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1. Impacts of Sex Ratio Meiotic Drive on Genome Structure and Function in a Stalk-Eyed Fly

   https://doi.org/10.1093/gbe/evad118  

   Reinhardt, Josephine A; Baker, Richard H; Zimin, Aleksey V; Ladias, Chloe; Paczolt, Kimberly A; Werren, John H; Hayashi, Cheryl Y; Wilkinson, Gerald S (July 2023, Genome Biology and Evolution)

   Zufall, Rebecca (Ed.)

   Abstract Stalk-eyed flies in the genus Teleopsis carry selfish genetic elements that induce sex ratio (SR) meiotic drive and impact the fitness of male and female carriers. Here, we assemble and describe a chromosome-level genome assembly of the stalk-eyed fly, Teleopsis dalmanni, to elucidate patterns of divergence associated with SR. The genome contains tens of thousands of transposable element (TE) insertions and hundreds of transcriptionally and insertionally active TE families. By resequencing pools of SR and ST males using short and long reads, we find widespread differentiation and divergence between XSR and XST associated with multiple nested inversions involving most of the SR haplotype. Examination of genomic coverage and gene expression data revealed seven X-linked genes with elevated expression and coverage in SR males. The most extreme and likely drive candidate involves an XSR-specific expansion of an array of partial copies of JASPer, a gene necessary for maintenance of euchromatin and associated with regulation of TE expression. In addition, we find evidence for rapid protein evolution between XSR and XST for testis expressed and novel genes, that is, either recent duplicates or lacking a Dipteran ortholog, including an X-linked duplicate of maelstrom, which is also involved in TE silencing. Overall, the evidence suggests that this ancient XSR polymorphism has had a variety of impacts on repetitive DNA and its regulation in this species. 

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2. Autosomal suppression of sex-ratio meiotic drive influences the dynamics of X and Y chromosome coevolution

   https://doi.org/10.1093/jhered/esae048  

   Gupta, Anjali; Unckless, Robert L (August 2024, Journal of Heredity)

   Fishman, Lila (Ed.)

   Sex-ratio meiotic drivers are selfish genes or gene complexes that bias the transmission of sex chromosomes resulting in skewed sex ratios. Existing theoretical models have suggested the maintenance of a four-chromosome equilibrium (with driving and standard X and suppressing and susceptible Y) in a cyclic dynamic, but studies of natural populations have failed to capture this pattern. Although there are several plausible explanations for this lack of cycling, interference from autosomal suppressors has not been studied using a theoretical population genetic framework even though autosomal suppressors and Y-linked suppressors coexist in natural populations of some species. In this study, we use a simulation-based approach to investigate the influence of autosomal suppressors on the cycling of sex chromosomes. Our findings demonstrate that the presence of an autosomal suppressor can hinder the invasion of a Y-linked suppressor under some parameter space, thereby impeding the cyclic dynamics, or even the invasion of Y-linked suppression. Even when a Y-linked suppressor invades, the presence of an autosomal suppressor can prevent cycling. Our study demonstrates the potential role of autosomal suppressors in preventing sex chromosome cycling and provides insights into the conditions and consequences of maintaining both Y-linked and autosomal suppressors. 

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3. Genomic Architecture of Hybrid Male Sterility in a Species Without Sex Chromosomes ( Tigriopus californicus , Copepoda: Harpacticoida)

   https://doi.org/10.1093/gbe/evad091  

   Olsen, Kevin C; Lima, Thiago G; Barreto, Felipe S; Burton, Ronald S (June 2023, Genome Biology and Evolution)

   Katz, Laura A (Ed.)

   Abstract Sterility among hybrids is one of the most prevalent forms of reproductive isolation delineating species boundaries and is expressed disproportionately in heterogametic XY males. While hybrid male sterility (HMS) due to the “large X effect” is a well-recognized mechanism of reproductive isolation, it is less clear how HMS manifests in species that lack heteromorphic sex chromosomes. We evaluated differences in allele frequencies at approximately 460,000 SNPs between fertile and sterile F2 interpopulation male hybrids to characterize the genomic architecture of HMS in a species without sex chromosomes (Tigriopus californicus). We tested associations between HMS and mitochondrial-nuclear and/or nuclear-nuclear signatures of incompatibility. Genomic regions associated with HMS were concentrated on a single chromosome with the same primary 2-Mbp regions identified in one pair of reciprocal crosses. Gene Ontology analysis revealed that annotations associated with spermatogenesis were the most overrepresented within the implicated region, with nine protein-coding genes connected with this process found in the quantitative trait locus of chromosome 2. Our results indicate that a narrow genomic region was associated with the sterility of male hybrids in T. californicus and suggest that incompatibilities among select nuclear loci may replace the large X effect when sex chromosomes are absent. 

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4. Modeling the evolution of Schizosaccharomyces pombe populations with multiple killer meiotic drivers

   https://doi.org/10.1093/g3journal/jkae142  

   López_Hernández, José Fabricio; Rubinstein, Boris Y; Unckless, Robert L; Zanders, Sarah E (June 2024, G3: Genes, Genomes, Genetics)

   McIntyre, L (Ed.)

   Meiotic drivers are selfish genetic loci that can be transmitted to more than half of the viable gametes produced by a heterozygote. This biased transmission gives meiotic drivers an evolutionary advantage that can allow them to spread over generations until all members of a population carry the driver. This evolutionary power can also be exploited to modify natural populations using synthetic drivers known as “gene drives.” Recently, it has become clear that natural drivers can spread within genomes to birth multicopy gene families. To understand intragenomic spread of drivers, we model the evolution of 2 or more distinct meiotic drivers in a population. We employ the wtf killer meiotic drivers from Schizosaccharomyces pombe, which are multicopy in all sequenced isolates, as models. We find that a duplicate wtf driver identical to the parent gene can spread in a population unless, or until, the original driver is fixed. When the duplicate driver diverges to be distinct from the parent gene, we find that both drivers spread to fixation under most conditions, but both drivers can be lost under some conditions. Finally, we show that stronger drivers make weaker drivers go extinct in most, but not all, polymorphic populations with absolutely linked drivers. These results reveal the strong potential for natural meiotic drive loci to duplicate and diverge within genomes. Our findings also highlight duplication potential as a factor to consider in the design of synthetic gene drives. 

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5. Condensin I ^DC , H4K20me1, and perinuclear tethering maintain X chromosome repression in C. elegans

   https://doi.org/10.1101/2024.04.05.588224  

   Trombley, Jessica; Rakozy, Audry I; Jash, Eshna; Csankovszki, Györgyi (April 2024, bioRxiv)

   Abstract Dosage compensation inCaenorhabditis elegansequalizes X-linked gene expression between XX hermaphrodites and XO males. The process depends on a condensin- containing dosage compensation complex (DCC), which binds the X chromosomes in hermaphrodites to repress gene expression. Condensin I^DCand an additional five DCC components must be present on the X during early embryogenesis in hermaphrodites to establish dosage compensation. However, whether the DCC’s continued presence is required to maintain the repressed state once established is unknown. Beyond the role of condensin I^DCin X chromosome compaction, additional mechanisms contribute to X- linked gene repression. DPY-21, a non-condensin I^DCDCC component, is an H4K20me2/3 demethylase whose activity enriches the repressive histone mark, H4 lysine 20 monomethylation, on the X chromosomes. In addition, CEC-4 tethers H3K9me3-rich chromosomal regions to the nuclear lamina, which also contributes to X- linked gene repression. To investigate the necessity of condensin I^DCduring the larval and adult stages of hermaphrodites, we used the auxin-inducible degradation system to deplete the condensin I^DCsubunit DPY-27. While DPY-27 depletion in the embryonic stages resulted in lethality, DPY-27 depleted larvae and adults survive. In these DPY-27 depleted strains, condensin I^DCwas no longer associated with the X chromosome, the X became decondensed, and the H4K20me1 mark was gradually lost, leading to X-linked gene derepression. These results suggest that the stable maintenance of dosage compensation requires the continued presence of condensin I^DC. A loss-of-function mutation incec-4, in addition to the depletion of DPY-27 or the genetic mutation ofdpy- 21, led to even more significant increases in X-linked gene expression, suggesting that tethering heterochromatic regions to the nuclear lamina helps stabilize repression mediated by condensin I^DCand H4K20me1. Author SummaryIn some organisms, whether an individual becomes male, female, or hermaphrodite is determined by the number of their sex chromosomes. In the nematodeCaenorhabditis elegans, males have one X chromosome, whereas hermaphrodites have two X chromosomes. This difference in the number of X chromosomes is crucial for deciding whether an individual becomes a hermaphrodite or a male. However, having two X chromosomes can lead to problems because it results in different gene expression levels, resulting in hermaphrodite lethality. To solve this issue, many organisms undergo a process called dosage compensation. Dosage compensation inC. elegansis achieved by a group of proteins known as the dosage compensation complex (DCC), which includes a protein called DPY-27. The function of DPY-27 is essential during early embryonic development. This study shows that in contrast to early embryonic development, larvae and adults can still survive when DPY-27 is missing. In these worms, all known mechanisms involved in dosage compensation are disrupted and the X is no longer repressed. Our results suggest that the maintenance of dosage compensation in nematodes is an active process, and that it is essential for survival when the organism is developing, but once fully developed, the process becomes dispensable. 

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