Rootstock-Mediated Genetic Variance in Cadmium Uptake by Juvenile Cacao (Theobroma cacao L.) Genotypes, and Its Effect on Growth and Physiology

Grafting typically offers a shortcut to breed tree orchards throughout a multidimensional space of traits. Despite an overwhelming spectrum of rootstock-mediated effects on scion traits observed across several species, the exact nature and mechanisms underlying the rootstock-mediated effects on scion traits in cacao (Theobroma cacao L.) plants often remain overlooked. Therefore, we aimed to explicitly quantify rootstock-mediated genetic contributions in recombinant juvenile cacao plants across target traits, specifically cadmium (Cd) uptake, and its correlation with growth and physiological traits. Content of chloroplast pigments, fluorescence of chlorophyll a, leaf gas exchange, nutrient uptake, and plant biomass were examined across ungrafted saplings and target rootstock × scion combinations in soils with contrasting levels of Cd. This panel considered a total of 320 progenies from open-pollinated half-sib families and reciprocal full-sib progenies (derived from controlled crosses between the reference genotypes IMC67 and PA121). Both family types were used as rootstocks in grafts with two commercial clones (ICS95 and CCN51) commonly grown in Colombia. A pedigree-based best linear unbiased prediction (A-BLUP) mixed model was implemented to quantify rootstock-mediated narrow-sense heritability (h2) for target traits. A Cd effect measured on rootstocks before grafting was observed in plant biomass, nutrient uptake, and content of chloroplast pigments. After grafting, damage to the Photosystem II (PSII) was also evident in some rootstock × scion combinations. Differences in the specific combining ability for Cd uptake were mostly detected in ungrafted rootstocks, or 2 months after grafting with the clonal CCN51 scion. Moderate rootstock effects (h2> 0.1) were detected before grafting for five growth traits, four nutrient uptake properties, and chlorophylls and carotenoids content (h2 = 0.19, 95% CI 0.05–0.61, r = 0.7). Such rootstock effects faded (h2< 0.1) when rootstock genotypes were examined in soils without Cd, or 4 months after grafting. These results suggest a pervasive genetic conflict between the rootstock and the scion genotypes, involving the triple rootstock × scion × soil interaction when it refers to Cd and nutrient uptake, early growth, and photosynthetic process in juvenile cacao plants. Overall, deepening on these findings will harness early breeding schemes of cacao rootstock genotypes compatible with commercial clonal scions and adapted to soils enriched with toxic levels of Cd.

Interacting host modifier systems control Wolbachia-induced cytoplasmic incompatibility in a haplodiploid mite

Many reproductive parasites such as Wolbachia spread within host populations by inducing cytoplasmic incompatibility (CI). CI occurs when parasite-modified sperm fertilizes uninfected eggs. In haplodiploid hosts, CI can lead to different phenotypes depending on whether the fertilized eggs die or develop into males. Genetic conflict theories predict the evolution of host modulation of CI, which in turn strongly influences the stability of reproductive parasitism. Yet, despite the ubiquity of CI-inducing parasites in nature, there is no conclusive evidence for strong intraspecific host modulation of CI strength and phenotype. Here, we tested for intraspecific host modulation of Wolbachia-induced CI in haplodiploid Tetranychus spider mites. Using a single CI-inducing Wolbachia variant and mitochondrion, a Tetranychus urticae nuclear panel was created that consisted of infected and cured near-isogenic lines. We performed a highly replicated age-synchronized full diallel cross comprised of incompatible and compatible control crosses. We uncovered host modifier systems that strongly suppress CI strength when carried by infected T. urticae males. Interspecific crosses showed that the male modifier systems suppress CI strength across species boundaries. We also observed a continuum of CI phenotypes in our crosses and identified strong intraspecific female modulation of CI phenotype when paired with a specific male genotype. Crosses established a recessive genetic basis for the maternal effect and were consistent with polygenic Mendelian inheritance. Our findings identify spermatogenesis as an important target of selection for host suppression of CI strength and underscore the importance of maternal genetic effects for the CI phenotype. Both mechanisms interacted with the genotype of the mating partner, revealing that intraspecific host modulation of CI strength and phenotype is underpinned by complex genetic architectures.

To export, or not to export: how nuclear export factor variants resolve Piwi's dilemma

Piwi-interacting RNAs (piRNAs) defend animal gonads by guiding PIWI-clade Argonaute proteins to silence transposons. The nuclear Piwi/piRNA complexes confer transcriptional repression of transposons, which is accompanied with heterochromatin formation at target loci. On the other hand, piRNA clusters, genomic loci that transcribe piRNA precursors composed of transposon fragments, are often recognized by piRNAs to define their heterochromatic identity. Therefore, Piwi/piRNA complexes must resolve this conundrum of silencing transposons while allowing the expression of piRNA precursors, at least in Drosophila germlines. This review is focused on recent advances how the piRNA pathway deals with this genetic conflict.

The X-linked splicing regulator MBNL3 has been co-opted to restrict placental growth in eutherians

The eutherian placenta is a major site for parental genetic conflict. Here, we identify the X-linked Mbnl3 gene as a novel player in this dispute. Mbnl3 belongs to an RNA binding protein family whose members regulate alternative splicing and other aspects of RNA metabolism in association with cellular differentiation. We find that, in eutherians, Mbnl3 has become specifically expressed in placenta and has undergone accelerated sequence evolution leading to changes in its RNA binding specificities. Although its molecular roles are partly redundant with those of Mbnl2, Mbnl3 has also acquired novel biological functions. In particular, whereas Mbnl2;Mbnl3 double knockout mice display severe placental maturation defects leading to strong histological and functional abnormalities, Mbnl3 knockout alone results in increased placental growth and favors placental and fetal resource allocation during limiting conditions.

Diversity of Modes of Reproduction and Sex Determination Systems in Invertebrates, and the Putative Contribution of Genetic Conflict

About eight million animal species are estimated to live on Earth, and all except those belonging to one subphylum are invertebrates. Invertebrates are incredibly diverse in their morphologies, life histories, and in the range of the ecological niches that they occupy. A great variety of modes of reproduction and sex determination systems is also observed among them, and their mosaic-distribution across the phylogeny shows that transitions between them occur frequently and rapidly. Genetic conflict in its various forms is a long-standing theory to explain what drives those evolutionary transitions. Here, we review (1) the different modes of reproduction among invertebrate species, highlighting sexual reproduction as the probable ancestral state; (2) the paradoxical diversity of sex determination systems; (3) the different types of genetic conflicts that could drive the evolution of such different systems.

Does degeneration or genetic conflict shape gene content on UV sex chromosomes?

Studies of sex chromosomes have played a central role in understanding the consequences of suppressed recombination and sex-specific inheritance among several genomic phenomena. However, we argue that these efforts will benefit from a more rigorous examination of haploid UV sex chromosome systems, in which both the female-limited (U) and male-limited (V) experience suppressed recombination and sex-limited inheritance, and both are transcriptionally active in the haploid and diploid states. We review the life cycle differences that generate UV sex chromosomes and genomic data showing that ancient UV systems have evolved independently in many eukaryotic groups, but gene movement on and off the sex chromosomes, and potentially degeneration continue to shape the current gene content of the U and V chromosomes. Although both theory and empirical data show that the evolution of UV sex chromosomes is shaped by many of the same processes that govern diploid sex chromosome systems, we highlight how the symmetrical inheritance between the UV chromosomes provide an important test of sex-limited inheritance in shaping genome architecture. We conclude by examining how genetic conflict (over sexual dimorphism, transmission-ratio distortion, or parent-offspring conflict) may drive gene gain on UV sex chromosomes, and highlight the role of breeding system in governing the action of these processes. Collectively these observations demonstrate the potential for evolutionary genomic analyses of varied UV sex chromosome systems, combined with natural history studies, to understand how genetic conflict shapes sex chromosome gene content.

Functional divergence of the bag of marbles gene in the Drosophila melanogaster species group

The combination of recent advances in both genomic and gene editing technologies have opened up new possibilities for assessing the functional consequences and drivers of positive selection. In Drosophila melanogaster, a key germline stem cell differentiation factor, bag of marbles (bam) shows rapid bursts of amino acid fixations between its D. melanogaster and its sibling species D. simulans, but not in the outgroup species D. ananassae. We previously hypothesized that a genetic conflict with the maternally inherited, intracellular bacteria W. pipientis could be driving the adaptive evolution of bam as W. pipientis increases the fertility of a bam partial loss of function mutant. However, we have not been able to further test this hypothesis by assessing bam variation in other Drosophila lineages and their interactions with W. pipientis because bam function has not been examined in non-melanogaster Drosophila species. Since bam is rapidly evolving at the protein level, its function may not be conserved between species, and therefore different evolutionary pressures may be shaping bam in individual lineages. Here, we ask if bam is necessary for GSC daughter differentiation in five Drosophila species in the melanogaster species group that span approximately 15 million years of divergence and show different patterns of nucleotide sequence evolution at bam. We find that bam function is not fully conserved across these species, and that bam function may change on a relatively short time scale. Ultimately, we conclude that a simple gain in function as the germline stem cell differentiation factor alone does not explain our population genetic and functional genetic results we have observed. Our findings provide a foundation on which to explore the evolution of bam as a GSC differentiation factor and its interactions with W. pipientis in specific lineages.

Hybrid Sterility, Genetic Conflict and Complex Speciation: Lessons From the Drosophila simulans Clade Species

The three fruitfly species of the Drosophila simulans clade— D. simulans, D. mauritiana, and D. sechellia— have served as important models in speciation genetics for over 40 years. These species are reproductively isolated by geography, ecology, sexual signals, postmating-prezygotic interactions, and postzygotic genetic incompatibilities. All pairwise crosses between these species conform to Haldane’s rule, producing fertile F1 hybrid females and sterile F1 hybrid males. The close phylogenetic proximity of the D. simulans clade species to the model organism, D. melanogaster, has empowered genetic analyses of their species differences, including reproductive incompatibilities. But perhaps no phenotype has been subject to more continuous and intensive genetic scrutiny than hybrid male sterility. Here we review the history, progress, and current state of our understanding of hybrid male sterility among the D. simulans clade species. Our aim is to integrate the available information from experimental and population genetics analyses bearing on the causes and consequences of hybrid male sterility. We highlight numerous conclusions that have emerged as well as issues that remain unresolved. We focus on the special role of sex chromosomes, the fine-scale genetic architecture of hybrid male sterility, and the history of gene flow between species. The biggest surprises to emerge from this work are that (i) genetic conflicts may be an important general force in the evolution of hybrid incompatibility, (ii) hybrid male sterility is polygenic with contributions of complex epistasis, and (iii) speciation, even among these geographically allopatric taxa, has involved the interplay of gene flow, negative selection, and positive selection. These three conclusions are marked departures from the classical views of speciation that emerged from the modern evolutionary synthesis.

Patterns and Mechanisms of Sex Ratio Distortion in the Collaborative Cross Mouse Mapping Population

In species with single-locus chromosome-based mechanisms of sex determination, the laws of segregation predict an equal ratio of females to males at birth. Here, we show that departures from this Mendelian expectation are commonplace in the 8-way recombinant inbred Collaborative Cross (CC) mouse population. More than one-third of CC strains exhibit significant sex ratio distortion (SRD) at wean, with twice as many male-biased than female-biased strains. We show that these pervasive sex biases persist across multiple breeding environments, are stable over time, are not fully mediated by maternal effects, and are not explained by sex-biased neonatal mortality. SRD exhibits a heritable component, but QTL mapping analyses and targeted investigations of sex determination genes fail to nominate any large effect loci. These findings, combined with the reported absence of sex ratio biases in the CC founder strains, suggest that SRD manifests from multilocus combinations of alleles only uncovered in recombined CC genomes. We speculate that the genetic shuffling of eight diverse parental genomes during the early CC breeding generations led to the decoupling of sex-linked drivers from their co-evolved suppressors, unleashing complex, multiallelic systems of sex chromosome drive. Consistent with this interpretation, we show that several CC strains exhibit copy number imbalances at co-evolved X- and Y-linked ampliconic genes that have been previously implicated in germline genetic conflict and SRD in house mice. Overall, our findings reveal the pervasiveness of SRD in the CC population and nominate the CC as a powerful resource for investigating sex chromosome genetic conflict in action.

Males That Silence Their Father’s Genes: Genomic Imprinting of a Complete Haploid Genome

Genetic conflict is considered a key driver in the evolution of reproductive systems with non-Mendelian inheritance, where parents do not contribute equally to the genetic makeup of their offspring. One of the most extraordinary examples of non-Mendelian inheritance is paternal genome elimination (PGE), a form of haplodiploidy which has evolved repeatedly across arthropods. Under PGE, males are diploid but only transmit maternally inherited chromosomes, while the paternally inherited homologues are excluded from sperm. This asymmetric inheritance is thought to have evolved through an evolutionary arms race between the paternal and maternal genomes over transmission to future generations. In several PGE clades, such as the mealybugs (Hemiptera: Pseudococcidae), paternal chromosomes are not only eliminated from sperm, but also heterochromatinized early in development and thought to remain inactive, which could result from genetic conflict between parental genomes. Here, we present a parent-of-origin allele-specific transcriptome analysis in male mealybugs showing that expression is globally biased toward the maternal genome. However, up to 70% of somatically expressed genes are to some degree paternally expressed, while paternal genome expression is much more restricted in the male reproductive tract, with only 20% of genes showing paternal contribution. We also show that parent-of-origin-specific gene expression patterns are remarkably similar across genotypes, and that genes with completely biparental expression show elevated rates of molecular evolution. Our results provide the clearest example yet of genome-wide genomic imprinting in insects and enhance our understanding of PGE, which will aid future empirical tests of evolutionary theory regarding the origin of this unusual reproductive strategy.