Sex chromosomes are susceptible to the evolution of selfish meiotic drive elements that bias transmission and distort progeny sex ratios. Conflict between such sex-ratio drivers and the rest of the genome can trigger evolutionary arms races resulting in genetically suppressed 'cryptic' drive systems. The Winters cryptic sex-ratio drive system of Drosophila simulans comprises a driver, Distorter on the X (Dox) and an autosomal suppressor, Not much yang, a retroduplicate of Dox that suppresses via production of endogenous small interfering RNAs (esiRNAs). Here we report that over 22 Dox-like (Dxl) sequences originated, amplified and diversified over the ~250,000-year history of the three closely related species, D. simulans, D. mauritiana and D. sechellia. The Dxl sequences encode a rapidly evolving family of protamines. Dxl copy numbers amplified by ectopic exchange among euchromatic islands of satellite DNAs on the X chromosome and separately spawned four esiRNA-producing suppressors on the autosomes. Our results reveal the genomic consequences of evolutionary arms races and highlight complex interactions among different classes of selfish DNAs.

Satellite DNA-mediated diversification of a sex-ratio meiotic drive gene family in Drosophila.

The three fruitfly species of the Drosophila simulans clade- D. simulans, D. mauritiana, and D. sechellia- have served as important models in speciation genetics for over 40 years. These species are reproductively isolated by geography, ecology, sexual signals, postmating-prezygotic interactions, and postzygotic genetic incompatibilities. All pairwise crosses between these species conform to Haldane's rule, producing fertile F1 hybrid females and sterile F1 hybrid males. The close phylogenetic proximity of the D. simulans clade species to the model organism, D. melanogaster, has empowered genetic analyses of their species differences, including reproductive incompatibilities. But perhaps no phenotype has been subject to more continuous and intensive genetic scrutiny than hybrid male sterility. Here we review the history, progress, and current state of our understanding of hybrid male sterility among the D. simulans clade species. Our aim is to integrate the available information from experimental and population genetics analyses bearing on the causes and consequences of hybrid male sterility. We highlight numerous conclusions that have emerged as well as issues that remain unresolved. We focus on the special role of sex chromosomes, the fine-scale genetic architecture of hybrid male sterility, and the history of gene flow between species. The biggest surprises to emerge from this work are that (i) genetic conflicts may be an important general force in the evolution of hybrid incompatibility, (ii) hybrid male sterility is polygenic with contributions of complex epistasis, and (iii) speciation, even among these geographically allopatric taxa, has involved the interplay of gene flow, negative selection, and positive selection. These three conclusions are marked departures from the classical views of speciation that emerged from the modern evolutionary synthesis.

/pdf/hybrid-sterility-genetic-conflict-and-complex-speciation-4o4c9js3ix.pdf

Hybrid Sterility, Genetic Conflict and Complex Speciation: Lessons From the Drosophila simulans Clade Species

Segregation Distorter (SD) is a male meiotic drive system in Drosophila melanogaster. Males heterozygous for a selfish SD chromosome rarely transmit the homologous SD+ chromosome. It is well established that distortion results from an interaction between Sd, the primary distorting locus on the SD chromosome and its target, a satellite DNA called Rsp, on the SD+ chromosome. However, the molecular and cellular mechanisms leading to post-meiotic SD+ sperm elimination remain unclear. Here we show that SD/SD+ males of different genotypes but with similarly strong degrees of distortion have distinct spermiogenic phenotypes. In some genotypes, SD+ spermatids fail to fully incorporate protamines after the removal of histones, and degenerate during the individualization stage of spermiogenesis. In contrast, in other SD/SD+ genotypes, protamine incorporation appears less disturbed, yet spermatid nuclei are abnormally compacted, and mature sperm nuclei are eventually released in the seminal vesicle. Our analyses of different SD+ chromosomes suggest that the severity of the spermiogenic defects associates with the copy number of the Rsp satellite. We propose that when Rsp copy number is very high (> 2000), spermatid nuclear compaction defects reach a threshold that triggers a checkpoint controlling sperm chromatin quality to eliminate abnormal spermatids during individualization.

/pdf/distinct-spermiogenic-phenotypes-underlie-sperm-elimination-3p0pk0v5sp.pdf

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

/pdf/distinct-spermiogenic-phenotypes-underlie-sperm-elimination-37swv00i1b.pdf

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

Many animal species employ short, positively charged proteins, called sperm nuclear basic proteins (SNBPs) or protamines, for tighter packaging of genomes in sperm. SNBP repertoires differ dramatically across animal lineages and signatures of rapid evolution have been reported in mammals. Both sperm competition and meiotic drive between sex chromosomes have been proposed as causes of SNBP innovation. We used a phylogenomic approach to investigate SNBP diversification and its underlying causes in Drosophila species. We found unambiguous signatures of positive selection in most SNBP genes except for genes essential for male fertility in D. melanogaster. Unexpectedly, evolutionarily young SNBP genes are more likely to encode essential functions for fertility than ancient, conserved SNBP genes like CG30056, which we found is dispensable for male fertility despite universal retention in Drosophila species. We found 19 independent amplification events involving eight SNBP genes that occurred preferentially on sex chromosomes in 78 Drosophila species. Conversely, we found that otherwise-conserved SNBP genes were lost in the montium group of Drosophila species, coincident with an X-Y chromosomal fusion. Furthermore, SNBP genes that became linked to sex chromosomes via chromosomal fusions are prone to degenerate or relocate back to autosomes. We hypothesize that SNBP genes ancestrally encoded by autosomes suppress meiotic drive, whereas sex-chromosomal SNBP expansions directly participate in meiotic drive. X-Y fusions in the montium group render autosomal SNBPs dispensable by making X-versus-Y meiotic drive obsolete or costly. We conclude that SNBP rapid evolution is driven by genetic conflicts between sex chromosomes during spermatogenesis in Drosophila species.

Genetic conflicts between sex chromosomes drive expansion and loss of sperm nuclear basic protein genes in Drosophila

Segregation Distorter (SD) is an autosomal meiotic drive system found worldwide in natural populations of Drosophila melanogaster. This gene complex induces the preferential and nearly exclusive transmission of the SD chromosome in SD/SD+ males. This selfish propagation occurs through the interplay of the Sd locus, its enhancers and the Rsps locus during spermatid development. The key distorter locus, Sd, encodes a truncated but enzymatically active RanGAP (RanGTPase-activating protein), a key nuclear transport factor in the Ran signaling pathway. When encoded by Sd, RanGAP is mislocalized to the nucleus interior, which then traps Ran inside the nucleus and disrupts nuclear import. As a result of this aberrant nuclear transport, a process known as the histone-to-protamine transition that is required for proper spermatid condensation fails to occur in SD/SD+ males. In this process, sperm-specific protamine proteins enter the spermatid nucleus and replace the formerly chromatin-complexed histones. Previously, we have shown that mutations affecting nuclear import and export can enhance distortion in an SD background, thus verifying that a defect in nuclear transport is responsible for the unequal transmission of chromosomes. Herein, we show that specifically reducing protamines induces distortion in an SD background, verifying that protamines are transported via the RanGAP/GEF pathway and indicating that E(SD) plays a significant and unique role in the process of distortion.

/pdf/a-protamine-knockdown-mimics-the-function-of-sd-in-515e6wo00p.pdf

Luke F Gingell

Papers

A Protamine Knockdown Mimics the Function of Sd in Drosophila melanogaster.