RESUMEN
Transposable elements (TEs) are genomic parasites found in nearly all eukaryotes, including humans. This evolutionary success of TEs is due to their replicative activity, involving insertion into new genomic locations. TE activity varies at multiple levels, from between taxa to within individuals. The rapidly accumulating evidence of the influence of TE activity on human health, as well as the rapid growth of new tools to study it, motivated an evaluation of what we know about TE activity thus far. Here, we discuss why TE activity varies, and the consequences of this variation, from an evolutionary perspective. By studying TE activity in nonhuman organisms in the context of evolutionary theories, we can shed light on the factors that affect TE activity. While the consequences of TE activity are usually deleterious, some have lasting evolutionary impacts by conferring benefits on the host or affecting other evolutionary processes.
Asunto(s)
Elementos Transponibles de ADN , Evolución Molecular , Humanos , AnimalesRESUMEN
Organisms use endogenous clocks to anticipate regular environmental cycles, such as days and tides. Natural variants resulting in differently timed behaviour or physiology, known as chronotypes in humans, have not been well characterized at the molecular level. We sequenced the genome of Clunio marinus, a marine midge whose reproduction is timed by circadian and circalunar clocks. Midges from different locations show strain-specific genetic timing adaptations. We examined genetic variation in five C. marinus strains from different locations and mapped quantitative trait loci for circalunar and circadian chronotypes. The region most strongly associated with circadian chronotypes generates strain-specific differences in the abundance of calcium/calmodulin-dependent kinase II.1 (CaMKII.1) splice variants. As equivalent variants were shown to alter CaMKII activity in Drosophila melanogaster, and C. marinus (Cma)-CaMKII.1 increases the transcriptional activity of the dimer of the circadian proteins Cma-CLOCK and Cma-CYCLE, we suggest that modulation of alternative splicing is a mechanism for natural adaptation in circadian timing.
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Aclimatación/genética , Chironomidae/genética , Relojes Circadianos/genética , Ritmo Circadiano/genética , Genoma de los Insectos/genética , Genómica , Olas de Marea , Empalme Alternativo/genética , Animales , Proteínas CLOCK/genética , Proteína Quinasa Tipo 2 Dependiente de Calcio Calmodulina/genética , Proteína Quinasa Tipo 2 Dependiente de Calcio Calmodulina/metabolismo , Chironomidae/clasificación , Chironomidae/fisiología , Drosophila melanogaster/enzimología , Drosophila melanogaster/genética , Estudios de Asociación Genética , Variación Genética , Masculino , Luna , Fenotipo , Sitios de Carácter Cuantitativo/genética , Reproducción/genética , Reproducción/fisiología , Especificidad de la Especie , Factores de Tiempo , Transcripción GenéticaRESUMEN
Genetic variation is the fuel of evolution, with standing genetic variation especially important for short-term evolution and local adaptation. To date, studies of spatiotemporal patterns of genetic variation in natural populations have been challenging, as comprehensive sampling is logistically difficult, and sequencing of entire populations costly. Here, we address these issues using a collaborative approach, sequencing 48 pooled population samples from 32 locations, and perform the first continent-wide genomic analysis of genetic variation in European Drosophila melanogaster. Our analyses uncover longitudinal population structure, provide evidence for continent-wide selective sweeps, identify candidate genes for local climate adaptation, and document clines in chromosomal inversion and transposable element frequencies. We also characterize variation among populations in the composition of the fly microbiome, and identify five new DNA viruses in our samples.
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Drosophila melanogaster/genética , Genoma de los Insectos , Variación Estructural del Genoma , Microbiota , Selección Genética , Aclimatación/genética , Altitud , Animales , Virus ADN , Drosophila melanogaster/virología , Europa (Continente) , Genoma Mitocondrial , Haplotipos , Virus de Insectos , Masculino , Filogeografía , Polimorfismo de Nucleótido SimpleRESUMEN
In a classic example of the invasion of a species by a selfish genetic element, the P-element was horizontally transferred from a distantly related species into Drosophila melanogaster. Despite causing 'hybrid dysgenesis', a syndrome of abnormal phenotypes that include sterility, the P-element spread globally in the course of a few decades in D. melanogaster. Until recently, its sister species, including D. simulans, remained P-element free. Here, we find a hybrid dysgenesis-like phenotype in the offspring of crosses between D. simulans strains collected in different years; a survey of 181 strains shows that around 20% of strains induce hybrid dysgenesis. Using genomic and transcriptomic data, we show that this dysgenesis-inducing phenotype is associated with the invasion of the P-element. To characterize this invasion temporally and geographically, we survey 631 D. simulans strains collected on three continents and over 27 years for the presence of the P-element. We find that the D. simulans P-element invasion occurred rapidly and nearly simultaneously in the regions surveyed, with strains containing P-elements being rare in 2006 and common by 2014. Importantly, as evidenced by their resistance to the hybrid dysgenesis phenotype, strains collected from the latter phase of this invasion have adapted to suppress the worst effects of the P-element.
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Elementos Transponibles de ADN/genética , Drosophila simulans/genética , Evolución Molecular , Infertilidad/genética , Animales , Cruzamientos Genéticos , Drosophila melanogaster/genética , Hibridación Genética , Especies Introducidas , Fenotipo , FilogeniaRESUMEN
[This corrects the article DOI: 10.1371/journal.pgen.1005920.].
RESUMEN
Meiosis is a potentially important source of germline mutations, as sites of meiotic recombination experience recurrent double-strand breaks (DSBs). However, evidence for a local mutagenic effect of recombination from population sequence data has been equivocal, likely because mutation is only one of several forces shaping sequence variation. By sequencing large numbers of single crossover molecules obtained from human sperm for two recombination hotspots, we find direct evidence that recombination is mutagenic: Crossovers carry more de novo mutations than nonrecombinant DNA molecules analyzed for the same donors and hotspots. The observed mutations were primarily CG to TA transitions, with a higher frequency of transitions at CpG than non-CpGs sites. This enrichment of mutations at CpG sites at hotspots could predominate in methylated regions involving frequent single-stranded DNA processing as part of DSB repair. In addition, our data set provides evidence that GC alleles are preferentially transmitted during crossing over, opposing mutation, and shows that GC-biased gene conversion (gBGC) predominates over mutation in the sequence evolution of hotspots. These findings are consistent with the idea that gBGC could be an adaptation to counteract the mutational load of recombination.
Asunto(s)
Intercambio Genético , Conversión Génica , Mutación , Recombinación Genética , Alelos , Femenino , Humanos , MasculinoRESUMEN
The P-element is one of the best understood eukaryotic transposable elements. It invaded Drosophila melanogaster populations within a few decades but was thought to be absent from close relatives, including Drosophila simulans. Five decades after the spread in D. melanogaster, we provide evidence that the P-element has also invaded D. simulans. P-elements in D. simulans appear to have been acquired recently from D. melanogaster probably via a single horizontal transfer event. Expression data indicate that the P-element is processed in the germ line of D. simulans, and genomic data show an enrichment of P-element insertions in putative origins of replication, similar to that seen in D. melanogaster. This ongoing spread of the P-element in natural populations provides a unique opportunity to understand the dynamics of transposable element spread and the associated piwi-interacting RNAs defense mechanisms.
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Elementos Transponibles de ADN , Drosophila/genética , Animales , Secuencia de Bases , ADN/genética , Drosophila melanogaster/genética , Evolución Molecular , Femenino , Frecuencia de los Genes , Transferencia de Gen Horizontal , Genética de Población , Genoma de los Insectos , Masculino , Datos de Secuencia Molecular , Filogenia , ARN/genética , Especificidad de la Especie , Factores de TiempoRESUMEN
BACKGROUND: Embryogenesis is a highly conserved, canalized process, and variation in the duration of embryogenesis (DOE), i.e., time from egg lay to hatching, has a potentially profound effect on the outcome of within- and between-species competition. There is both intra- and inter-specific variation in this trait, which may provide important fuel for evolutionary processes, particularly adaptation. However, while genetic variation underlying simpler morphological traits, or with large phenotypic effects is well described in the literature, less is known about the underlying genetics of traits, such as DOE, partly due to a lack of tools with which to study them. RESULTS: Here, we establish a novel microscope-based assay to survey genetic variation for the duration of embryogenesis (DOE). First, to establish the potential importance of DOE in competitive fitness, we performed a set of experiments where we experimentally manipulated the time until hatching, and show that short hatching times result in priority effect in the form of improved larval competitive ability. We then use our assay to measure DOE for 43 strains from the Drosophila Genetic Reference Panel (DGRP). Our assay greatly simplifies the measurement of DOE, making it possible to precisely quantify this trait for 59,295 individual embryos (mean ± S.D. of 1103 ± 293 per DGRP strain, and 1002 ± 203 per control). We find extensive genetic variation in DOE, with a 15 % difference in rate between the slowest and fastest strains measured, and 89 % of phenotypic variation due to DGRP strain. Using sequence information from the DGRP, we perform a genome-wide association study, which suggests that some well-known developmental genes affect the speed of embryonic development. CONCLUSIONS: We showed that the duration of embryogenesis (DOE) can be efficiently and precisely measured in Drosophila, and that the DGRP strains show remarkable variation in DOE. A genome-wide analysis suggests that some well-known developmental genes are potentially associated with DOE. Further functional assays, or transcriptomic analysis of embryos from the DGRP, can validate the role of our candidates in early developmental processes.
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Drosophila melanogaster/embriología , Drosophila melanogaster/genética , Variación Genética , Animales , Desarrollo Embrionario/genética , GenomaRESUMEN
Transposable elements (TEs) are mobile genetic elements that parasitize genomes by semi-autonomously increasing their own copy number within the host genome. While TEs are important for genome evolution, appropriate methods for performing unbiased genome-wide surveys of TE variation in natural populations have been lacking. Here, we describe a novel and cost-effective approach for estimating population frequencies of TE insertions using paired-end Illumina reads from a pooled population sample. Importantly, the method treats insertions present in and absent from the reference genome identically, allowing unbiased TE population frequency estimates. We apply this method to data from a natural Drosophila melanogaster population from Portugal. Consistent with previous reports, we show that low recombining genomic regions harbor more TE insertions and maintain insertions at higher frequencies than do high recombining regions. We conservatively estimate that there are almost twice as many "novel" TE insertion sites as sites known from the reference sequence in our population sample (6,824 novel versus 3,639 reference sites, with on average a 31-fold coverage per insertion site). Different families of transposable elements show large differences in their insertion densities and population frequencies. Our analyses suggest that the history of TE activity significantly contributes to this pattern, with recently active families segregating at lower frequencies than those active in the more distant past. Finally, using our high-resolution TE abundance measurements, we identified 13 candidate positively selected TE insertions based on their high population frequencies and on low Tajima's D values in their neighborhoods.
Asunto(s)
Elementos Transponibles de ADN/genética , Drosophila melanogaster/genética , Mutagénesis Insercional/genética , Selección Genética/genética , Análisis de Secuencia de ADN/métodos , Animales , Evolución Molecular , Frecuencia de los Genes , Genoma de los Insectos/genética , Portugal , Recombinación Genética/genéticaRESUMEN
X chromosome meiotic drive (XCMD) kills Y-bearing sperm during spermatogenesis, leading to the biased transmission of the selfish X chromosome. Despite this strong transmission, some natural XCMD systems remain at low and stable frequencies, rather than rapidly spreading through populations. The reason may be that male carriers can have reduced fitness, as they lose half of their sperm, only produce daughters, and may carry deleterious alleles associated with XCMD. Thus, females may benefit from avoiding mating with male carriers, yielding a further reduction in fitness. Genetic suppressors of XCMD, which block the killing of Y sperm and restore fair Mendelian inheritance, are also common and could prevent the spread of XCMD. However, whether suppressed males are as fit as a wild-type male remains an open question, as the effect that genetic suppressors may have on a male's mating success is rarely considered. Here, we investigate the mating ability of XCMD males and suppressed XCMD males in comparison to wild-type males in the fruit fly Drosophila subobscura, where drive remains at a stable frequency of 20% in wild populations where it occurs. We use both competitive and non-competitive mating trials to evaluate male mating success in this system. We found no evidence that unsuppressed XCMD males were discriminated against. Remarkably, however, their suppressed XCMD counterparts had a higher male mating success compared to wild-type controls. Unsuppressed XCMD males suffered 12% lower offspring production in comparison to wild-type males. This cost appears too weak to counter the transmission advantage of XCMD, and thus the factors preventing the spread of XCMD remain unclear.
RESUMEN
Transposable elements (TEs) are genomic parasites that proliferate within host genomes, and which can also invade new species. The P-element, a DNA-based TE, recently invaded two Drosophila species: Drosophila melanogaster in the 20th century, and D. simulans in the 21st. In both species, lines collected before the invasion are susceptible to "hybrid dysgenesis", a syndrome of abnormal phenotypes apparently due to P-element-inflicted DNA damage. In D. melanogaster, lines collected after the invasion have evolved a maternally acting mechanism that suppresses hybrid dysgenesis, with extensive work showing that PIWI-interacting small RNAs (piRNAs) are a key factor in this suppression. Most of these studies use lines collected many generations after the initial P-element invasion. Here, we study D. simulans collected early, as well as late in the P-element invasion of this species. Like D. melanogaster, D. simulans from late in the invasion show strong resistance to hybrid dysgenesis and abundant P-element-derived piRNAs. Lines collected early in the invasion, however, show substantial variation in how much they suffer from hybrid dysgenesis, with some lines highly resistant. Surprisingly, although, these resistant lines do not show high levels of cognate maternal P-element piRNAs; in these lines, it may be that other mechanisms suppress hybrid dysgenesis.
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Drosophila melanogaster , Drosophila simulans , Animales , Drosophila melanogaster/genética , Drosophila simulans/genética , ARN de Interacción con Piwi , ARN Interferente Pequeño/genética , Drosophila/genética , Elementos Transponibles de ADN/genéticaRESUMEN
In contrast to the rest of the genome, the Y chromosome is restricted to males and lacks recombination. As a result, Y chromosomes are unable to respond efficiently to selection, and newly formed Y chromosomes degenerate until few genes remain. The rapid loss of genes from newly formed Y chromosomes has been well studied, but gene loss from highly degenerate Y chromosomes has only recently received attention. Here, we identify and characterize a Y to autosome duplication of the male fertility gene kl-5 that occurred during the evolution of the testacea group species of Drosophila. The duplication was likely DNA based, as other Y-linked genes remain on the Y chromosome, the locations of introns are conserved, and expression analyses suggest that regulatory elements remain linked. Genetic mapping reveals that the autosomal copy of kl-5 resides on the dot chromosome, a tiny autosome with strongly suppressed recombination. Molecular evolutionary analyses show that autosomal copies of kl-5 have reduced polymorphism and little recombination. Importantly, the rate of protein evolution of kl-5 has increased significantly in lineages where it is on the dot versus Y linked. Further analyses suggest this pattern is a consequence of relaxed purifying selection, rather than adaptive evolution. Thus, although the initial fixation of the kl-5 duplication may have been advantageous, slightly deleterious mutations have accumulated in the dot-linked copies of kl-5 faster than in the Y-linked copies. Because the dot chromosome contains seven times more genes than the Y and is exposed to selection in both males and females, these results suggest that the dot suffers the deleterious effects of genetic linkage to more selective targets compared with the Y chromosome. Thus, a highly degenerate Y chromosome may not be the worst environment in the genome, as is generally thought, but may in fact be protected from the accumulation of deleterious mutations relative to other nonrecombining regions that contain more genes.
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Proteínas de Drosophila/genética , Drosophila/genética , Evolución Molecular , Duplicación de Gen , Animales , Cromosomas de Insectos/fisiología , ADN/genética , Proteínas de Drosophila/metabolismo , Femenino , Fertilidad , Genoma , Masculino , Mutación , Filogenia , Recombinación Genética , Selección Genética , Análisis de Secuencia de ADN , Factores Sexuales , Cromosoma Y/genéticaRESUMEN
We have used a polymorphism dataset on introns and coding sequences of X-linked loci in Drosophila americana to estimate the strength of selection on codon usage and/or biased gene conversion (BGC), taking into account a recent population expansion detected by a maximum-likelihood method. Drosophila americana was previously thought to have a stable demographic history, so that this evidence for a recent population expansion means that previous estimates of selection need revision. There was evidence for natural selection or BGC favouring GC over AT variants in introns, which is stronger for GC-rich than GC-poor introns. By comparing introns and coding sequences, we found evidence for selection on codon usage bias, which is much stronger than the forces acting on GC versus AT basepairs in introns.
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Composición de Base/genética , Codón/genética , Drosophila/genética , Selección Genética/genética , Animales , Secuencia de Bases , Funciones de Verosimilitud , Masculino , Missouri , Datos de Secuencia Molecular , Dinámica Poblacional , Alineación de Secuencia , Análisis de Secuencia de ADNRESUMEN
Drosophila melanogaster is an important model for antiviral immunity in arthropods, but very few DNA viruses have been described from the family Drosophilidae. This deficiency limits our opportunity to use natural host-pathogen combinations in experimental studies, and may bias our understanding of the Drosophila virome. Here, we report fourteen DNA viruses detected in a metagenomic analysis of 6668 pool-sequenced Drosophila, sampled from forty-seven European locations between 2014 and 2016. These include three new nudiviruses, a new and divergent entomopoxvirus, a virus related to Leptopilina boulardi filamentous virus, and a virus related to Musca domestica salivary gland hypertrophy virus. We also find an endogenous genomic copy of galbut virus, a double-stranded RNA partitivirus, segregating at very low frequency. Remarkably, we find that Drosophila Vesanto virus, a small DNA virus previously described as a bidnavirus, may be composed of up to twelve segments and thus represent a new lineage of segmented DNA viruses. Two of the DNA viruses, Drosophila Kallithea nudivirus and Drosophila Vesanto virus are relatively common, found in 2 per cent or more of wild flies. The others are rare, with many likely to be represented by a single infected fly. We find that virus prevalence in Europe reflects the prevalence seen in publicly available datasets, with Drosophila Kallithea nudivirus and Drosophila Vesanto virus the only ones commonly detectable in public data from wild-caught flies and large population cages, and the other viruses being rare or absent. These analyses suggest that DNA viruses are at lower prevalence than RNA viruses in D.melanogaster, and may be less likely to persist in laboratory cultures. Our findings go some way to redressing an earlier bias toward RNA virus studies in Drosophila, and lay the foundation needed to harness the power of Drosophila as a model system for the study of DNA viruses.
RESUMEN
In previous work (Betancourt, Genetics 181:1535, 2009), I propagated three large laboratory populations of an RNA phage (MS2) as they adapted to a controlled laboratory environment. These populations were large enough so that evolution might be expected to be mostly repeatable, but they nevertheless fixed different suites of mutations over the course of the experiment. Here, I investigate one possible explanation for these results: epistasis, in which the effect of a mutation depends on its genetic background, may have prevented populations with different initial substitutions from fixing the same set of subsequent mutations. I show that two mutations that previously occurred in different genetic backgrounds are beneficial on either background. This result suggests that sign epistasis-in which a mutation is beneficial on one background, but deleterious on another-is not the cause of different evolutionary trajectories observed in the Betancourt (2009) experiment. However, they can be explained by either magnitude epistasis-in which mutations have stronger or weaker beneficial effects depending on the background-or by the simultaneous fixation of multiple beneficial mutations. Surprisingly, the large populations of the previous experiment showed less parallel evolution than the small populations of this experiment, which lends support to the fixation of multiple beneficial mutations contributing to the patterns seen in both experiments.
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Epistasis Genética , Levivirus/genética , Mutación/genética , Secuencia de Bases , Evolución Molecular , Genotipo , Datos de Secuencia Molecular , Polimorfismo GenéticoRESUMEN
Experimental evolution of bacteriophage provides a powerful means of studying the genetics of adaptation, as every substitution contributing to adaptation can be identified and characterized. Here, I use experimental evolution of MS2, an RNA bacteriophage, to study its adaptive response to a novel environment. To this end, three lines of MS2 were adapted to rapid growth and lysis at cold temperature for a minimum of 50 phage generations and subjected to whole-genome sequencing. Using this system, I identified adaptive substitutions, monitored changes in frequency of adaptive mutations through the course of the experiment, and measured the effect on phage growth rate of each substitution. All three lines showed a substantial increase in fitness (a two- to threefold increase in growth rate) due to a modest number of substitutions (three to four). The data show some evidence that the substitutions occurring early in the experiment have larger beneficial effects than later ones, in accordance with the expected diminishing returns relationship between the fitness effects of a mutation and its order of substitution. Patterns of molecular evolution seen here--primarily a paucity of hitchhiking mutations--suggest an abundant supply of beneficial mutations in this system. Nevertheless, some beneficial mutations appear to have been lost, possibly due to accumulation of beneficial mutations on other genetic backgrounds, clonal interference, and negatively epistatic interactions with other beneficial mutations.
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Adaptación Fisiológica/genética , Sustitución de Aminoácidos/genética , Evolución Molecular , Levivirus/genética , Secuencia de Bases , Mapeo Cromosómico , Frecuencia de los Genes , Genoma Viral , Datos de Secuencia Molecular , Conformación de Ácido Nucleico , Fenotipo , ARN/química , ARN/genéticaRESUMEN
The mutational landscape model is a theoretical model describing sequence evolution in natural populations. However, recent experimental work has begun to test its predictions in laboratory populations of microbes. Several of these studies have focused on testing the prediction that the effects of beneficial mutations should be roughly exponentially distributed. The prediction appears to be borne out by most of these studies, at least qualitatively. Another study showed that a modified version of the model was able to predict, with reasonable accuracy, which of a ranked set of beneficial alleles will be fixed next. Although it remains to be seen whether the mutational landscape model adequately describes adaptation in organisms other than microbes, together these studies suggest that adaptive evolution has surprisingly general properties that can be successfully captured by theoretical models.
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Adaptación Biológica/genética , Evolución Molecular , Modelos Genéticos , Mutación , Selección GenéticaRESUMEN
Meiotic recombination has strong, but poorly understood effects on short tandem repeat (STR) instability. Here, we screened thousands of single recombinant products with sperm typing to characterize the role of polymorphic poly-A repeats at a human recombination hotspot in terms of hotspot activity and STR evolution. We show that the length asymmetry between heterozygous poly-A's strongly influences the recombination outcome: a heterology of 10 A's (9A/19A) reduces the number of crossovers and elevates the frequency of non-crossovers, complex recombination products, and long conversion tracts. Moreover, the length of the heterology also influences the STR transmission during meiotic repair with a strong and significant insertion bias for the short heterology (6A/7A) and a deletion bias for the long heterology (9A/19A). In spite of this opposing insertion-/deletion-biased gene conversion, we find that poly-A's are enriched at human recombination hotspots that could have important consequences in hotspot activation.
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Intercambio Genético/genética , Heterocigoto , Meiosis/genética , Repeticiones de Microsatélite/genética , Poli A/genética , Alelos , Conversión Génica/genética , Genotipo , Haplotipos/genética , Humanos , Masculino , Inestabilidad de Microsatélites , Tasa de Mutación , Polimorfismo de Nucleótido Simple/genética , Espermatozoides/citología , Donantes de TejidosRESUMEN
In many organisms, local deviations from Chargaff's second parity rule are observed around replication and transcription start sites and within intron sequences. Here, we use expression data as well as a whole-genome data set of nearly 200 haplotypes to investigate such compositional skews in Drosophila melanogaster genes. We find a positive correlation between compositional skew and gene expression, comparable in strength to similar correlations between expression levels and genome-wide sequence features. This correlation is relatively stronger for germline, compared with somatic expression, consistent with the process of transcription-associated mutation bias. We also inferred mutation rates from alleles segregating at low frequencies in short introns, and show that, whereas the overall GC content of short introns does not conform to the equilibrium expectation, the level of the observed deviation from the second parity rule is generally consistent with the inferred rates.
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Drosophila melanogaster/genética , Evolución Molecular , Genes de Insecto , Transcripción Genética , Animales , Composición de Base , Acumulación de MutacionesRESUMEN
BACKGROUND: As species diverge, so does their transposable element (TE) content. Within a genome, TE families may eventually become dormant due to host-silencing mechanisms, natural selection and the accumulation of inactive copies. The transmission of active copies from a TE families, both vertically and horizontally between species, can allow TEs to escape inactivation if it occurs often enough, as it may allow TEs to temporarily escape silencing in a new host. Thus, the contribution of horizontal exchange to TE persistence has been of increasing interest. RESULTS: Here, we annotated TEs in five species with sequenced genomes from the D. pseudoobscura species group, and curated a set of TE families found in these species. We found that, compared to host genes, many TE families showed lower neutral divergence between species, consistent with recent transmission of TEs between species. Despite these transfers, there are differences in the TE content between species in the group. CONCLUSIONS: The TE content is highly dynamic in the D. pseudoobscura species group, frequently transferring between species, keeping TEs active. This result highlights how frequently transposable elements are transmitted between sympatric species and, despite these transfers, how rapidly species TE content can diverge.