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“Sex Ratio” Meiotic Drive in Drosophila Testacea

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“Sex Ratio” Meiotic Drive in Drosophila Testacea Copyright Q 1990 by the Genetics Society of America “Sex Ratio” Meiotic Drive in Drosophila 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 mushrooms, 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 driven much 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 STIST 2o 1 w 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: Flies 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 Agaricus 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 the frequency 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).
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