Heredity 64 (1990) 255—262 The Genetical Society of Great Britain Received 6 September 1989

Developmental anomalies in Drosophila hybrids are apparently caused by loss of microchromosome

H. Allen Orr Department of Ecology and Evolution, University of Chicago, 1103 E. 57th Street, Chicago, IL 60637, U.S.A.

Hybrids produced by crossing Drosophila virilis females to D. lummei males suffer from many developmental anomalies; the reciprocal hybridization yields normal offspring. Genetic analysis reveals that these anomalies involve a maternal effect: whether or not an individual will show an anomaly depends upon his mother's nuclear genotype. Several lines of evidence suggest that the proximal cause of the anomalies is the elimination of the D. lummei microchromosome (chromosome 6) from hybrids. Loss of the D. lum,nei microchromosome in this hybridization is known to involve a maternal effect (Evgen'ev, 1973), as mitosis in early development is under the control of maternally-acting genes.

INTRODUCTION architecture" of morphological anomalies will resemble the architecture of normal morphological Developmentaland morphological anomalies are differences between species. common among species hybrids. Drosophila During a study of the basis of postzygotic isola- melanogaster-D. simulans hybrids, for example, tion in the yin/is group of Drosophila (Orr and often suffer from missing bristles and incomplete Coyne, 1989), we noticed that hybrids between D. scierotization of the abdomen (Sturtevant, 1920, virilis and D. lummei frequently showed several 1929). Unfortunately, almost nothing is known morphological anomalies. The following about the genetic causes of such hybrid anomalies. anomalies were observed: greatly reduced eye Elucidation of the basis of these anomalies may resembling the "eyeless" mutation of D. throw some light on speciation. In particular, it tnelanogaster (usually only one eye affected), will be useful to determine whether the genetic unequal wing lengths, broken or incomplete wing basis of developmental anomalies more closely veins, twisted abdomen, and missing or reduced resembles the basis of hybrid inviability/sterility thoracic bristles. The first three anomalies were or that of normal morphological differences particularly common. Anomalies only appeared between species. We know that the former when D. virilis females were crossed to D. lummei phenomena affect hybrid males more than females males; the reciprocal cross yielded normal pro- (Haldane's rule), involve a large effect of the X geny. This result was previously reported by chromosome (Coyne and Orr, 1989), and often Sokolov (1948, 1959) (although he misidentified show maternal effects (Orr, 1989). The genes D. lummei as "D. littoralis" (Throckmorton, underlying morphological differences between 1982)). As the D. lummei strains that Sokolov species, however, do not map disproportionately found to produce the most frequent anomalies to the X (see Coyne and Orr, 1989), and do not have been lost, little additional work on these seem to involve frequent maternal effects. As anomalies has been undertaken (however, as this Coyne and Orr (1989) note, certain explanations paper goes to press, an abstract by Heikkinen and of these different patterns predict that morpho- Lumme (1989) confirms the non-reciprocal nature logical/developmental anomalies in hybrids will of these anomalies; see below). Fortunately, the behave like postzygotic isolation (e.g., obey D. lummei strain we possessed produced frequent Haldane's rule and show a large effect of the X), anomalies when hybridized with D. yin/is. Also, while other explanations predict that the "genetic fortunately, male and female hybrids between D. 256 H. ALLEN ORR virilis and D. lummei are viable and fertile, allow- autosomes. The following anomalies were scored: ing genetic analysis of the basis of these anomalies. (1) reduced eye ("eyeless"); (2) obvious wing I report the results of this analysis here. length asymmetries; (3) wing vein anomalies (usually broken or missing veins; more rarely, small extra vein-segments appeared and were MATERIALSAND METHODS included in this category). As preliminary results demonstrated that the Thefollowing D. virilis and D. lummei stocks were D. virilis cytoplasm plays a large role in the produc- used: D. yin/is Pasadena, D. yin/is white (w: 1—105 tion of anomalies, most crosses were designed to [all map positions from Alexander (1976)]), D. determine whether this effect results from a mater- virilis peach; glossy (pe: 5—203; gl: 6—1.0), D. virilis nal effect (i.e., a mother's nuclear genotype deter- varnished (va 2—231.5), D. vinilis broken; tiny mining her progeny's phenotype) or from a true bristles, gap; cardinal; peach (b 2—1880; tb 3— cytoplasmic effect (e.g., an endosymbiont or 1040, gp 3-1180; cd 4-322; pe) and D. lummei mitochondrial gene). The role of an endosymbiont Finland. A few crosses involving D. americana Red was tested by rearing flies on tetracycline, follow- Cloud, D. novamexicana San Antonio, and D. ing the protocol of Hoffman and Turelli (1988). texana Morrilton were also made. Unless otherwise indicated, all crosses were The method used to determine the genetic basis made for one week at 18°C and then transferred of the hybrid anomalies is similar to that used by to fresh vials at 22°C. Orr and Coyne (1989) to analyse the basis of hybrid sterility in the D. virilis group: D. virilis flies carry- ing morphological markers are hybridized with RESULTS wild-type D. lummei flies, and the fertile F1 hybrids are backcrossed to either parental species. By cor- Individualsfrom the pure species stocks of D. relating the presence of hybrid anomalies with virilis and D. lummei show no developmental particular markers, one can determine which anomalies (table 1). However, the D. yin/is w chromosomes play a large role in the production female x D. lummei male hybridization produces of the anomalies. Inmost cases only the X chromo- males and females who frequently suffer develop- some carried a marker, allowing one to separate mental anomalies (table 1). Hybrid females and the effects of the X from that of the unmarked males are affected at the same rate (27.8 vs. 261

Table 1Number of individuals showing various developmental anomalies in pure species, F1 hybrids, and hybrid backerosses. In this and all subsequent tables, V =D.yin/is and L =D.lummei. In a cross, the species origin of the maternal species is given first, followed by the paternal species, e.g., VL D. virilis 9 x D. lurnmei 5. (VL)L= F19 (D. virilis9 x D. Iummeid)x D. lummeid

Winglength Wing vein Genotype Eyeless asymmetry anomaly Normal Total D. virilis w 9 0 0 0 200 200 5 0 0 0 200 200 D. lummej Finland 9 0 0 0 195 195 5 0 0 0 211 211 VL 9 17 38 24 205 284 5 16 23 18 161 218 LV 9 0 1 0 327 328 5 0 0 0 325 325 (VL)L 9 0 0 13 358 371 wS 0 2 1 102 105 +5 0 1 2 152 155 HYBRID ANOMALIES 257 per cent anomalous, respectively; x2= 121,df= 3, involved: although these backcross hybrids carry P>O•75). Therefore, the hybrid anomalies do not mitochondria and any endosymbionts from D. obey Haldane's rule. yin/is on a largely D. lummei genetic background, The reciprocal cross does not produce they show a greatly reduced frequency of anomalous progeny (table 1). The difference anomalies. This result instead suggests that the between the frequency of anomalies in the two anomalies involve a maternal effect: these back- reciprocal hybridizations is highly significant (for cross hybrids show few anomalies because their females, x2= 10144,df= 3, P

Table 2Test of tetracycline treatment. Progeny from cross ofD. virilis w x D. lummei .Seetext for details

Winglength Wing vein Treatment Eyeless asymmetry anomaly Normal Total

Tetracycline 1 4 10 34 49 d 0 2 9 26 37 No tetracycline ? 2 42 6 221 271 d 1 28 6 164 199 258 H. ALLEN ORR

Table 3 Frequency of developmental anomalies among progeny of backcross females. The two classes of backcross mothers, w(LV)V and + (LV)V, differ only in their X chromosome genotype. These females were crossed to D. lummei males. The genotype of the offspring is given below that of the mother. Note that the cytoplasm is ultimately derived from D. lunimei

Mother's Winglength Wing vein genotype Eyeless asymmetry anomaly Normal Total w(LV)V 9(+) 1 7 3 228 239 d(w) 1 2 4 174 181 +9(LV)V ?(+) 2 4 3 224 233 d(w) 1 5 3 131 140 d(+) 0 3 0 88 91 of anomalous offspring (comparing daughters in early development is under the control of mater- from two genotypes of mothers, x2= 111,df= 3, nally-acting genes). These D. yin/is alleles are P>075; comparing white sons from two nearly completely recessive (Evgen'ev and genotypes of mothers, x2= 229, df=3, P> 0.50). Sidorova, 1976). These similarities suggest that the One cannot, however, rule out the possibility that hybrid developmental anomalies may result from X-linked loci far to the left of the wlocusare loss of the D. lummei microchromosome during involved: although D. yin/is and D. /ummei are development. fixed for two large, overlapping inversion differen- To test this possibility, I performed two addi- ces in the right end of the X, almost surely includ- tional experiments. First, Evgen'ev and Sidorova ing the w locus (see Gubenko and Evgen'ev, 1984), (1976) showed that elimination of the D. lummei the left ends of the X are apparently homosequen- microchromosome in D. yin/is cytoplasm is tem- tial (see Throckmorton, 1982, and references perature-sensitive: loss is far more frequent at therein). lower temperatures. I thus crossed D. yin/is w The fact that so few hybrid anomalies (4.4 per females to D. /ummei males at 18°C vs. 22°C. Low cent) appear among the progeny of these backcross temperature treatment greatly increases the females suggests that more than one maternally- frequency of developmental anomalies (table 4, acting locus from D. virilis may be involved: if pooling homogeneous female and male data, x2= only one locus were involved approximately 14 11084,df= 1, P < 00001; because anomalies were per cent (=05x27 per cent) of these progeny so common at 18°C, producing many hybrids would show an anomaly. If, however, two genes carrying multiple anomalies, flies were simply are involved, the expected percentage drops to 7 scored as "anomalous" or "normal"). per cent (=025x27 per cent), closer to the Next, I determined whether hybrids who had observed 44 per cent. lost the D. lummei microchromosome were more The results obtained thus far—hybrid likely to show anomalies than hybrids who had anomalies are non-reciprocal, and involve a mater- not lost a microchromosome. Loss of the D. lummei nal effect; the maternally-acting genes are likely to microchromosome is easily detected among be autosomal; and the alleles from D. virilis are recessive—are strikingly similar to the genetics of microchromosome loss in D. virilis—D. lummei Table 4 Effect of temperature on frequency of hybrid develop- hybrids. Sokolov (1948, 1959) showed that the tiny mental anomalies. All flies result from the cross D. virilis D. lummei sixth chromosome is frequently elimi- w x D. lummei nated from D. virilis female x D. lummei male hybrids, but not from hybrids from the reciprocal Per cent Temperature Anomalous Normal anomalous cross. He demonstrated that this non-reciprocality results from a maternal effect, not from some 18°C independent cytoplasmic agent. Evgen'ev (1973) 101 53 656 and Evgen'ev and Sidorova (1976) further showed d 41 22 651 that loss of the microchromosome involves mater- 22°C nally-acting "mitosis genes" from D. yin/is on the 63 189 250 second and fourth chromosomes (mitotic division 48 146 247 HYBRID ANOMALIES 259 hybrids by crossing D. virilis gi/gi females to D. associated with the appearance of hybrid lummei wild-type males: loss results in flies anomalies. Loss in early development (producing expressing the recessive gi allele from D. virilis. If an extreme glossy phenotype) renders hybrids par- the microchromosome is lost in very early ticularly prone to anomalies. These results strongly cleavages, hybrids possess one or both glossy eyes; suggest that the hybrid anomalies result from elimi- loss later in development results in hybrids who nation of the D. lummei microchromosome from are mosaics showing progressively less of the hybrids. glossy phenotype (Evgen'ev and Sidorova, 1976). Analogous crosses using the D. virilis markers It is important to note that even if anomalies va (II), tb (III), cd (IV), and pe (V) showed that occur only when the D. lummei microchromosome the D. lummei major chromosomes are very rarely is lost, the observed association between the lost from hybrids (0/306 varnished mosaics, 0/35 1 appearance of the anomalies and of the glossy cardinal mosaics, 0/351 peach mosaics were phenotype will be imperfect for two reasons. First, recovered; although 3/351 possible tiny bristle one cannot detect all anomalies (many may be too mosaics were recovered, these "mosaics" arose at subtle or may be internal (Sokolov, 1959)). Second, far too low a frequency to account for the one cannot detect cases where the D. lummei sixth anomalies). The extreme rarity of major chromo- is lost late in development in small patches of some loss is not surprising as loss would probably tissue, causing localized anomalies, but is not lost be lethal except in very small patches of tissue. in the eye tissue. The first "error" will result in To determine if anomalies arise when D. virilis flies showing the glossy phenotype but no hybridizes with other species in the virilis group, anomalies, while the second "error" will result in I crossed D. virilis females to D. novamexicana, flies showing no glossy, but suffering from slight D. americana, and D. texana males. As table 5 anomalies. shows, less than 4 per cent of D. virilis—D. Control crosses show that microchromosome novamexicana hybrids show any discernible loss is very rare within the species D. virilis (table anomaly. All these anomalies were very slight, 5, top). However, in the D. virilis pe; gi female x usually involving subtle disturbances in wing vena- D. lummei male hybridization, two-thirds of the tion. Loss of the D. novamexicana microchromo- hybrids showed loss of the D. lummei micro- some is also fairly rare (<3 per cent); loss never chromosome (table 5). Flies with anomalies occurred early enough in development to produce showed microchromosome loss far more often than an entirely glossy eye. Anomalous flies are sig- did non-anomalous flies (tableS; x2= 3409,df= 2, nificantly more likely than normal flies to be glossy P<0.0001). Indeed, a third of all anomalous flies mosaics (x2withcontinuity correction= 592, df= showed an extreme ("whole-eye")glossy 1, P<0.02), although the anomalies and mosaic- phenotype, and half were glossy mosaics, while ism are too rare to allow much confidence in any only 17 per cent showed no loss of the D. lummei statistical association. It is interesting, however, sixth. Among flies showing no anomalies, only 9 that in a hybridization in which microchromosome per cent showed an extreme glossy, while 49 per loss is rare and occurs late in development, cent were glossy mosaics, and 41 per cent showed developmental anomalies are also rare and, when no loss of the sixth. Thus loss of the D. lummei they occur, are relatively subtle. Anomalies were microchromosome in development is strongly extremely rare in the D. virilis x D. americana and

Table 5 Frequency of loss of microchromosome among anomalous vs. normal-appearing individuals in various crosses. Loss of microchromosome is indicated by appearance of glossy phenotype among hybrids

+-eye gl mosaic gi whole eye

D. virilis pe; gi 9 x D. virilis Pasadena Anomalous 0 0 0 Normal 154 0 1 D. virilis pe; gI 9 x D. lummei Finland Anomalous 16 48 31 Normal 93 111 21 D. virilis pe; gI 9 x D. novamexicana San Antonio d Anomalous 8 2 0 Normal 242 5 0 D. virilis pe; gI 9 x D. americana Red Cloud d Anomalous 1 0 0 Normal 63 0 0 D. virilis pe; gI 9 x D. texana Morrilton Anomalous 1 0 0 Normal 165 0 0 260 H. ALLEN ORR

D. virilis x D. texana hybridizations. No glossy anomalous offspring (Evgen'ev and Sidorova, mosaics were observed. 1976)). Because these experiments employed Thus there is strong, but indirect, evidence sug- different strains, and probably different tem- gesting that anomalies result from microchromo- perature regimes, it is difficult to compare these some loss. Unfortunately, it would seem prohibi- results (i.e., as Evgen'ev and Sidorova (1976) tively difficult to obtain more direct evidence on showed, whether a chromosome appears to have this point. Although one could examine mitotic a large or smaller effect on chromosome loss preparations of anomalous vs. control normal depends on the temperature regime). It would be tissue for absence of one of the very small dot interesting to simultaneously analyze the genetic chromosomes, this approach seems unlikely to suc- basis of microchromosome loss and anomaly pro- ceed: because anomalies are usually seen in adult duction using the same strains under identical eye and wing tissues—which do not polytenize— environmental conditions. The results of this paper one has little hope of unambiguously scoring the suggest that the same chromosomes showing a presence or absence of the tiny D. lummei maternal effect on microchromosome loss early in homologue. While, in principle, molecular tests of development will show a large maternal effect on anomalous vs. normal tissue might be more likely anomaly production. to succeed, no 6-linked electrophoretic markers Loss of a homolog may be uncommon in animal are known in D. virilis; similarly, no DNA probes hybridizations: I am aware of no other cases of for 6-linked sequences are available. Moreover, chromosome elimination in the literature. It is thus such a marker or probe would be useful only if D. perhaps not surprising that the anomalies do not virilis and D. lummei showed fixed differences at obey two of the known "rules" of speciation: the the relevant locus. anomalies do not affect males more than females ("Haldane's rule"), nor involve a large effect of the X chromosome (Coyne and Orr, 1989). DISCUSSION The anomalies do, however, involve a maternal effect: maternal effects on postzygotic isolation are Itappears that developmental anomalies among quite common in Drosophila (Orr, 1989). Although D. virilis—D. lummei hybrids are caused by loss the specific mechanisms involved are usually of the D. lummei microchromosome during de- unknown (but see Kinsey [1967]), the basis of the velopment. The evidence for this is: (1) both maternal effect seems clear in this case. Mitosis in microchromosome loss and the anomalies occur early development is under maternal control; non-reciprocally (D. yin/is female x D. lummei because at least two maternally-acting "mitosis male only) and involve a maternal effect; (2) in genes" have diverged between D. yin/is and D. both cases the maternally-acting alleles from D. lummei, the late-replicating D. lunimei micro- virilis act as recessives; (3) the maternal genes chromosome is frequently eliminated during causing microchromosome loss are autosomal; the mitosis when present in cytoplasm conditioned by maternal genes causing the anomalies appear to these homozygous D. virilis alleles (Evgen'ev, be autosomal; (4) the incidence of both micro- 1973; Evgen'ev and Sidorova, 1976; Evgen'ev and chromosome elimination and production of Gubenko, 1977). Anomalies apparently arise anomalies increases with cold temperature treat- because the resulting tissues are haplo-6. It is inter- ment; (5)thereis a strong association between esting to note that most of the abnormalities microchromosome loss (as indicated by glossy observed among the D. virilis-D. /ummei hybrids phenotype) and the appearance of anomalies; (6) resemble mutations that are known on the D. virilis loss of the microchromosome early in development microchromosome or on the homologous D. is particularly strongly correlated with appearance melanogaster microchromosome (Sturtevant and of the anomalies. Novitski, 1941): eyeless (ey), cubitus interruptus Although they do not suggest that the hybrid (ci=Gap[Gp]), and abdomen rotatum (ar) (see anomalies result from loss of a microchromosome, Gubenko and Evgen'ev, 1984; Lindsley and Grell, Heikkinen and Lummei (1989) claim in their recent 1968). Although these similarities may be co- note that the anomalies involve maternally-acting incidental, this phenotypic resemblance might be genes on chromosomes 2 and 5 (no data are presen- expected if these mutants are loss-of-function ted). Loss of the D. lummei microchromosome mutations. apparently involves maternally-acting genes on It is important to note that while the proximal chromosomes 2 and 4 (mothers who are D. yin/is cause of the hybrid anomalies may be "chromo- homozygotes for either chromosome can produce somal", the ultimate cause of the anomalies is HYBRID ANOMALIES 261 nonetheless "genic". That is, chromosome loss many characters may have a common genetic results from the inability of maternally-acting cause, and a simple genetic basis. Thus the fact genes in D. virilis to interact properly with certain that D. viri!is-D. lummei hybrids show unusual dominant, zygotically-acting gene(s) in D. lummei. eye, wing length, wing vein, abdomen, and bristle Evgen'ev and Gubenko (1977) present evidence phenotypes does not demonstrate that each of suggesting that the latter factor(s) is (are) on the these characters has a different, somewhat incom- D. lummei microchromosome itself. Thus while patible, genetic basis in these closely related the manifestation of hybrid incompatibility is species. Instead, these unusual phenotypes are rather unusual (chromosome loss), the cause of likely symptoms of a single problem (micro- this breakdown is quite ordinary: a disruption chromosome loss), which almost certainly has a of normal epistatic interactions between genes simple genetic basis. (Muller, 1942a). Dobzhansky (1937) has similarly To determine whether hybrid anomalies result argued that in most (if not all) animal hybridiz- from cryptic divergence of many independent ations, the failure of chromosomes to pair properly characters under stabilizing selection or are in meiosis reflects a genic, not a chromosomal, pleiotropic effects of some single genic incompati- incompatibility. In short, one cannot attribute bility (not necessarily involving chromosome loss) unusual chromosome behaviour in hybrids— one must perform genetic analysis, e.g., hybrid whether mitotic or meiotic—to structural differen- backcross analysis. The former hypothesis allows ces in chromosomes between species, as chromo- that a particular chromosome substitution can some behaviour is under the control of genes which affect different hybrid characters differently. The may fail to properly interact in species hybrids. latter hypothesis predicts that a substitution affects Although mere speculation, maternal control all anomalies similarly as all share a common of mitosis in early development could explain the genetic cause. Unfortunately,thesetwo frequent observation of maternal effects on hybrid possibilities—with their very different evolutionary viability in Drosophila (e.g., Kaufmann, 1940): implications—have been disentangled in few, if hybrid embryonic inviability may result from a any, other animal hybridizations. breakdown in mitosis (not necessarily involving chromosome elimination). Similarly, frequent Acknowledgments I thank Kevin Matthews and Jim Shorts for maternal effects on hybrid fertility (e.g., Orr, 1989) their invaluable conversation; this work would not have been are not unexpected as the primordial germ cells possible without their Constant input and inspiration. I also are set aside early in Drosophila development and thank M. Evgen'ev for his helpful correspondence, and J. Coyne so are under strong maternal control (Mahowald for his valuable comments on this manuscript. This work was supported by training grant GM 07197 from the National et a!., 1976). It is important to note, however, that Institute of General and Medical Sciences of the National even if correct, one must explain why these mater- Institutes of Health to the University of Chicago, and by nally-acting mitosis/meiosis genes are especially National Institutes of Health grant GM 38462 to J. Coyne. likely to diverge between species, and thus be involved in postzygotic isolation. Last, these results show that some caution is needed when interpreting the evolutionary sig- nificance of unusual morphologies among the hybrids of sibling species. Anomalies in a character REFERENCES obviously show that the similar phenotypes of the ALEXANDER,M. L. 1976. The genetics of Drosophila virilis. In two species have different genetic bases, i.e., there Ashburner, M. and Novitski, E. (eds) The Genetics and has been cryptic divergence in the genes underlying Biology of Drosophila, vol. ic, Academic Press, Inc., this character. Similarly, anomalies in several London. characters among hybrids (e.g., missing bristles, COYNE, .1. A. AND ORR, H. A. 1989. Two rules of speciation. In inD. Otte, D. and Endler, J. A. (eds) Speciation and its consequen- heavier trident, and eye-reduction ces, Sinauer Associates, Sunderland, MA, pp. 180—207. metanogaster-D. simulans partial hybrids) are DOBZHANSKY, T. 1937. Genetics and the Origin of Species. usually taken as evidence that there has been exten- Columbia Univ. Press, New York. sive genetic divergence (e.g., Muller, 1942b), i.e., EVGEN'EV, M. B. 1973. Genetic regulation of mitosis in inter- so many gene substitutions have occurred between specific hybrids of Drosophila. I. Maternal effect on chromosome segregation and elimination. Genetica, 9, 92- these sibling species that many different characters 99. are affected among hybrids. EVGEN'EV,M. B. AND SIDOROVA, N. V. 1976. Genetic regulation However, as the present results show, an of chromosome behavior in interspecific hybrids of alternative explanation is possible: disturbances in Drosophila. Theor. App!. Gen., 48, 55-61. 262 H. ALLEN ORR

EVGEN'EV, M. B. ANDGUBENKO,1. S. 1977. Genetic regulation MULLER, H. .i. 1942b. Recessive genes causing interspecific of the replication pattern of polytene chromosomes in sterilityand other disarmonies between Drosophila interspecific hybrids of Drosophila. Chromosoma, 63, 89— melanogaster and simulans. Genetics, 27,157. 100. ORR,H. A. 1989. Genetics of sterility in hybrids between two GUBENKO, 1. S. AND EVGEN'EV, M. B. 1984. Cytological and subspecies of Drosophila. Evolution, 43, 180-189. linkagemaps of Drosophilavirilis chromosomes.Genetica, ORR, H. A. AND COYNE, J. A. 1989. The genetics of postzygotic 65, 127—139. isolation in the Drosophila virilis group. Genetics, 121, HE!KKINEN,E. AND LUMME, J. 1989.Maternally determined 527—537. eye syndrome in interspecific hybrids. EuropeanDrosophila SOKOLOV,N. N. 1948. Elimination of chromosomes ininter- Research Conference (Abstracts), 11, 22. specific hybrids of Drosophila and the problems of distant HOFFMAN, A. A. AND TURELLI, M. 1988. Unidirectional incom- hybrids. DokladiAcademii Nauk, 59, 163-166 (In Russian). patibility in Drosophila simulans: inheritance, geographic sOKOLOv, N. N. 1959. The interaction of nucleus and cytoplasm variation and fitness effects. Genetics, 119, 435—444. in distant hybrids. Moscow: Izdatelstvo Academii Nauk, KAUFMAN N, B. p 1940. The nature of hybrid sterility-abnormal 1-148 (In Russian). development in eggs of hybrids between Drosophila STURTEVANT, A. H. 1920. Genetic studies on Drosophila miranda and Drosophila pseudoobscura. J. Morphol., 66, simulans.I. Introduction. Hybrids with Drosophila 197—213. melanogaster. Genetics, 5, 488—500. KINSEY, J. D. 1967. Studies on an embryonic lethal hybrid in STURTEVANT, A. H. 1929. The Genetics of Drosophila simulans. Drosophila. I Embryo!. Exp. Morphof, 1 7 405-423. Carnegie Inst. Wash. Publ. 399, pp. 1-62. LINDSLEY, D. L. AND GRELL, E. H. 1968. Genetic Variations of STURTEVANT, A. H. AND NOVITSKI, E. 1941. The homologies Drosophila melanogaster. Carnegie InSL. Wash.Publ. 627. of the chromosome elements in the genus Drosophila. MAHOWALD,A. P.,ILLMENSEE,K. AND TURNER, F. R. 1976. Genetics, 26, 517—541. Interspecific transplantation of polar plasm between THROCKMORTON,L. H. 1982.Thevirilis species group. In Drosophila embryos.Journalof Cell Biology, 70, 358-373. Ashburner, M., Carson, H. L. and Thompson, J. N. Jr. MULLER,H. .i. 1942a. Isolating mechanisms, evolution and (eds)TheGenetics and Biology of Drosophila, vol.3b, temperature. Biol. Symposia, 6, 71—125. AcademicPress, London, pp. 227-296.