PERSISTENCE OF MALE STERILITY IN STRAINS ISSUED FROM HYBRIDS BETWEEN C. BOCQUET 2 F. LEMEUNIER 2 AND L. TSACAS 2.
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1 Journal of Genetics Volume 6Z, Nun~ber 3 Ju,~e 1 97 PERSISTENCE OF MALE STERILITY IN STRAINS ISSUED FROM HYBRIDS BETWEEN TWO SIBLING SPECIES : DROSOPHILA SIMULANS AND D. MAURITIANA. BY J. DAVID I C. BOCQUET 2 F. LEMEUNIER 2 AND L. TSACAS 2. l - Laboratoire d'entomologie exp@rimentale et de G~n@tique, Universit@ Claude Bernard, VILLEURBANNE F. 2 - Laboratoire de G@n~tique ~volutive du CNRS GIF SUR YVETTE F. ABSTRACT The cross between two sibling species, D. si,~lans and D. maur~tiana, produced F l fertile females and sterile males. Backcrosses of these females to parental males resulted in the production of a small proportion of fertile males. From this second generation, four lines were propagated by mass mating and the frequency of fertile males was determined up to the 20th generation. In all cases, a linear increase of the proportion of fertile males was observed between the 2d and 8th generations and then the proportion remained stable at a level of 9]%. From these observations several conclusions seem possible. (1) Male fertility was determined by several genes existing under different allelic conditions in the two sibling species ; (2) the progressive restoration of male fertility was due to a normalizing selection which favored the homozygotes against the heterozygotes ; (3) the persistence of a small frequency of sterile males after the 8th generation was the consequence of a balancing selection favoring the heterozygous condition (possibly in the females) ; (4) introgression of genes from one species into the genome of another species appeared capable of increasing the genetic heterogeneity of the population for a long time.
2 94 Sterility in Drosophila hybrids INTRODUCTION Drosophila mauritiana, a species recently found in Mauritius (Tsacas and David, 1974) is genetically very close to O. simul~zs (David et al., 1974). Hybridization experiments produced F 1 sterile males and fertile females. Backcrosses of the F I females to males of the parental species gave a small proportion of fertile male offspring. From this second generation, it was possible to keep true breeding lines, propagated by mass mating the adults, and to observe the effects of natural selection on the frequency of fertile males. As would be expected, the proportion of fertile males increased rapidly during the first generations, in the free running lines. Then an unexpected stabilization was observed after the 8th generation. Such a result implies the interaction of different selective processes which will be discussed in this paper. MATERIAL AND METHODS Parental strains used were D. mmwitiana from Mauritius (Le Chaland) and D. simulans from the neighbouring island R~union (St Denis). The two reciprocal crosses were made and the two kinds of fertile females were backcrossed to the parent species. Altogether, the four following lines were founded : line I : ~ F I (~ sim. ommaur.) x ~simulans line 2 : ~ F I (~ sire. ~maur. ) x ~mauritiana line 3 : ~ F I (~ maur. o~sim. ) X ~simulans line 4 : ~ F I (~ maur. cssim. ) x O~mauritiana Flies obtained from these crosses constitued the B 2 (backcross 2) generation. After the B 2, each line was propagated by mass mating the emerged adults, without any further introduction of parental flies. For each generation, at least 50 couples were used as reproductive individuals. Experiments were carried out at 25~ with a killed yeast medium (David and Clavel, 1965) at a high larval density favoring competition and natural selection. Fertility was checked after dissection of males, aged 4-5 days, in Drosophila physiological solution. Mobile sperm in the seminal vesicles was the criterion of fertility. At each generation, about 70 males were examined in each line.
3 J. Davkd et al ~.~... x/ 9 x e "~x~ x..., x ~X~x." _ / 25. ~ 100. I I l I i I' ~ x-= x.~'~,_.kx).>~\, ~ "/ _ 25- F~ BI2 ; 1'0 1; 2'0 Generations Figure! : yariation of the percentage of fertile males in the four lines (B 2 : second generation obtained by backcrossing F I hybrid females to parental species ; further generations were obtained by mass mating the adults). Fig. A : lines ] and 2 ; Fig. B : lines 3 and 4 (see methods) X : lines backcrossed to simulans males O: lines backcrossed to ma~itiana males
4 96 Sterility ia Drosophila hybrids RESULTS Variations of the frequency of fertile males during the successive generations are shown in Figure I. Results are very similar in the four lines. At the second, B 2 generation, a small proportion, about 6% of fertile males, was observed. The percentage then increased almost 'linearly up to the 8th generation. Finally the proportion of fertile males became stable in each line at a level clearly below 100%. Chi square statistical analysis, comparing the four lines at each generation showed that, in 13 cases out of 19 generations, the homogeneity hypothesis could be accepted (a lack of homogeneity was found in generations 3, 6, 7, 9, I0, 17). When: in each line, the percent of fertile males was considered from the 9th to the 20th generation, no significant differences were observed (table 1). Finally, if the average percentages of the various lines as shown in table I~ were compared, the differences, although not important, appeared significant (~(2=19.21 for 3 d.f., p < 0.01). Table 1 : Average percentages of fertile males in the 4 lines from the 9th to the 20th generation of mass mating line fertile males number % I (siz~tlans) 2 (mauritiana) 3 (sinn~lans) 4 (mauritiana) 93,64 87,7 90,09 9, ,56 II > 0, ,90 > 0, ,27 ] > 0, ,83 II > 0,05 n = number of males d.f. = degrees of freedom p = probability of~ 2 The nature of the initial cross did not seem to influence the stabilization level reached in each line. For lines I and 2, both issued from simulc~s females, the average fertility level was 90.7%. The stability level was at 90.9% for the two other lines, originating from ma~witiana females. The direction of the backcrosses did not seem important either. For the two lines (I and 3) backcrossed to simulans males, the average
5 J. David et al 97 percent was 91.9%. A value of 89.7% was <~bserved in the two lines (2 and 4) backcros~ed to mauvitiana males~ The small differences in the equilibrium values reached in the four experimental lines are finally very slight and can be considered as having a small biological significance. Fertile male frequency sta- bilizes itself at about 91%, In the parental strains of D. simulans and mauritiana, the proportion of fertile males was always 100%. DISCUSSION AND CONCLUSIONS rn the Drosophila genus, several cases are known of genetically close species which, crossed together, produce sterile hybrids males and fertile females (Dobzhansky, 1934: 1936, 1974 ; Ehrman, 1960 ; Bock, 1971 ; Gupta, 1973 ; De Campos Bicudo, 1973 ; Ayala et al., 1974). Thig seems, however, to be the first case where the restoration of male fertility by natural selection was studied after backcrossing.the F 1 females to the parental species. For the genetic determination of male sterility, the great analogies between the four reciprocal lines excludes the intervention of cytoplas- mic factors and even of a matroclinous influence. The chromosomal struc- tures of D. simulans and mauritiana are very similar (Lemeunier and Ashburner, 1976) so that the sterility certainly has a genic and not a chromosomal determination. According to Dobzhansky (1970), we can assume that the two species possess homologous fertility genes but that the species are homozygous for different alleles of these genes. The hetero- zygous stage results in sterility for the production of normal sperm. while an homozygous stage is necessary The localization of these fertility genes remains hypothetical. In D. melanogaster and, probably also in simulans and ma~ritiana, such fac- tors are known on the Y chromosome (Lindsley and Grell, 1968 ; Suzuki, 1970). In the case of interspecific hybrids, however, the role of genes located on the Y can be excluded because of the hemizygous state of this chromosome. An autosomal localization of the fertility factors appears highly probable although we did not have marked chromosomes in our sim~z- fans or mauritiana strains to verify this hypothesis. Such a conclusion was demonstrated in the cross D. psgudoobscura x O. persimilis (Dobzhan-
6 98 Sterility in Drosophila hybrids sky, 1936) and in the cross D. melanogaster x D. si~lans Pontecorvo, 1940). The number of male fertility (Muller and genes involved in the cross D. simulans x D. mauritiana is unknown. If, however, a single gene was implied, the proportion of fertile males in B 2 should be 50% and the restoration of fertility in the following generations would be very rapi~ Taking into account the low frequency (6%) of fertile B 2 males and the slowness of its further increase, the existence of several genes seems necessary. The determination of male fertility appears polygenic, as it was previously shown to be for other interspecific crosses (D. pseudoobs- cura x D. persimilis and D. melanogaster X D. simulans). The progressive restoration of male fertility in the f~ree running lines can be considered as a typical case of normalizing selection : sterile gel:otypes are excluded from the gene pool producing the gametes of the next generation. Our results appear interesting and original for two main reasons : first, the natural selection was acting on a polygenic system and, second, it eliminated the heterozygotes and favored the homozygotes. The success of the normalizing selection is not total and a noticea- ble proportion (9%) of sterile males proved to be able to persist, pro- bably indefinitely, in the lines. Such a phenomenon demonstrates the persistence of some level of heterozygosity. Similar observations are often made in population genetics experiments (Dobzhansky, 1970 ; Boesiger, 1972 ; etc.). In the present case, the most likely explaination ;is to assume a selective advantage of the heterozygotes. For example, hetero- zygosity, although unfavorable in the males, could be advantageous in the females. Finally, it is worth emphasizing that, after an interspecific cross and a further backcross, the natural selection was unable to eliminate all the introgressed genes and to restore the original coadapted geno- type of the parental species. This conclusion is enforced by the obser- vation of testis color. In D. simulans testis are deep yellow while they are lightly colored in D. mauritiana. In the four experimental lines, a persistence of both types of coloration was observed until the end of experiment. Introgression after interspecific hybridization thus appears as a mean of increasing the average genetic heterogeneity of the natural populations and their adaptation capacities (Van Valen, 1963 ; Lewontin and Birch, 1966 ; McClelland, 1967).
7 J. David et a[ 99 REFERENCES AYALA, O., TRACEY, M.L., BARR, L.G. AND EHRENFELD, J.G. (1974). Genetic and reproductive differenciation of the subspecies, Drosophila equinoxialis cari~ensis. Evolution OESIGER, E.(1972). Le maintien des polymorphismes et de la polyg~notypie par l'avantage s~lectif des h~tgrozygotes. Soc. Zool. Fr BOCK, I.R. (1971). Intra and interspecific chromosomal inversions in the Drosophila ~ip~tinata species complex. Chromosoma (Berl.) N DAVID,J., CLAVEL, M.F. (1965). Interaction entre le g~notype et le milieu d'~levage. Consequences sur les caract&ristiques du d~veloppement de la Drosophile. Bull. Biol. Fr. Belg DAVID, O., LEMEUNIER, F., TSACAS, [. AND 80CQUET, C. (1975). Hybridation d'une nouvelles esp~ce, Drosophila mau~tiana avec D. melanogaster et D. simulans. Ann. G~n DE CAMPOS 8ICUDO, H.s (1973). Reproductive isolation in the saltan8 group of Drosophila. I. The saltcscs subgroup. Genetics DOBZHANSKY, T. (1934). Studies on hybrid sterility. I. Spermatogenesis in pure and hybrid Drosophila pseudoobscura. Zeit. Zef. mikr. Anat DOBZHANSKY, T. (1936). Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics DOBZHANSKY, T. (1970). Genetics of the evolutionary process. Columbia Univ. Press, N.Y. DOBZHANSKY, T. (1974). Genetic analysis of hybrid within the species Drosophila subobscura. Hereditas EHRMAN, L. (1960). The genetics of hybrid sterility in Drosophila paulistorum. Evolution GUPTA, O.P. (1973). Comparative studies of male genital structures of hybrids and their parental species. Experientia [EMEUNIER, F. AND ASHBURNER, M. (1976). Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora). II. Phylogenetic relationships between six species based upon polytene chromosome banding sequences. Proc. Roy. Soc. Lond. (sous presse)
8 100 Ster~l~ty ~n DrosophHa hybrids LEWONTIN, R.C. AND BIRCH, L.C. (1966). Hybridization as a source of variation to new environment. Evolution LINDSLEY, D.L. AND GRELL, E.H. (1968); Genetic variations of Drosophila melanogaster. Carnegie Inst. ~as~. P~l p. MULLER, H.J. AND ~ONTECORVO, G. (1940). Recombinants between Drosophila species the F] hybrids of which are sterile. Nature McCLELLAND, G.A.(]967). Speciation and evolution in Aedes in Genetics Of ~sect vectors of disease. J.W. Wright' and R. Pal : Elsevier, Amsterdam ] SUZUKI, D.T. (1970). Temperature-sensitive mutations in Drosophila melanogaster. Science TSACAS, L. AND DAyID, J. (1974). Drosophila mauritiana n. sp. du groupe melanogaster de l'ile Maurice. Bull. Soc. Entomol. Fr VAN VALEN, L. (1963). Introgression in laboratory population of D. persimills and D. pseudoobscura. Heredity
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