Nematode histone H2A variant evolution reveals diverse histories of retention and loss and evidence for conserved core-like variant histone genes.

Histone variants are paralogs that replace canonical histones in nucleosomes, often imparting novel functions. However, how histone variants arise and evolve is poorly understood. Reconstruction of histone protein evolution is challenging due to large differences in evolutionary rates across gene lineages and sites. Here we used intron position data from 108 nematode genomes in combination with amino acid sequence data to find disparate evolutionary histories of the three H2A variants found in Caenorhabditis elegans: the ancient H2A.ZHTZ-1, the sperm-specific HTAS-1, and HIS-35, which differs from the canonical S-phase H2A by a single glycine-to-alanine C-terminal change. Although the H2A.ZHTZ-1 protein sequence is highly conserved, its gene exhibits recurrent intron gain and loss. This pattern suggests that specific intron sequences or positions may not be important to H2A.Z functionality. For HTAS-1 and HIS-35, we find variant-specific intron positions that are conserved across species. Patterns of intron position conservation indicate that the sperm-specific variant HTAS-1 arose more recently in the ancestor of a subset of Caenorhabditis species, while HIS-35 arose in the ancestor of Caenorhabditis and its sister group, including the genus Diploscapter. HIS-35 exhibits gene retention in some descendent lineages but gene loss in others, suggesting that histone variant use or functionality can be highly flexible. Surprisingly, we find the single amino acid differentiating HIS-35 from core H2A is ancestral and common across canonical Caenorhabditis H2A sequences. Thus, we speculate that the role of HIS-35 lies not in encoding a functionally distinct protein, but instead in enabling H2A expression across the cell cycle or in distinct tissues. This work illustrates how genes encoding such partially-redundant functions may be advantageous yet relatively replaceable over evolutionary timescales, consistent with the patchwork pattern of retention and loss of both genes. Our study shows the utility of intron positions for reconstructing evolutionary histories of gene families, particularly those undergoing idiosyncratic sequence evolution.

Digest: A sex chromosome driver without a sperm deficit.

Meiotic drivers that act during spermatogenesis derive a transmission advantage by disabling sperm that do not carry the driver, often leading to substantially reduced overall sperm number and function. A new study by Bates et al. shows no sperm deficit for a driver in a stalk-eyed fly, in contrast to a related species. This observed sperm compensation is possibly due to secondary testes-expanding mutations linked to the driving genomic locus.

Digest: Mating systems, intragenomic conflict, and speciation.

Conflict over the degree of maternal investment in an offspring can exist between an offspring's maternally inherited and paternally inherited alleles. Such conflict is not expected under self-fertilization. A new study led by Rifkin and Ostevik suggests that divergence in the degree of conflict between closely related outcrossing and selfing species can lead to aberrant early development of hybrids in morning glories. This dynamic represents a potentially powerful driver of reproductive incompatibility and thus speciation.

Digest: Rare male offspring highlight an alternative pathway to obligate asexuality.

Obligate asexuality has arisen many times in eukaryotes, often related to the disrupted function of the core meiotic machinery. For obligately asexual lineages that evolve from facultatively asexual ancestors, there exists another possibility, namely altered regulation of preexisting asexual reproductive processes to produce obligate asexuality. These different pathways leave different signatures in properties of meiosis and recombination that could provide insights into the origin of asexuality. A new study by Molinier et al. (2023) investigates this problem and finds largely typical recombination rates during spermatogenesis of rare, asexually produced sons of obligately asexual Daphnia pulex, suggesting that regulation of reproduction, rather than disruption of meiosis, underpins obligate asexuality in Daphnia.

Did the creeping vole sex chromosomes evolve through a cascade of adaptive responses to a selfish x chromosome?

The creeping vole Microtus oregoni exhibits remarkably transformed sex chromosome biology, with complete chromosome drive/drag, X-Y fusions, sex reversed X complements, biased X inactivation, and X chromosome degradation. Beginning with a selfish X chromosome, I propose a series of adaptations leading to this system, each compensating for deleterious consequences of the preceding adaptation: (1) YY embryonic inviability favored evolution of a selfish feminizing X chromosome; (2) the consequent Y chromosome transmission disadvantage favored X-Y fusion ("XP "); (3) Xist-based silencing of Y-derived XP genes favored a second X-Y fusion ("XM "); (4) X chromosome dosage-related costs in XP XM males favored the evolution of XM loss during spermatogenesis; (5) X chromosomal dosage-related costs in XM 0 females favored the evolution of XM drive during oogenesis; and (6) degradation of the non-recombining XP favored the evolution of biased X chromosome inactivation. I discuss recurrent rodent sex chromosome transformation, and selfish genes as a constructive force in evolution.

Sex chromosomes: How to make a hermaphrodite.

The existence of sex chromosomes complicates the evolution of cosexuality (hermaphroditism). Four new genomic studies from haploid-dominant plants show commonalities and differences in mechanisms of the evolution of cosexuality, raising questions about the genetics of sexual dimorphism and the fate of cosexual lineages.

Where the minor things are: a pan-eukaryotic survey suggests neutral processes may explain much of minor intron evolution.

Spliceosomal introns are gene segments removed from RNA transcripts by ribonucleoprotein machineries called spliceosomes. In some eukaryotes a second 'minor' spliceosome is responsible for processing a tiny minority of introns. Despite its seemingly modest role, minor splicing has persisted for roughly 1.5 billion years of eukaryotic evolution. Identifying minor introns in over 3000 eukaryotic genomes, we report diverse evolutionary histories including surprisingly high numbers in some fungi and green algae, repeated loss, as well as general biases in their positional and genic distributions. We estimate that ancestral minor intron densities were comparable to those of vertebrates, suggesting a trend of long-term stasis. Finally, three findings suggest a major role for neutral processes in minor intron evolution. First, highly similar patterns of minor and major intron evolution contrast with both functionalist and deleterious model predictions. Second, observed functional biases among minor intron-containing genes are largely explained by these genes' greater ages. Third, no association of intron splicing with cell proliferation in a minor intron-rich fungus suggests that regulatory roles are lineage-specific and thus cannot offer a general explanation for minor splicing's persistence. These data constitute the most comprehensive view of minor introns and their evolutionary history to date, and provide a foundation for future studies of these remarkable genetic elements.

Xp22.33p22.13 Duplication in a Male Patient Carrying a Recombinant X Chromosome Derived from an Inherited Intrachromosomal Insertion.

Intrachromosomal insertions are complex structural rearrangements that are challenging to interpret using classical cytogenetic methods. We report a male patient carrying a recombinant X chromosome derived from a maternally inherited intrachromosomal insertion. The patient exhibited developmental delay, intellectual disability, behavioral disorder, and dysmorphic facial features. To accurately identify the rearrangements in the abnormal X chromosome, additional cytogenetic studies were conducted, including fluorescence in situ hybridization (FISH), multicolor-banding FISH, and array comparative genomic hybridization. The results showed a recombinant X chromosome, resulting in a 13.05 Mb interstitial duplication of segment Xp22.33-Xp22.13, which was inserted at cytoband Xq26.1. The duplicated region encompasses 99 genes, some of which are associated with the patient's clinical manifestations. We propose that the combined effects of the Xp-duplicated genes may contribute to the patient's phenotype.

Genomic Assessment of the Contribution of the Wolbachia Endosymbiont of Eurosta solidaginis to Gall Induction.

We explored the genome of the Wolbachia strain, wEsol, symbiotic with the plant-gall-inducing fly Eurosta solidaginis with the goal of determining if wEsol contributes to gall induction by its insect host. Gall induction by insects has been hypothesized to involve the secretion of the phytohormones cytokinin and auxin and/or proteinaceous effectors to stimulate cell division and growth in the host plant. We sequenced the metagenome of E. solidaginis and wEsol and assembled and annotated the genome of wEsol. The wEsol genome has an assembled length of 1.66 Mbp and contains 1878 protein-coding genes. The wEsol genome is replete with proteins encoded by mobile genetic elements and shows evidence of seven different prophages. We also detected evidence of multiple small insertions of wEsol genes into the genome of the host insect. Our characterization of the genome of wEsol indicates that it is compromised in the synthesis of dimethylallyl pyrophosphate (DMAPP) and S-adenosyl L-methionine (SAM), which are precursors required for the synthesis of cytokinins and methylthiolated cytokinins. wEsol is also incapable of synthesizing tryptophan, and its genome contains no enzymes in any of the known pathways for the synthesis of indole-3-acetic acid (IAA) from tryptophan. wEsol must steal DMAPP and L-methionine from its host and therefore is unlikely to provide cytokinin and auxin to its insect host for use in gall induction. Furthermore, in spite of its large repertoire of predicted Type IV secreted effector proteins, these effectors are more likely to contribute to the acquisition of nutrients and the manipulation of the host's cellular environment to contribute to growth and reproduction of wEsol than to aid E. solidaginis in manipulating its host plant. Combined with earlier work that shows that wEsol is absent from the salivary glands of E. solidaginis, our results suggest that wEsol does not contribute to gall induction by its host.

Intron-rich dinoflagellate genomes driven by Introner transposable elements of unprecedented diversity.

Spliceosomal introns, which interrupt nuclear genes, are ubiquitous features of eukaryotic nuclear genes.1 Spliceosomal intron evolution is complex, with different lineages ranging from virtually zero to thousands of newly created introns.2,3,4,5 This punctate phylogenetic distribution could be explained if intron creation is driven by specialized transposable elements ("Introners"), with Introner-containing lineages undergoing frequent intron gain.6,7,8,9,10 Fragmentation of nuclear genes by spliceosomal introns reaches its apex in dinoflagellates, which have some twenty introns per gene11,12; however, little is known about dinoflagellate intron evolution. We reconstructed intron evolution in five dinoflagellate genomes, revealing a dynamic history of intron gain. We find evidence for historical creation of introns in all five species and identify recently active Introners in 4/5 studied species. In one species, Polarella glacialis, we find an unprecedented diversity of Introners, with recent Introner insertion leading to creation of some 12,253 introns, and with 15 separate families of Introners accounting for at least 100 introns each. These Introner families show diverse mechanisms of moblization and intron creation. Comparison within and between Introner families provides evidence that biases in the so-called intron phase, intron position relative to codon periodicity, could be driven by Introner insertion site requirements.9,13,14 Finally, we report additional transformations of the spliceosomal system in dinoflagellates, including widespread loss of ancestral introns, and novelties of tolerated and favored donor sequence motifs. These results reveal unappreciated diversity of intron-creating elements and spliceosomal evolutionary capacity and highlight the complex evolutionary dependencies shaping genome structures.

Transposable elements drive intron gain in diverse eukaryotes.

There is massive variation in intron numbers across eukaryotic genomes, yet the major drivers of intron content during evolution remain elusive. Rapid intron loss and gain in some lineages contrast with long-term evolutionary stasis in others. Episodic intron gain could be explained by recently discovered specialized transposons called Introners, but so far Introners are only known from a handful of species. Here, we performed a systematic search across 3,325 eukaryotic genomes and identified 27,563 Introner-derived introns in 175 genomes (5.2%). Species with Introners span remarkable phylogenetic diversity, from animals to basal protists, representing lineages whose last common ancestor dates to over 1.7 billion years ago. Aquatic organisms were 6.5 times more likely to contain Introners than terrestrial organisms. Introners exhibit mechanistic diversity but most are consistent with DNA transposition, indicating that Introners have evolved convergently hundreds of times from nonautonomous transposable elements. Transposable elements and aquatic taxa are associated with high rates of horizontal gene transfer, suggesting that this combination of factors may explain the punctuated and biased diversity of species containing Introners. More generally, our data suggest that Introners may explain the episodic nature of intron gain across the eukaryotic tree of life. These results illuminate the major source of ongoing intron creation in eukaryotic genomes.

Digest: Recurrent evolution of worker production by interspecific hybridization in harvester ants: Parasitism or kludge?

Multiple ant lineages have evolved a bizarre system called social hybridogenesis, involving multiple co-occurring genetic lineages, in which mating between lineages produces workers but mating within a lineage produces daughter queens. A new study reveals that this system evolved multiple times within harvester ants, each time from interspecific hybridization. A third finding, that the system likely evolves in small or isolated populations, could be explained either by exploitation of heterospecific males for their sperm, or simply by failure to avoid interspecific mating.

Digest: Detecting genomic adaptation to sexual selection at scale using available data.

The availability of genome sequences from large numbers of species offers the prospect of studying genotype-phenotype correlations across various phylogenetic scales using only available data. A new study illustrates the power of this approach, showing an association across primates between morphological sexual dimorphism and the prevalence of a class of DNA elements that stimulate gene expression in response to male androgens.

Digest: Social context underlies subordinate status in a primitively social bee.

Why it is that some individuals in some species assume lifelong subordinate nonreproductive status has been debated since Darwin. Subordinates may be physically incapable of assuming dominant roles or may not do so in response to specific social contexts. By manipulating social context in the primitively eusocial bee Euglossa dilemma, Saleh and coauthors show that subordinate individuals are capable of adopting many traits of dominant individuals.

Gene-rich X chromosomes implicate intragenomic conflict in the evolution of bizarre genetic systems.

Haplodiploidy and paternal genome elimination (HD/PGE) are common in invertebrates, having evolved at least two dozen times, all from male heterogamety (i.e., systems with X chromosomes). However, why X chromosomes are important for the evolution of HD/PGE remains debated. The Haploid Viability Hypothesis posits that X-linked genes promote the evolution of male haploidy by facilitating purging recessive deleterious mutations. The Intragenomic Conflict Hypothesis holds that conflict between genes drives genetic system turnover; under this model, X-linked genes could promote the evolution of male haploidy due to conflicts with autosomes over sex ratios and genetic transmission. We studied lineages where we can distinguish these hypotheses: species with germline PGE that retain an XX/X0 sex determination system (gPGE+X). Because evolving PGE in these cases involves changes in transmission without increases in male hemizygosity, a high degree of X linkage in these systems is predicted by the Intragenomic Conflict Hypothesis but not the Haploid Viability Hypothesis. To quantify the degree of X linkage, we sequenced and compared 7 gPGE+X species' genomes with 11 related species with typical XX/XY or XX/X0 genetic systems, representing three transitions to gPGE. We find highly increased X linkage in both modern and ancestral genomes of gPGE+X species compared to non-gPGE relatives and recover a significant positive correlation between percent X linkage and the evolution of gPGE. These empirical results substantiate longstanding proposals for a role for intragenomic conflict in the evolution of genetic systems such as HD/PGE.

Novel RNA viruses associated with avian haemosporidian parasites.

Avian haemosporidian parasites can cause malaria-like symptoms in their hosts and have been implicated in the demise of some bird species. The newly described Matryoshka RNA viruses (MaRNAV1 and MaRNAV2) infect haemosporidian parasites that in turn infect their vertebrate hosts. MaRNAV2 was the first RNA virus discovered associated with parasites of the genus Leucocytozoon. By analyzing metatranscriptomes from the NCBI SRA database with local sequence alignment tools, we detected two novel RNA viruses; we describe them as MaRNAV3 associated with Leucocytozoon and MaRNAV4 associated with Parahaemoproteus. MaRNAV3 had ~59% amino acid identity to the RNA-dependent RNA-polymerase (RdRp) of MaRNAV1 and ~63% amino acid identity to MaRNAV2. MaRNAV4 had ~44% amino acid identity to MaRNAV1 and ~47% amino acid identity to MaRNAV2. These findings lead us to hypothesize that MaRNAV_like viruses are widespread and tightly associated with the order Haemosporida since they have been described in human Plasmodium vivax, and now two genera of avian haemosporidians.

Optimality Versus Opportunity: The Recurrent Evolution of Similar Sex Determination Mechanisms.

Sex determination mechanisms vary widely across animals, but show remarkable degrees of recurrent evolution. Recurrent features of sex determination have largely been attributed to recurrent cooption of shared ancestral regulatory circuits. However, a new study on sex determination in Daphnia magna reveals both recurrent evolution of specific regulatory logic and apparently recurrent recruitment of a regulator, suggesting a role for optimization in recurrent patterns of sex determination mechanisms.

Digest: Study associates squamate rates, traits, and climates.

The large variation in evolutionary rates across species remains unexplained. A new many-species multivariate study of evolutionary rates in skinks found that environmental temperature explains 45% of rate variation. These results, together with previous studies highlighting different determinants in other organisms, urge a pluralistic understanding of the determinants of evolutionary rate, in contrast to reductive models.

Distinct Minor Splicing Patterns across Cancers.

In human cells, the U12 spliceosome, also known as the minor spliceosome, is responsible for the splicing of 0.5% of introns, while the major U2 spliceosome is responsible for the other 99.5%. While many studies have been done to characterize and understand splicing dysregulation in cancer, almost all of them have focused on U2 splicing and ignored U12 splicing, despite evidence suggesting minor splicing is involved in cell cycle regulation. In this study, we analyzed RNA-seq data from The Cancer Genome Atlas for 14 different cohorts to determine differential splicing of minor introns in tumor and adjacent normal tissue. We found that in some cohorts, such as breast cancer, there was a strong skew towards minor introns showing increased splicing in the tumor; in others, such as the renal chromophobe cell carcinoma cohort, the opposite pattern was found, with minor introns being much more likely to have decreased splicing in the tumor. Further analysis of gene expression did not reveal any candidate regulatory mechanisms that could cause these different minor splicing phenotypes between cohorts. Our data suggest context-dependent roles of the minor spliceosome in tumorigenesis and provides a foundation for further investigation of minor splicing in cancer, which could then serve as a basis for novel therapeutic strategies.

How illuminates why in plant germline methylation.

In modern biology, inquiry into proximal mechanistic and ultimate evolutionary causes are often segregated, pursued by different communities of specialists. Yet, the two are often mutually informative. As a case in point, a recent study by Long et al. on mechanisms of arabidopsis (Arabidopsisthaliana) male germline methylation promises insights into long-obscure ultimate causes.