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A Genome-Wide Survey of Hybrid Incompatibility Factors by the Introgression of Marked Segments of Drosophila Mauritiana Chromosomes Into Drosophila Simulans

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A Genome-Wide Survey of Hybrid Incompatibility Factors by the Introgression of Marked Segments of Drosophila Mauritiana Chromosomes Into Drosophila Simulans Copyright Q 1996 by the Genetics Society of America A Genome-Wide Survey of Hybrid Incompatibility Factors by the Introgression of Marked Segments of Drosophila mauritiana Chromosomes into Drosophila simulans John R. True,* Bruce S. Weirt and Cathy C. Laurie” *Department of Zoology, Duke University, Durham, North Carolina 27708 and tDepartrnent of Statistics, North Carolina State University, Raleigh, North Carolina 27695 Manuscript received August 31, 1995 Accepted for publication November 29, 1995 ABSTRACT In hybrids between Drosophila simulans and D. mauritiana, males are sterile and females are fertile, in compliance with HALDANE’S rule. The geneticbasis of this phenomenon was investigated by introgression of segments of the mauritiana genome into a simulans background. A total of 87 positions throughout the mauritiana genome were marked with P‘lement insertions and replicate introgressionswere made by repeated backcrossing to simulans for 15 generations. The fraction of hemizgyous X chromosomal introgressions that aremale sterile is -50% greater than the fractionof homozygous autosomal segments. This result suggests that male sterility factors have evolvedat a higher rate on the X, but chromosomal differences in segment length cannot be ruled out. The fractionof homozygous autosomal introgressions that are male sterile is several times greater than the fraction that are either female sterile or inviable. This observation strongly indicates that male sterility factors have evolved more rapidly than either female sterility or inviability factors. These results, combined with previous work on these and other species, suggest that HALDANE’S rule has at least two causes: recessivity of incompatibility factors and differential accumulation of sterility factors affecting males and females. NE of the most general and striking patterns in hybrids have different genotypes (due to heteroga- 0 evolutionary biology is known as HALDANE’S rule, mety) or whether it reflects a difference in the rates which describes the results of interspecific crosses: of accumulation of male us. female incompatibility whenever hybrids of just onesex are inviable or sterile, factors. it is nearly always the heterogametic sex (HALDANE 3. In Drosophila and mammals, there are many more 1922). This rule applies very well to a great diversity of hybridizations that follow HALDANE’S rule forsterility different organisms, including insects and mammals (in thanfor inviability (Wu and DAVIS 1993), which which males are heterogametic) aswell as birds and raises the question of whether male sterility factors lepidopterans(in which females areheterogametic) accumulate morerapidly during evolution than invi- (COWE and ORR1989a; WU and DAVIS1993). In recent ability factors. years, several other patterns have been detected in the 4. In lepidopterans and birds, the numberof hybridiza- descriptive data onhybrid incompatibilities, which have tions that follow HALDANE’S rule for sterility (36 and stimulated theoretical work and raised important ques- 21, respectively) is similar to the number that follow tions about the evolution of postzygoticisolating mech- the rule for inviability (15 and 30, respectively) (WU anisms: and DAVIS 1993). This observation, in contrast to that in the preceding paragraph, raises the question In Drosophila, reciprocal crosses often producester- of whether the relative rates of evolution of male ile males in one direction, but not the other (BOCK sterility, female sterility and inviability factors differ 1984).This asymmetryis expected under simple between organisms with heterogametic males or fe- models for theevolution of genetic incompatibilities males. (Wu and BECKENBACH1983; TURELLIand ORR 5. There appear to be more exceptions to HALDANE’S 1995). rule for inviability in Drosophila than in birds or In Drosophila, hybridizations in which females are lepidopterans (WUand DAVIS1993). One hypothesis sterile involve more distantly related species than to explain this effect is that maternal us. zygotic in- those in which only males are sterile (COYNEand compatibilities are expected to occurmore fre- ORR1989b). An important question is whether this quently when the motheris homogametic than when observation is due to the fact that male and female she is heterogametic (Wu and DAVIS 1993). Excep- tions to HALDANE’S rule may also depend on the Curresponding author: Cathy C. Laurie, DCMB/Zoology, Box 91000, Duke University, Durham, NC 27708. number of incompatibility factors and their degree E-mail: [email protected] of dominance (TURELLIand ORR1995). Genetics 142 819-837 (March, 1996) 820 J. R. True, B. S. Weir and C. C. Laurie It is clear that resolution of the issues raised by the specific gene interactions are particularly deleterious descriptive data on hybridization patterns can be re- when at least one member of the gene pair is hemizy- solvedonly by careful genetic analyses. Fortunately, gous or homozygous for species A and the othermem- because at least one sex is viable and fertile in many ber is heterozygous or homozygous for species B. interspecific crosses, the genetic basis of hybrid incom- Recently, MULLER’Sideas about heterospecific gene patibility is amenable to direct experimental analysis interactions have been formalized and expanded into and many such studies have been done with Drosophila a “dominance theory” of HALDANE’Srule (Om 1993a; species in the past several years (see COYNEand Om TURELLIand Om 1995). This theory explicitly deals 1989a; COYNE 1992;WU and DAVIS1993; Wu and PALO- with an important factor that was not considered by POLI 1994). MULLER,which is that hybrid females with two Xchro- The most common experimental design in genetic mosomes have, on the average, twice as many potential studies of male hybrid sterility in Drosophila is the stan- X-autosome incompatibilities as XY hybrid males. dard backcrossanalysis. In this design, females with Therefore, if heterozygous gene pairs have some degree markers on each chromosome arecrossed to unmarked of deleterious interaction, it is possible for hybrid fe- males of another species, the heterozygous hybrid fe- males to have a lower fitness than hybrid males even if males are backcrossed to males of the multiply marked hemizygous-heterozygous interactions are worse than species, and progeny genotypes are analyzed for differ- heterozygous-heterozygous ones. The model of hybrid ences in sterility level. Several different pairs of Dro- fitness developed by TURELLIand Om (1995) shows sophila species have been analyzed in this way (reviewed that X-linked incompatibility factors have greater cumu- by COYNEand ORR 1989a).Segregation of the X chro- lative effects in the hemizygous XY male than in the mosome marker typically has a much larger effect on heterozygous XXfemale onlyif they are partially or fully male fertility than segregation of any of the autosomal recessive. markers, although each autosomal marker usually has A potentially powerful test of the X-autosome imbal- a significant effect. In some cases the Y chromosome anceand dominance theories is to comparethe fit- plays an importantrole (VIGNEAULTand ZOUROS1986), nesses ofhybrid males and females that have equivalent while in others it has no apparent effect (JOHNSON et genotypes in terms of X-autosome imbalance. COYNE al. 1992; ZEN(; and SINCH1993). (1985) used an attached-X stock of D. simulans to pro- The causes of the large effect of the Xchromosome duce unbalanced hybrid females that are homozygous in backcross analyses withDrosophila species has gener- for the simulans X and heterozygous for simulans and ated much discussion in the literature, but the issue is maum‘tiana (or sechellia) autosomes. In crosses to both still not resolved. One possibility is that the Xcontains maum‘liana and sechellia, the unbalanced females are fer- a disproportionate number of sterility factors, which tile, whereas the genotypically similar males (hemizy- may be due to a higher Xchromosomesubstitution rate gous for the simulans X and heterozygous for the au- in the pure species populations (CHARLESWORTHet al. tosomes) are sterile. COYNEargued that if ordinary 1987; COYNEand Om 1989a). Anotherpossibility is that hybrid females are fertile (while males are sterile) be- the large Xeffect is due to dominance because, in the cause of the recessiveness of X-linked incompatibility backcross design, hemizygous X effects are compared factors, then the unbalanced females should be sterile. with heterozygous autosomal effects (COYNE and Om However, this interpretation is complicated by the fact 1989a; Wu and PALOPOLI1994). If the autosomal genes that male and female fertility are controlled by largely that cause hybrid sterility are not fully dominant, the different sets of genes (LINDSLEYand TOKUYASU1980), hemizygous X chromosome will have a greater effect which mayevolve at different rates (Om 199313; WU than a heterozygous autosome, even though it may con- and DAVIS1993). Thesimulans Xchromosome may not tain the same number and type of sterility factors. contain incompatibility factors that arecapable of caus- The relative effects of hemizygous and heterozygous ing hybrid female sterility even when homozygous. chromosomes in hybrids is a central issue in the X- Therefore, these results do not provide a strong argu- autosome imbalance hypothesis proposed by MULLER ment against the notion that sterility factors are gener- (1940) to explain HALDANE’S rule. Homogametic hy- ally recessive. brids have one complete set of chromosomes
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