A Genome-Wide Survey of Genetic Instability by Transposition in Drosophila Hybrids

Vela, Doris; Fontdevila, Antonio; Vieira, Cristina; Guerreiro, María Pilar García

doi:10.1371/journal.pone.0088992

Cited by 36 publications

(52 citation statements)

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“…In another Drosophila model, with hybrids between D. buzzatti and D. koepferae , Vela et al . (2014) showed, in a genome-wide manner, massive rearrangements in the F1 hybrids24. In both systems, a wide variety of TEs were responsible for most of the genomic instability in the hybrids.…”

Section: Discussionmentioning

confidence: 95%

“…In artificially interspecific hybrids between D. melanogaster and D. simulans , TEs are derepressed due to adaptive divergence in the piRNA genes of both species rather than differences in TE contents23. Other studies with crosses between D. buzzatti and D. koepferae have shown that 70% of the genomic rearrangements observed in hybrids was due to TE insertions24.…”

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confidence: 99%

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Identification of misexpressed genetic elements in hybrids between Drosophila-related species

Lopez-Maestre

Carnelossi

Lacroix

et al. 2017

Sci Rep

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Crosses between close species can lead to genomic disorders, often considered to be the cause of hybrid incompatibility, one of the initial steps in the speciation process. How these incompatibilities are established and what are their causes remain unclear. To understand the initiation of hybrid incompatibility, we performed reciprocal crosses between two species of Drosophila (D. mojavensis and D. arizonae) that diverged less than 1 Mya. We performed a genome-wide transcriptomic analysis on ovaries from parental lines and on hybrids from reciprocal crosses. Using an innovative procedure of co-assembling transcriptomes, we show that parental lines differ in the expression of their genes and transposable elements. Reciprocal hybrids presented specific gene categories and few transposable element families misexpressed relative to the parental lines. Because TEs are mainly silenced by piwi-interacting RNAs (piRNAs), we hypothesize that in hybrids the deregulation of specific TE families is due to the absence of such small RNAs. Small RNA sequencing confirmed our hypothesis and we therefore propose that TEs can indeed be major players of genome differentiation and be implicated in the first steps of genomic incompatibilities through small RNA regulation.

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Section: Discussionmentioning

confidence: 95%

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confidence: 99%

Identification of misexpressed genetic elements in hybrids between Drosophila-related species

Lopez-Maestre

Carnelossi

Lacroix

et al. 2017

Sci Rep

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“…Previous work in our laboratory showed that new TE insertions occur in hybrids between the species Drosophila buzzatii and Drosophila koepferae (buzzatii complex, repleta group) [15,22,23], which is likely at the origin of a genome expansion in hybrid females [24]. These TE bursts have been associated with abnormal TE expression patterns, first of the retrotransposons Osvaldo and Helena [25,26] and then in a global transcriptomic study including the whole-genome TEs [27].…”

Section: Introductionmentioning

confidence: 97%

Drosophila Interspecific Hybridization Causes a Deregulation of the piRNA Pathway Genes

Gámez-Visairas

Romero‐Soriano

Martí-Carreras

et al. 2020

Genes

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Almost all eukaryotes have transposable elements (TEs) against which they have developed defense mechanisms. In the Drosophila germline, the main transposable element (TE) regulation pathway is mediated by specific Piwi-interacting small RNAs (piRNAs). Nonetheless, for unknown reasons, TEs sometimes escape cellular control during interspecific hybridization processes. Because the piRNA pathway genes are involved in piRNA biogenesis and TE control, we sequenced and characterized nine key genes from this pathway in Drosophila buzzatii and Drosophila koepferae species and studied their expression pattern in ovaries of both species and their F1 hybrids. We found that gene structure is, in general, maintained between both species and that two genes—armitage and aubergine—are under positive selection. Three genes—krimper, methyltransferase 2, and zucchini—displayed higher expression values in hybrids than both parental species, while others had RNA levels similar to the parental species with the highest expression. This suggests that the overexpression of some piRNA pathway genes can be a primary response to hybrid stress. Therefore, these results reinforce the hypothesis that TE deregulation may be due to the protein incompatibility caused by the rapid evolution of these genes, leading to a TE silencing failure, rather than to an underexpression of piRNA pathway genes.

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“…The stressors include both biotic factors, such as inbreeding [88, 89] and interspecific hybridization [90–92], and abiotic factors. Among environmental stressors is the physical factor of heat shock which has been demonstrated to increase transposition rates of a variety of elements by one or two orders of magnitude in diverse organisms from yeast to flies [81–83, 93, 94].…”

Section: Introductionmentioning

confidence: 99%

Profuse evolutionary diversification and speciation on volcanic islands: transposon instability and amplification bursts explain the genetic paradox

Craddock

2016

Biol Direct

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BackgroundSpecies-rich adaptive radiations arising from rare plant and animal colonizers are common on remote volcanic archipelagoes. However, they present a paradox. The severe genetic bottleneck of founder events and effects of inbreeding depression, coupled with the inherently stressful volcanic environment, would seem to predict reduced evolutionary potential and increased risk of extinction, rather than rapid adaptive divergence and speciation. Significantly, eukaryotic genomes harbor many families of transposable elements (TEs) that are mobilized by genome shock; these elements may be the primary drivers of genetic reorganization and speciation on volcanic islands.Presentation of the hypothesisHere I propose that a central factor in the spectacular radiation and diversification of the endemic Hawaiian Drosophila and other terrestrial lineages on the Hawaiian and other oceanic islands has been repeated bursts of transposition of multiple TEs induced by the unique ecological features of volcanic habitats. Founder individuals and populations on remote volcanic islands experience significant levels of physiological and genomic stress as a consequence of both biotic and abiotic factors. This results in disruption of the usual epigenetic suppression of TEs, unleashing them to proliferate and spread, which in turn gives rise to novel genetic variation and remodels genomic regulatory circuits, facilitating rapid morphological, ecological and behavioral change, and adaptive radiation.Testing the hypothesisTo obtain empirical support for the hypothesis, test organisms should be exposed to prolonged heat stress, high levels of carbon dioxide and other volcanic gases, along with inbreeding. Data from subsequent whole genome sequencing and bioinformatics screening for TE numbers and locations would then be compared with initial pre-exposure TE information for the test strains, a labor-intensive project. Several predicted outcomes arising from the hypothesis are discussed. Currently available data are consistent with the proposed concept of stress-induced TE mobilization as a trigger of evolutionary diversification and speciation on volcanic islands.Implications of the hypothesisThe main implication is that both TEs and species should proliferate at a much higher rate on volcanic islands than elsewhere. Second, the evolvability of a lineage may correlate with the abundance and distribution of TEs in the genome. Successful colonizers of volcanic habitats with high genomic proportions of TEs may be best poised to found a speciose lineage that gives rise to a dramatic adaptive radiation. Colonizers that are depauperate in TEs are likely to be evolutionarily constrained and diversify little, if at all.ReviewersThis article was reviewed by Dr. James Shapiro and Dr. Wolfgang Miller (nominated by Editorial Board member Dr. I. King Jordan).

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A Genome-Wide Survey of Genetic Instability by Transposition in Drosophila Hybrids

Cited by 36 publications

References 55 publications

Identification of misexpressed genetic elements in hybrids between Drosophila-related species

Identification of misexpressed genetic elements in hybrids between Drosophila-related species

Drosophila Interspecific Hybridization Causes a Deregulation of the piRNA Pathway Genes

Profuse evolutionary diversification and speciation on volcanic islands: transposon instability and amplification bursts explain the genetic paradox

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