Abstract
As a rule, progeny of crosses between Drosophila simulans females and D. melanogaster males are formed by sterile males, because females die as embryos. However, populations of these species have been found that produce a certain frequency of viable hybrid females. We have found that 94% of the females of a D. simulans population from Tel Aviv gave hybrid progenies with both sexes. The segregation of phenotypes with different rescue success adjusts to the action of a single, dominant, zygotic-acting gene involved in hybrid female viability. This gene, which we named ‘Simulans hybrid females rescue’ (Shfr), is temperature-sensitive, showing a much smaller effect as temperature increases. Reciprocal crosses between Tel Aviv and a nonrescue population indicate some influence of cytoplasm or maternal effect in rescue. Using a chromosome substitution analysis we have located Shfr on the second chromosome. Using synthetic lines with this chromosome having different segments from Tel Aviv and from a multimarker strain we have mapped Shfr between black (2 L-43.0) and pearly (2 R-74.0).
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Introduction
From an evolutionary perspective, the most important topic about speciation is to understand the biological and genetic phenomena that lead to species differentiation. There are several theories that attempt to explain the development of new species from an ancestral population (Mayr, 1963; Dobzhansky, 1970; Paterson, 1985; Templeton, 1987), all of which concur in the necessity of genetic changes affecting reproductive isolation, either by modification of sexual behaviour, rendering interspecific mating difficult (premating isolation), or by hybrid breakdown (postmating isolation).
Perhaps the most drastic barriers to avoid gene flow between species are hybrid inviability and/or sterility, because they act when sexual isolation has failed. In most species, the genetic factors involved in postmating isolation are classified in accordance with these two different hybrid phenotypic classes.
Classical theories about the genetics of reproductive isolation hypothesized the existence of many genes with small effect located throughout the genome (Mayr, 1963; Dobzhansky, 1970), whereas modern ideas propose the action of few genes with large effect (Gould, 1977; Wright, 1982). Regardless of the numerous experimental studies on speciation, mainly in the genus Drosophila (see Coyne, 1992 and Wu & Davis, 1993 for reviews), there is, to date, no conclusive support for either of these theories. It is more likely that the type of genetic change during speciation depends on the evolutionary history of each species.
A handful of genes with large effects on hybrid inviability have been found in crosses among Drosophila species of the melanogaster group; three of them are located in D. simulans: the Lethal hybrid rescue (Lhr, 2–95) (Watanabe, 1979; Takamura & Watanabe, 1980), the maternal hybrid rescue (mhr, 2) (Sawamura et al., 1993a) and an anonymous gene(s) in chromosome II (Orr, 1996); and the other two in D. melanogaster: the Hybrid male rescue (Hmr, 1-31.84) (Hutter & Ashburner, 1987; Hutter et al., 1990) and the Zygotic hybrid rescue (Zhr, 1-62.5) (Sawamura et al., 1993b). These examples suggest that hybrid inviability is controlled by some special genes, which are dysfunctional (incompatible) for the development of hybrids, but perfectly functional for individuals within species.
Understanding the nature of speciation genes requires that their products and the development stages at which they act be identified. However, careful genetic analysis of gene action and fine location of these genes are necessary steps to be taken before molecular biological work can be undertaken.
There are basically two methodologies to analysing the genetic basis of postreproductive isolation. When species give hybrids with only one viable, fertile sex, the usual approach is to introgress genetic material from one species into another by repeated backcrosses of the hybrids. Such an analysis allows for the detection of the influence of particular chromosome fragments on the trait under study (Davis et al., 1994). The second approach is generally used in species that yield inviable and/or sterile hybrids, and is based on the existence, in some populations, of genetic polymorphisms associated with a particular trait of reproductive isolation (Watanabe, 1979; Hutter & Ashburner, 1987; Hutter et al., 1990; Sawamura et al., 1993a,b).
We have used this latter method to study the production of hybrid progeny in crosses between Drosophila melanogaster males and D. simulans females. Our interest in this interspecific cross direction lies in the facts that: (i) it has scarcely been studied, because premating isolation is very strong so that hybrids are difficult to obtain; and (ii) the hybrid progenies consist of males only, so this postmating isolation does not follow Haldane’s rule.
From a screening of around 40 D. simulans populations, we first detected populational polymorphism for hybrid female viability, a fact already observed by Orr (1996). Then we selected a population, Tel Aviv, where the females showed a high frequency of daughters in their hybrid progenies. A chromosomal substitution analysis indicated that hybrid female viability was largely caused by genes located on the second chromosome. From classical genetic analysis, we found a good fit of this trait with the segregation of a single gene with a dominant inheritance mode. We demonstrate that this gene is temperature-sensitive, does not have maternal effects and is not Lhr.
In an attempt to map this gene, we constructed synthetic lines with the second chromosome carrying fragments of different length from the Tel Aviv population and from a multimarker D. simulans strain. Our results indicate that the gene that affects hybrid female lethality is located between black (2 L-43.0) and pearly (2R-74.0). We named it ‘Simulans hybrid females rescue’ (Shfr).
Materials and methods
Fly stocks and culture conditions
1 A D. simulans population from Israel, named Tel Aviv, that was kindly provided to us by J. R. David.
2 A D. simulans multimarker strain that carries the following mutations: forked (f2: 1-56.7), net (net: 2 L-0.0), brown (bw: 2R-104.5), scarlet (st: 3R-40.0) and ebony (e: 3 L-60.0) (strain 2008 from Bloomington Stock Center).
3 A D. simulans multimarker strain homozygous for five recessive mutations on chromosome 2: left arm, net (net, 2 L-0.0) and black (b, 2 L-43.0); right arm, pearly (py, 2R-74.0), spread (sd, 2R-80.0) and plum (pm, 2R-103.0) (strain 923 from Bloomington Stock Center). The given map positions are from D. simulans (Sturtevant, 1929; Ohnishi & Voelker, 1979), except for net and bw which correspond to D. melanogaster (Lemeunier & Ashburner, 1976).
4 A strain homozygous for the dominant mutation Lethal hybrid rescue (Lhr, 2R-95) (Bloomington Stock Center); a description of this strain is in Watanabe (1979) and in Takamura & Watanabe (1980).
5 A D. simulans wild population from Asturias, Spain, named Albandi.
6 A D. melanogaster wild stock caught in Asturias (Spain), named MC.
Unless otherwise specified, all fly cultures were reared on medium made up of agar (1.2%), baker’s yeast (20%) and sugar (5%), and were maintained at 21°C.
Collection of hybrids
Interspecific crosses were carried out following the methods of Carracedo et al. (1998). In brief, 10 pairs of D. simulans females and D. melanogaster males, newly emerged, were put into a vial with food. Five days later, each female was transferred to a new vial. The vials showing hybrid progeny were examined daily, and the number of emerged males and females recorded. Using this method we obtain the progeny of each single female which facilitates interpretation of results. This differs from other authors who, by measuring the mixed progenies of several females, cannot identify the sex ratio of individual progenies, and mix the contribution of large and small broods into a single value, so female variation in rescue success cannot be detected.
Criterion for female hybrid progeny viability
We consider that a D. simulans female presents the hybrid female rescue (HFR) trait when her hybrid daughters comprise at least 20% of the progeny. We established this criterion because the appearance of a few females in some vials in which most of the progeny are males is frequent (Sawamura et al., 1993a; Orr, 1996), and because hybrid progenies are subject to a large sex ratio variability because of their characteristically small number (around 25 males, plus females). For this reason, vials with fewer than 15 hybrid adults were discarded to avoid misclassification; for instance, a vial with only 14 males (0% females) does not differ at the 5% level from 4 females and 10 males (29% females) (Fisher’s Exact P value=0.098); similarly, a vial with a small progeny of only 3 females and 7 males is not significantly different from 6 + 4 (P=0.37, which would suggest a clear rescue effect) or from 1 + 9 (P=0.58, suggesting no rescue).
Chromosome substitution scheme
Eight lines carrying 0, 1, 2 or 3 homozygous chromosomes from the Tel Aviv population or from the 2008 strain were necessary. Two lines were Tel Aviv and the 2008 strain, and the other six were obtained from two types of crosses. In cross A, males from the Tel Aviv population were paired with virgin females from the multimarker 2008 strain. The reverse process was carried out in cross B. In each cross, we obtained the F1 and F2 generations. From the different phenotypes that appeared in the F2 generation we only selected, according to the visible marker mutations, six phenotypic classes, which corresponded to females homozygous for entire chromosomes from Tel Aviv or from the 2008 strain (see Fig. 1). Because homozygotes and heterozygotes for wild alleles are indistinguishable, the genotypes of these females were determined later (see below).
Approximately 300 females from each of the eight phenotypic classes were tested for hybrid production as follows. Ten newly emerged females from the same class were placed into a vial with 10 D. melanogaster males for 5 days, sufficient time for heterospecific matings to occur (Carracedo et al., 1998). Then each female was put singly in a fresh vial for 5 days to produce hybrid progeny. Females without hybrid progeny were discarded. The remaining females were individually crossed, for their genotypic identification, with two multimarked males. The vials with hybrids from heterozygous females were discarded, and only the hybrid progenies of females homozygous for the selected markers (see Fig. 1) were scored daily until exhaustion.
Introgression scheme
We constructed the following seven synthetic lines with the second chromosome composed of different homozygous fragments from the multimarker strain and from the Tel Aviv genome: (i) net, black; (ii) black, pearly; (iii) pearly, spread; (iv) spread, plum; (v) net, black, pearly; (vi) black, pearly, spread; and (vii) pearly, spread, plum.
Figure 2 outlines the crosses carried out to construct the net, black line. Homozygous males for five recessive markers (net, b, py, sd and pm) on the second chromosome were crossed (i) to wild females from Tel Aviv. Adult flies from the F1 generation were crossed (ii) to obtain the F2. From the different phenotypes that segregated in the F2 generation we selected homozygous males for net and black. Each of these was backcrossed (iii) to Tel Aviv females (one male and five females per vial). Males and females that emerged from each vial were crossed en masse (iv) and, from their progeny, we selected net, black males, which were individually crossed (v) with Tel Aviv females. Crosses (iv) and (v) were carried out 10 times to obtain finally lines with cytoplasm and chromosomes from Tel Aviv except for the net to black fragment of the second chromosome, that came from the multimarker strain. A similar cross procedure was followed to obtain the remaining six synthetic lines.
To confirm that the 10 backcrosses were effective in removing the heterozygous markers present in cross (iii), several males from each line were crossed to multimarked females. In all cases the phenotypes of their progenies matched well with the expected, indicating that the synthetic lines only carried the selected markers.
Results
Chromosome location of the FHR trait
From a total of 146 Tel Aviv hybridized females, 111 (76%) produced progenies with males and 20% or more females (FHR trait), indicating the presence of genes in the Tel Aviv strain that rescue female hybrid viability. In contrast, only 10 out of 60 (17%) females from the 2008 strain exhibited the FHR trait. The percentages of females that rescued female hybrid viability for each of the eight chromosome substitution lines are given in Fig. 3. The large effect of the second chromosome is evident.
In order to examine statistically the contribution of each chromosome to the trait, we constructed a four-way table of rescue frequencies which was analysed using an iterative method that generates maximum likelihood estimates (Bishop et al., 1975). No chromosome interactions were detected, and only the second chromosome had a significant effect (G5=213.7; P < 0.001), indicating that the gene (or genes) that rescues viability of hybrid females is located in this chromosome. The rescue genes Lhr, mhr and the anonymous gene of Orr are also located in the second chromosome of D. simulans.
Rescue is temperature-dependent
Several genes involved in hybrid viability in Drosophila are temperature-dependent, being able to rescue viability at low temperatures only (Lee, 1978; Sawamura & Yamamoto, 1993; Sawamura et al., 1993a). We performed a study of hybrid viability from crosses between females from Tel Aviv and D. melanogaster males at three temperatures. Heterospecific matings were performed at 21°C, but the hybrid progenies of single females were reared at 17, 21 or 24°C.
Figure 4 shows the distribution of females according to the percentage of daughters in their hybrid progenies. The effect of the temperature is evident, with a larger rescue success as temperature decreases. At 17°C, females seems to be distributed into three phenotypic classes, with means around 0%, 30% and 50% rescue.
Table 1 shows, at each temperature, the numbers of Tel Aviv strain females that failed to rescue their daughters (<20% females in their progenies) and those that showed the rescue trait. The pooled number of hybrid males and females, and the average percentages of daughters at each temperature are also shown. A homogeneity G-test applied to these percentages (Sokal & Rohlf, 1995) was significant (G2=585.4; P < 0.001), confirming that the FHR trait is temperature-dependent.
Rescue fits to segregation of a single gene
The percentages of females in hybrid progenies show a large variability, ranging from 0 to 60% (see Fig. 4), which suggests that different rescue genotypes are present in the Tel Aviv population. At 17°C, three phenotypic classes are clearly discernible, from which we hypothesized that a single, dominant gene, with two alleles, R and r, with p and q allele frequencies, respectively, is present in the Tel Aviv population and causes the HFR trait as follows. In crosses involving D. simulans RR females and D. melanogaster rr males all the Rr female hybrids are rescued, so we expect around 50% females in the progeny (50% plus the usual binomial sex ratio variation). Crosses of D. simulans Rr females with D. melanogaster rr males produce Rr and rr hybrids in a 1:1 ratio; because only Rr genotypes are rescued, we expect around 33% females in their hybrid progenies. Lastly, D. simulans rr females only produce rr hybrids that are not rescued.
To estimate the frequency of the rescue allele R we have calculated the expected variation of percentages of daughters from RR mothers, variation which corresponds with the theoretical binomial distribution for a 50:50 female:male sex ratio. Similarly, we have calculated the expected binomial distribution of percentages of daughters from Rr mothers, that is, for a 33:67 sex ratio. The two distributions were calculated for a progeny size of 30 (males plus females), which can be considered as representative in our hybrid progenies. Then, the first distribution was applied to p2 × N data and the second to 2pq × N data (N=70 observed progenies, see Table 1). The obtained data represent the expected percentages of daughters from RR and Rr mothers, respectively, and they were compared to the observed distribution in Fig. 4 by the nonparametric Kolmogorov–Smirnov test.
Several observed vs. expected comparison runs were carried out using different p and q allele frequencies. The best fit corresponded to a P=0.8 value for the R rescue allele (Dmax=0.136, P=0.58). Therefore, the Tel Aviv population carries a gene(s) at this frequency that rescues the female hybrids.
At 21°C the HFR trait was less effective and the failure in rescue was even more accentuated at 24°C (Table 1 and Fig. 4). This reduced effectiveness of rescue with increasing temperature could be determined by the R locus itself, as all the percentages of daughters per female diminish with increased temperature, so their distribution is displaced to lower values (see Fig. 4). However, this reduced rescue effect could also be determined by the background genotype of the mother, so a maternal effect, temperature-dependent, and independent of the R locus could be involved in the rescue trait.
Inheritance of the rescue trait
We crossed our D. simulans Tel Aviv (T) with another D. simulans population, Albandi (A), characterized by showing a low frequency of females with the HFR trait (8.75%). None of these females rescued more than 25% of their hybrid daughters. As most D. simulans populations have some females that produce occasional hybrid females, we assumed that the rescue value is low enough to assign the rr genotype to the Albandi population.
Crosses between Tel Aviv and Albandi were made in the two directions, T × A and A × T (female cited first), and F1 females were crossed with D. melanogaster males for hybrid production. Table 2 shows the number of females examined and the number of these in each phenotypic class. Comparison between A × T and T × A phenotypes was made using a 2 × 2 contingency chi-squared calculation (χ21=0.002, P=0.96). No significant differences between these reciprocal crosses were found, which supports our model of a single, autosomal locus for the main determination of the HFR trait. However, the pooled percentage of rescued females was higher in the A × T cross direction which points to some sort of maternal effect or cytoplasmic influence.
All the presented results support the HFR trait being based on a single dominant gene with a temperature-dependent expression. Another possible interpretation is that this trait results from the action of a maternal, semidominant gene, with the rescue allele at the same estimated frequency of P=0.8. We are not too inclined to accept this view, as it implies that: (i) whereas all eggs from RR females express the maternal R genotype and are rescued (50% females in their progenies), only a fraction of eggs from Rr females express the maternal genotype; and (ii), this fraction of maternally determined rescue, that could have any value, must be, for adjusting to observed data, around 50% (33% females in their progenies), a value that coincides, surprisingly, with the expected allele segregation of Rr females under the alternative hypothesis of a nuclear, zygotic-acting gene.
Our gene differs from previously described rescue genes
We reject the hypothesis that our gene is the mhr gene of Sawamura et al. (1993a), because mhr behaves as a recessive and shows clear maternal inheritance. We also discard Orr’s anonymous gene(s) (Orr, 1996), as this shows a dominant, fully penetrating maternal effect and is not temperature-dependent. The only described D. simulans gene that, like ours, rescues hybrid female viability, has a dominant inheritance mode and is temperature-sensitive, is the Lethal hybrid rescue (Lhr) (Watanabe, 1979; Takamura & Watanabe, 1980). This gene rescues the viability of hybrid females in crosses between D. melanogaster males and D. simulans females, and of hybrid males in the opposite cross. To test whether Lhr is the gene present in the Tel Aviv population, we performed crosses between males from the Lhr strain or from Tel Aviv with D. melanogaster females. The hybrid progenies from these crosses are shown in Table 3. Males from the Tel Aviv population are unable to rescue hybrid male viability, whereas Lhr males can do so.
We conclude that the gene in the Tel Aviv population is a new gene that rescues hybrid female viability in crosses between simulans females and melanogaster males. We named this gene Simulans hybrid females rescue (Shfr).
Mapping Shfr
The percentages of females with the rescue trait were 76.02% in Tel Aviv and 10.72% in the L923 strain. The corresponding values of the seven introgressed lines are shown in Fig. 5. These percentages were not homogeneous (χ27=49.45; P < 0.001), as is indicated by a test of variance for the binomial distribution (Snedecor & Cochran, 1967). A posteriori comparison of these percentages by an unplanned test of homogeneity (Sokal & Rohlf, 1995) classified the lines into the following two homogeneous groups.
1 Group 1: [b, py]; [net, b, py]; [b, py, sd]; with a rescue average of 37.5%.
2 Group 2: [net, b]; [py, sd]; [sd, pm]; [py, sd, pm]; with a rescue average of 67.6%.
The lines of the first group are homozygous for the recessive markers black and pearly, two mutations that do not appear together in the lines of the second group. These results indicate that the Shfr gene is located between b (2 L-43.0) and py (2 R-74.0).
Discussion
Hybridization between simulans females and melanogaster males occurs rarely (Sturtevant, 1929; Carracedo & Casares, 1985), and success in this cross direction has been reported only recently for some populations (Uenoyama & Inoue, 1995; Carracedo et al., 1998). This fact, together with the paucity of markers linked to structural chromosome changes in D. simulans, can explain the relatively few studies on the genetics of hybrid lethality, and consequently the scarcity of knowledge about this subject.
Only four major genes affecting the viability of hybrid females in the above-mentioned cross have been described. One is in D. melanogaster, Zhr (Sawamura et al., 1993b), which is located in the X chromosome. The other three, Lhr (Watanabe, 1979; Takamura & Watanabe, 1980), mhr (Sawamura et al., 1993a) and Orr’s (1996) anonymous gene(s) are located in the second chromosome of D. simulans. Curiously, our D. simulans Shfr gene, also maps in this chromosome, and the same occurs for several sterility and inviability factors affecting hybrids among species of the D. simulans clade (Davis et al., 1994). With only four rescue genes known in D. simulans to date, it is premature to suggest a bias for the accumulation of speciation genes in the second chromosome of this species.
Given that the number of genes identified as being involved in postzygotic isolation in the melanogaster group of species is currently increasing, a question is raised as to whether these genes have appeared recently or whether they correspond to the earliest genetic systems involved in speciation. It is known that postzygotic isolation in these species involves sterility and inviability factors, and it is commonly assumed that the former appeared first during speciation (Wu & Davis, 1993) and were efficient enough to achieve isolation. In consequence, one can suppose that inviability genes appeared once species were largely isolated by sterility factors, as has been found by Seeger & Kaufman (1990) and Brady & Richmond (1990) between D. melanogaster and D. pseudoobscura.
The other reason for the recent origin of the newly discovered rescue genes is that if only one major gene suffices to cause hybrid inviability, the presence of other inviability genes is redundant, which suggests that they were not involved in the speciation event. In such a case, different populations may exhibit different inviability genes originated by mutation. These genes would be selectively neutral, so they could be lost, fixed or segregating according to each population’s evolutionary history. The fact that the recently discovered rescue genes were each detected in particular strains is compatible with this view that different sets of incompatibility genes are fixed in different populations (Nei et al., 1983). Thus populations could show variation in the frequency of hybrid female rescue depending on the frequencies at which these genes occur. In our previous screening searching for D. simulans populations highly crossable with D. melanogaster males, we found, in several of them, the appearance of females in the hybrid progeny, which suggests the presence of rescue genes. Whether these are new rescue genes or are the ones already reported is at present being studied.
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Acknowledgements
We would like to thank Amparo Villabrille, Julio Santiago and Nina Martinez for technical assistance. We acknowledge the Bloomington Stock Center for supplying us with the 923, 2008 and Lhr D. simulans strains. This work was supported by the Ministry of Education and Culture of Spain (DGICYT Grant DG-94-PB-1347).
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Carracedo, M., Asenjo, A. & Casares, P. Location of Shfr, a new gene that rescues hybrid female viability in crosses between Drosophila simulans females and D. melanogaster males. Heredity 84, 630–638 (2000). https://doi.org/10.1046/j.1365-2540.2000.00658.x
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DOI: https://doi.org/10.1046/j.1365-2540.2000.00658.x
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