Homologous recombination is an essential DNA repair mechanism that also promotes chromosome pairing and ensures allele segregation during meiosis in sexual organisms. Here, we explore the dual function of homologous recombination in the bdelloid rotifer Adineta vaga, an ancient asexual species known for its remarkable resilience to extreme genotoxic stresses. Genomic analyses reveal that A. vaga uses meiotic recombination, both to promote spontaneous crossovers and gene conversion during oogenesis and to repair the genome in response to DNA damage. Our study identifies a novel transgenerational DNA repair mechanism, termed break induced homologous extension repair (BIHER), which operates on single DNA ends to repair fragmented chromosomes over successive generations. Our findings suggest that meiotic BIHER, coupled with the holocentric structure of chromosomes, represents a key adaptation of life in extreme environments.

Evolutionary transitions to asexuality are often studied by comparing asexuals found in nature with closely related sexuals. Yet, asexuals sampled in nature may represent only the most successful lineages and therefore provide limited information about the average properties of newly emerging asexuals. These properties are crucial in determining the success of asexual lineages and hence the frequency with which transitions to asexual life cycles evolve. Here, we generate new asexual lineages of Daphnia pulex through contagious asexuality, in which rare males from obligate asexual lineages transmit asexuality to new lineages by mating with sexual females. Unlike asexuals found in nature, most new lineages were capable of both sexual and asexual reproduction (facultative asexuality) and produced non-identical (i.e. non-clonal) daughters when reproducing asexually. They also showed reduced fertility compared to natural asexuals, especially when reproducing asexually, which is expected to reduce the success rate of sex-asex transitions in nature. Taken together, these results suggest that creating new asexual lineages by contagion is more complex than previously thought and may result in diverse, non-clonal offspring, on which subsequent selection can act. If general, such initial fitness valleys associated with sex-asex transitions may be key to resolving the evolutionary 'paradox of sex'.

The definition of biological sex has become a renewed focus of societal debate, fuelled by the conflation of biological principles with discussions of human gender diversity. Here, we argue that conceptual clarity critically depends on separating these domains. Drawing on evolutionary theory and empirical evidence, we maintain that biological sex is best defined as a binary classification of male and female reproductive strategies rooted in anisogamy, characterised by the production of two discrete gamete types of different sizes. We stress that gamete size constitutes the ultimate criterion for biological sex and that this definition applies consistently across sexual systems, from separate-sexed species to hermaphrodites, irrespective of variation in karyotype, hormonal profile, somatic phenotype, or behaviour. Further, we emphasise that evolutionary insights offer a coherent explanation for recurring, though not universal, associations between biological sex and patterns of sex-specific selection, sexual dimorphism and parental care. We conclude that the definition of biological sex as a binary classification based on gamete size is a powerful scientific framework compatible with the diversity of sexual phenotypes found in anisogamous organisms and distinct from the concept of human gender.

Deleterious mutations have multiple effects on the fate of chromosomal inversions. In this article, we use individual-based simulations to estimate the fixation probabilities of neutral inversions under a constant input of deleterious mutations. As shown previously, we find that "lucky" inversions carrying a lower-than-average mutation load are initially favored and tend to selectively spread. Our results also outline the importance of Muller's ratchet caused by the absence of recombination in Y-linked and rare autosomal inversions, reducing their fixation probabilities. Despite the fact that Y-linked inversions are more susceptible to Muller's ratchet, they can more easily fix than autosomal inversions despite initially carrying mutations when these mutations have sufficiently low selection or dominance coefficients (sheltering effect). Similarly, the sheltering of deleterious alleles can increase the fixation probability of inversions capturing a mating-type locus, particularly under intermediate rates of self-fertilization. Overall, our results confirm that when mating is random and for realistic parameter values, the presence of deleterious alleles reduces the average fixation probability of autosomal, sex-linked, or mating type-linked inversions below that of a neutral mutation. Nevertheless, the occasional fixation of a lucky inversion may have important macroevolutionary consequences, potentially contributing to the evolution of recombination arrest on sex chromosomes.

Abstract Fitness landscapes offer a compact representation of adaptation, yet are rarely inferred from sparse multi-environment data. We present a Bayesian approach to infer an effective multi-host phenotypic fitness landscape from cross-inoculation assays by linking successful infection probabilities to Fisher’s geometrical model and to an explicit decomposition of establishment routes. The model estimates (i) the distance matrix among host-specific phenotypic optima, (ii) target-host permissiveness through the widths of fitness peaks, (iii) target-specific differences in the efficiency with which phenotypic suitability translates into successful infection, and (iv) the conditional probabilities that successful infections are attributed to direct establishment, rescue from standing variation in the source inoculum, or de novo rescue in the target host. We apply the approach to an experimental evolution dataset for endive necrotic mosaic virus evolved on five Asteraceae hosts and challenged in a full cross-inoculation design. The inferred landscape can be visualized as a phenotypic map of the host community, revealing pronounced heterogeneity in target-host permissiveness and a geometry broadly concordant with host phylogeny. By grounding assay-derived distances in an explicit mechanistic model, the approach provides a parsimonious representation of multi-host constraints that can be used to discuss establishment barriers and potential springboard hosts in heterogeneous communities. More broadly, it offers a general method for inferring effective fitness landscapes from sparse multi-environment data.

Rare sexual reproduction in otherwise asexual lineages is predicted to strongly alleviate the long-term costs of asexuality while avoiding most of the cost of sex. Here, we test for rare sexual reproduction in females of obligate parthenogenetic (OP) lineages of Daphnia cf. pulex. We find that a small proportion of ~0.5% of offspring contain paternal alleles when they are produced in the presence of males from a so-called cyclical parthenogenetic lineage of the species, thus demonstrating sexual reproduction. Rare sexual reproduction occurred in two independent tests, using females from two different OP lineages, suggesting that it may be a regular feature in OP lineages of the species. Even though it could not be established whether the sexual events involved fertilization of haploid or diploid eggs, these results disclose a reproductive trait entirely new to Daphnia biology, aligning with recent results in other organisms. Indeed, the occurrence of rare or cryptic events of sexual reproduction may be a common feature in lineages previously characterized as obligately parthenogenetic, with significant implications for the evolution of obligate asexuality, its long-term costs, and its genomic consequences, including the evolution of polyploidy.

Sex chromosomes are involved in three major empirical patterns: (i) Y (or W) chromosomes are often nonrecombining and degenerate; (ii) heterogametic offspring (XY or ZW) from interspecific crosses are more often sterile or inviable compared with homogametic offspring (Haldane's rule); and (iii) the X (or Z) has a disproportionately large effect on reproductive isolation between species compared with autosomes (the large X effect). Each observation has received its own tailored explanation involving multiple genetic and evolutionary causes. In this work, we show that these empirical patterns all emerge from a single theory for sex chromosome evolution incorporating the coevolution of cis- and trans-acting regulators of gene expression and leading to systematic misexpression of dosage-compensated genes in heterogametic F1 hybrids, for both young and old sex chromosomes.

Whether partially recessive deleterious mutations should favor the spread of chromosomal inversions extending permanently heterozygous sex determining regions (SDR) has led to some debate. In this article, we use individual-based simulations to estimate fixation probabilities of inversions arising on autosomes and sex chromosomes under a wide range of parameter values. As shown previously, ‘lucky’ inversions carrying a lower-than-average mutation load are initially favored and tend to spread. Our results show that linkage to a permanently heterozygous SDR (on a Y or W chromosome) or to a mating-type locus hinders the spread of inversions when Ns is high (where N is population size and s the strength of selection against deleterious alleles), as the absence of recombination leads to mutation accumulation. However, it may help the spread of inversions when Ns is lower and/or when the dominance coefficient of deleterious alleles is low, by allowing the fixation of inversions that initially carry deleterious alleles, despite the fact that they eventually become deleterious (‘sheltering’ effect). Finally, we show that partial selfing may either help or hinder the spread of inversions capturing a mating-type locus, as they benefit from the masking of deleterious alleles, but also suffer from a higher equilibrium mutation load. ### Competing Interest Statement The authors have declared no competing interest.

Homologous recombination plays a fundamental role in the evolution of organisms. It serves as a DNA repair mechanism which, in sexual organisms, contributes to genetic diversity through the shuffling of alleles during meiosis. Here we investigate the two functions of homologous recombination in the bdelloid rotifer Adineta vaga , an ancient asexual species also known for its tolerance to extreme genotoxic stresses. Genomic analyses reveal that A. vaga retained meiotic recombination mechanisms, both for DNA repair and occurrence of spontaneous crossovers during oogenesis. Our study introduces a novel transgenerational DNA repair mechanism termed break-induced homologous extension repair (BIHER). BIHER operates on single DNA ends, enabling the repair of fragmented chromosomes. Our findings suggest that the BIHER mechanism, combined with a holocentric structure of chromosomes and a modified meiosis, constitutes a key adaptation for life in extreme environments. Identifying such a mechanism in bdelloid rotifers sheds a new light on the strategies that evolved to maintain genome structure in asexually reproducing species.### Competing Interest StatementThe authors have declared no competing interest.

Y and W chromosomes often stop recombining and degenerate. Most work on recombination suppression has focused on the mechanisms favoring recombination arrest in the short term. Yet, the long-term maintenance of recombination suppression is critical to evolving degenerate sex chromosomes. This long-term maintenance has been little investigated. In the long term, recombination suppression may be maintained for selective reasons (e.g., involving the emergence of nascent dosage compensation), or due to mechanistic constraints preventing the reestablishment of recombination, for instance when complex chromosomal rearrangements evolve on the Y. In this paper, we investigate these 'constraint' theories. We show that they face a series of theoretical difficulties: they are not robust to extremely low rates of recombination restoration; they would rather cause population extinction than Y degeneration; they are less efficient at producing a non-recombining and degenerate Y than scenarios adding a selective pressure against recombination, whatever the rate of recombination restoration. Finally, whether such very high constraints exist is questionable. Very low rates of recombination reestablishment are sufficient to prevent Y degeneration, given the large fitness advantage to recover a non-degenerate Y or W for the heterogametic sex. The assumption of a lack of genetic variation to restore recombination seems also implausible given known mechanisms to restore a recombining pair of sex chromosomes.

Local adaptation is pervasive. It occurs whenever selection favors different phenotypes in different environments, provided that there is genetic variation for the corresponding traits and that the effect of selection is greater than the effect of drift and migration. In many cases, ecologically relevant traits are quantitative and controlled by many genes. It has been repeatedly proposed that the localization of these genes in the genome may not be random, but could be an evolved feature. In particular, the clustering of local adaptation genes may be theoretically expected and has been observed in several situations. Previous theory has focused on two-patch or continent-island models to investigate this phenomenon, reaching the conclusion that such clustering could evolve, but in relatively limited conditions. In particular, it required that migration rate was neither too low nor too large and that the full optimization of trait values could not be eventually achieved by a mutation at a single locus. Here, we investigate this question in a spatially-explicit model, considering two contiguous habitats with distinct trait optima on a circular stepping-stone. We find that clustering of local-adaptation genes is pervasive within clines during both the establishment phase of local adaptation and the subsequent “reconfiguration” phase where different genetic architectures compete with each other. We also show that changing the fitness function relating trait to fitness has a strong impact on the overall evolutionary dynamics and resulting architecture.

Obligate parthenogenesis (OP) is often thought to evolve by disruption of reductional meiosis and suppression of crossover recombination. In the crustacean Daphnia pulex, OP lineages, which have evolved from cyclical parthenogenetic (CP) ancestors, occasionally produce males that are capable of reductional meiosis. Here, by constructing high-density linkage maps, we find that these males show only slightly and nonsignificantly reduced recombination rates compared to CP males and females. Both meiosis disruption and recombination suppression are therefore sex-limited (or partly so), which speaks against the evolution of OP by disruption of a gene that is essential for meiosis or recombination in both sexes. The findings may be explained by female-limited action of genes that suppress recombination, but previously identified candidate genes are known to be expressed in both sexes. Alternatively, and equally consistent with the data, OP might have evolved through a reuse of the parthenogenesis pathways already present in CP and through their extension to all events of oogenesis. The causal mutations for the CP to OP transition may therefore include mutations in genes involved in oogenesis regulation and may not necessarily be restricted to genes of the “meiosis toolkit.” More generally, our study emphasizes that there are many ways to achieve asexuality, and elucidating the possible mechanisms is key to ultimately identify the genes and traits involved.

How social organisation (number of queens and mating partners) and reproductive system (use of thelytoky vs sex) evolved in ants and how they interplay is still far from clear. The Cataglyphis desert ants represent a fascinating group as it harbours variation in both levels of polyandry and the use of thelytoky, with polyandry and sexual reproduction probably being the ancestral state. In this study, we compared the colony and population genetic structure of two populations of the Cataglyphis cursor group distributed in a remote small geographic area in central Spain with two closest geographic species C. piliscapa and C. cursor . We found that the two populations are genetically isolated from C. piliscapa and C. cursor. However, the population genetic diversity was like C. piliscapa and C. cursor . We observed a lower level of polyandry in C. cursor from Spain compared to C. piliscapa and C. cursor. We found no evidence that C. cursor queens from Spain reproduce thelytokously. This supports the hypothesis that thelytoky is disfavored in systems with lower levels of polyandry. The reversion from polyandry towards monandry has rarely been observed in ants. We present multiple hypotheses that could explain this phenomenon. We raise the possibility that these remote populations belong to a putatively new species. However, this requires a careful taxonomic investigation. Our study confirms the lability of the reproductive system in this group and provides an exciting system to investigate the coevolution of polyandry and thelytoky.

In some asexual species, parthenogenetic females occasionally produce males, which may strongly affect the evolution and maintenance of asexuality if they cross with related sexuals and transmit genes causing asexuality to their offspring ("contagious parthenogenesis"). How these males arise in the first place has remained enigmatic, especially in species with sex chromosomes. Here, we test the hypothesis that rare, asexually produced males of the crustacean Artemia parthenogenetica are produced by recombination between the Z and W sex chromosomes during non-clonal parthenogenesis, resulting in ZZ males through loss of heterozygosity at the sex determination locus. We used RAD-sequencing to compare asexual mothers with their male and female offspring. Markers on several sex-chromosome scaffolds indeed lost heterozygosity in all male but no female offspring, suggesting that they correspond to the sex-determining region. Other sex-chromosome scaffolds lost heterozygosity in only a part of the male offspring, consistent with recombination occurring at a variable location. Alternative hypotheses for the production of these males (such as partial or total hemizygosity of the Z) could be excluded. Rare males are thus produced because recombination is not entirely suppressed during parthenogenesis in A. parthenogenetica. This finding may contribute to explaining the maintenance of recombination in these asexuals.

In a minority of flowering plants, separate sexes are genetically determined by sex chromosomes. The Y chromosome has a non-recombining region that degenerates, causing a reduced expression of Y genes. In some species, the lower Y expression is accompanied by dosage compensation (DC), a mechanism that re-equalizes male and female expression and/or brings XY male expression back to its ancestral level. Here, we review work on DC in plants, which started as early as the late 1960s with cytological approaches. The use of transcriptomics fired a controversy as to whether DC existed in plants. Further work revealed that various plants exhibit partial DC, including a few species with young and homomorphic sex chromosomes. We are starting to understand the mechanisms responsible for DC in some plants, but in most species, we lack the data to differentiate between global and gene-by-gene DC. Also, it is unknown why some species evolve many dosage compensated genes while others do not. Finally, the forces that drive DC evolution remain mysterious, both in plants and animals. We review the multiple evolutionary theories that have been proposed to explain DC patterns in eukaryotes with XY or ZW sex chromosomes. This article is part of the theme issue ‘Sex determination and sex chromosome evolution in land plants’.

The climate is currently warming fast, threatening biodiversity all over the globe. Populations often adapt rapidly to environmental change, but for climate warming very little evidence is available. Here, we investigate the pattern of adaptation to an extreme +10°C climate change in the wild, following the introduction of brine shrimp Artemia franciscana from San Francisco Bay, USA, to Vinh Chau saltern in Vietnam. We use a resurrection ecology approach, hatching diapause eggs from the ancestral population and the introduced population after 13 and 24 years (∼54 and ∼100 generations, respectively). In a series of coordinated experiments, we determined whether the introduced Artemia show increased tolerance to higher temperatures, and the extent to which genetic adaptation, developmental plasticity, transgenerational effects, and local microbiome differences contributed to this tolerance. We find that introduced brine shrimp do show increased phenotypic tolerance to warming. Yet strikingly, these changes do not have a detectable additive genetic component, are not caused by mitochondrial genetic variation, and do not seem to be caused by epigenetic marks set by adult parents exposed to warming. Further, we do not find any developmental plasticity that would help cope with warming, nor any protective effect of heat-tolerant local microbiota. The evolved thermal tolerance might therefore be entirely due to transgenerational (great)grandparental effects, possibly epigenetic marks set by parents who were exposed to high temperatures as juveniles. This study is a striking example of "missing heritability," where a large adaptive phenotypic change is not accompanied by additive genetic effects.

Current theory proposes that degenerated sex chromosomes—such as the mammalian Y—evolve through three steps: (i) recombination arrest, linking male-beneficial alleles to the Y chromosome; (ii) Y degeneration, resulting from the inefficacy of selection in the absence of recombination; and (iii) dosage compensation, correcting the resulting low expression of X-linked genes in males. We investigate a model of sex chromosome evolution that incorporates the coevolution of cis and trans regulators of gene expression. We show that the early emergence of dosage compensation favors the maintenance of Y-linked inversions by creating sex-antagonistic regulatory effects. This is followed by degeneration of these nonrecombining inversions caused by regulatory divergence between the X and Y chromosomes. In contrast to current theory, the whole process occurs without any selective pressure related to sexual dimorphism.