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Genetic map lengths of D. virilis chromosomes in centiMorgans reported in previous studies and this study
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Background:
Transposable elements (TEs) are endogenous mutagens and their harmful effects are especially evident in syndromes of hybrid dysgenesis. In Drosophila virilis, hybrid dysgenesis is a syndrome of incomplete gonadal atrophy that occurs when males with multiple active TE families fertilize females that lack active copies of the same famili...
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Context 1
... determine how hybrid dysgenesis influences recombination genome-wide in Drosophila females, fine-scale genetic maps are required. D. virilis genetic maps have been obtained only with a limited number of markers which show that the rate of recombination in D. virilis is significantly higher than in D. melanogaster even though previously estimated rates also differ between studies [55][56][57] (Table 1). Here, we provide the first fine-scale genetic map for D. virilis using thousands of genotypic markers. ...Context 2
... studies indicate that the genetic map of D. virilis is approximately three times larger than the genetic map of D. melanogaster [56,57]. Critically, the map lengths obtained in those two studies are quite different (Table 1), perhaps due to the limited number of genetic markers used in previous studies. Our combined sample has a sufficient density of markers to provide the first high-resolution recombination map for D. virilis. ...Context 3
... total genetic map length of D. virilis estimated in our combined sample is 732 cM (centiMorgans) or 2.5 times longer than the genetic map length of D. melanogaster [59] (Table 1). The genetic map length estimated in the current study is more than 100 cM shorter than the first detailed genetic map of D. virilis [56] (Table 1). ...Context 4
... total genetic map length of D. virilis estimated in our combined sample is 732 cM (centiMorgans) or 2.5 times longer than the genetic map length of D. melanogaster [59] (Table 1). The genetic map length estimated in the current study is more than 100 cM shorter than the first detailed genetic map of D. virilis [56] (Table 1). This may be partly explained by our stringent exclusion of problematic genomic regions. ...Context 5
... were no major changes in the distribution of recombination along the length of the chromosomes (Fig. 3). The chromosomal recombination rates between all three groups are strongly correlated (Additional file 1: Table S1). Interference plays a role in determining CO positioning. ...Context 6
... each sample, 10 μl of genomic DNA was digested with 3.3 U of MseI in 20 μls of reaction volume for four hours at 37 °C, followed by heat inactivation at 65 °C for 20 min. and FC2 adaptors [58] (Additional file 1: Tables S4- S5) were ligated to the digested DNA with 1 U of T4 DNA ligase (New England Biolabs) in 50 μl of reaction volume at 16 °C for 5 h and inactivated at 65 °C for 10 min. The samples were pooled and concentrated using isopropanol precipitation (1/10 vol NaOAc at pH 5.2, 1 vol of 100% isopropanol, and 1 μl glycogen). ...Citations
... Genome-wide estimates of recombination rate are available for several Drosophila species, including a D. serrata estimate of ∼ 1.4 cM/Mb (Stocker et al. 2012), D. pseudoobscura of 3.3-4.6 cM/Mb, D. miranda of 4.9-6.1 cM/Mb (Heil et al. 2015), D. persimilis of 4.1 cM/Mb for autosomes and 5.0 cM/Mb for X Chromosome (Stevison and Noor 2010), D. virilis of 4.6 cM/Mb (Hemmer et al. 2020), and D. melanogaster of 2.5 cM/Mb (Comeron et al. 2012). However, experimental studies of Drosophila have rarely looked at variation in genome-wide recombination rates in natural populations of outbred individuals, and wild populations may differ systematically from populations that have been strongly selected by adaptation to the laboratory (Aggarwal et al. 2021). ...
The rates of mutation, recombination, and transposition are core parameters in models of evolution. They impact genetic diversity, responses to ongoing selection, and levels of genetic load. However, even for key evolutionary model species such as Drosophila melanogaster and D. simulans, few estimates of these parameters are available, and we have little idea of how rates vary between individuals, sexes, or populations. Knowledge of this variation is fundamental for parameterizing models of genome evolution. Here, we provide direct estimates of mutation, recombination, and transposition rates and their variation in a West African and a European population of D. melanogaster and a European population of D. simulans Across 89 flies, we observe 58 single nucleotide mutations, 286 crossovers, and 89 transposable elements (TE) insertions. Compared to the European D. melanogaster, we find the West African population has a lower mutation rate (1.67 vs. 4.86 × 10-9 site-1 gen-1) and a lower transposition rate (8.99 vs. 23.36 × 10-5 copy-1 gen-1), but a higher recombination rate (3.44 vs. 2.06 cM/Mb). The European D. simulans population has a similar mutation rate to European D. melanogaster, but a significantly higher recombination rate and a lower, but not significantly different, transposition rate. Overall, we find paternal-derived mutations are more frequent than maternal ones in both species. Our study quantifies the variation in rates of mutation, recombination, and transposition among different populations and sexes, and our direct estimate of these parameters in D. melanogaster and D. simulans will benefit future studies in population and evolutionary genetics.
... Despite the variety of intrinsic mechanisms that have been evolved to control TE activity, certain conditions, such as "genomic stress" caused by cytonuclear imbalances and/or genomic incompatibilities, can reactivate TEs, as demonstrated in Drosophila-hybrids (Kidwell 1985, Orsi et al. 2010, Romero-Soriano et al. 2017, Hemmer et al. 2020. In contrast to a massive burst of TEs, which is usually associated with deleterious effects on the organism (e.g. ...
Der mitteleuropäische Wasserfroschkomplex umfasst Pelophylax lessonae (Genotyp LL), Pelophylax ridibundus (RR) und deren Hybriden Pelophylax esculentus (LR), der sich hemiklonal durch Rückkreuzen mit LL in lessonae-esculentus (L-E)-Populationen oder RR in ridibundus-esculentus (R-E)-Populationen reproduziert. Außerdem können Hybriden in reine Hybridpopulationen (E) bilden, in denen triploide Individuen die Elternarten funktionell ersetzen. Bislang ist wenig über die molekularen Mechanismen bekannt, die der klonalen Gametenbildung in der Keimbahn der Hybridform zugrunde liegen. In dieser Studie wurden erstmalig 160 Gene der Elternarten untersucht, die an der Gametenbildung beteiligt sind. Zusätzlich wurden 131 SNPs von 52 dieser Gene von 652 Wasserfröschen aus 26 Populationen analysiert. Im Ergebnis wurden 14 SNPs von 10 Genen entdeckt, deren Frequenzen mit dem Populationssystem assoziiert waren. In Übereinstimmung mit ihren Funktionen könnten diese Gene im Zusammenheng mit den system-spezifischen hybridogenetischen Reproduktionsmodi stehen. Sowohl transkriptomische als auch SNP-Daten lieferten Hinweise auf genetische Introgression, d. h. einen Transfer lessonae-spezifischer Allelen in den ridibundus-Genpool oder umgekehrt. Außerdem wurde bei P. lessonae eine kryptische genetische Diversität beobachtet. SNP-Analysen ergaben auch, dass LR-Individuen aus E-Populationen eine höhere genetische Ähnlichkeit mit LR-Individuen aus R-E als aus L-E-Populationen aufweisen. Diese Ergebnisse werfen die Frage nach dem Ursprung der E-Populationen auf, von denen bisher angenommen wurde, dass sie aus L-E-Populationen hervorgegangen sind. Die neuen molekularen Daten stehen mit den hemiklonalen Fortpflanzungsmodi von P. esculentus im Einklang und unterstreichen, dass diese wahrscheinlich auf komplexen Wechselwirkungen zwischen verschiedenen Genen und Faktoren basieren.
... A new D. virilis TE library was generated using RepeatModeler2 [28] on a PacBio assembly of cdi A strain 160 [29] and a nanopore assembly of cdi I strain 9 [22]. Additional nanopore reads were further obtained for the cdi A strain using the same approach as in [30]. ...
... piRNA sequences were obtained from a previous study [27] and mapping was performed with BWA aln, randomly assigning multiple mappers [33]. Mapping was performed to whole genome assemblies from cdi A strain 160 [29] and cdi I strain 9 [22]. In the case of the cdi A strain, the artifictual telomeric TART array (with only a fragment remaining) was removed from the assembly image in Figures 2 and 3 based on being present in only one read among all individual PacBio and nanopore reads and that read most likely being a duplex read. ...
... To determine whether there are structural differences at the telomere that might explain the difference between the cdi I and cdi A alleles, we examined available assemblies and single long reads. A previous PacBio assembly of the strain carrying the cdi A allele [29] contains an array more than 27 kb in length composed of TART elements at the end of this chromosome. However, a manual inspection of individual PacBio reads carrying the cdi gene sequence showed that there was no single long read that contained such a TART array connected to cdi. ...
First discovered in maize, paramutation is a phenomenon in which one allele can trigger an epigenetic conversion of an alternate allele. This conversion causes a genetically heterozygous individual to transmit alleles that are functionally the same, in apparent violation of Mendelian segregation. Studies over the past several decades have revealed a strong connection between mechanisms of genome defense against transposable elements by small RNA and the phenomenon of paramutation. For example, a system of paramutation in Drosophila melanogaster has been shown to be mediated by piRNAs, whose primary function is to silence transposable elements in the germline. In this paper, we characterize a second system of piRNA-mediated paramutation-like behavior at the telomere of Drosophila virilis. In Drosophila, telomeres are maintained by arrays of retrotransposons that are regulated by piRNAs. As a result, the telomere and sub-telomeric regions of the chromosome have unique regulatory and chromatin properties. Previous studies have shown that maternally deposited piRNAs derived from a sub-telomeric piRNA cluster can silence the sub-telomeric center divider gene of Drosophila virilis in trans. In this paper, we show that this silencing can also be maintained in the absence of the original silencing allele in a subsequent generation. The precise mechanism of this paramutation-like behavior may be explained by either the production of retrotransposon piRNAs that differ across strains or structural differences in the telomere. Altogether, these results show that the capacity for piRNAs to mediate paramutation in trans may depend on the local chromatin environment and proximity to the uniquely structured telomere regulated by piRNAs. This system promises to provide significant insights into the mechanisms of paramutation.
... In Drosophila, long-read WGAs of homozy-e124 Nucleic Acids Research, 2022, Vol. 50, No. 21 PAGE 2 OF 14 gous diploid genomes such as those from inbred fly stocks can achieve high contiguity and permit detailed analysis of structural variation including TE insertions (29)(30)(31)(32)(33)(34)(35)(36). However, successful WGA using long reads remains limited by complex genome features including polyploidy, heterozygosity, and high repeat content, all of which are present in cell lines such as Drosophila S2 cells (5,8,(17)(18)(19)(20)22). ...
Animal cell lines often undergo extreme genome restructuring events, including polyploidy and segmental aneuploidy that can impede de novo whole-genome assembly (WGA). In some species like Drosophila, cell lines also exhibit massive proliferation of transposable elements (TEs). To better understand the role of transposition during animal cell culture, we sequenced the genome of the tetraploid Drosophila S2R+ cell line using long-read and linked-read technologies. WGAs for S2R+ were highly fragmented and generated variable estimates of TE content across sequencing and assembly technologies. We therefore developed a novel WGA-independent bioinformatics method called TELR that identifies, locally assembles, and estimates allele frequency of TEs from long-read sequence data (https://github.com/bergmanlab/telr). Application of TELR to a ∼130x PacBio dataset for S2R+ revealed many haplotype-specific TE insertions that arose by transposition after initial cell line establishment and subsequent tetraploidization. Local assemblies from TELR also allowed phylogenetic analysis of paralogous TEs, which revealed that proliferation of TE families in vitro can be driven by single or multiple source lineages. Our work provides a model for the analysis of TEs in complex heterozygous or polyploid genomes that are recalcitrant to WGA and yields new insights into the mechanisms of genome evolution in animal cell culture.
... 1.4 cM/Mb (Stocker, et al. 2012), D. pseudoobscura of 3.3 -4.6 cM/Mb, D. miranda of 4.9 -6.1 cM/Mb 119 (Heil, et al. 2015), D. persimilis of 4.1 cM/Mb for autosomes and 5.0 cM/Mb for X chromosome 120 (Stevison and Noor 2010), D. virilis of 4.6 cM/Mb (Hemmer, et al. 2020) and D. melanogaster of 2.5 121 cM/Mb (Comeron, et al. 2012). However, experimental studies of Drosophila have rarely looked at 122 variation in genome-wide recombination rates in natural populations of outbred individuals, and wild 123 populations may differ systematically from populations that have been strongly selected by 124 adaptation to the laboratory (Aggarwal, et al. 2021). ...
Mutation, recombination, and transposition occurring during meiosis provide the variation on which natural selection can act and the rates at which they occur are important parameters in models of evolution. The de novo mutation rate determines levels of genetic diversity, responses to ongoing selection, and levels of genetic load. Recombination breaks up haplotypes and reduces the effects of linkage, helping to spread beneficial alleles and purge deleterious ones. Transposable elements (TE) selfishly replicate themselves through the genome, imposing fitness costs on the host and introducing complex mutations that can affect gene expression and give rise to new genes. However, even for key evolutionary models such as Drosophila melanogaster and D. simulans few estimates of these parameters are available, and we have little idea of how rates vary between individuals, sexes, populations, or species. Here, we provide direct estimates of mutation, recombination, and transposition rates and their variation in a West African and a European population of D. melanogaster and a European population of D. simulans . Across 89 flies, we observe 58 single nucleotide mutations, 286 crossovers, and 89 TE insertions. Compared to the European D. melanogaster , we find the West African population has a lower mutation rate (1.67 vs . 4.86 × 10 ⁻⁹ site ⁻¹ gen ⁻¹ ) and transposition rate (8.99 vs . 23.36 × 10 ⁻⁵ copy ⁻¹ gen ⁻¹ ), but a higher recombination rate (3.44 vs . 2.06 cM/Mb). The European D. simulans population has a similar mutation rate to European D. melanogaster but a significantly higher recombination rate and a lower but not significantly different transposition rate. Overall, we find paternal-derived mutations are more frequent than maternal ones in both species.
Highlights
De novo mutation rates are 1.67 × 10 ⁻⁹ site ⁻¹ gen ⁻¹ (95% HPD CI: 0.54 – 3.14 × 10 ⁻⁹ ), 4.86 × 10 ⁻⁹ site ⁻¹ gen ⁻¹ (2.11 – 8.02 × 10 ⁻⁹ ), and 4.51 × 10 ⁻⁹ site ⁻¹ gen ⁻¹ (1.94 – 7.75 × 10 ⁻⁹ ) for the West African D. melanogaster , the European D. melanogaster and the European D. simulans population, respectively.
In females, recombination rates in the absence of large genomic inversions are 3.44 cM/Mb (2.72 – 4.18), 2.06 cM/Mb (1.57 - 2.57), and 3.04 cM/Mb (2.45 - 3.73) for the three populations, respectively. There was no strong evidence of recombination observed in males.
Mutations (SNMs and indels) are male-biased.
The West African D. melanogaster population has a lower TE activity than the other populations and CMC-Transib is the dominant active TE. The European D. melanogaster population has multiple active TEs: Gypsy, CMC-Transib, Pao, Jockey and hAT-hobo ; while in European D. simulans , they are Gypsy, CMC-Transib, Pao, hAT-hobo, Copia and TcMar-Mariner .
... TE mobilization can be triggered by hybrid dysgenesis (due to asymmetric piRNA profiles), environmental changes, stress and proteinopathy (due to interference with siRNA silencing [234,235]. Moreover, exogenous viral infections in flies can modulate the expression of TEs through modulation of piRNA and siRNA profiles [236]. ...
The study of human neurological infection faces many technical and ethical challenges. While not as common as mammalian models, the use of Drosophila (fruit fly) in the investigation of virus–host dynamics is a powerful research tool. In this review, we focus on the benefits and caveats of using Drosophila as a model for neurological infections and neuroimmunity. Through the examination of in vitro, in vivo and transgenic systems, we highlight select examples to illustrate the use of flies for the study of exogenous and endogenous viruses associated with neurological disease. In each case, phenotypes in Drosophila are compared to those in human conditions. In addition, we discuss antiviral drug screening in flies and how investigating virus–host interactions may lead to novel antiviral drug targets. Together, we highlight standardized and reproducible readouts of fly behaviour, motor function and neurodegeneration that permit an accurate assessment of neurological outcomes for the study of viral infection in fly models. Adoption of Drosophila as a valuable model system for neurological infections has and will continue to guide the discovery of many novel virus–host interactions.
... Although there are other types of stress defined in the literature, in the current work we will not discuss, for instance, neither about psychological/perceived stress, since it is not applicable to the aim of this work, nor about 'genomic' stress, as we do not consider it as a form of stress, but just a common genetic phenomenon [38,39]. Finally, old age approached in some studies will be considered as an accumulation of stress factors. ...
Transposable elements, also known as “jumping genes,” have the ability to hop within the host genome. Nonetheless, this capacity is kept in check by the host cell defense systems to avoid unbridled TE mobilization. Diferent types of stressors can activate TEs in Drosophila, suggesting that TEs may play an adaptive role in the stress response, especially in generating genetic variability for adaptive evolution. TE activation by stressors may also lead to the notion, usually found in the literature, that any form of stress could activate all or the majority of TEs. In this review, we defne what stress is. We then present and discuss RNA sequencing results from several studies demonstrating that stress does not trigger TE transcription broadly in Drosophila. An explanation for the LTR order of TEs being the most overexpressed is also proposed.
... The reference genome strain (UCSD stock number 15010-1051.87) contains TEs not present in the TE− strain, and as a result induces dysgenesis in intraspecies crosses (Blumenstiel, 2014); we refer to this strain as TE+. The TE− and TE+ strains differ at more than just presence/absence of TEs; for example, one study estimates ~7.35 SNP/ kb differentiate them (Hemmer et al., 2020). This level of genetic differentiation is consistent with that expected between strains within a diverse species. ...
... Although one D. lummei sample was nearly identical to the noninducing Strain 9 (TE−), the other strain had a higher copy number and average major allele frequency, however Polyphemus was still lower in both D. lummei samples than in the inducing strains ( Figure S1). We also assessed evidence for ac- This is consistent with analyses that suggest Polyphemus induced DNA breaks in dysgenic progeny (Hemmer et al., 2020). ...
... ductive isolation in the interspecific cross fits better than alternative models of genic incompatibilities. In addition, with genomic data, we also assessed which candidate TE might be responsible for observed dysgenesis patterns among inducing D. virilis strains compared with noninducing D. virilis and D. lummei, and confirmed previous reports that Polyphemus is a strong candidate for causing dysgenesis(Funikov et al., 2018;Hemmer et al., 2020).Although a role for selfish genetic elements in the expression of postzygotic reproductive isolation is consistent with the Dobzhansky-Muller model of hybrid incompatibility(Castillo & Moyle, 2012;Crespi & Nosil, 2013;Johnson, 2010), the difficulty of explicitly disentangling TE effects from the effects of other hybrid incompatibilities is underappreciated. For example, one-way TEs are thought to contribute to reproductive isolation is through transcriptional misregulation that causes sterility or inviability(Dion-Cote et al., 2014;Martienssen, 2010;Michalak, 2010).However, this is not a unique feature of TE−based hybrid incompatibility; divergence in trans and cis-regulatory elements are common and can also cause misregulation and hybrid incompatibilities, via ordinary genic effects (reviewed inMack & Nachman, 2017). ...
Mismatches between parental genomes in selfish elements are frequently hypothesized to underlie hybrid dysfunction and drive speciation. However, because the genetic basis of most hybrid incompatibilities is unknown, testing the contribution of selfish elements to reproductive isolation is difficult. Here, we evaluated the role of transposable elements (TEs) in hybrid incompatibilities between Drosophila virilis and D. lummei by experimentally comparing hybrid incompatibility in a cross where active TEs are present in D. virilis (TE+) and absent in D. lummei, to a cross where these TEs are absent from both D. virilis (TE-) and D. lummei genotypes. Using genomic data, we confirmed copy number differences in TEs between the D. virilis (TE+) strain and both the D. virilis (TE-) strain and D. lummei. We observed F1 postzygotic reproductive isolation exclusively in the interspecific cross involving TE+ D. virilis but not in crosses involving TE- D. virilis. This mirrors intraspecies dysgenesis where atrophied testes only occur when TE+ D. virilis is the paternal parent. A series of backcross experiments, that accounted for alternative models of hybrid incompatibility, showed that both F1 hybrid incompatibility and intrastrain dysgenesis are consistent with the action of TEs rather than genic interactions. Thus, our data suggest that this TE mechanism manifests as two different incompatibility phenotypes. A further Y-autosome interaction contributes to additional, sex-specific, inviability in one direction of this cross-combination. These experiments demonstrate that TEs that cause intraspecies dysgenesis can increase reproductive isolation between closely related lineages, thereby adding to the processes that consolidate speciation.
... Additionally, there are potential biases associated with maps based on visible markers or P-elements with reporter genes, resulting from combinations of markers with different viability or the presence of transposable elements (TEs) that can directly affect recombination frequencies near insertion sites [110][111][112]. The use of WGS-based high-resolution crossover maps, however, reduces many of such limitations [113][114][115][116][117][118][119]. ...
... We analyzed a large number of individual meiotic events (more than 1,600) and identified the precise localization of more than 5,300 crossover events. Amongst Drosophila species, D. yakuba shows an intermediate total map length (339 cM), longer than D. melanogaster (287 cM [41, 113,136]) and shorter than D. mauritiana (about 500cM; [31]), D. pseuddobscura (>450 cM; [193,194]) or D. virilis (732 cm [117]). This high degree of variation is consistent with the proposal that the number and distribution of crossovers have the potential to evolve very fast, possibly as a result of adaptive processes ( [118,126] see also [127,129,195]). ...
The number and location of crossovers across genomes are highly regulated during meiosis, yet the key components controlling them are fast evolving, hindering our understanding of the mechanistic causes and evolutionary consequences of changes in crossover rates. Drosophila melanogaster has been a model species to study meiosis for more than a century, with an available high-resolution crossover map that is, nonetheless, missing for closely related species, thus preventing evolutionary context. Here, we applied a novel and highly efficient approach to generate whole-genome high-resolution crossover maps in D . yakuba to tackle multiple questions that benefit from being addressed collectively within an appropriate phylogenetic framework, in our case the D . melanogaster species subgroup. The genotyping of more than 1,600 individual meiotic events allowed us to identify several key distinct properties relative to D . melanogaster . We show that D . yakuba , in addition to higher crossover rates than D . melanogaster , has a stronger centromere effect and crossover assurance than any Drosophila species analyzed to date. We also report the presence of an active crossover-associated meiotic drive mechanism for the X chromosome that results in the preferential inclusion in oocytes of chromatids with crossovers. Our evolutionary and genomic analyses suggest that the genome-wide landscape of crossover rates in D . yakuba has been fairly stable and captures a significant signal of the ancestral crossover landscape for the whole D . melanogaster subgroup, even informative for the D . melanogaster lineage. Contemporary crossover rates in D . melanogaster , on the other hand, do not recapitulate ancestral crossovers landscapes. As a result, the temporal stability of crossover landscapes observed in D . yakuba makes this species an ideal system for applying population genetic models of selection and linkage, given that these models assume temporal constancy in linkage effects. Our studies emphasize the importance of generating multiple high-resolution crossover rate maps within a coherent phylogenetic context to broaden our understanding of crossover control during meiosis and to improve studies on the evolutionary consequences of variable crossover rates across genomes and time.
... Доля мутантных потомков в семье в такой линии зависела от стадии сперматогенеза, на которой проходила рекомбинация. Полногеномный сиквенс гибридных геномов подтверждает данные о том, что большая часть рекомбинаций идет на премейотической стадии [35]. В некоторых случаях получали каскад производных, где норма чередовалась с мутантным фенотипом, то есть рекомбинации в гене yellow приводили к чередованию в ряду поколений инверсий и реинверсий регуляторной зоны между соседними hobo [31][32][33]. ...
Phenotypically Unstable Mutations as Markers
of Chromosomal Rearrangements Involving DNA Transposons
L. P. Zakharenko*
The Federal Research Center Institute of Cytology and Genetics of Siberian Branch of the Russian Academy of Sciences,
Novosibirsk, 630090 Russia
*e-mail: zakharlp@bionet.nsc.ru
The suitability of using unstable alleles of Drosophila melanogaster to estimate the rate of movement of transposable
elements (TEs) by the frequency of phenotype change was investigated. Several examples show that
the instability of alleles with TE introduced in them is due more to recombinations between TEs than to the
true movement of TEs by transposase.
