Genomic Imprinting and Maternal Effect Genes in Haplodiploid Sex Determination

Zande, Louis van de; Verhulst, Eveline C.

doi:10.1159/000357146

Cited by 28 publications

(18 citation statements)

References 41 publications

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“…In the light of our results, it seems more likely that the different CSD loci have different functions and were not generated via duplication but recruited independently as upstream signals in sex determination. There are currently two known genetic mechanisms underlying haplodiploid sex determination in Hymenoptera [27]: 240 sl-CSD, in the honey bee Apis mellifera, and parental genome imprinting, in the jewel wasp Nasonia vitripennis [28]. Functional investigation of the CSD regions in L. fabarum are likely to reveal a third molecular mechanism of sex determination in Hymenoptera.…”

Section: Discussionmentioning

confidence: 99%

Mapping of multiple complementary sex determination loci in a parasitoid wasp

Matthey-Doret¹,

Kooi

Jeffries³

et al. 2019

Preprint

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Sex determination has evolved in a variety of ways and can depend on environmental and genetic signals. A widespread form of genetic sex determination is haplodiploidy, where unfertilized, haploid eggs develop into males and fertilized diploid eggs into females. One of the molecular mechanisms underlying haplodiploidy in Hymenoptera, a 5 large insect order comprising ants, bees and wasps, is known as complementary sex determination (CSD). In species with CSD, heterozygosity at one or several loci induces female development. Here, we identify the genomic regions putatively underlying multi-locus CSD in the parasitoid wasp Lysiphlebus fabarum using restriction-site associated DNA sequencing. By analysing segregation patterns at polymorphic sites 10 among 331 diploid males and females, we identify four CSD candidate regions, all on different chromosomes. None of the candidate regions feature evidence for homology with the csd gene from the honeybee, the only species in which CSD has been characterized, suggesting that CSD in L. fabarum is regulated via a novel molecular mechanism. Moreover, no homology is shared between the candidate loci, in contrast to 15 the idea that multi-locus CSD should emerge from duplications of an ancestral single-locus system. Taken together, our results suggest that the molecular mechanisms underlying CSD in Hymenoptera are not conserved between species, raising the question as to whether CSD may have evolved multiple times independently in the group. Author summary 20The genetic or environmental signals that govern whether an organism develops into a male or female differ across species, and understanding their evolution is a key aspect of biology. In this paper, we focus on complementary sex determination (CSD), a genetic sex determination system found in many species of bees, ants and wasps where heterozygosity at one or multiple genetic regions determines the sex of the individual. 25 We identify multiple genetic regions in the parasitoid wasp species Lysiphlebus fabarum that are likely underlying CSD. We show that these candidate CSD regions share no similarity with each other and that they differ from the CSD region known in the honey April 26, 2019 1/21 bee, the only species with a well-characterized CSD system. Our results suggest a different molecular mechanism underlying CSD in the wasp and that multiple CSD 30 regions do not necessarily arise from duplications as generally thought.65 75 CSD regions, all on different chromosomes and of which three are close to putative centromeric regions. These loci feature no homology to each other or the known CSD locus in the honeybee, suggesting that the molecular mechanism underlying April 26, 2019 2/21 90 Such vestigial (haploid) male production is fairly common in asexuals [14,15]. Since our approach relies on the comparison of heterozygosity between diploid males and females, haploid males are not informative. Because haploid and diploid males are phenotypically identical in L. fabarum, we used 899 high confidence SNPs with a minimum s...

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Section: Discussionmentioning

confidence: 99%

Mapping of multiple complementary sex determination loci in a parasitoid wasp

Matthey-Doret¹,

Kooi

Jeffries³

et al. 2019

Preprint

View full text Add to dashboard Cite

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“…Common for all hymenopteran species (ants, wasps, and bees) is the principle of haplodiploidy in which males are haploid and develop from unfertilized eggs, whereas females are diploid and arise from fertilized eggs (Bull, 1983 ). The underlying molecular signals and regulatory key genes involved in the sex determination pathway have been studied in greater detail for only two hymenopteran species, the parasitic wasp Nasonia vitripennis (Beukeboom et al, 2007 ; Verhulst et al, 2013 ; van de Zande and Verhulst, 2014 ) and the western European honey bee Apis mellifera (Beye et al, 2003 ; Hasselmann and Beye, 2004 ; Hasselmann et al, 2008 ; Gempe et al, 2009 ) with an estimated divergence time of about 170 million years ago (Werren et al, 2010 ).…”

Section: Introductionmentioning

confidence: 99%

The evolutionary dynamics of major regulators for sexual development among Hymenoptera species

2015

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All hymenopteran species, such as bees, wasps and ants, are characterized by the common principle of haplodiploid sex determination in which haploid males arise from unfertilized eggs and females from fertilized eggs. The underlying molecular mechanism has been studied in detail in the western honey bee Apis mellifera, in which the gene complementary sex determiner (csd) acts as primary signal of the sex determining pathway, initiating female development by csd-heterozygotes. Csd arose from gene duplication of the feminizer (fem) gene, a transformer (tra) ortholog, and mediates in conjunction with transformer2 (tra2) sex-specific splicing of fem. Comparative molecular analyses identified fem/tra and its downstream target doublesex (dsx) as conserved unit within the sex determining pathway of holometabolous insects. In this study, we aim to examine evolutionary differences among these key regulators. Our main hypothesis is that sex determining key regulators in Hymenoptera species show signs of coevolution within single phylogenetic lineages. We take advantage of several newly sequenced genomes of bee species to test this hypothesis using bioinformatic approaches. We found evidences that duplications of fem are restricted to certain bee lineages and notable amino acid differences of tra2 between Apis and non-Apis species propose structural changes in Tra2 protein affecting co-regulatory function on target genes. These findings may help to gain deeper insights into the ancestral mode of hymenopteran sex determination and support the common view of the remarkable evolutionary flexibility in this regulatory pathway.

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“…Inbreeding leads to production of diploid males. In contrast, in species with routine inbreeding, such as Nasonia, sex determination appears to involve an interaction among maternal and zygotic gene products (16)(17)(18)(19). Haplodiploid species pose interesting questions for SD at the gene expression level: How does the degree and profile of sex-biased expression compare with other insect species with sex chromosomal sex determination?…”

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confidence: 99%

Genetic and epigenetic architecture of sex-biased expression in the jewel wasps Nasonia vitripennis and giraulti

Wang

Werren

Clark

2015

Proc. Natl. Acad. Sci. U.S.A.

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There is extraordinary diversity in sexual dimorphism (SD) among animals, but little is known about its epigenetic basis. To study the epigenetic architecture of SD in a haplodiploid system, we performed RNA-seq and whole-genome bisulfite sequencing of adult females and males from two closely related parasitoid wasps, Nasonia vitripennis and Nasonia giraulti. More than 75% of expressed genes displayed significantly sex-biased expression. As a consequence, expression profiles are more similar between species within each sex than between sexes within each species. Furthermore, extremely male-and female-biased genes are enriched for totally different functional categories: male-biased genes for key enzymes in sexpheromone synthesis and female-biased genes for genes involved in epigenetic regulation of gene expression. Remarkably, just 70 highly expressed, extremely male-biased genes account for 10% of all transcripts in adult males. Unlike expression profiles, DNA methylomes are highly similar between sexes within species, with no consistent sex differences in methylation found. Therefore, methylation changes cannot explain the extensive level of sex-biased gene expression observed. Female-biased genes have smaller sequence divergence between species, higher conservation to other hymenopterans, and a broader expression range across development. Overall, female-biased genes have been recruited from genes with more conserved and broadly expressing "house-keeping" functions, whereas male-biased genes are more recently evolved and are predominately testis specific. In summary, Nasonia accomplish a striking degree of sex-biased expression without sex chromosomes or epigenetic differences in methylation. We propose that methylation provides a general signal for constitutive gene expression, whereas other sex-specific signals cause sex-biased gene expression.sex-biased expression | DNA methylation | RNA-seq | WGBS-seq | fatty acid desaturase

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Genomic Imprinting and Maternal Effect Genes in Haplodiploid Sex Determination

Cited by 28 publications

References 41 publications

Mapping of multiple complementary sex determination loci in a parasitoid wasp

Mapping of multiple complementary sex determination loci in a parasitoid wasp

The evolutionary dynamics of major regulators for sexual development among Hymenoptera species

Genetic and epigenetic architecture of sex-biased expression in the jewel wasps Nasonia vitripennis and giraulti

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