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

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.

SUBMITTER: Reinhardt JA

PROVIDER: S-EPMC10319772 | biostudies-literature | 2023 Jul

REPOSITORIES: biostudies-literature

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

Reinhardt Josephine A JA Baker Richard H RH Zimin Aleksey V AV Ladias Chloe C Paczolt Kimberly A KA Werren John H JH Hayashi Cheryl Y CY Wilkinson Gerald S GS

Genome biology and evolution 20230701 7

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 ...[more]

PMID: 37364298

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Project description:Stalk-eyed flies (family Diopsidae) are a model system for studying sexual selection due to the elongated and sexually dimorphic eye-stalks found in many species. These flies are of additional interest because their X chromosome is derived largely from an autosomal arm in other flies. To identify candidate genes required for development of dimorphic eyestalks and investigate how sex-biased expression arose on the novel X, we compared gene expression between males and females using oligonucleotide microarrays and RNA from developing eyestalk tissue or adult heads in the dimorphic diopsid, Teleopsis dalmanni. Microarray analysis revealed sex-biased expression for 26% of 3,748 genes expressed in eye-antennal imaginal discs and concordant sex-biased expression for 86 genes in adult heads. Overall, 415 female-biased and 482 male-biased genes were associated with dimorphic eyestalk development but not differential expression in the adult head. Functional analysis revealed that male-biased genes are disproportionately associated with growth and mitochondrial function while female-biased genes are associated with cell differentiation and patterning or are novel transcripts. With regard to chromosomal effects, dosage compensation occurs by elevated expression of X-linked genes in males. Genes with female-biased expression were more common on the X and less common on autosomes than expected, while male-biased genes exhibited no chromosomal pattern. Rates of protein evolution were lower for female-biased genes but higher for genes that moved on or off the novel X chromosome. These findings cannot be due to meiotic sex chromosome inactivation or by constraints associated with dosage compensation. Instead, they could be consistent with sexual conflict in which female-biased genes on the novel X act primarily to reduce eyespan in females while other genes increase eyespan in both sexes. Additional information on sex-biased gene expression in other tissues and related sexually monomorphic species could confirm this interpretation.

Project description:BackgroundStalk-eyed flies of the family Diopsidae have proven to be an excellent model organism for studying the evolution of ornamental sexual traits. In diopsid flies the eyes and antennae are borne at the end of lateral head projections called 'eye-stalks'. Eyespan, the distance between the eyes, and the degree of sexual dimorphism in eyespan vary considerably between species and several sexually dimorphic species show sexual selection through female mate preference for males with exaggerated eyespan. Relatively little is known about the molecular genetic basis of intra- or inter-species variation in eyespan, eye-stalk development or growth regulation in diopsids. Molecular approaches including comparative developmental analyses, EST screening and QTL mapping have identified potential candidate loci for eyespan regulation in the model species Teleopsis dalmanni. Functional analyses of these genes to confirm and fully characterise their roles in eye-stalk growth require the development of techniques such as germline transformation to manipulate gene activity in vivo.ResultsWe used in vivo excision assays to identify transposon vector systems with the activity required to mediate transgenesis in T. dalmanni. Mariner based vectors showed no detectable excision while both Minos and piggyBac were active in stalk-eyed fly embryos. Germline transformation with an overall efficiency of 4% was achieved using a Minos based vector and the 3xP3-EGFP marker construct. Chromosomal insertion of constructs was confirmed by Southern blot analysis. Both autosomal and X-linked inserts were recovered. A homozygous stock, established from one of the X-linked inserts, has maintained stable expression for eight generations.ConclusionsWe have performed stable germline transformation of a stalk-eyed fly, T. dalmanni. This is the first transgenic protocol to be developed in an insect species that exhibits an exaggerated male sexual trait. Transgenesis will enable the development of a range of techniques for analysing gene function in this species and so provide insight into the mechanisms underlying the development of a morphological trait subject to sexual selection. Our X-linked insertion line will permit the sex of live larvae to be determined. This will greatly facilitate the identification of genes which are differentially expressed during eye-stalk development in males and females.

Project description:Background: Stalk-eyed flies (family Diopsidae) are a model system for studying sexual selection due to the presence of elongated and sexually dimorphic eye-stalks in many species. Recent genomic studies on these flies have revealed a neo-X chromosome and evidence of gene movement onto or off of this X chromosome. To determine if sex linkage and gene movement are related to sexual dimorphism and sexual conflict, we compared gene expression between males and females using oligonucleotide microarrays and RNA from either developing eyestalk tissue or adult heads from a dimorphic species, Teleopsis dalmanni, or from developing eyestalk tissue in a congeneric monomorphic species, T. quinqueguttata. Results: Comparison of gene expression between the sexes for 3,748 genes indicates that dosage compensation is present due to elevated expression of X-linked genes in males. However, sex-biased expression was detected in 26% of the genes present in eye-antennal imaginal discs of larval T. dalmanni. Functional annotation reveals that female-biased genes are associated with transcription, anatomical development and cell communication in the nucleus, while male-biased genes are associated with metabolism and the mitochondria. Comparison of gene expression between experiments identified 140 genes with concordant sex-biased expression in the larval and adult tissues of T. dalmanni and 17 genes with identical sex-biased expression between species. There were only five reversals of sex-biased expression across experiments. In T. dalmanni, male-biased genes are more common on autosomes than on the X while female-biased genes are more common on the X in T. quinqueguttata. Female-biased expression is especially common among genes that moved onto the ancestral X while male-biased expression is more common among genes that moved onto an autosome. Conclusions: Genes with sex-biased expression exhibit different functions in each sex as expected if sexual conflict has influenced their evolution. The strong relationship between sex-biased expression and gene movement found in this study is consistent with resolution of sexual conflict by an RNA- or DNA-mediated process that moves genes between chromosomes. Measurement of gene expression in additional species should provide a more complete picture of how gene expression change occurs over evolutionary time in these extraordinary flies. Two-condition experiment, female vs. male RNA using larval eye discs for two species (Teleopsis dalmanni, Teleopsis quinqueguttata), and adult heads for one species (Teleopsis dalmanni).

Project description:Stalk-eyed flies (family Diopsidae) are a model system for studying sexual selection due to the elongated and sexually dimorphic eye-stalks found in many species. These flies are of additional interest because their X chromosome is derived largely from an autosomal arm in other flies. To identify candidate genes required for development of dimorphic eyestalks and investigate how sex-biased expression arose on the novel X we compared gene expression between males and females using oligonucleotide microarrays and RNA from developing eyestalk tissue or adult heads in the dimorphic diopsid, Teleopsis dalmanni. Microarray analysis revealed sex-biased expression for 26% of 3,748 genes expressed in eye-antennal imaginal discs and concordant sex-biased expression for 86 genes in adult heads. Overall, 415 female-biased and 482 male-biased genes were associated with dimorphic eyestalk development but not differential expression in the adult head. Functional analysis revealed that male-biased genes are disproportionately associated with growth and mitochondrial function while female-biased genes are associated with cell differentiation and patterning or are novel transcripts. With regard to chromosomal effects, dosage compensation occurs by elevated expression of X-linked genes in males. Genes with female-biased expression were more common on the X and less common on autosomes than expected, while male-biased genes exhibited no chromosomal pattern. Rates of protein evolution were lower for female-biased genes but higher for genes that moved on or off the novel X chromosome. These findings cannot be due to meiotic sex chromosome inactivation or by constraints associated with dosage compensation. Instead, they could be consistent with sexual conflict in which female-biased genes on the novel X act primarily to reduce eyespan in females while other genes increase eyespan in both sexes. Additional information on sex-biased gene expression in other tissues and related sexually monomorphic species could confirm this interpretation.

Dataset Information

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

Publications

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

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