Journal of Heredity 2004:95(4):284-290
© 2004 The American Genetic Association
Accumulation of Transposable Elements in the Genome of Drosophila melanogaster is Associated with a Decrease in Fitness
From the Institute of Molecular Genetics of the Russian Academy of Sciences, Moscow 123182, Russia (Pasyukova and Morozova); Section of Evolution and Ecology, University of California at Davis, Davis, CA 95616 (Nuzhdin); and Department of Genetics, North Carolina State University, Raleigh, NC 27695 (Mackay).
Address correspondence to E. G. Pasyukova at the address above, or e-mail: egpas{at}img.ras.ru.
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Replicates of the two isogenic laboratory strains of Drosophila melanogaster, 2b and Harwich, contain different average transposable element (TE) copy numbers in the same genetic background. These lines were used to analyze the correlation between TE copy number and fitness. Assuming a weak deleterious effect of each TE insertion, a decrease in fitness is expected with an increase in genomic TE copy number. Higher rates of ectopic exchanges and, consequently, chromosomal rearrangements resulting in early embryonic death are also predicted from an increase in TE copy number. Therefore egg hatchability is expected to decrease as the genomic TE copy number increases. In 2b, where replicate lines have diverged up by 90 TE copies per haploid genome, a negative correlation between the number of TE insertions and both fitness and egg hatchability were found. Neither correlation was significant for the Harwich replicates, which have only diverged by 30 TE copies. The average deleterious effect of a TE insertion on fitness and its components was estimated as 0.004. Both homozygous and heterozygous TE insertions were shown to have deleterious effects on fitness and its components.
Experimental and theoretical studies of transposable elements (TEs) in Drosophila led to the hypothesis that TEs are maintained as a result of the balance between the process of TE transposition and natural selection against their deleterious effects (Charlesworth and Charlesworth 1983; Kaplan and Brookfield 1983). The similarity of copy numbers of TEs belonging to the same family in different Drosophila lines, populations, and related species (Belyaeva et al. 1984; Nuzhdin 1995; Vieira and Biemont 1996) confirms an equilibrium between the forces operating on TE copy number.
Three main sources of deleterious effects of TEs on fitness have been postulated: insertional mutations with weak effects (Charlesworth and Charlesworth 1983), chromosomal rearrangements generated by ectopic exchange (Charlesworth and Langley 1989; Langley et al. 1988), and damage from the transposition process itself (Brookfield 1991). None of these mechanisms are mutually exclusive. Indirect evidence from analysis of frequency spectra of insertion sites supports the action of weak natural selection on TEs (Biemont 1992; Charlesworth and Langley 1991). Direct estimations of TE effects on fitness in Drosophila have given somewhat contradictory results (Eanes et al. 1988; Mackay et al. 1992; Lyman et al. 1996) and were limited to a single TE family of P elements as a source of deleterious mutations. The effects of all other TEs, including retrotransposons (except for the I element; Pignatelli and Mackay 1989), remained unknown. There is experimental evidence, mostly indirect, of ectopic exchange affecting the fitness of Drosophila (Charlesworth et al. 1994; Sniegowski and Charlesworth 1994). The conclusions with respect to the role of ectopic exchange in maintaining the TE copy number have ranged from barely significant (Biemont et al. 1997b) to very important (Lim and Simmons 1994). Direct damage from the transposition process have not been addressed experimentally. Finally, the comparative impact of different sources of deleterious effects of TE on fitness remains unclear (Biemont et al. 1997a; Charlesworth et al. 1997).
Therefore more direct data concerning TE effects on fitness are needed. Replicates of isogenic or highly inbred Drosophila lines, with different average TE copy numbers in the same genetic background, provide an ideal model system to assess the correlation between TE copy number and fitness. Assuming a weak deleterious effect of each TE insertion, a decrease in fitness is expected with an increase in TE copy number in the genome. Furthermore, a higher rate of ectopic exchange is predicted from an increase in TE copy number. As a result, chromosomal rearrangements would raise the rate of dominant lethal mutations, resulting in early embryonic death and a decrease in hatchability as TE copy number increases. Here we present data on TE copy numbers, fitness, and hatchability of replicates derived from two homozygous laboratory strains of Drosophila melanogaster—2b and Harwich.
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Drosophila Lines
Strain 2b is an isogenic wild-type laboratory line (Pasyukova and Nuzhdin 1993). It was synthesized in 1986 and divided into three independently maintained replicates (2b1, 2b2, 2b3) in 1988 (Figure 1). Replicates 2b1, 2b2, and 2b3 were further divided into a number of other replicates (Figure 1) which were then maintained independently as small mass cultures (about 20 pairs of flies per generation). Two substitution lines—2b3;2b2;2b2.I and 2b3;2b2;2b2.II—were also used, with the X and third chromosomes of the 2b2 replicate and the second chromosome of the 2b3 replicate (Figure 1). Twenty-four euchromatic copia sites (4EF, 18C, 33F, 34EF, 35C, 38A, 40A, 41A, 42A, 42B, 47B, 52D, 53E, 64E, 66C, 71C, 73C, 80A, 82C, 87F, 94E, 96B, 98B, 99B) and 27 euchromatic Doc sites (4B, 24D, 27AB, 33A, 33D, 35A, 36E, 37C, 37D, 38EF, 41AB, 41C, 41F, 42A, 44CD, 45A, 65A, 67B, 67E, 70A, 75C, 77E, 78E, 80A, 86A, 92F, 93F) have been fixed in the original 2b line, and these were still fixed in all the replicates after 10 years of maintenance (Pasyukova et al. 1998). The presence of all the fixed sites was checked in all the individuals analyzed by in situ hybridization throughout the experiments (see below) and was used as a control against contamination. However, in addition to the fixed sites, new polymorphic copia and Doc sites were found in some replicates. These polymorphic sites appeared to be due to transposition and accumulated during the maintenance of replicates. Transposition rates of copia and Doc are elevated up to 1 x 10–2 transpositions per copy per generation in some 2b replicates (Pasyukova et al. 1997, 1998), whereas transpositions of other TEs, including mdg1, mdg2, mdg3, mdg4, 297, H.M.S.Beagle, roo, jockey, I element, and FB4, were not found (Pasyukova and Nuzhdin 1993). All the replicates of 2b lack P elements.
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Harwich is a highly inbred wild-type strain of P cytotype (Mackay et al. 1992). In 1987 it was divided into about 30 replicates, which were further maintained as small mass cultures (about 20 pairs of flies per generation) for more than 300 generations. Thirty euchromatic copia sites (4F, 7D, 9A, 9E, 11B, 22A, 29F, 30B, 32A, 34A, 40A, 41A, 45D, 47C, 48E, 55F, 65E, 66E, 68C, 70C, 70E, 75C, 78E, 80A, 83D (2), 84E, 90B, 92B, 97D) and 66 euchromatic roo sites (1F, 2D, 3A, 3C, 3D, 4E, 6A, 6B, 6E, 8C, 8D, 9B, 10B, 10D, 12E, 15D, 16F, 18B, 19A, 19E, 20A, 22B, 22E, 24E, 25A, 26A, 26C, 28A, 33A, 33B, 34B, 34C, 35D, 36D, 36E, 38E, 39A, 42B, 44C, 46C, 49C, 50F, 53A, 55D, 56E, 58A, 58B, 59B, 61A, 61E, 68A, 68B, 70B, 76C, 77B, 79C, 81F, 83E, 85D, 86E, 87B, 92D, 94A, 94E, 95D, 98A) were fixed in all the replicates (Nuzhdin and Mackay 1994). The presence of all the fixed sites was checked in all the individuals analyzed by in situ hybridization throughout the experiments and was used as a control against contamination. However, in addition to the fixed sites, new polymorphic copia and roo sites were found in some replicates. These polymorphic sites appeared to be due to transposition and accumulated during the maintenance of replicates. Transposition rates of copia and roo are elevated up to 1 x 10–2 transpositions per copy per generation in some Harwich replicates (Nuzhdin and Mackay 1994; Nuzhdin et al. 1996), whereas transposition rates of other TEs, including hobo, 297, 412, 1731, gypsy, mdg1, mdg3, jockey, and FB4, did not exceed spontaneous rates (Nuzhdin and Mackay 1994, 1995). Though not measured directly, the P-element transposition rate is elevated in Harwich replicates as well (Mackay et al. 1992).
Oregon RC-iso is an isogenic derivative of the Oregon RC line described elsewhere (Nuzhdin et al. 1996; Pasyukova et al. 1997). It has 14, 37, and 72 fixed euchromatic insertion sites of copia (11C, 21D, 34B, 34EF, 42B, 42C, 47A, 52B, 57E, 59D, 68B, 75C, 86E, 96A), Doc (3A, 4E, 5D, 7C, 10F, 11C, 14B, 17B, 19E, 32F, 34EF, 53B, 35E, 36DE, 38E, 39E, 41AB, 41D, 56F, 64E, 65A, 67F, 74A, 76B, 77A, 79A, 79D, 80A, 81F, 83D, 85F, 95B, 96D, 97AB, 98B, 99E), and roo (2F, 4F, 7D, 7E, 11B, 11C, 11D, 12F, 13A, 13D, 14C, 15B, 19C, 20A, 21E, 22F, 24D, 25B, 27B, 28F, 29F, 30D, 38E, 39A, 41AC, 43F, 44F, 46C, 48D, 49D, 49F, 50B, 50D, 61A, 61D, 62B, 62C, 64B, 65B, 65D, 67D, 68B, 68C, 70C, 72A, 73D, 76B, 77A, 78D, 80A, 81F, 85A, 85D, 85F, 86D, 87D, 87E, 91A, 91D, 92A, 92E, 93B, 94A, 94D, 94F, 95A, 97D, 98A, 98C, 98E, 99A, 99B), respectively. The copia, Doc, and roo transposition rates in Oregon RC-iso are less than 10–4 per element per generation. It was used as a tester line to measure TE haploid copy numbers and hatchability in replicates of the 2b and Harwich lines.
C(2L)RM, dp; C(2R)RM, px is a strain with attached left and right arms of the second chromosome. It was used to measure competition indices of the 2b and Harwich replicates.
Fitness Assay
The competition index of Jungen and Hartl (1979) was used to characterize the fitness of 2b and Harwich replicates. To imitate both competition and reproductive isolation, five males and five females of each replicate (tested line) were put into vials together with 15 males and 15 females of C(2L)RM, dp; C(2R)RM, px (tester line). The progeny of any cross between the tested and tester lines die due to the lack of chromosomal balance. As a result, progeny of each tested line developed in a vial, competing for food and other supplies against the common tester line. Progeny of the tester line are dp px phenotype, as compared with the wild-type (+) progeny of the tested lines. The competition index is defined as the fraction of the tested line progeny relative to the total number (CI = N(+)/N(+) + N(dp px)). Virgin males and females of all lines were collected simultaneously over 5 days from parental vials with controlled culture density. Parents were transferred to fresh vials after 7 days and discarded in another 7 days. All vials were maintained at 25°C on a standard medium. The numbers of progeny were scored for 9 days in each brood. From 10 to 20 replicate vials were set per tested line.
Hatchability Assay
Virgin males and females of 2b and Harwich replicates and males of Oregon RC-iso were collected simultaneously for 3 days from parental vials with controlled culture density. Three- to 5-day-old females were placed into vials with regular medium together with males of the same replicate or with Oregon RC-iso males. After approximately 24 h, females were transferred into vials in which the regular medium was substituted for black paper saturated with sucrose plus acetic acid, yeast suspension, and ethanol. Females were discarded after 4 h and eggs were transferred into regular vials, about 50 eggs per vial. The number of unhatched dead eggs in each vial was recorded after 24 h. The procedure was repeated from three to six times for each 2b and Harwich replicate. Hatchability was evaluated as a fraction of hatched eggs.
In situ Hybridization
Insertion sites were determined by in situ hybridization of labeled TE DNA to polytene salivary gland chromosomes of third instar larvae according to the procedure described in Ashburner (1989). Plasmids containing full-size copies of copia, roo, and Doc retrotransposons and the P element (Finnegan 1992) were labeled with biotin (bio-7-dATP, BRL) by nick translation. Hybridization was detected using the Elite Vectastain ABC kit (Vector Labs) and diaminobenzidine (Sigma). Chromosomal locations of retrotransposons were determined at the level of cytological subsections on the standard Bridges map of D. melanogaster.
Haploid TE Copy Number Assay
A number of euchromatic TE insertion sites on polytene chromosomes revealed by in situ hybridization were used to characterize TE copy number. Females of each 2b and Harwich replicate were individually crossed to Oregon RC-iso males and polytene chromosome squashes were made from their progeny larvae to use for in situ hybridization with biotinilated TE probes. TE locations were determined in 10 larvae per TE per replicate. Oregon RC-iso TE insertion sites were then subtracted from the analysis. The remaining sites characterized haploid sets of TE insertions in 2b and Harwich replicates.
Statistical Analyses
Distribution statistics, correlations, and analyses of variance (ANOVAs) and tests of significance of F ratios using type III mean squares were estimated using MEANS, CORR, and GLM procedures in SAS (SAS 1988). To account for traits shared through common origin, correlation between TE copy number and fitness in 2b replicates was confirmed by the method of independent phylogenetic contrasts (Felsenstein 1985; Harvey and Pagel 1991), as implemented by the COMPARE computer program. The branch lengths were fixed at 1.0 except for polythomy (0.0001).
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Both low and high rates of copia and Doc and copia, roo, and P-element transposition were recorded in different replicates of the 2b and Harwich lines, respectively, while TEs of many other families retained their characteristic low spontaneous transposition rates in these replicates (Nuzhdin and Mackay 1994, 1995; Pasyukova and Nuzhdin 1993; Pasyukova et al. 1998). Given the low effective population sizes of these cultures, an accumulation of TE insertion sites was anticipated in replicates of the 2b and Harwich lines, the number of accumulated insertions being higher for replicates with higher transposition rates of particular TEs. This differential accumulation of copia and Doc copies (copia, roo, and P-element copies) was predicted to make a substantial impact in the total accumulation of insertions in replicates of 2b (Harwich), while the difference in the number of insertion sites of other TEs can be neglected. As a result, two sets of transposition accumulation (TA) replicates, each set characterized by replicates with different average TE copy numbers in the same genetic background, were available to analyze a correlation between TE copy number and fitness.
The number of insertion sites of copia and Doc per haploid genome was determined in 13 TA replicates of 2b (Table 1), and the number of insertion sites of copia, roo, and P element per haploid genome was determined in 18 TA replicates of Harwich (Table 2). The competition index used, measure of fitness, and hatchability were also evaluated in each TA replicate of both lines (Tables 3 and 4).
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There is significant variation in copia, Doc, and total TE copy numbers (P <.001 in each case), in fitness (P <.001), and in hatchability of heterozygous and homozygous embryos (P <.001 for both) between the 2b TA replicates. There is also significant variation in copia, roo, P-element, and total TE copy numbers (P <.001, P <.05, P <.05, and P <.01, respectively), in fitness (P <.001), and in hatchability of heterozygous and homozygous embryos (P <.001 for both) between the Harwich TA replicates.
In 2b there was a negative correlation between the number of copia and Doc insertions, and both fitness (P <.001; Figure 2) and hatchability of heterozygous and homozygous eggs (P <.001 for both; Figure 3). There was also a significant correlation between the competition index and hatchability of homozygous eggs (P <.001), which is not unexpected, given that hatchability is one component of fitness.
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The 2b replicates are related to each other to different extents (Figure 1). This biases the estimation of correlation coefficients between TE copy numbers and fitness, since the replicates are not independent. For instance, if a mutation happened in the 2b3.1 lineage possessing a higher TE copy number, fitness of the four derivatives—2b3.1.1.1, 2b3.1.1.2, 2b3.1.2, and 2b3.1.3—could be simultaneously affected, increasing the significance due to pseudoreplication. After correction by the technique of phylogenetic independent contrast, the regressions of the three fitness components on total TE copy number were still significant. The intercepts and slopes (standard errors) were 0.88 (0.209) and –0.004 (0.0017) for the competition index, 1.17 (0.149) and –0.004 (0.0012) for the hatchability of heterozygous eggs, and 1.18 (0.14) and –0.004 (0.0011) for the hatchability of homozygous eggs. These were all significant at P <.05.
Hatchability of TA replicates should primarily be decreased due to deleterious homozygous TE inserts. Potential ectopic recombinations between TE copies should have no impact, since homozygous TEs are usually not involved in ectopic exchanges (Langley et al. 1988). In heterozygous embryos, derived from a cross between 2b replicates and the unrelated Oregon RC-iso strain, TEs are heterozygous. Their recessive deleterious effects are not expressed (Charlesworth and Langley 1989), but the hatchability decrease should be caused by dominant lethal mutations which appear to be due to ectopic recombinations. As shown above, the per copy decrease of hatchability caused by each mechanism was comparable (Figure 3).
The correlations between the number of copia, roo, and P-element insertions and fitness and hatchability were not significantly different from zero in the Harwich TA replicates (Figures 2 and 3). However, the difference in TE copy number between the Harwich TA replicates barely exceeds 30 copies per haploid genome, whereas in the 2b TA replicates it is 90. The correlation between TE copy number and fitness is not significant for the fraction of 2b replicates with the same small range of TE copy numbers (Figures 2 and 3). In both 2b and Harwich there are TA replicates in which copia copy number exceeds the normal range by twofold. Furthermore, in 2b replicates, Doc copy number exceeds the normal range by the same order, and the copia copy number strongly correlates with the Doc copy number (P =.0001). In contrast, in Harwich replicates' copy numbers of copia, roo, and P element are not correlated, which results in the small difference in TE copy number between the replicates. Thus the power of analysis could be somewhat reduced, and the negative effect of TE accumulation significant in 2b replicates is not significant in Harwich. Alternatively this result could be explained if a correlation between TE copy number and fitness is not linear.
Our data show that an increase in TE copy number in the genome is associated with a decrease in fitness and its components. Thus fitness of the host organism depends on the presence of virus-like elements such as TE in its genome. Our data confirm that not only homozygous TE insertions have deleterious effects on fitness and its components, but heterozygous TE insertions also reduce fitness, presumably via ectopic exchange. Analysis of the distribution of TE insertion sites between and within chromosomes of Drosophila (Biemont et al. 1997b) led to the conclusion that deleterious effects of homozygous TE insertions represent the main source of fitness decrease associated with TE accumulation, whereas the contribution of ectopic exchange between heterozygous TE copies to the reduction in fitness can be neglected. Our results can be similar of those of Biemont et al. (1997a) if we suppose that above and beyond selection against deleterious effects of ectopic exchange, the chromosomal distribution of TE is influenced by many other factors, and their joint effects disguise the role of ectopic exchange in the maintenance of TE copy number.
In this study the average deleterious effect of a TE insert on fitness and its components is approximately 0.004. This estimate is an order of magnitude lower than the average selection coefficient of a random spontaneous mutation, which was estimated as 0.02 (Crow and Simmons 1983; Mukai et al. 1972; Ohnishi 1977), though this high value has been the subject of recent criticism (Keightley 1996). Estimates of selection coefficients of P-element insertions vary from 0.01 (Eanes et al. 1988) to 0.1 (Mackay et al. 1992). They are both higher than our estimate for copia and Doc insertion mutations taken together. In natural populations, TE insertions with strong deleterious effects are eliminated by selection, while TE insertions with weak effects (selection coefficients comparable with spontaneous transposition rates, i.e., 10–4) continue to segregate (Charlesworth 1991). Different estimates of TE selection coefficients probably reflect different exposure to selection in different experimental designs; for example, whether new mutations were maintained as heterozygotes against a balancer chromosome and thus sheltered from natural selection (e.g., Mackay et al. 1992; Mukai et al. 1972) or not (this study). Variation in estimates of selection coefficients could also be explained by specific properties of different TEs with respect to their impact on fitness.
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Acknowledgments |
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This work was supported by the Russian Fund of Basic Research (grants 00-04-48770 and 03-04-48605; to E.G.P.), National Science Foundation (grant 9815621; to S.V.N.), and National Institutes of Health (grants GM 45344 and GM 45146; to T.F.C.M.).
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Footnotes |
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Corresponding Editor: Ross MacIntyre
Received July 5, 2003
Accepted March 29, 2004
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