Sex-ratio segregation distortion associated with reproductive isolation inDrosophila

Abstract

Sex-ratio distortion is the most common form of non-Mendelian segregation observed in natural populations. It may occur even more frequently than direct observations suggest, because the dysgenic population consequences of a biased sex ratio are expected to result in the rapid evolution of suppressors, resulting in suppressed or ''cryptic'' segregation distortion. Here we report evidence for cryptic sex-ratio distortion that was discovered by introgressing segments of the genome of Drosophila mauritiana into the genome of Drosophila simulans. The autosomal suppressor of sex-ratio distortion, which is also associated with a reduction in hybrid male fertility, has been genetically localized to a region smaller than 80-kb pairs in chromosome 3.M endelian segregation is the foundation of almost every important principle in population genetics theory. It is also widely observed. Examples of non-Mendelian segregation-also called segregation distortion or meiotic drive-though sometimes dramatic, are rare. However, the apparent nearuniversality of Mendelian segregation may be misleading. Nearly 50 years ago Sandler and Novitski (1) pointed out that new mutant alleles showing segregation distortion might occur frequently within populations, but be concealed by the fixation of suppressor mutations soon after the distorters arise. In this case, the infrequency of non-Mendelian segregation in natural populations would reflect only its transience as an evolutionary phenomenon, not its rarity as a biological phenomenon.A newly arisen segregation distorter can be fixed, lost, or become a stable polymorphism. Stable polymorphism may occur when the advantage of favored gametic transmission is balanced by lower fitness (2, 3) or suppressed by modifiers (4, 5). The evolution of modifiers of the degree of distortion depends on genetic linkage: loose linkage favors suppressors, tight linkage favors enhancers (6). Although much of our understanding of segregation distortion comes from two well studied autosomal systems, segregation distortion in Drosophila melanogaster (7) and the t-haplotype in Mus musculus (8), the multiple reports of sex-ratio distortion (9), as well as theoretical arguments (10, 11), suggest that segregation distortion of the sex chromosomes may evolve more readily than that of autosomes. Theory further suggests that the deleterious effect of a biased sex ratio results in rapid selection of Y-linked or autosomal suppressors (12, 13), thus rendering the distortion cryptic. Evidence bearing on the hypothesis that cycles of distortion and suppression may have happened multiple times in the evolutionary history of a species (14, 15) is scarce and controversial (16)(17)(18)(19)(20)(21)(22).There is a test of the distortion-suppression hypothesis. Among genetically isolated subpopulations, each would acquire its own independent sequence of distorters and suppressors, depending on the chance order of occurrence. Because the distorters present in any one subpopulation might not be affected by suppressor alleles present i...

Interspecific Y chromosome variation is sufficient to rescue hybrid male sterility and is influenced by the grandparental origin of the chromosomes

“…Aided by molecular markers, these introgressed segments of D. mauritiana had their lengths well delimited in previous work (see Tao et al, 2001Tao et al, , 2003. All introgression lines used here have the genotype of simB, w; nt; P/ III (Nmy), and each has a different segment of D. mauritiana's third chromosome with the semidominant P-element transgene P [w + ] inserted (True et al, 1996) in positions that were previously mapped by Araripe et al (2006).…”

“…The 38.9/38.6 introgressions have the hybrid male sterility factors and sex-ratio distortion suppressor too much ying (tmy) (Tao et al, 2001(Tao et al, , 2003. When homozygous, tmy mau males (the tmy region from D. mauritiana in an otherwise D. simulans background) have very low fertility and offspring with female-biased sex ratio (~75% female).…”

“…Aided by molecular markers, these introgressed segments of D. mauritiana are well delimited (see Tao et al, 2001Tao et al, , 2003. We crossed seven pairs of introgression lines, each carrying a different segment of D. mauritiana's chromosome 3, in order to produce homozygotes of certain portions of these segments.…”

Genome-wide patterns of natural variation reveal strong selective sweeps and ongoing genomic conflict in Drosophila mauritiana

“…Indeed, consistent with the idea that genomic conflict is a common phenomenon, detailed analysis of hybrids showed that ''speciation'' genes tend to be involved in intragenomic conflict, but their effect could be only detected in hybrids (Perez et al 1993;Dermitzakis et al 2000;Tao et al 2001;Presgraves et al 2003;Phadnis and Orr 2009;Tang and Presgraves 2009).…”

Higher levels of sex chromosome heteromorphism are associated with markedly stronger reproductive isolation

“…On the other hand, evidence that faster-heterogametic-sex (genomic conflict) can lead to the large X-effect is still rare, but two cases are known in Drosophila, where a correlation between genes that are involved in drive or suppression within species also lead to male hybrid sterility 28,29 , suggesting that these processes occur at least in some cases. Interestingly, the large X-effect only contributes to the evolution of sterility incompatibilities, which is evident in the results from Masly and Presgraves 7 , where the majority of incompatibilities that are X-linked contribute to sterility and not inviability.…”