Large-Scale Selective Sweep among Segregation Distorter Chromosomes in African Populations of Drosophila melanogaster

Segregation Distorter (SD) is a selfish, coadapted gene complex on chromosome 2 of Drosophila melanogaster that strongly distorts Mendelian transmission; heterozygous SD/SD+ males sire almost exclusively SD-bearing progeny. Fifty years of genetic, molecular, and theory work have made SD one of the best-characterized meiotic drive systems, but surprisingly the details of its evolutionary origins and population dynamics remain unclear. Earlier analyses suggested that the SD system arose recently in the Mediterranean basin and then spread to a low, stable equilibrium frequency (1–5%) in most natural populations worldwide. In this report, we show, first, that SD chromosomes occur in populations in sub-Saharan Africa, the ancestral range of D. melanogaster, at a similarly low frequency (∼2%), providing evidence for the robustness of its equilibrium frequency but raising doubts about the Mediterranean-origins hypothesis. Second, our genetic analyses reveal two kinds of SD chromosomes in Africa: inversion-free SD chromosomes with little or no transmission advantage; and an African-endemic inversion-bearing SD chromosome, SD-Mal, with a perfect transmission advantage. Third, our population genetic analyses show that SD-Mal chromosomes swept across the African continent very recently, causing linkage disequilibrium and an absence of variability over 39% of the length of the second chromosome. Thus, despite a seemingly stable equilibrium frequency, SD chromosomes continue to evolve, to compete with one another, or evade suppressors in the genome

CHROMOSOMAL CONTROL OF FERTILITY IN <i>DROSOPHILA MELANOGASTER</i>. I. RESCUE OF <i>T</i>(<i>Y;A</i>)/<i>bb</i> <i>l</i>-158 MALE STERILITY BY CHROMOSOME REARRANGEMENT

ABSTRACT Many translocations between the Y chromosome and a major autosome have no effect on the fertility of Drosophila melanogaster males. However, when such translocation-bearing males also carry an X chromosome deficient for a large portion of the centric heterochromatin, they are generally sterile. This has been interpreted to be the result of an interaction between the deficiency and the subterminally capped autosome. Using this observation as a starting point, we have developed a selection scheme for radiation-induced translocation resealings that depends on the prediction that fertility in the presence of such a deficient X is restored whenever the displaced autosomal tip is brought back in association with an autosomal centromere. The observation and the prediction form the basis for what is referred to as the autosomal continuity model for male fertility.—Such a mutagenesis scheme offers several advantages. (1) It is efficient, producing upward of 1% resealings in some cases. (2) It is simple; since fertility is the basis for the selective screen, many males can be tested in a single vial. (3) It can be used to simultaneously generate both duplications and deficiencies specific for chromosomal material adjacent to the original translocation breakpoints. (4) The target for mutagenesis can be mature sperm.—Analysis of the pattern of male-fertile rearrangements obtained from several translocation lines using this protocol indicates that continuity of the autosomal tips and their centromeres is neither a necessary nor sufficient condition for male fertility in the presence of a bobbed-deficient X. Thus, the simple autosomal continuity model is not adequate to explain this complicated mechanism of chromosomal control of fertility and will have to be revised accordingly. Potential future lines of inquiry toward this goal are discussed.</jats:p

EXPERIMENTAL POPULATION GENETICS OF MEIOTIC DRIVE SYSTEMS I. PSEUDO-<i>Y</i> CHROMOSOMAL DRIVE AS A MEANS OF ELIMINATING CAGE POPULATIONS OF <i>DROSOPHILA MELANOGASTER</i>

ABSTRACT The experimental population genetics of Y-chromosome drive in Drosophila melanogaster is approximated by studying the behavior of T(Y;2),SD lines. These exhibit "pseudo-Y" drive through the effective coupling of the Y chromosome to the second chromosome meiotic drive locus, Segregation distorter (SD). T(Y;2),SD males consequently produce only male offspring. When such lines are allowed to compete against structurally normal SD  + flies in population cages, T(Y;2),SD males increase in frequency according to the dynamics of a simple haploid selection model until the cage population is eliminated as a result of a deficiency in the number of adult females. Cage population extinction generally occurs within about seven generations.—Several conclusions can be drawn from these competition cage studies: (1) Fitness estimates for the T(Y;2),SD lines (relative to SD  +) are generally in the range of 2–4, and these values are corroborated by independent estimates derived from studies of migration-selection equilibrium. (2) Fitness estimates are unaffected by cage replication, sample time, or the starting frequency of T(Y;2),SD males, indicating that data from diverse cages can be legitimately pooled to give an overall fitness estimate. (3) Partitioning of the T(Y;2),SD fitnesses into components of viability, fertility, and frequency of alternate segregation (Y + SD from X + SD  +) suggests that most of the T(Y;2),SD advantage derives from the latter two components. Improvements in the system might involve increasing both the viability and the alternate segregation to increase the total fitness. While pseudo-Y drive operates quite effectively against laboratory stocks, it is less successful in eliminating wild-type populations which are already segregating for suppressors of SD action. This observation suggests that further studies into the origin and rate of accumulation of suppressors of meiotic drive are needed before an overall assessment can be made of the potential of Y-chromosome drive as a tool for population control.</jats:p

EXPERIMENTAL POPULATION GENETICS OF MEIOTIC DRIVE SYSTEMS II. ACCUMULATION OF GENETIC MODIFIERS OF SEGREGATION DISTORTER (<i>SD</i>) IN LABORATORY POPULATIONS

ABSTRACT The accumulation of modifiers of the meiotic-drive locus Segregation Distorter (SD) in Drosophila melanogaster was monitored by measuring the changes in the mean and variance of drive strength (in terms of "make" value) that occur in laboratory populations when SD and SD+ chromosomes are in direct competition. The particular SD lines used are T(Y;2),SD translocations showing pseudo-Y drive. Four sets of population cages were analyzed. Two sets were monitored for changes in SD fitness and drive strength (presumed to be positively correlated) and analyzed for the presence of autosomal dominant or X-linked modifiers after long periods of time. The remaining two sets were made up of cages either made isogenic or variable for background genetic material, and these were used to test whether the rate of accumulation of modifiers was dependent on initial genetic variability.—Contrary to previous studies in which most suppression of SD action could apparently be attributed to a few dominantly acting modifiers of large effect, the conclusion here is that laboratory populations that are initially free of such major dominant loci evolve to suppress SD action by accumulating polygenic, recessive modifiers, each of small effect, and that much of the required genetic variability can be generated de novo by mutation. Possible explanations for these seemingly incompatible results and the evolutionary implications for SD are considered.</jats:p

EXPERIMENTAL POPULATION GENETICS OF MEIOTIC DRIVE SYSTEMS. III. NEUTRALIZATION OF SEX-RATIO DISTORTION IN DROSOPHILA THROUGH SEX-CHROMOSOME ANEUPLOIDY

ABSTRACT Laboratory populations of Drosophila melanogaster were challenged by pseudo-Y drive, which mimics true Y-chromosome meiotic drive through the incorporation of Segregation Distorter (SD) in a T(Y;2) complex. This causes extreme sex-ratio distrotion and can ultimately lead to population extinction. Populations normally respond by the gradual accumulation of drive suppressors, and this reduction in strength of distortion allows the sex ratio to move closer to the optimal value of 1:1. One population monitored, however, was rapidly able to neutralize the effects of sex-ratio distortion by the accumulation of sex-chromosome aneuploids (XXY, XYY). This apparently occurs because XX-bearing eggs, produced in relatively high numbers (~4%) by XXY genotypes, become the main population source of females under strong Y-chromosome drive. Computer simulation for a discrete generation model incorporating random mating with differences in fitness and segregation permits several predictions that can be compared to the data. First, sex-chromosome aneuploids should rapidly attain equilibrium, while stabilizing the population at ~60% males. This sex ratio should be roughly independent of the strength of the meiotic drive. Moreover, conditions favoring the accumulation of drive suppressors (e.g., weak distortion, slow population extinction) are insufficient for maintaining aneuploidy, while conditions favoring aneuploidy (e.g., strong distortion, low production of females) lead to population extinction before drive suppressors can accumulate. Thus, the different mechanisms for neutralizing sex-ratio distortion are complementary. In addition, Y drive and sex-chromosome aneuploidy are potentially co-adaptive, since under some conditions neither will survive alone. Finally, these results suggest the possibility that genetic variants promoting sex-chromosome nondisjunction may have a selective advantage in natural populations faced with sex-ratio distortion.</jats:p