Intergenomic Conflict Research Articles

Inheritance through the cytoplasm

Most heritable information in eukaryotic cells is encoded in the nuclear genome, with inheritance patterns following classic Mendelian segregation. Genomes residing in the cytoplasm, however, prove to be a peculiar exception to this rule. Cytoplasmic genetic elements are generally maternally inherited, although there are several exceptions where these are paternally, biparentally or doubly-uniparentally inherited. In this review, we examine the diversity and peculiarities of cytoplasmically inherited genomes, and the broad evolutionary consequences that non-Mendelian inheritance brings. We first explore the origins of vertical transmission and uniparental inheritance, before detailing the vast diversity of cytoplasmic inheritance systems across Eukaryota. We then describe the evolution of genomic organisation across lineages, how this process has been shaped by interactions with the nuclear genome and population genetics dynamics. Finally, we discuss how both nuclear and cytoplasmic genomes have evolved to co-inhabit the same host cell via one of the longest symbiotic processes, and all the opportunities for intergenomic conflict that arise due to divergence in inheritance patterns. In sum, we cannot understand the evolution of eukaryotes without understanding hereditary symbiosis.

Evaluating evidence of mitonuclear incompatibilities with the sex chromosomes in an avian hybrid zone.

The exploration of hybrid zones and the intergenomic conflicts exposed through hybridization provide windows into the processes of divergence and speciation. Sex chromosomes and mitonuclear incompatibilities have strong associations with the genetics of hybrid dysfunction. In ZW sex-determining systems, maternal co-inheritance of the mitochondrial and W chromosomes immediately exposes incompatibilities between these maternal contributions of one species and the Z chromosome of another. We analyze mitochondrial and Z chromosome admixture in the long-tailed finch (Poephila acuticauda) of Australia, where hybridizing subspecies differ prominently in Z chromosome genotype and in bill color, yet the respective centers of geographic admixture for these two traits are offset by 350 km. We report two well-defined mitochondrial clades that diverged ∼0.5 million years ago. Mitochondrial contact is geographically co-located within a hybrid zone of Z chromosome admixture and is displaced from bill color admixture by nearly 400 km. Consistent with Haldane's rule expectations, hybrid zone females are significantly less likely than males to carry an admixed Z chromosome or have mismatched Z-mitochondrial genotypes. Furthermore, there are significantly fewer than expected mitonuclear mismatches in hybrid zone females and paternal backcross males. Results suggest a potential for mitonuclear/sex chromosome incompatibilities in the emergence of reproductive isolation in this system.

Elucidating Mitochondrial DNA Markers of Ogura-Based CMS Lines in Indian Cauliflowers (Brassica oleracea var. botrytis L.) and Their Floral Abnormalities Due to Diversity in Cytonuclear Interactions.

Mitochondrial markers can be used to differentiate diverse mitotypes as well as cytoplasms in angiosperms. In cauliflower, cultivation of hybrids is pivotal in remunerative agriculture and cytoplasmic male sterile lines constitute an important component of the hybrid breeding. In diversifying the source of male sterility, it is essential to appropriately differentiate among the available male sterile cytoplasms in cauliflower. PCR polymorphism at the key mitochondrial genes associated with male sterility will be instrumental in analyzing, molecular characterization, and development of mitotype-specific markers for differentiation of different cytoplasmic sources. Presence of auto- and alloplasmic cytonuclear combinations result in complex floral abnormalities. In this context, the present investigation highlighted the utility of organelle genome-based markers in distinguishing cytoplasm types in Indian cauliflowers and unveils the epistatic effects of the cytonuclear interactions influencing floral phenotypes. In PCR-based analysis using a set of primers targeted to orf-138, 76 Indian cauliflower lines depicted the presence of Ogura cytoplasm albeit the amplicons generated exhibited polymorphism within the ofr-138 sequence. The polymorphic fragments were found to be spanning over 200–280 bp and 410–470 bp genomic regions of BnTR4 and orf125, respectively. Sequence analysis revealed that such cytoplasmic genetic variations could be attributed to single nucleotide polymorphisms and insertion or deletions of 31/51 nucleotides. The cytoplasmic effects on varying nuclear-genetic backgrounds rendered an array of floral abnormalities like reduction in flower size, fused flowers, splitted style with the exposed ovule, absence of nonfunctional stamens, and petaloid stamens. These floral malformations caused dysplasia of flower structure affecting female fertility with inefficient nectar production. The finding provides an important reference to ameliorate understanding of mechanism of cytonuclear interactions in floral organ development in Brassicas. The study paves the way for unraveling developmental biology of CMS phenotypes in eukaryotic organisms and intergenomic conflict in plant speciation.

Male spiders control offspring sex ratio through greater production of female-determining sperm

Sex allocation theory predicts that when sons and daughters have different reproductive values, parents should adjust offspring sex ratio towards the sex with the higher fitness return. Haplo-diploid species directly control offspring sex ratio, but species with chromosomal sex determination (CSD) were presumed to be constrained by Mendelian segregation. There is now increasing evidence that CSD species can adjust sex ratio strategically, but the underlying mechanism is not well understood. One hypothesis states that adaptive control is more likely to evolve in the heterogametic sex through a bias in gamete production. We investigated this hypothesis in males as the heterogametic sex in two social spider species that consistently show adaptive female-biased sex ratio and in one subsocial species that is characterized by equal sex ratio. We quantified the production of male (0) and female (X) determining sperm cells using flow cytometry, and show that males of social species produce significantly more X-carrying sperm than 0-sperm, on average 70%. This is consistent with the production of more daughters. Males of the subsocial species produced a significantly lower bias of 54% X-carrying sperm. We also investigated whether inter-genomic conflict between hosts and their endosymbionts may explain female bias. Next generation sequencing showed that five common genera of bacterial endosymbionts known to affect sex ratio are largely absent, ruling out that endosymbiont bacteria bias sex ratio in social spiders. Our study provides evidence for paternal control over sex allocation through biased gamete production as a mechanism by which the heterogametic sex in CSD species adaptively adjust offspring sex ratio.

Reductions in complexity of mitochondrial genomes in lichen-forming fungi shed light on genome architecture of obligate symbioses.

Symbioses among co-evolving taxa are often marked by genome reductions such as a loss of protein-coding genes in at least one of the partners as a means of reducing redundancy or intergenomic conflict. To explore this phenomenon in an iconic yet under-studied group of obligate symbiotic organisms, mitochondrial genomes of 22 newly sequenced and annotated species of lichenized fungi were compared to 167 mitochondrial genomes of nonlichenized fungi. Our results demonstrate the first broad-scale loss of atp9 from mitochondria of lichenized fungi. Despite key functions in mitochondrial energy production, we show that atp9 has been independently lost in three different lineages spanning 10 of the 22 studied species. A search for predicted, functional copies of atp9 among genomes of other symbionts involved in each lichen revealed the full-length, presumably functional copies of atp9 in either the photosynthetic algal partner or in other symbiotic fungi in all 10 instances. Together, these data yield evidence of an obligate symbiotic relationship in which core genomic processes have been streamlined, likely due to co-evolution.

Genomic Signatures of Sexual Conflict.

Sexual conflict is a specific class of intergenomic conflict that describes the reciprocal sex-specific fitness costs generated by antagonistic reproductive interactions. The potential for sexual conflict is an inherent property of having a shared genome between the sexes and, therefore, is an extreme form of an environment-dependent fitness effect. In this way, many of the predictions from environment-dependent selection can be used to formulate expected patterns of genome evolution under sexual conflict. However, the pleiotropic and transmission constraints inherent to having alleles move across sex-specific backgrounds from generation to generation further modulate the anticipated signatures of selection. We outline methods for detecting candidate sexual conflict loci both across and within populations. Additionally, we consider the ability of genome scans to identify sexually antagonistic loci by modeling allele frequency changes within males and females due to a single generation of selection. In particular, we highlight the need to integrate genotype, phenotype, and functional information to truly distinguish sexual conflict from other forms of sexual differentiation.

Transposons to toxins: the provenance, architecture and diversification of a widespread class of eukaryotic effectors.

Enzymatic effectors targeting nucleic acids, proteins and other cellular components are the mainstay of conflicts across life forms. Using comparative genomics we identify a large class of eukaryotic proteins, which include effectors from oomycetes, fungi and other parasites. The majority of these proteins have a characteristic domain architecture with one of several N-terminal ‘Header’ domains, which are predicted to play a role in trafficking of these effectors, including a novel version of the Ubiquitin fold. The Headers are followed by one or more diverse C-terminal domains, such as restriction endonuclease (REase), protein kinase, HNH endonuclease, LK-nuclease (a RNase) and multiple distinct peptidase domains, which are predicted to carry their toxicity determinants. The most common types of these proteins appear to have originated from prokaryotic transposases (e.g. TN7 and Mu) and combine a CDC6/ORC1-STAND clade NTPase domain with a C-terminal REase domain. Other than the so-called Crinkler effectors of oomycetes and fungi, these effectors are encoded by other eukaryotic parasites such as trypanosomatids (the RHS proteins) and the rhizarian Plasmodiophora, and symbionts like Capsaspora. Remarkably, we also find these proteins in free-living eukaryotes, including several viridiplantae, fungi, amoebozoans and animals. These versions might either still be transposons or function in other poorly understood eukaryote-specific inter-organismal and inter-genomic conflicts. These include the Medea1 selfish element of Tribolium that spreads via post-zygotic killing. We present a unified mechanism for the recombination-dependent diversification and action of this widespread class of molecular weaponry deployed across diverse conflicts ranging from parasitic to free-living forms.

KARYOTYPE ALTERATIONS AFTER HYBRIDIZATION BETWEEN Pennisetum purpureum AND Pennisetum glaucum

ABSTRACTNapier grass and pearl millet are tropical forages from the genus Pennisetum. The variability in those species is explored in breeding programs of forages, as well as in the production of interspecific hybrids. Hybridization is a phenomenon that leads to intergenomic conflicts following the elimination of genomic sequences. In this sense, the present work aimed to study the genomic alterations occurring after interspecific hybridization of pearl millet and Napier grass with the use of cytogenetics and flow cytometry tools. These methods allowed the evaluation of chromosome morphometry, DNA content and genomic ratio in pearl millet, Napier grass and hybrids. It was observed that pearl millet and Napier grass have chromosomes with superposed size. The hybrid presents chromosomes that are smaller than expected, leading to karyotype alterations. Additionally, comparing the DNA content of parents and hybrids, loss of DNA content was demonstrated. Further, changes in the pearl millet and Napier grass genome ratio were also verified in the hybrid nucleus. Moreover, genomic rearrangements were shown to occur through karyotype alterations in the hybrid.

Dispatches

Dispatches

The Potential Role of Sexual Conflict and Sexual Selection in Shaping the Genomic Distribution of Mito-nuclear Genes

Mitochondrial interactions with the nuclear genome represent one of life’s most important co-evolved mutualisms. In many organisms, mitochondria are maternally inherited, and in these cases, co-transmission between the mitochondrial and nuclear genes differs across different parts of the nuclear genome, with genes on the X chromosome having two-third probability of co-transmission, compared with one-half for genes on autosomes. These asymmetrical inheritance patterns of mitochondria and different parts of the nuclear genome have the potential to put certain gene combinations in inter-genomic co-adaptation or conflict. Previous work in mammals found strong evidence that the X chromosome has a dearth of genes that interact with the mitochondria (mito-nuclear genes), suggesting that inter-genomic conflict might drive genes off the X onto the autosomes for their male-beneficial effects. Here, we developed this idea to test coadaptation and conflict between mito-nuclear gene combinations across phylogenetically independent sex chromosomes on a far broader scale. We found that, in addition to therian mammals, only Caenorhabditis elegans showed an under-representation of mito-nuclear genes on the sex chromosomes. The remaining species studied showed no overall bias in their distribution of mito-nuclear genes. We discuss possible factors other than inter-genomic conflict that might drive the genomic distribution of mito-nuclear genes.

Two novel PIWI families: roles in inter-genomic conflicts in bacteria and Mediator-dependent modulation of transcription in eukaryotes

BackgroundThe PIWI module, found in the PIWI/AGO superfamily of proteins, is a critical component of several cellular pathways including germline maintenance, chromatin organization, regulation of splicing, RNA interference, and virus suppression. It binds a guide strand which helps it target complementary nucleic strands.ResultsHere we report the discovery of two divergent, novel families of PIWI modules, the first such to be described since the initial discovery of the PIWI/AGO superfamily over a decade ago. Both families display conservation patterns consistent with the binding of oligonucleotide guide strands. The first family is bacterial in distribution and is typically encoded by a distinctive three-gene operon alongside genes for a restriction endonuclease fold enzyme and a helicase of the DinG family. The second family is found only in eukaryotes. It is the core conserved module of the Med13 protein, a subunit of the CDK8 subcomplex of the transcription regulatory Mediator complex.ConclusionsBased on the presence of the DinG family helicase, which specifically acts on R-loops, we infer that the first family of PIWI modules is part of a novel RNA-dependent restriction system which could target invasive DNA from phages, plasmids or conjugative transposons. It is predicted to facilitate restriction of actively transcribed invading DNA by utilizing RNA guides. The PIWI family found in the eukaryotic Med13 proteins throws new light on the regulatory switch through which the CDK8 subcomplex modulates transcription at Mediator-bound promoters of highly transcribed genes. We propose that this involves recognition of small RNAs by the PIWI module in Med13 resulting in a conformational switch that propagates through the Mediator complex.ReviewersThis article was reviewed by Sandor Pongor, Frank Eisenhaber and Balaji Santhanam.

The role of endosymbionts in the evolution of haploid-male genetic systems in scale insects (Coccoidea).

There is an extraordinary diversity in genetic systems across species, but this variation remains poorly understood. In part, this is because the mechanisms responsible for transitions between systems are often unknown. A recent hypothesis has suggested that conflict between hosts and endosymbiotic microorganisms over transmission could drive the transition from diplodiploidy to systems with male haploidy (haplodiploidy, including arrhenotoky and paternal genome elimination [PGE]). Here, we present the first formal test of this idea with a comparative analysis across scale insects (Hemiptera: Coccoidea). Scale insects are renowned for their large variation in genetic systems, and multiple transitions between diplodiploidy and haplodiploidy have taken place within this group. Additionally, most species rely on endosymbiotic microorganisms to provide them with essential nutrients lacking in their diet. We show that species harboring endosymbionts are indeed more likely to have a genetic system with male haploidy, which supports the hypothesis that endosymbionts might have played a role in the transition to haplodiploidy. We also extend our analysis to consider the relationship between endosymbiont presence and transitions to parthenogenesis. Although in scale insects there is no such overall association, species harboring eukaryote endosymbionts were more likely to be parthenogenetic than those with bacterial symbionts. These results support the idea that intergenomic conflict can drive the evolution of novel genetic systems and affect host reproduction.

Is the COI barcoding gene involved in speciation through intergenomic conflict?

We here test the proposition that changes in the barcoding region of COI are commonly involved in speciation through intergenomic conflict. We demonstrate that this is unlikely given that even with incomplete taxon sampling, 78–90% of closely-related animal species have identical COI amino acid sequences. In addition, in those cases where amino acid substitutions between closely related species are observed, the inter- and intra-specific substitution patterns are very similar and/or lack consistent differences in the number, position and type of amino acid change. Overall, we conclude that there is little evidence for a widespread involvement of the barcoding gene in speciation.

Nuclear and genome dynamics in multinucleate ascomycete fungi.

Genetic variation between individuals is essential to evolution and adaptation. However, intra-organismic genetic variation also shapes the life histories of many organisms, including filamentous fungi. A single fungal syncytium can harbor thousands or millions of mobile and potentially genotypically different nuclei, each having the capacity to regenerate a new organism. Because the dispersal of asexual or sexual spores propagates individual nuclei in many of these species, selection acting at the level of nuclei creates the potential for competitive and cooperative genome dynamics. Recent work in Neurospora crassa and Sclerotinia sclerotiorum has illuminated how nuclear populations are coordinated for fungal growth and other behaviors and has revealed both molecular and physical mechanisms for preventing and policing inter-genomic conflict. Recent results from population-level genomic studies in a variety of filamentous fungi suggest that nuclear exchange between mycelia and recombination between heterospecific nuclei may be of more importance to fungal evolution, diversity and the emergence of newly virulent strains than has previously been recognized.

Genomic conflict in scale insects: the causes and consequences of bizarre genetic systems

It is now clear that mechanisms of sex determination are extraordinarily labile, with considerable variation across all taxonomic levels. This variation is often expressed through differences in the genetic system (XX-XY, XX-XO, haplodiploidy, and so on). Why there is so much variation in such a seemingly fundamental process has attracted much attention, with recent ideas concentrating on the possible role of genomic conflicts of interest. Here we consider the role of inter- and intra-genomic conflicts in one large insect taxon: the scale insects. Scale insects exhibit a dizzying array of genetic systems, and their biology promotes conflicts of interest over transmission and sex ratio between male- and female-expressed genes, parental- and offspring-expressed genes (both examples of intra-genomic conflict) and between scale insects and their endosymbionts (inter-genomic conflict). We first review the wide range of genetic systems found in scale insects and the possible evolutionary transitions between them. We then outline the theoretical opportunities for genomic conflicts in this group and how these might influence sex determination and sex ratio. We then consider the evidence for these conflicts in the evolution of sex determination in scale insects. Importantly, the evolution of novel genetic systems in scale insects has itself helped create new conflicts of interest, for instance over sex ratio. As a result, a major obstacle to our understanding of the role of conflict in the evolution of sex-determination and genetic systems will be the difficulty in identifying the direction of causal relationships. We conclude by outlining possible experimental and comparative approaches to test more effectively how important genomic conflicts have been.

Signature of Diversifying Selection on Members of the Pentatricopeptide Repeat Protein Family in Arabidopsis lyrata

Pentatricopeptide repeat (PPR) proteins compose a family of nuclear-encoded transcriptional regulators of cytoplasmic genes. They have shown dramatic expansion in copy number in plants, and although the functional importance of many remains unclear, a subset has been repeatedly implicated as nuclear restorers for cytoplasmic male sterility. Here we investigate the molecular population genetics and molecular evolution of seven single-copy PPR genes in the outcrossing model plant Arabidopsis lyrata. In comparison with neutral reference loci, we find, on average, elevated levels of polymorphism and an excess of high-frequency variants at these PPR genes, suggesting that natural selection is maintaining polymorphism at some of these loci. This elevation in diversity persists when we control for divergence and generally decreases in the flanking regions, suggesting that these genes are themselves the targets of selection. Some of the PPR genes also demonstrate elevated population differentiation, which is consistent with spatially varying selection. In contrast, no comparable patterns are observed at these loci in A. thaliana, providing no evidence for the action of balancing selection in this selfing species. Taken together, these results suggest that a subset of PPR genes may be subject to balancing selection associated with ongoing cytonuclear coevolution in the outcrossing A. lyrata, which is possibly mediated either by intergenomic conflict or by compensatory evolution.

Pre‐ and post‐fertilization maternal provisioning in livebearing fish species and their hybrids (Poeciliidae: Poeciliopsis)

Summary 1. Viviparous organisms vary greatly in their level of post-fertilization maternal provisioning and extensive provisioning (including very complex placentas) has evolved dozens of times in vertebrates. Through the use of species representing transitional states we aim to explore and develop empirically supported hypotheses that explain how such a complex trait has evolved. 2. In this study, we investigated the life histories and patterns of post-fertilization maternal provisioning in naturally occurring, all-female, hybrids between Poeciliopsis monacha , a viviparous species that produces large eggs and nourishes its embryos via stored yolk (lecithotrophy) and P. lucida , which produces small eggs and nourishes its embryos after fertilization via a follicular placenta (matrotrophy). Hybrids can be diploid or triploid, leading to different levels of gene dosage from the parental species. 3. We found that the extent of superfetation and average brood size of the hybrids did not differ significantly from their sexual parental species even though the latter was much lower in the hybrids. Moreover, the allodiploid, P. monacha-lucida , has intermediate sized eggs, whereas the allotriploid, P. monacha-monacha-lucida , produces eggs of similar size to those of P. monacha . The degree of post-fertilization maternal provisioning was unrelated to genomic dosages, with wild-caught hybrids being lecithotrophic, as seen in the maternal species ( P. monacha ). 4. Our results with naturally occurring P. monacha-lucida hybrids differed from those obtained with laboratory-synthesized hybrid clones, which were either lecithotrophic or weakly matrotrophic. Consequently, we propose two non-mutually exclusive hypotheses to explain why lecithotrophic clones might be favoured in the wild. One hypothesis suggests that lecithotrophic hybrids minimize competition with the matrotrophic paternal sexual species from which they require sperm to reproduce. Alternatively, we propose that natural selection has eliminated matrotrophic hybrids that suffer from intergenomic conflict in the degree of post-fertilization maternal provisioning. 5. We have thus identified an empirical system and developed testable hypotheses that will help elucidate the selective pressures that caused the evolution of post-fertilization maternal provisioning and potentially provide an opportunity to explore how epigenetic factors (e.g., intergenomic conflict) might influence this complex trait.

Intergenomic conflict revealed by patterns of sex-biased gene expression

Intergenomic conflict can affect the distribution of genes across eukaryotic genomes. Because the phenotypic optima of males and females often differ, the fitness consequences of newly arisen alleles might not be concordant between the sexes and can be sexually antagonistic--genetic variants favored in one sex are deleterious in the other. In this article, we demonstrate that previously unexplained patterns of sex-biased gene expression in Drosophila melanogaster might have evolved by sexual antagonism, and that the majority of sex-biased expression is due to adaptive changes in males, implying that males experience stronger selection than females.

RAPID EVOLUTION OF POSTZYGOTIC REPRODUCIVE ISOLATION IN STALK-EYED FLIES

We test the relative rates of evolution of pre- and postzygotic reproductive isolation using eight populations of the sexually dimorphic stalk-eyed flies Cyrtodiopsis dalmanni and C. whitei. Flies from these populations exhibit few morphological differences yet experience strong sexual selection on male eyestalks. To measure reproductive isolation we housed one male and three female flies from within and between these populations in replicate cages and then recorded mating behavior, sperm transfer, progeny production, and hybrid fertility. Using a phylogeny based on partial sequences of two mitochondrial genes, we found that premating isolation, postmating isolation prior to hybrid eclosion, and female hybrid sterility evolve gradually with respect to mitochondrial DNA sequence divergence. In contrast, male hybrid sterility evolves much more rapidly-at least twice as fast as any other form of reproductive isolation. Hybrid sterility, therefore, obeys Haldane's rule. Although some brood sex ratios were female biased, average brood sex ratio did not covary with genetic distance, as would be expected if hybrid inviability obeyed Haldane's rule. The likelihood that forces including sexual selection and intra- and intergenomic conflict may have contributed to these patterns is discussed.

Reproductive mode and speciation: the viviparity-driven conflict hypothesis.

In birds and frogs, species pairs retain the capacity to produce viable hybrids for tens of millions of years, an order of magnitude longer than mammals. What accounts for these differences in relative rates of pre- and postzygotic isolation? We propose that reproductive mode is a critically important but previously overlooked factor in the speciation process. Viviparity creates a post-fertilization arena for genomic conflicts absent in egg-laying species. With viviparity, conflict can arise between: mothers and embryos; sibling embryos in the womb, and maternal and paternal genomes within individual embryos. Such intra- and intergenomic conflicts result in perpetual antagonistic coevolution, thereby accelerating interpopulation postzygotic isolation. In addition, by generating intrapopulation genetic incompatibility, viviparity-driven conflict favors polyandry and limits the potential for precopulatory divergence. Mammalian diversification is characterized by rapid evolution of incompatible feto-maternal interactions, asymmetrical postzygotic isolation, disproportionate effects of genomically-imprinted genes, and "F(2) hybrid enhancement. " The viviparity-driven conflict hypothesis provides a parsimonious explanation for these patterns in mammalian evolution.