Copyright Q 1990 by the Genetics Society of America

“Sex Ratio” Meiotic Drive in testacea

Avis C. James and John Jaenike Department of Biology, University of Rochester, Rochester,New York 14627 Manuscript receivedMay 2 1, 1990 Accepted for publication August 1, 1990

ABSTRACT We document the occurrence of “sex ratio” meiotic drive in natural populations of Drosophila testacea. “Sex ratio” males sire >95% female offspring. Genetic analysis reveals that this effect is due to a meiotically driven X chromosome, as in other species of Drosophila in which “sex ratio” has been found. In contrast to other drosophilids, the “sex ratio” and standard chromosomes of D.testacea do not differ in gene arrangement,implying that the effect may be due to a single genetic factor in this species. In all likelihood, the “sex ratio” condition has evolved independently in D. testacea and in the Drosophila obscura species group, as the loci responsible for the effect occur on different chromosomal elements. An important ecological consequence of “sex ratio” is that natural populations of D. testacea exhibit a strong female bias. Because D. testacea mates, oviposits, and feeds as adults and larvae on , this species providesan excellent opportunityto study the selective factors innature that prevent “sex ratio” chromosomes from increasing tofixation and causingthe extinction of the species.

EIOTICALLYdriven sex chromosomesnot and DOBZHANSKY1936) and Drosophilasubobscura M only violate Mendelianrules of segregation, (JUNGEN 1967). They have also been found outside but because of their influence on the relative propor- the obscura group in Drosophilaparamelanica tions of males and females in a population, they can (STALKER196 1) and Drosophilamediopunctata (DE affectrates of populationgrowth, the intensity of CARVALHO,PEIXOTO and KLACZKO1989). sexual selection, and effective population sizes. Fur- Previous efforts to understand the selective factors thermore, unrestrained meiotic drive of either the X that prevent spreadof SR chromosomes have focused or the Y can quickly result in failure to produce any on D. pseudoobscura (e.g., WALLACE1948; ANDERSON individuals of one sex, thus leading to the extinction 1968; POLICANSKY1974, 1979; BECKENBACH1978, of a population or species (HAMILTON 1967). 1983; CURTSINGERand FELDMAN1980; Wu 1983a,b). Wuand HAMMER (1990) argue on conceptual Unfortunately, because the ecology of this species is grounds that X chromosomes should be meiotically poorly known, most studies on the fitness effects of drivenmuch more commonly thanautosomal loci, SR have been limited to laboratory populations, and because such distortion results from suppression of there is no assurance that selective differences(or recombination between a locus causing meiotic drive similarities) found in the lab will apply to individuals on one chromosome and a target heterochromatic in natural populations. As BECKENBACH(1 983, p. 647) region on anotherchromosome whose transmission is concludes, “If we wish to discover how SR is main- thereby suppressed. With no recombination between tained in nature, nature is where we should look.” the X and Y chromosomes and the extensive hetero- None of the other Drosophila species in which “sex chromatization of the Y, there may be many oppor- ratio” has been discovered is obviously superior to D. tunities for such interaction. If this hypothesis is cor- pseudoobscura for ecological study in the wild. rect, sex ratio meiotic drive may turn out tobe more Here we report the occurrence of “sex ratio” in than a mere evolutionary curiosity, representinga Drosophilatestacea, a species eminentlysuitable for perpetual threat to the persistenceof a species. field studies of differential fitness. This Holarctic spe- Sex ratio meiotic drive is best known in a number cies is common in temperate and boreal forests, where of species of Drosophila. Male carriers of a driven X all stages of its life center around fleshy mushrooms. chromosome, designated SR for “sex ratio,” transmit Adults feed, mate andoviposit on these fungi, which only X-bearing sperm and thus sire only daughters. also serve as larval food. Among the ecological factors Such chromosomes were first discovered in several already known to have importanteffects on their members of the Drosophila obscura species group, in- populations are larval competition for food (GRIMALDI cluding Drosophilaaffinis (MORGAN, BRIDGESand and JAENIKE 1984) and parasitism by nematodes (J. STWRTEVANT 1925),D. obscura (GERSHENSON1928), JAENIKE, unpublished results). Drosophilapseudoobscura, Drosophila persimilis, Dro- As we will show, “sex ratio” in D. testacea is unique sophila athabasca and Drosophila azteca (STURTEVANT among known casesin Drosophila in that it is not

Genetics 146 651-656 (November, 1990) 652 A. C. James and J. Jaenike

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0.0 0.2 0.1 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 Fraction of female offspring 50%femald offspring. discard FIGURE1 .-Offspring sex ratios of male D. testacea, which were captured as adults at Mendon Ponds Park, New York, in June 1990. Each male was mated to a single female and the sex of all progeny was determined. Only families in which at least 20 offspring were E produced are included. associated with chromosomal inversions. This suggests that the“sex ratio” effect may be produced by a single locus in this species, thus making it a good candidate for molecular genetic analysis of the phenomenon. It also implies that the meiotic drive locus, rather than an entire inversion, is the unit of selection in natural cross 10 males individually to STET females and detarmne populations. Finally, we present evidence that the“sex offspring sex ratio ratio” factor does affect population-level sex ratios. FIGURE2.-Crossing scheme fordetermination of inheritance of “sex ratio.”Genotypes illustrated assume that “sex ratio” isX-linked. MATERIALSAND METHODS were mated to laboratory reared virgin females. Characterization of “sex ratio”: “Sex ratio” was initially Inheritance of “sex ratio”: The following mating scheme detected in D. testacea by the occurrence of all-female prog- was carried out to distinguish among the X chromosome, eny in crosses between wild-caught males and virgin females the Y, the autosomes, and cytoplasmic inheritance as causes in studiesof female mate choice (JAENIKE 1988).Initial of the “sex ratio” effect (Figure 2). “Sex ratio” males from crosses of individual males to females of several different natural populations were crossed to females of a non-sex strains revealed that “sex ratio” is clearly a property of the ratio laboratory strain (ST/ST). The SRIST offspring (all male and not the female of a cross. To characterize the females) from such crosses were mated to ST males, and the expression of “sex ratio,” males known to begenetically “sex resulting sons were crossed to ST/ST females. Only families ratio” (SR)or standard (ST) were mated to ST/ST females yielding all-female progeny from this last cross were tested and offspring sex ratios determined. further. Females from such families were crossed to ST The possibility of meiotic drive in heterozygous females males, and 10 male offspring from each female were mated was tested in SR/ST females, which were produced by cross- to ST/ST females in order to determine whetherthese males ing SR males to ST/ST females. The genotypes of the sons expressed “sex ratio.” The mode of inheritance of five of 29 of these heterozygous females were determined by independently derived “sex ratio” factors from two natural crossing them to virgin ST/ST females and scoring their populations (Maine and North Carolina) was determined in progeny for distorted sex ratios. this fashion. All matings consisted of one male and two The fertility ofthe occasionally produced sons of SR males virgin females. was tested in D. testacea by crossing them to ST/ST females Cytologicalanalysis: Polytenechromosomes were ex- in the laboratory and scoring for the presence of viable amined to determine if SR is associated with inversions, as offspring. it is in other species of Drosophila. Salivary glands were Occurrence of “sex ratio” in natural populations: dissected in saline solution from third instar larvae that had were collected from natural populations by sweeping over beenraised in uncrowdedconditions at 18”. They were naturally occurring mushrooms or commercial bis- fixed in 45% acetic acid for one minute and stained with porus that had been set out as bait. Such collections have 2% lacto-acetic orcein. The glands were placed in a pool of been made in New York, Maine, Pennsylvania, North Car- orcein inside an outline of wax on a slide and covered with olina, West Virginia and Virginia, representing a major a coverslip. Because chromosomes of D. testacea are prone fraction of D. teslacea’s range in eastern North America. In to ectopic pairing, separation of them without breaking was our general survey work, males are scored if they sire at achieved by gently tapping the coverslip. least 20 offspring. Males producing 290%female offspring The X chromosome, which is a rod in D. testacea (PAT- are classified as “sex ratio” (Figure 1). TERSON and STONE1952), was distinguished from the au- Temporal fluctuations in thefrequency of “sex ratio” tosomes in male larvae by its narrower width and lighter were monitored at two sites-Mendon Ponds Park, Monroe staining., Female larvae heterozygous for the SR and ST County, New York, and Loyalsocksville, Lycoming County, chromosomes were produced by mating SR males to ST/ST Pennsylvania. Collections madeat regular intervals con- females. The X was identified in females on the basis of sisted of an average of over 200 wild-caught males, which puffing and banding patternsseen in males. “Sex Ratio” in Drosophila testacea 653

0.4 1

0.0- 0.0- May June July Aug. May June July AUg. 1988 1989 1988 FIGURE4.-Temporal variation in the frequency (t. standard error) of “sex ratio” males of D. testacea at Mendon Ponds Park, New York (0)and Loyalsocksville, Pennsylvania(0).

Inheritance of “sex ratio”: Cross A (Figure 2) of SR males to ST/ST females yielded only daughters which, when crossed to ST males (cross B), produced some sons exhibiting the “sex ratio” trait(cross D) and some that had normal offspring sex ratios (cross C). The expression of “sex ratio” in this generation rules out the possibility of Y-linked inheritance, as the “sex ratio” males in cross D carry a Y chromosome from the standard stock. The passageof the “sex ratio” factors through females of a non-sex ratio stock elim- FIGURE3.-Frequency of “sex ratio” males innatural populations inates the possibility of cytoplasmic inheritance. of D. festacea. Asterisks denote localities where “sex ratio” has been found among small samples of flies. The occurrence of the “sex ratio” males from cross E eliminates the possibility that anautosomal recessive Population-level consequences of “sex ratio”: The fre- quency of “sex ratio” was determined among males of D. is the basis for this trait. If “sex ratio” is due to an testacea capturedfrom Mendon Ponds Park, Monroe autosomal recessive allele (a), cross E would yield only County, New York, in 1986 and Mt. Lake Biological Station, AA and Aa sons, none of which would be classified as Giles County, Virginia, in 1989. Simultaneously, estimates “sex ratio.” of the population-levelsex ratios were determinedby sexing If “sex ratio” is due to anautosomal dominant, then flies that emerged from naturally occurring mushrooms. one-half of the type E crosses would be expected to yield only standard males, the other half both “sex RESULTS ratio” and standard males. Infact, all families pro- Characterization of “sex ratio”: Offspring of males duced both “sex ratio” and standard males in cross E; known to be genetically “sex ratio” are 98.5%female the overall fraction of males resulting from E crosses (n= 826), whereas genetically standard males produce that were “sex ratio” was 48%, as expected if “sex 48.9% female offspring (n = 1,253). Females known ratio” is X linked. Thus, the gene orgenes responsible to be heterozygous for “sex ratio” (ie., SR/ST) pro- for the “sex ratio” trait are carried on theX chromo- duced 48% “sex ratio” sons among 265 male offspring some, with meiotic drive expressed only in male car- tested. Thus, there is no evidence of meiotic drive in riers. females. Cytological analysis: The X chromosome was iden- In other species of Drosophila, the occasional sons tified in male larvae. The terminal 10% is character- of “sex ratio” males are sterile (PEACOCK,MILKOS and ized by a lightly staining tip, followed proximally by a GOODCHILD1975). Of 68 sons of “sex ratio” fathers constriction with three bands, a puff containing two tested, not one producedviable offspring when mated lightly stainingbands, three regularly spaced dark to laboratory females. Thus, the few male offspring bands, and a second constriction. produced by “sex ratio” males are sterile. In three female larvae heterozygous for ST and SR Occurrence in natural populations: Every popu- and in which the entire X was visible, no evidence of lation sampled has been found to harbor “sex ratio” inversions was seen over the length of the X chromo- at frequencies generally around 20% (Figure 3). At some (Figure 5). The chromosome illustrated has a the Mendon Ponds Park and Loyalsocksville sites, the small region of asynapsis, proving that it is a diploid frequency of “sex ratio” fluctuated somewhat, ranging and thus a female, notone of the rare male offspring from 15% to 30% (Figure 4). The only statistically produced from “sex ratio” males. significant change in month to month frequency of Population-level effects of “sex ratio”: A signifi- “sex ratio” is between the June andJuly 1988 samples cant excess of females of D. testacea is found among at theMendon site. At the Mendon site, the frequency emergent adults bred from naturally occurringmush- of SR declined from spring until August suggesting rooms(Table 1). It is notablethat the Mt. Lake that it may undergo frequency variation on a seasonal population, in which the frequency of SR is greater, basis. produced asignificantly greater proportionof females 654 andA. C. James J. Jaenike sions on the right arm of the X chromosome (STUR- TEVANT andDORZHANSKY 1936), which is homolo- ‘4 gous to the left arm of the third chromosome in D. melanogaster (PATTERSON andSTONE 1952, Table27). As a member of the subgenus Drosophila, the X of D. testacea is in all likelihood homologous to the X of D. melanogaster (PATTERSONand STONE 1952). Thus, there may be different genetic bases to the “sex ratio” phenomenon. While the initial discoveries of“sex ratio” were FIGURE5.-Polytene X chromosome of a female SR/ST . limited to species of the D. obscura group of the The white arrow marks the chromocenter, and the black arrow marks a region of asynapsis. Note that in the region of asynapsis, subgenus Sophophora, ourdiscovery of “sex ratio” in the banding patterns show that the two chromosomes arehomose- D. testacea brings to three the number of different quential. species groups in the subgenus Drosophila in which it has been found. (We also have evidence for its exist- TABLE 1 ence in afourth species group in this subgenus- Frequencies of females and SR males in natural populations of Drosophilaquinaria of the quinaria species group. Drosophila However, we have not yet carried out genetic analyses to see if “sex ratio” is due to the X chromosome). The Mendon (I 086) Ut. Lake (I 080) great evolutionary distance between these subgenera- Species f (SR) f (females) f (SR) f (females) THROCKMORTON(1 975) suggests that they split in the D. testacea 0.23 (180)” 0.60* (465) 0.31(165) 0.67* (1,189) Oligocene-and the absence of“sex ratio” in other D. putrida(358) 0.53 (476) 0.48 species groups in the subgenus Sophophora suggest D.falleni (4,130) 0.47 (680) 0.51 that the “sex ratio”trait has arisen independently D. recens (329) 0.53 ~~ ~ several times in Drosophila. The supposition that the E Sample size in parentheses. genetic basis for “sex ratio” differs between species in * Significant excess of females (P < 0.001). theSophophora and Drosophila subgenerafurther than the Mendon population (x2= 8.14; P < 0.005). supports this hypothesis. The excess of female D. testacea can be contrasted In all other species of Drosophila in which“sex with the relative numbers of males and females of ratio” has been described, it is associated with one or other species of Drosophila emerging from the same more inversions on the X chromosome (Table 2). In mushrooms and in which there is no evidence of the D. testacea, females heterozygous for SR and ST show “sex ratio” trait.In Drosophila recens, Drosophila falleni no evidence of any inversions over the length of their and Dosophila putrida, the proportion of females was X chromosomes. Wu and BECKENBACH(1983) have not significantly greater than 50%. argued that the association of “sex ratio” with inver- sions is the result of tying together genes on the X DISCUSSION that serve to counteract the effect of evolved suppres- The expression of “sex ratio” in D. testacea is similar sors of “sex ratio” meiotic drive. Thus, association in several respects tothat seen in other species of with inversions probably means that “sex ratio” is Drosophila. It is characterized by extreme meiotic evolutionarily old. Conversely, the lack of inversions drive of the X chromosome in males, resulting in the seen in D. testacea suggests that “sex ratio” has arisen production of virtually all-female progeny. As in other relatively recently in this species. Our failure to find drosophilids, the occasional male offspring of “sex any evidence of“sex ratio” in D. putrida, the only ratio” males are invariably sterile. These sons are other member of the testacea species group, also probably XO, resultingfrom nondisjunction in the supports a relatively recent origin of “sex ratio” in D. “sex ratio” fathers, as in D. pseudoobscura (HENAHAN testacea. and COBBS1983). If so, this would support the notion The “sex ratio” polymorphism presumably results that meiotic drive results from the selective failure of from a balance between meiotic drive favoring SR and Y-bearing spermatids to differentiate into functional natural selection against carriers of SR. In species in sperm (PEACOCK,MIKLOS and GOODCHILD1975; POL- which “sex ratio” loci are tied up within inversions, it ICANSKY and ELLISON1970.). is not possible to determine if the reduced fitness of Although the X chromosome is responsible for “sex SR-carrying flies is due to the “sex ratio” loci or to ratio” in all species of Drosophila in which this effect linked alleles. In D. testacea “sex ratio” is not associated has been found, the particulargenetic element re- with inversions, suggesting that any reduced fitness of sponsible varies among species. In D.pseudoobscura SR-carriers might be apleiotropic effect of the meiotic and D. persimilis, “sex ratio” is associated with inver- drive locus. The lack ofinversions associated with “sex “Sex Ratio”in Drosophila testacea 655

TABLE 2

“Sex ratio” X chromosomes in the Drosophila

No. of inverions Subgenus Species with associated SR Reference Sophophora obscura ? GERSHENSON(1 928) pseudoobscura 3 STURTEVANTand DOBZHANSKY(1 936) persimilis 1 STURTEVANTand DOBZHANSKY(1936) subobscura 5 JUNGEN ( 1967) afinis I STURTEVANTand DOBZHANSKY(1 936) athabasca 5 MILLER (1971) azteca 3 DOBZHANSKYand SOCOLOV(1939) Drosophila paramelanica 4 STALKER(1 96 1) mediopunctata 1 DE CARVALHO,PEIXOTO and KLACZKO(1 989) testaceca 0 This study ratio” in this species makes it unlikely that polymor- quency of SR there is a significantly greater excess of phism for this trait is maintained by associative over- emergent females. In fact, the 1989 Mountain Lake dominance in females, a theoretical possibility in other population of D. testacea exhibited a 2:l ratio of fe- species (EDWARDS1961). Since single locus heterosis males to males among emergent adults. The frequen- is apparently very rare, some form of frequency-de- cies of females are not significantly different from pendent selection may beresponsible forthe “sex expected value of (p/2 + 0.5), where p is the fre- ratio”polymorphism in D. testacea. Inaddition, we quency of SR, and assuming there is no selection note that if “sex ratio” in this species is due to the against SR-carriers. However, this doesnot imply that action of a single locus, as one might conclude from there is no selection against these individuals, as sim- its lack of association with inversions, this species could ilar femalefrequencies could be produced if “sex be particularly suitable for molecular genetic analyses ratio” males suffer both reduced fertility and larval of meiotic drive. viability. Every population of D. testacea that we have sur- BRYANT,BECKENBACH and COBBS(1982) have at- veyed in eastern North America is polymorphic for temptedto relate the “sex ratio” polymorphism to “sex ratio,” with most populations having a frequency population-level sex ratios in D.pseudoobscura, using of SR of about 20% among males. Although there is the numbers of adult males and females captured at modesttemporal variation in its frequencyat the orange and grapefruit baits. However, baits may be Mendon Ponds and Loyalsocksville sites (Figure 4), moreattractive to individuals of one sex thanthe we observe no obvious geographical variation in its other (e.g., JAENIKE 1986; HOFFMANN1988), thus frequency. The ubiquitous occurrence of SR and the biasing estimates of population-level sex ratio. This is lack ofnoticeable geographic variation in its fre- perhapsthe reason that in most of the collections quency means either that thereis a great dealof gene made by BRYANT,BECKENBACH and COBBS(1982), flow among D. testacea populations or that “sex ratio” females constituted well under 50% of the captured frequencies are subject to strong balancing selection flies. Our estimates of population sex ratioswere within populations. “Sex ratio” cannot be considered based on flies bred directlyfrom natural breeding a selectively neutral trait: in the absence of selection sites and are thus not compromised by differences against carriers of SR, its frequency is expected to between males and females in their responses to bait increase very rapidly-about 3-5% pergeneration types, time of collection, weather, etc. from its current frequencies in the range of 15% to Strongly female-biased sex ratios could have a num- 30%. ber of important ecological effects on these popula- Two observations show that SR has a significant tions. If there are enough males to fertilize all of the effect on population-level sex ratios in nature (Table eggs produced by females, such populations should 1). (1) The fraction of female D. testacea emerging have a greater potential rate of population growth. from mushrooms is significantly greater than 0.5. In With all else equal, a population that is 67% female contrast, D.putrida, D.falleni and D.recens, which are shouldhave areproductive rate about one-third not polymorphic for “sex ratio,” yielded approxi- greater than one thatis 50% female. Withinterspecific mately equal numbersof males and females from field- scramblecompetition for larval foodresources, fe- collected mushrooms. (2) For two populations of D. male-biased populations of D.testacea may fare better, testacea we have data on both SR frequencies among as they are capable of laying relatively more eggs on wild-caught males and sex ratio of flies emerging from the mushrooms competed for. Thus, the greater re- mushrooms. Inthe population with ahigher fre- productive potential of such populations could result 656 A. C. James and J. Jaenike in greater equilibrium numbers. With twofemales for GRIMALDI,D., and J. JAENIKE, 1984 Competition in natural pop- everyadult male in apopulation, the intensity of ulations of mycophagous Drosophila. Ecology 65: 1 113-1 120. sexual selection may becomparatively less than in HAMILTON,W. D., 1967 Extraordinary sex ratios. Science 156 477-488. other drosophilids with population-level sex ratios HENAHAN, J., andG. COBBS,1983 Origin of X/O progeny from closer to 50:50. Finally, if the frequency of “sex ratio” crosses of sex-ratio trait males of Drosophila pseudoobscura. J. were to increase unchecked for even a few genera- Hered. 74: 145-148. tions, thefraction of males in apopulation might HOFFMANN,A. A., 1988 Early adult experience in Drosophila become so low as to render a population particularly melanogaster. J. Physiol. 34: 197-204. JAENIKE,J., 1986 Intraspecific variation for resource use in Dro- susceptible to extinction via demographic stochasticity sophila. Biol. J. Linn. SOC.27: 47-56. (WALLACE1968; GILPINand SOULE1986). JAENIKE, J., 1988 Parasitism and male mating success in Drosophila The possibility of extinction resulting from unbri- testacea. Am. Nat. 131: 774-780. dled increase of a meiotically driven X chromosome JUNGEN, H., 1967 Abnormal sex ratio, linked with inverted gene raises the question of what selective factors prevent sequence, in populations of Drosophila subobscura in Tunisia. Drosophila Inform. Serv. 42 109. the spread of such chromosomes. Because D. testacea MILLER,D. D., 1971 On the identity of the “sex ratio” X chro- spends its life around mushrooms, the relative fitness mosome of “eastern” Drosophila athabasca. Drosophila Inform. of different genotypescan be studied atall life stages Serv. 46: 95. in the wild. As aresult, it should be possible to MORGAN,T. H., C. B. BRIDGESand A. H.STURTEVANT, 1925 The determine how selection against carriers of a particu- genetics of Drosophila. Bibliogr. Genet. 2 1-262. PATTERSON,J. T., and W. S. STONE,1952 Evolution in the Genus lar chromosome prevents the extinction of this spe- Drosophila. Macmillan, New York. cies. PEACOCK,W. J., G. L. G. MIKLOSand D. J. GOODCHILD,1975 Sex We are most grateful to UZI NUR for his guidance and assistance chromosome meiotic drive systems in Drosophila melanogaster. in the cytological analysis of “sex ratio.” We thank the ERDMAN I. Abnormal spermatid development in males with a hetero- family for allowing A.C.J. to camp on their propertyin Pennsylvania chromatin deficient X chromosome (sc‘ sc’). Genetics 79: 6 13- while surveying nearby populations. We thank TIMANDERSON, 634. POLICANSKY,D., 1974 “Sex ratio,” meiotic drive, and group selec- WYATTANDERSON, UU NUR,JACK WERRENand CHUNG-IWu for comments onthe manuscript. This research was supported by tion in Drosophila pseudoobscura. Am. Nat. 108 75-90. National Science Foundation B.S.R. grants 86-05196 and 89- POLICANSKY,D., 1979 Fertility differences as a factor in the 05399 to J.J. maintenance of the “sex ratio” polymorphism in Drosophila pseudoobscura. Am. Nat. 114: 672-680. LITERATURECITED POLICANSKY,D., and J. ELLISON,1970 “Sex ratio” in Drosophila pseudoobscura: spermiogenic failure. Science 169 888-889. ANDERSON,W. W., 1968 Elimination of sex ratio X chromosome STALKER,H. D., 1961 The genetic systems modifying meiotic in experimental populations of Drosophila pseudoobscura. Dro- drive in Drosophila paramelandca. Genetics 46: 177-202. sophila Inform. Serv. 43: 100. STURTEVANT,A. H., and TH. DOBZHANSKY,1936 Geographical BECKENBACH,A. T.,1978 The “sex ratio”trait in Drosophila distribution and cytology of “sex ratio” in Drosophila pseudoob- pseudoobscura: fertility relations ofmales and meiotic drive. scura and related species. Genetics 21: 473-490. Am. Nat. 114: 97-177. THROCKMORTON,L. H., 1975 The phylogeny, ecology, and ge- BECKENBACH,A. 1983 Fitness analysis the “sex ratio” T., of poly- ography of Drosophila, pp. 421-460 in Handbook of Genetics, morphism in experimental populations of Drosophila Pseudoob- Vol. 3, edited by R. C. KING.Plenum, New York. scura. Am. Nat. 121: 630-648. WALLACE,B., 1948 Studies on “sex ratio” in Drosophila pseudoob- BRYANT,S. H., A. T. BECKENBACHand G. A. COBBS,1982 “Sex scwa. I. Selection and “sex ratio”. Evolution 2 189-21 7. ratio” trait, sex composition, and relative abundance in Dro- WALLACE,B., 1968 Topicsin Population Genetics. Norton, New sophila pseudoobscura. Evolution 36 27-34. York. CURTSINGER,J. W., and M. W. FELDMAN, 1980Experimental and Wu, C.-I., 1983a Virility deficiency andthe sex ratiotrait in theoretical analysis of the “sex-ratio” polymorphism in Drosoph- Drosophilapseudoobscura. I. Sperm displacement and sexual ila pseudoobscura. Genetics 94: 445-466. selection. Genetics 105: 651-662. DE CARVALHO,A. B., A.A. PEIXOTOand L. B. KLACZKO, Wu, C.-I., 1983b Virility deficiency and the sex ratiotrait in 1989 “Sex ratio” in Drosophilamediopunctata. Heredity 62: Drosophila pseudoobscura. 11. Multiple matings and overall viril- 425-428. ity selection. Genetics 105: 663-679. DOBZHANSKY,TH., andD. SOCOLOV,1939 Structure andvariation Wu, C.-I., and A. T. BECKENBACH,1983 Evidence for extensive of the chromosomes in Drosophila axecta. J. Hered. 30 3-19. genetic differentiation between the sex-ratio and standard ar- EDWARDS,A. W. F., I961 The population genetics of “sex ratio” rangement of Drosophila pseudoobscura and D. persimilis and in Drosophila pseudoobscura. Heredity 16 291-304. identification of hybrid sterility factors. Genetics 105: 7 1-86. GERSHENSON,S., 1928 A new sex ratio abnormality in Drosophila Wu. C.-I., and M. E. HAMMER,1990 Molecular evolution of ultra obscura. Genetics 13: 488-507. selfish genes, in Evolution at the Molecular Level, edited by R. CILPIN,M. E., and M. E. SOULE,1986 Minimumviable popula- K. SELANDER,T. WHITTAMand A. G. CLARK. Sinauer,Sun- tions: processesof species extinction, pp. 19-34, in Conservation derland, Mass. (in press). Biology: The Science of Scarcity and Diversity, edited byM. E. SOULE.Sinauer, Sunderland, Mass. Communicating editor: A. G. CLARK