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.

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.

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.

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.

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.

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.

Haldane's duel: intragenomic conflict, selfish Y chromosomes and speciation.

Haldane's rule, which states that the heterogametic sex (XY or ZW females) fares more poorly in interspecific hybrids, is generally attributed to absence of one of the two species' X/Z chromosomes. However, Haldane's rule is also observed in mouse placentas despite paternal X silencing. This pattern could reflect Y chromosomes having evolved to promote growth due to maternal-paternal conflict. If so, balanced sex investment arises from a complex intra- and intergenomic duel.

Sex determination: Ant supergenes link sex ratio to social structure.

A new study maps individual Formica ant queens' tendency to produce single-sex offspring to a so-called 'supergene' locus. This supergene neighbors another supergene determining social structure. Consequently, single-queen and multi-queen colonies disproportionately produce daughters and sons, respectively. This association mirrors the predictions of kin selection, though other possible explanations remain.

Costly circRNAs, Effective Population Size, and the Origins of Molecular Complexity.

While much excitement has attended the discovery and study of circular RNAs, a new study in Cell Reports suggests that most mammalian circRNAs are not only functionless, but in fact costly. Comparison across three species is also consistent with the influential but rarely tested Drift-Barrier Hypothesis of molecular complexity. According to this hypothesis, nonessential genomic elements are slightly deleterious elements that fix by genetic drift and, thus, are generally more abundant in species with small effective population sizes. I discuss the implications of these new results for the Drift-Barrier hypothesis. In particular, I note the distinction between two classes of genomic elements, based on whether they are created by 'standard' small-scale mutations (basepair substitutions, indels, etc.) or larger, more idiosyncratic mutations (segmental duplications, transposable element propagation, etc.) I suggest that the Drift-Barrier Hypothesis is likely to apply to the former class, but perhaps not the latter class.

Digest: Three sexes from two loci in one genome: A haploid alga expands the diversity of trioecious species.

Multicellular eukaryotes exhibit a remarkable diversity of sexual systems; however, trioecy, the coexistence of male, female, and cosexual or hermaphrodite individuals in a single species, is remarkably rare. Takahashi et al. (2021) report the first known instance of trioecy in a haploid organism. In contrast to other known cases of trioecy, the authors report evidence for genetic control of all three sexes by two loci. These results complicate models for sexual system turnover and expand the known diversity of trioecy species in several ways.

CRISPR-Cas Toxin-Antitoxin Systems: Selfishness as a Constructive Evolutionary Force.

A recent paper (Li et al.) reports a novel RNA-based Cas-dependent toxin-antitoxin system with the effect of 'addicting' cells to the cassette. Broadly-defined addiction systems could stabilize diverse genomic features, raising the question of the role of selfish elements and intragenomic conflict in the evolution of biological complexity.

On the utility of oddities: exceptional bee reproduction illuminates fundamental questions of recombination.

Despite its importance, the selective and mechanistic forces governing recombination remain obscure. A recent study of facultatively asexual honeybees suggests a clear case of adaptive adjustment of recombination rate. That these bees' atypical genetics were central to the experiment underscores the utility of genetic oddities as model organisms for studying fundamental questions.