Analysis of a Strong Suppressor of Segregation Distorter in Drosophila melanogaster

Abstract

Segregation distorter (SD) is a naturally occurring male meiotic drive system in Drosophila melanogaster characterized by almost exclusive transmission of the SD chromosome owing to dysfunction of sperm receiving the SD+ homologue. Previous studies identified at least three closely linked loci on chromosome 2 required for distortion: Sd, the primary distorting gene; E(SD), Enhancer, which increases the strength of distortion; and Rsp (Responder), the apparent target of Sd. Strength of distortion is also influenced by linked upwards modifiers including M(SD), Modifier, and St(SD), Stabilizer, and by various unlinked suppressors. Although Sd is known to encode a mutant RanGAP protein none of the modifiers have been molecularly identified. This work focuses on the genetic and cytological characterization of a strong X-linked suppressor, Su(SD), capable of restoring Mendelian transmission in SD/SD+ males. Sd and its cohort of positive modifiers appear to act semi-quantitatively in opposition to Su(SD) with distortion strength depending primarily on the total number of distorting elements rather than which particular elements are present. Su(SD) can also suppress male sterility observed in certain SD genotypes. To facilitate its eventual molecular identification, Su(SD) was localized by deletion mapping to polytene region 13C7-13E4. These studies highlight the polygenic nature of distortion and its dependence on a constellation of positive and negative modifiers, they provide insight into the stability of Mendelian transmission in natural populations even when a drive system arises, and they pave the way for molecular characterization of Su(SD) whose identity should reveal new information about the mechanism of distortion.

A method for low-coverage single-gamete sequence analysis demonstrates adherence to Mendel’s first law across a large sample of human sperm

“…A second and related consideration is that if not balanced by countervailing forces, alleles that are subject to TD may rapidly fix in the population, such that detecting these alleles during their ephemeral existence as polymorphisms may be unlikely. Work in model organisms has also demonstrated the possibility that after distorter alleles arise, suppressors may subsequently evolve to re-balance the transmission ratio (e.g., Greenberg Temin, 2020 ). Admixture between populations may then separate the distorter from the suppressor, revealing hidden distorter alleles.…”

Distinct spermiogenic phenotypes underlie sperm elimination in the Segregation Distorter meiotic drive system

“…SD is a co-adapted gene complex that involves several linked enhancers of drive [4,[50][51][52][53][54][55] and both linked and unlinked suppressors that counteract drive [2,4,[56][57][58]. While the existence and contribution of these genetic factors to levels of distortion is well documented, it seems also important to consider their impact on spermiogenesis.…”

Distinct spermiogenic phenotypes underlie sperm elimination in theSegregation Distortermeiotic drive system

“…SD is a co-adapted gene complex that involves several linked enhancers of drive (Ganetzky, 1977;Sandler and Hiraizumi, 1960;Hiraizumi et al, 1980;Brittnacher and Ganetzky, 1984;Sharp et al, 1985;Temin, 1991;Larracuente and Presgraves, 2012) and both linked and unlinked suppressors that counteract drive (Hiraizumi et al, 1984;Trippa and Loverre, 1975;Courret et al, 2019;Larracuente and Presgraves, 2012;Greenberg Temin, 2020). While the existence and contribution of these genetic factors to levels of distortion is well documented, it seems also important to consider their impact on spermiogenesis.…”