ABSTRACT
Meiotic drive biases the transmission of alleles in heterozygous individuals, such that Mendel's law of equal segregation is violated. Most examples of meiotic drive have been discovered over the past century based on causing sex ratio distortion or the biased transmission of easily scoreable genetic markers that were linked to drive alleles. More recently, several approaches have been developed that attempt to identify distortions of Mendelian segregation genome wide. Here, we test a candidate female meiotic drive locus in Drosophila melanogaster, identified previously as causing a â¼54:46 distortion ratio using sequencing of large pools of backcross progeny. We inserted fluorescent visible markers near the candidate locus and scored transmission in thousands of individual progeny. We observed a small but significant deviation from the Mendelian expectation; however, it was in the opposite direction to that predicted based on the original experiments. We discuss several possible causes of the discrepancy between the 2 approaches, noting that subtle viability effects are particularly challenging to disentangle from potential small-effect meiotic drive loci. We conclude that pool sequencing approaches remain a powerful method to identify candidate meiotic drive loci but that genotyping of individual progeny at early developmental stages may be required for robust confirmation.
Subject(s)
Drosophila melanogaster , Meiosis , Humans , Animals , Female , Drosophila melanogaster/genetics , Heterozygote , Meiosis/geneticsABSTRACT
The molecular mechanisms underlying the stress response are poorly described in crustaceans. This includes the snow crab (Chionoecetes opilio), a commercially important stenotherm species distributed throughout the northern hemisphere. A better understanding of the stress response in C. opilio is desperately needed for commercial and conservation purposes. The purpose of this study was to investigate the transcriptional and metabolomic response of C. opilio exposed to stressors. Crabs were randomly assigned to 24 or 72 h treatment groups where they were exposed to conditions simulating live transport (handling and air exposure). A control group was kept in cold (2 °C) and welloxygenated saltwater. The hepatopancreas of the crabs was sampled to perform RNA-sequencing and high-performance chemical isotope labeling metabolomics. Differential gene expression analyses showed that classic crustaceans' stress markers, such as crustacean hyperglycemic hormones and heat shock proteins, were overexpressed in response to stressors. Tyrosine decarboxylase was also up-regulated in stressed crabs, suggesting an implication of the catecholamines tyramine and octopamine in the stress response. Deregulated metabolites revealed that low oxygen was an important trigger in the stress response as intermediate metabolites of the tricarboxylic acid cycle (TCA) accumulated. Lactate, which accumulated unevenly between crabs could potentially be used to predict mortality. This study provides new information on how stressors affect crustaceans and provides a basis for the development of stress markers in C. opilio.
Subject(s)
Brachyura , Stress, Physiological , Animals , Brachyura/genetics , Transcriptome , MetabolomeABSTRACT
Genomes can vary significantly even within the same individual. The underlying mechanisms are manifold, ranging from somatic mutation and recombination, development-associated ploidy changes and genetic bottlenecks, over to programmed DNA elimination during germline/soma differentiation. In this perspective piece, we briefly review recent developments in the study of within-individual genome variation in eukaryotes and prokaryotes. We highlight a Society for Molecular Biology and Evolution 2020 virtual symposium entitled "Within-individual genome variation and germline/soma distinction" and the present Special Section of the same name in Genome Biology and Evolution, together fostering cross-taxon synergies in the field to identify and tackle key open questions in the understanding of within-individual genome variation.
Subject(s)
Adult Germline Stem Cells , Biological Evolution , Genetic Variation , Genome , Genomics/methodsABSTRACT
Drosophila telomeres have been maintained by three families of active transposable elements (TEs), HeT-A, TAHRE, and TART, collectively referred to as HTTs, for tens of millions of years, which contrasts with an unusually high degree of HTT interspecific variation. While the impacts of conflict and domestication are often invoked to explain HTT variation, the telomeres are unstable structures such that neutral mutational processes and evolutionary tradeoffs may also drive HTT evolution. We leveraged population genomic data to analyze nearly 10,000 HTT insertions in 85 Drosophila melanogaster genomes and compared their variation to other more typical TE families. We observe that occasional large-scale copy number expansions of both HTTs and other TE families occur, highlighting that the HTTs are, like their feral cousins, typically repressed but primed to take over given the opportunity. However, large expansions of HTTs are not caused by the runaway activity of any particular HTT subfamilies or even associated with telomere-specific TE activity, as might be expected if HTTs are in strong genetic conflict with their hosts. Rather than conflict, we instead suggest that distinctive aspects of HTT copy number variation and sequence diversity largely reflect telomere instability, with HTT insertions being lost at much higher rates than other TEs elsewhere in the genome. We extend previous observations that telomere deletions occur at a high rate, and surprisingly discover that more than one-third do not appear to have been healed with an HTT insertion. We also report that some HTT families may be preferentially activated by the erosion of whole telomeres, implying the existence of HTT-specific host control mechanisms. We further suggest that the persistent telomere localization of HTTs may reflect a highly successful evolutionary strategy that trades away a stable insertion site in order to have reduced impact on the host genome. We propose that HTT evolution is driven by multiple processes, with niche specialization and telomere instability being previously underappreciated and likely predominant.
Subject(s)
DNA Transposable Elements , Evolution, Molecular , Telomere/genetics , Animals , Drosophila melanogaster , Genomic Instability , Polymorphism, Genetic , Recombination, GeneticABSTRACT
Wild, asexual, vertebrate hybrids have many characteristics that make them good model systems for studying how genomes evolve and epigenetic modifications influence animal physiology. In particular, the formation of asexual hybrid lineages is a form of reproductive incompatibility, but we know little about the genetic and genomic mechanisms by which this mode of reproductive isolation proceeds in animals. Asexual lineages also provide researchers with the ability to produce genetically identical individuals, enabling the study of autonomous epigenetic modifications without the confounds of genetic variation. Here, we briefly review the cellular and molecular mechanisms leading to asexual reproduction in vertebrates and the known genetic and epigenetic consequences of the loss of sex. We then specifically discuss what is known about asexual lineages of Fundulus diaphanus x F. heteroclitus to highlight gaps in our knowledge of the biology of these clones. Our preliminary studies of F. diaphanus and F. heteroclitus karyotypes from Porter's Lake (Nova Scotia, Canada) agree with data from other populations, suggesting a conserved interspecific chromosomal arrangement. In addition, genetic analyses suggest that: (a) the same major clonal lineage (Clone A) of F. diaphanus x F. heteroclitus has remained dominant over the past decade, (b) some minor clones have also persisted, (c) new clones may have recently formed, and iv) wild clones still mainly descend from F. diaphanus â x F. heteroclitus â crosses (96% in 2017-2018). These data suggest that clone formation may be a relatively rare, but continuous process, and there are persistent environmental or genetic factors causing a bias in cross direction. We end by describing our current research on the genomic causes and consequences of a transition to asexuality and the potential physiological consequences of epigenetic variation.
ABSTRACT
In some eukaryotes, germline and somatic genomes differ dramatically in their composition. Here we characterise a major germline-soma dissimilarity caused by a germline-restricted chromosome (GRC) in songbirds. We show that the zebra finch GRC contains >115 genes paralogous to single-copy genes on 18 autosomes and the Z chromosome, and is enriched in genes involved in female gonad development. Many genes are likely functional, evidenced by expression in testes and ovaries at the RNA and protein level. Using comparative genomics, we show that genes have been added to the GRC over millions of years of evolution, with embryonic development genes bicc1 and trim71 dating to the ancestor of songbirds and dozens of other genes added very recently. The somatic elimination of this evolutionarily dynamic chromosome in songbirds implies a unique mechanism to minimise genetic conflict between germline and soma, relevant to antagonistic pleiotropy, an evolutionary process underlying ageing and sexual traits.
Subject(s)
Chromosomes/genetics , DNA/metabolism , Finches/genetics , Genes, Developmental/genetics , Genome/genetics , Germ Cells/metabolism , Animals , Evolution, Molecular , Female , Genomics , Gonads/embryology , Gonads/metabolism , Liver/innervation , Liver/metabolism , Male , Muscle, Skeletal/metabolism , Sex Chromosomes/genetics , Songbirds/genetics , Testis/metabolismABSTRACT
Repetitive DNAs are ubiquitous in eukaryotic genomes and, in many species, comprise the bulk of the genome. Repeats include transposable elements that can self-mobilize and disperse around the genome and tandemly-repeated satellite DNAs that increase in copy number due to replication slippage and unequal crossing over. Despite their abundance, repetitive DNAs are often ignored in genomic studies due to technical challenges in identifying, assembling, and quantifying them. New technologies and methods are now allowing unprecedented power to analyze repetitive DNAs across diverse taxa. Repetitive DNAs are of particular interest because they can represent distinct modes of genome evolution. Some repetitive DNAs form essential genome structures, such as telomeres and centromeres, that are required for proper chromosome maintenance and segregation, while others form piRNA clusters that regulate transposable elements; thus, these elements are expected to evolve under purifying selection. In contrast, other repeats evolve selfishly and cause genetic conflicts with their host species that drive adaptive evolution of host defense systems. However, the majority of repeats likely accumulate in eukaryotes in the absence of selection due to mechanisms of transposition and unequal crossing over. However, even these "neutral" repeats may indirectly influence genome evolution as they reach high abundance. In this Special Issue, the contributing authors explore these questions from a range of perspectives.
Subject(s)
Repetitive Sequences, Nucleic Acid/genetics , Repetitive Sequences, Nucleic Acid/physiology , Animals , Centromere , DNA Transposable Elements , DNA, Satellite , Evolution, Molecular , Genome , Genomics , Heterochromatin , Humans , TelomereABSTRACT
Single-cell RNA sequencing in fruit flies gives an unprecedented picture of how new genes are expressed during the formation of sperm.
Subject(s)
Drosophila/genetics , Testis , Animals , Drosophila melanogaster/genetics , Male , RNA-Seq , Transcription, GeneticABSTRACT
Genomic divergence can cause reproductive isolation between species. The molecular mechanisms underlying reproductive isolation can thus reveal which genomic features evolve rapidly and become unstable or incompatible in hybrids. In a recent paper in Nature, Gibeaux et al. (2018) report paternal genome instability and metabolic imbalance in hybrids between frog species.
Subject(s)
Genome , Reproductive Isolation , Genomics , Hybridization, Genetic , MitochondriaABSTRACT
Understanding the function of cellular systems requires describing how proteins assemble with each other into transient and stable complexes and to determine their spatial relationships. Among the tools available to perform these analyses on a large scale is Protein-fragment Complementation Assay based on the dihydrofolate reductase (DHFR PCA). Here we test how longer linkers between the fusion proteins and the reporter fragments affect the performance of this assay. We investigate the architecture of the RNA polymerases, the proteasome and the conserved oligomeric Golgi (COG) complexes in living cells and performed large-scale screens with these extended linkers. We show that longer linkers significantly improve the detection of protein-protein interactions and allow to measure interactions further in space than the standard ones. We identify new interactions, for instance between the retromer complex and proteins related to autophagy and endocytosis. Longer linkers thus contribute an enhanced additional tool to the existing toolsets for the detection and measurements of protein-protein interactions and protein proximity in living cells.
Subject(s)
Protein Interaction Mapping/methods , Tetrahydrofolate Dehydrogenase/metabolism , Biological Assay , Escherichia coli/genetics , Tetrahydrofolate Dehydrogenase/genetics , Yeasts/geneticsABSTRACT
Genome stability ensures individual fitness and reliable transmission of genetic information. Hybridization between diverging lineages can trigger genome instability, highlighting its potential role in post-zygotic reproductive isolation. We argue that genome instability is not merely one of several types of hybrid incompatibility, but rather that genome stability is one of the very first and most fundamental traits that can break down when two diverged genomes are combined. Future work will reveal how frequent and predictable genome instability is in hybrids, how it affects hybrid fitness, and whether it is a direct cause or consequence of speciation.
Subject(s)
Genetic Speciation , Genomic Instability/genetics , Hybridization, Genetic , Reproduction/genetics , Animals , Reproductive IsolationABSTRACT
The maintenance of duplicated genes is thought to protect cells from genetic perturbations, but the molecular basis of this robustness is largely unknown. By measuring the interaction of yeast proteins with their partners in wild-type cells and in cells lacking a paralog, we found that 22 out of 56 paralog pairs compensate for the lost interactions. An equivalent number of pairs exhibit the opposite behavior and require each other's presence for maintaining their interactions. These dependent paralogs generally interact physically, regulate each other's abundance, and derive from ancestral self-interacting proteins. This reveals that gene duplication may actually increase mutational fragility instead of robustness in a large number of cases.
Subject(s)
Gene Duplication , Genes, Duplicate , Protein Interaction Maps/genetics , Saccharomyces cerevisiae Proteins/metabolism , Saccharomyces cerevisiae/genetics , Saccharomyces cerevisiae/metabolism , Evolution, MolecularABSTRACT
The role of chromosome changes in speciation remains a debated topic, although demographic conditions associated with divergence should promote their appearance. We tested a potential relationship between chromosome changes and speciation by studying two Lake Whitefish (Coregonus clupeaformis) lineages that recently colonized postglacial lakes following allopatry. A dwarf limnetic species evolved repeatedly from the normal benthic species, becoming reproductively isolated. Lake Whitefish hybrids experience mitotic and meiotic instability, which may result from structurally divergent chromosomes. Motivated by this observation, we test the hypothesis that chromosome organization differs between Lake Whitefish species pairs using cytogenetics. While chromosome and fundamental numbers are conserved between the species (2n = 80, NF = 98), we observe extensive polymorphism of subtle karyotype traits. We describe intrachromosomal differences associated with heterochromatin and repetitive DNA, and test for parallelism among three sympatric species pairs. Multivariate analyses support the hypothesis that differentiation at the level of subchromosomal markers mostly appeared during allopatry. Yet we find no evidence for parallelism between species pairs among lakes, consistent with colonization effect or postcolonization differentiation. The reported intrachromosomal polymorphisms do not appear to play a central role in driving adaptive divergence between normal and dwarf Lake Whitefish. We discuss how chromosomal differentiation in the Lake Whitefish system may contribute to the destabilization of mitotic and meiotic chromosome segregation in hybrids, as documented previously. The chromosome structures detected here are still difficult to sequence and assemble, demonstrating the value of cytogenetics as a complementary approach to understand the genomic bases of speciation.
Subject(s)
Genetic Speciation , Genetics, Population , Salmonidae/genetics , Sympatry , Animals , Chromosomes/genetics , Heterochromatin/genetics , Lakes , PhenotypeABSTRACT
Press stop, erase everything from now till some arbitrary time in the past and start recording life as it evolves once again. Would you see the same tape of life playing itself over and over, or would a different story unfold every time? The late Steven Jay Gould called this experiment replaying the tape of life and argued that any replay of the tape would lead evolution down a pathway radically different from the road actually taken (Gould 1989). This thought experiment has puzzled evolutionary biologists for a long time: how repeatable are evolutionary events? And if history does indeed repeat itself, what are the factors that may help us predict the path taken? A powerful means to address these questions at a small evolutionary scale is to study closely related populations that have evolved independently, under similar environmental conditions. This is precisely what Pereira et al. (2016) set out to do using marine copepods Tigriopus californicus, and present their results in this issue of Molecular Ecology. They show that evolution can be repeatable and even partly predictable, at least at the molecular level. As expected from theory, patterns of divergence were shaped by natural selection. At the same time, strong genetic drift due to small population sizes also constrained evolution down a similar evolutionary road, and probably contributed to repeatable patterns of genomic divergence.
Subject(s)
Copepoda/genetics , Evolution, Molecular , Genetics, Population , Transcriptome , AnimalsABSTRACT
Parallel changes in body shape may evolve in response to similar environmental conditions, but whether such parallel phenotypic changes share a common genetic basis is still debated. The goal of this study was to assess whether parallel phenotypic changes could be explained by genetic parallelism, multiple genetic routes, or both. We first provide evidence for parallelism in fish shape by using geometric morphometrics among 300 fish representing five species pairs of Lake Whitefish. Using a genetic map comprising 3438 restriction site-associated DNA sequencing single-nucleotide polymorphisms, we then identified quantitative trait loci underlying body shape traits in a backcross family reared in the laboratory. A total of 138 body shape quantitative trait loci were identified in this cross, thus revealing a highly polygenic architecture of body shape in Lake Whitefish. Third, we tested for evidence of genetic parallelism among independent wild populations using both a single-locus method (outlier analysis) and a polygenic approach (analysis of covariation among markers). The single-locus approach provided limited evidence for genetic parallelism. However, the polygenic analysis revealed genetic parallelism for three of the five lakes, which differed from the two other lakes. These results provide evidence for both genetic parallelism and multiple genetic routes underlying parallel phenotypic evolution in fish shape among populations occupying similar ecological niches.
Subject(s)
Genome , Quantitative Trait Loci , Salmonidae/genetics , Animals , Biological Evolution , Chromosome Mapping , Female , Genetic Markers , Genetic Variation , Genotype , Male , Phenotype , Polymorphism, Single Nucleotide , Salmonidae/anatomy & histology , Sequence Analysis, DNAABSTRACT
Speciation may occur when the genomes of two populations accumulate genetic incompatibilities and/or chromosomal rearrangements that prevent inter-breeding in nature. Chromosome stability is critical for survival and faithful transmission of the genome, and hybridization can compromise this. However, the role of chromosomal stability on hybrid incompatibilities has rarely been tested in recently diverged populations. Here, we test for chromosomal instability in hybrids between nascent species, the 'dwarf' and 'normal' lake whitefish (Coregonus clupeaformis). We examined chromosomes in pure embryos, and healthy and malformed backcross embryos. While pure individuals displayed chromosome numbers corresponding to the expected diploid number (2n = 80), healthy backcrosses showed evidence of mitotic instability through an increased variance of chromosome numbers within an individual. In malformed backcrosses, extensive aneuploidy corresponding to multiples of the haploid number (1n = 40, 2n = 80, 3n = 120) was found, suggesting meiotic breakdown in their F1 parent. However, no detectable chromosome rearrangements between parental forms were identified. Genomic instability through aneuploidy thus appears to contribute to reproductive isolation between dwarf and normal lake whitefish, despite their very recent divergence (approx. 15-20 000 generations). Our data suggest that genetic incompatibilities may accumulate early during speciation and limit hybridization between nascent species.
Subject(s)
Aneuploidy , Salmonidae/genetics , Animals , Chromosomal Instability , Embryo, Nonmammalian/abnormalities , Female , Genetic Speciation , Hybridization, Genetic , Male , Reproduction/genetics , Reproductive Isolation , Salmonidae/abnormalities , Salmonidae/embryologyABSTRACT
Identifying the molecular basis of reproductive isolation among diverging lineages represents an essential step toward understanding speciation in natural populations. Postzygotic barriers can lead to hybrid breakdown, a syndrome that has been documented in several systems, potentially involving the reactivation of transposable elements. In northeastern North America, two lake whitefish lineages have repeatedly colonized postglacial lakes ~12,000 years ago, and a dwarf limnetic species has evolved multiple times from the normal benthic species. Reproductive isolation is incomplete between them; viable hybrids can be generated in the laboratory but significant mortality occurs and is associated with a malformed phenotype in backcross embryos, thus revealing a hybrid breakdown syndrome. By means of RNA-seq analyses, the objective of this study was to determine which genes were misregulated in hybrids and rigorously test the hypothesis of transposable element reactivation. We compared the transcriptomic landscape in pure embryos, F1-hybrids, and healthy and malformed backcrosses at the late embryonic stage. Extensive expression differences consistent with previously documented adaptive divergence between pure normal and dwarf embryos were identified for the first time. Pronounced transcriptome-wide deregulation in malformed backcrosses was observed, with over 15% of transcripts differentially expressed in all comparisons, compared with 1.5% between pure parental forms. Convincing evidence of transposable elements and noncoding transcripts reactivation in malformed backcrosses is presented. We propose that hybrid breakdown likely results from extensive genomic incompatibilities, plausibly encompassing transposable elements. Combined with previous studies, these results reveal synergy among many reproductive barriers, thus maintaining divergence between these two young whitefish species.
Subject(s)
DNA Transposable Elements/genetics , Salmonidae/genetics , Animals , Evolution, Molecular , Gene Expression Regulation, Developmental , Genetic Speciation , Hybridization, Genetic , Lakes , Models, Genetic , RNA, Untranslated/genetics , Salmonidae/abnormalities , Salmonidae/embryology , Sequence Analysis, RNA , TranscriptomeABSTRACT
Next-generation sequencing (NGS) is revolutionising marker development and the rapidly increasing amount of transcriptomes published across a wide variety of taxa is providing valuable sequence databases for the identification of genetic markers without the need to generate new sequences. Microsatellites are still the most important source of polymorphic markers in ecology and evolution. Motivated by our long-term interest in the adaptive radiation of a non-model species complex of whitefishes (Coregonus spp.), in this study, we focus on microsatellite characterisation and multiplex optimisation using transcriptome sequences generated by Illumina® and Roche-454, as well as online databases of Expressed Sequence Tags (EST) for the study of whitefish evolution and demographic history. We identified and optimised 40 polymorphic loci in multiplex PCR reactions and validated the robustness of our analyses by testing several population genetics and phylogeographic predictions using 494 fish from five lakes and 2 distinct ecotypes.
Subject(s)
Fishes/genetics , Microsatellite Repeats/genetics , Transcriptome/genetics , Animals , Databases, Genetic , Expressed Sequence Tags/metabolism , Fishes/metabolism , Genetic Markers/genetics , Genetics, Population/methods , High-Throughput Nucleotide Sequencing/methodsABSTRACT
Allopatric speciation may be the principal mechanism generating new species. Yet, it remains difficult to judge the generality of this process because few studies have provided evidence that geographic isolation has triggered the development of reproductive isolation over multiple species of a regional fauna. Here, we first combine results from new empirical data sets (7 taxa) and published literature (9 taxa) to show that the eastern Great Lakes drainage represents a multispecies suture zone for glacial lineages of freshwater fishes with variable levels of genetic divergence. Second, we performed amplified fragment length polymorphism analyses among four pairs of lineages. Results indicate that lineages with relatively deep levels of mtDNA 5' COI (barcode) sequence divergence (>2%) developed strong reproductive barriers, while lineages with lower levels of divergence show weaker reproductive isolation when found in sympatry. This suggests that a threshold of 2% sequence divergence at mtDNA could be used as a first step to flag cryptic species in North American freshwater fishes. By describing different levels of divergence and reproductive isolation in different co-occurring fishes, we offer strong evidence that allopatric speciation has contributed significantly to the diversification of north-eastern American freshwater fishes and confirm that Pleistocene glacial cycles can be viewed as a 'speciation pump' that played a predominant role in generating biodiversity.