres et al. 1999), suggesting that the inversion polymorphism might be relatively old.
It may be argued that the significant associations detected in the global sample might be a multilocus equivalent of the Walhund effect due to the pooling of genetically differentiated populations for both inversion and allozyme polymorphisms (Rodríguez et al. 2000), since the rate of decay of disequilibrium in subdivided populations is retarded due to a deficiency of double heterozygotes (Hedrick 2000, p. 412). However, the patterns of clustering observed in the phenograms suggest that allozyme frequencies are quite homogeneous within each chromosomal class (Figure 2 and Table 2). Furthermore, differentiation among populations within arrangements was not significant for most loci, indicating that the direction of disequilibrium between allozyme loci and inversions was consistent across populations (Tables 2 and 3). On the contrary, the situation depicted by Est-2 is coincident with reports in Australian populations where the direction of linkage disequilibrium with inversions varied across collections (Knibb et al. 1987).
Thus other evolutionary processes such as natural selection may have played a role in the maintenance of the associations. In this sense, Ohta (1982) has developed a method aimed at elucidating the mechanisms responsible for linkage disequilibrium in subdivided populations with finite population size by means of the partition of total variance of disequilibrium. Under the null hypothesis, that is, when linkage disequilibrium is a consequence of genetic drift and limited migration between subpopulations, the expected variance of disequilibrium within subpopulations (DIS2) is expected to be smaller than the variance in the expected frequencies of gametic types (DST2). On the contrary, DIS2 is expected to be larger than DST2 when epistatic selection is responsible for the disequilibrium. According to these conditions the null hypothesis cannot be rejected in the present case (data not shown).
Population bottlenecks followed by an explosive expansion can also account for the gametic associations. Moreover, supporting evidence favoring this interpretation comes from a recent survey of mitochondrial DNA sequence variation, showing a very low degree of genetic differentiation among D. buzzatii populations from Argentina, probably associated with changes in the distribution of arid zones due to cycles of glaciation during the late Pleistocene, 13,000–18,000 years ago (Rossi et al. 1996). When this information is compared with estimates of genetic differentiation using other markers such as inversion polymorphism (Hasson et al. 1995) and allozymes (Rodríguez et al. 2000) the picture is clear: inversions respond adaptively to macroenvironmental variation (Hasson et al. 1995; Rodríguez et al. 2000), while allozymes seem to be influenced by historical events and more subtle environmental factors (Fernandez Iriarte 1999; Rossi et al. 1996).
In this sense, the patterns of variation observed at a macrogeographic scale for certain loci such as Est-1 and Aldox can be easily explained by hitchhiking with the inversion polymorphism, rather than by natural selection acting directly on the allozyme loci or tightly linked gene regions. However, clines for Est-2 and Xdh, also in linkage disequilibrium with inversions, are probably due to direct selection acting on these loci or on tightly linked gene regions (Rodríguez et al. 2000).
Linkage disequilibria between Est-1, Est-2, and Aldox and inversions can be at least partially explained because of their linkage with the segments rearranged by inversions. However, this is not the case for Xdh, since this locus is neither inside the inverted segment nor even close to the distal break point of inversions J and Z3. Indeed, conditional Xdh allele frequencies (Table 2) showed coincident trends (Xdhc is relatively more frequent in 2ST and Xdhb in 2J) in most populations, except Otamendi. However, if we remove Otamendi from the dataset, D values and their significance did not change substantially (data not shown). Thus we suggest that epistatic interactions of Xdh with loci located inside the rearranged chromosomal segments might be a plausible alternative explanation (Rodríguez et al. 2000). Of interest, O'Brien and MacIntyre (1978) have reported in D. melanogaster that Xdh mutants affect pleiotropically the expression of Aldox, which in D. buzzatii is located inside the inverted chromosomal segments. The expected consequence of such interaction would be the association between Xdh and Aldox. Although the latter was not significant in the present study (data not shown), unequal systematic disequilibrium (Black and Krafsur 1985) between these loci was observed in a recent survey of microgeographic population structure (Fernandez Iriarte 1999), suggesting that linkage disequilibrium might be, in this case, a response to microenvironmental variables.
Knibb et al. (1987) and Betrán et al. (1995) claimed that gametic disequilibria between inversion arrangements and linked allozyme loci detected in Old World and Australian populations of D. buzzatii may be the consequence of founder events during colonization. However, as the authors acknowledged, the absence of data from the area of origin did not allow the evaluation of this hypothesis. Our present data show that the associations between alleles Est-2a and Aldoxb with 2ST observed in two Spanish populations (Betrán et al. 1995) and the associations between Est-1a and 2ST, and Est-1b and 2J in Australia are also present in original populations, suggesting that the species' history in South America can account for gametic disequilibria detected in recently derived populations. However, it should be emphasized that the loci analyzed in Australian and Old World populations are not totally coincident, and that data of associations between inversions and some of the loci included in the present survey are reported in this article for the first time. Thus the evaluation of the relative role of founder events in both colonizations must await more complete datasets in colonizing populations.
Finally, questions about the antiquity of the inversion polymorphism, the date of possible population bottlenecks and range expansions, and their impact on genetic variation cannot be answered with the present type of data. More information on nucleotide variation at loci tightly linked to inversions is necessary to respond to these open questions as well as to confirm the monophyletic origin of inversions.
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Acknowledgments |
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We would like to thank Antonio Fontdevila for sharing flies collected in two of the populations reported in this article and Pedro Fernandez Iriarte for help during some of the collections. We want to express our appreciation to J. Stuart F. Barker who kindly sent us the strains Antp and
5 to construct the balancer stock and for suggestions on earlier versions of the manuscript. We wish to thank two anonymous reviewers for their suggestions. Roberto Kissling is greatly acknowledged for the identification of cactus species. This work was supported by Universidad de Buenos Aires and CONICET grants (to E.H.). R. Piccinali is a fellow of CONICET and E. Hasson is a member of Carrera del Investigador Científico (CONICET). |
Footnotes |
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Corresponding Editor: Ross MacIntyre
Received January 14, 2000
Accepted April 30, 2001
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References |
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