ORIGINAL ARTICLE
doi:10.1111/j.1558-5646.2011.01497.x
LOCAL SELECTION UNDERLIES THE GEOGRAPHIC DISTRIBUTION OF SEX-RATIO DRIVE IN DROSOPHILA NEOTESTACEA
Kelly A. Dyer1,2 1Department of Genetics, University of Georgia, Athens, Georgia 30602 2E-mail: [email protected]
Received August 17, 2011 Accepted October 2, 2011
“Selfish” genetic elements promote their own transmission to the next generation, often at a cost to the host individual. A sex-ratio (SR) driving X chromosome prevents the maturation of Y-bearing sperm, and as a result is transmitted to 100% of the offspring, all of which are female. Because the spread of a SR chromosome can result in a female-biased population sex ratio, the ecological and evolutionary consequences of harboring this selfish element can be severe. In this study, we show that the prevalence of SR drive in Drosophila neotestacea varies between 0% and 30% among populations, and is common in the south whereas rare in the north. The prevalence of SR is not associated with the presence of suppressors of drive, geographic distance, or genetic distance based on autosomal microsatellite loci. Instead, our results indicate that ecological selection on SR drive varies among populations, as the prevalence of SR is highly correlated with climatic factors, with the severity of winter the best determinant of SR frequency. Thus, ecological and demographic factors may have significant consequences for the short and long term evolutionary dynamics of selfish elements and the manner with which they coevolve with the rest of the genome.
KEY WORDS: Genetic conflict, meiotic drive, X chromosome drive.
Some genes violate the fundamental genetic law of equal seg- In addition to these population-level effects, the presence of regation to increase their own transmission to the next genera- a sex ratio distorter can create intense conflict among elements of tion (Werren et al. 1988). When a heterogametic male carries an the host genome over the offspring sex ratio (reviewed in Burt and X chromosome that harbors such a driving gene, it causes the Trivers 2006). Because males have a higher mean fitness when Y-bearing sperm fail to develop and thus the male sires only a population is nonadaptively female biased, selection favors au- daughters (reviewed in Jaenike 2001). Theory predicts that if this tosomal and Y-linked suppressors of X chromosome drive that selfish sex-ratio (SR) element goes unchecked by selection, it will restore the production of sons (Hamilton 1967). The driving X, spread rapidly through a population (Hamilton 1967). The conse- in turn, may evolve modifying alleles that restore drive, and the quence of harboring a sex ratio distorting element can be severe for following intragenomic dynamics may resemble a coevolutionary the host population, and may include changes in the strength and “arms race,” with subsequent periods of drive polymorphism and direction of sexual selection (Emlen and Orin 1977), the popula- apparent loss as the drive system accumulates modifiers and sup- tion growth rate, and the effective population size (Charlesworth pressors (Hurst et al. 1996; Jaenike 1999). Eventually, the drive and Hartl 1978). If the population becomes severely female bi- system may become genetically complicated, with the accumula- ased, a sex ratio distorting element may even cause extinction of tion of multiple X-linked driving genes and autosomal and/or Y the host population due to a lack of males (Hamilton 1967; Hatcher suppressors of drive. Recent work in autosomal and sex ratio drive et al. 1999). systems, as well in systems where the sex ratio distorting element