Heredity

Heat Shock Protein 90 (HSP90) functions as an evolutionary capacitor, allowing populations to store cryptic genetic variation that can be released under stress. While former studies have described the release of morphological variation, its behavioural consequences remain unexplored. In the red flour beetle, Tribolium castaneum, HSP90 inhibition released a phenotype with much smaller, less defined eyes that confers fitness benefits in continuous light and was subsequently assimilated. We hypothesized that altered eye morphology affects light perception and thereby changes light-dependent behaviours. To test whether phenotypes released via evolutionary capacitance can beneficially alter behaviour, we examined locomotor activity rhythm entrainment to light-dark cycles as well as individual and group light choice behaviour. Males of the reduced-eye phenotype exhibited a diminished startle response to sudden light exposure in locomotor activity assays. We also found reduced negative phototaxis in groups of beetles with reduced eyes. This modified behaviour, indicating reduced light sensitivity, may stem from impaired light perception caused by altered eye morphology. Lower light sensitivity could be beneficial under stressful environmental conditions by promoting the exploration of alternative niches. Therefore, this study provides the first evidence for potentially beneficial behavioural changes in a HSP90-released phenotype, reinforcing HSP90s role as an evolutionary capacitor.

Alleles with opposing effects on fitness characters are said to exhibit selectional antagonistic pleiotropy (broadly construed so that effects are not necessarily confined to the same individual). A number of theoretical investigations considered the case where a pair of alleles at a locus influences two fitness components and derived the conditions giving rise to stable polymorphism under various assumptions about the mode of trait-interaction. Strikingly, many of these analyses concluded that the potential for maintaining polymorphism is strongly constrained by the joint influence of two factors: (1) the prevalence of weak selection coefficients over coefficients of large magnitude, and (2) the absence of beneficial dominance reversals (where the deleterious effects of each allele are partially or completely masked in the heterozygous genotype). Consequently, the conclusion that selective polymorphism is unlikely to be maintained by intralocus mechanisms of antagonistic pleiotropy has achieved widespread acceptance. Here we argue that such conclusions do not apply to any of the following models of antagonism: (i) additive trait-interaction, (ii) multiplicative trait-interaction, (iii) bivoltine selection, (iv) soft selection, (v) hard selection, and (vi) sexual antagonism. We demonstrate that the parameter space giving rise to stable allelic variation is quite large throughout, and moreover, the plenitude of suitable parameters neither depends on the strength of selection nor requires dominance reversal. Dominance coefficients associated with stringent conditions for stable polymorphism are shown to be atypical as compared to all feasible parameters, and best regarded as an outcome of adherence to a special relation: dominance with a constant magnitude and direction, which includes the case of additive allelic effects at a locus. Properties of single-locus equilibria (heterozygosity, allele frequency differentiation) are investigated, as well as the contribution of dominance schemes to the genetic variance in fitness characters in populations at multilocus linkage equilibrium. Author summaryAllelic variants at a locus with opposing effects on multiple fitness components (antagonistic fitness pleiotropy) have long been appreciated as a possible source of balancing selection. The prevalence of polymorphism owing to this form of natural selection, however, has been doubted on theoretical grounds due to the fact that standard assumptions of genetic models (namely, constant magnitudes for the dominance coefficients) are hardly conducive to the maintenance of polymorphism. The major exception to this conclusion lies with schemes that exhibit dominance reversal (where the direction of dominance for antagonistic alleles flips across fitness components). Here we conduct a geometric analysis of the space of polymorphism-promoting dominance parameters and conclude that the conditions for maintaining balanced alleles is unrestrictive, with non-reversals playing an underappreciated role.

Deciphering the genetic architecture of complex quantitative phenotypes remains challenging in quantitative genetics. These traits not only depend of multiple genetic factors but are also established over time and environments. Although quantitative genetics has investigated the genetic determinism of phenotypic plasticity in contrasted environmental conditions, the time related phenotypic plasticity has received less attention. Here we proposed a multivariate Bayesian framework, the Bayesian Varying Coefficient Model, designed for analysing the genetic architecture of the time related phenotypic plasticity by a multilocus approach. We applied the BVCM to time series phenotypes measured at various time scales (daily, monthly, yearly) across a diverse set of biological species. We included in this study: yeast (Saccharomyces cerevisiae), fungi (Fusarium graminearum), eucalyptus (Eucalyptus urophylla x E. grandis), and sweet cherry tree (Prunus avium). The BVCM results were compared with those obtained with a known genome-wide association method carried out time by time. For all species and traits, the BVCM was able to detect the major QTL identified by marker-trait association methods and revealed additional genetic regions of weak effect. It also increased the phenotypic variance explained for most of the phenotypes considered. It revealed dynamic QTLs with transitory, increasing or decreasing effects over time. By considering both the temporal and genetic multivariate structures in a single statistical model, we increased our understanding of the genetic architecture of complex traits notably by reducing the issue of missing heritability. More broadly, this work raises the foundation for extended applications in functional genomics, evolutionary ecology, and crop breeding programs, in which time-related phenotypic plasticity remains crucial for predicting and selecting key quantitative complex traits. Key messageBy capturing the genetic factors influencing the time related phenotypic plasticity, our approach contributes to a deeper understanding of the dynamic nature of genotype-phenotype relationships.

Trees accumulate somatic mutations throughout their long lifespan, resulting in genetic mosaicism among branches. While recent genomic studies quantified these mutations, they were largely limited to describing static patterns of variation. In this study, we developed a mathematical model to infer the dynamic processes of somatic mutation accumulation from snapshot genomic data obtained from four tropical trees (Dipterocarpaceae), which dominate tropical rain forests in Southeast Asia. Our model focus on genetic differences between shoot apical meristems (SAMs) at branch tips and explicitly incorporate stem cell dynamics within SAMs during shoot elongation and branching, enabling us to quantify somatic genetic drift arising from stem cell lineage replacement. By comparing model predictions with empirical data from Dipterocarpaceae trees, we estimated key parameters governing stem cell dynamics and somatic mutation rates. Our results indicate that both shoot elongation and branching involve replacement of stem cell lineages, leading to a moderate degree of somatic genetic drift. Accounting for stem cell dynamics resulted in slightly lower mutation rate estimates than previous approaches that ignored these processes. Using the estimated parameters, we further performed stochastic simulations to predict patterns of somatic mutations, including features not directly observed in the sampled trees, such as occasional deviations of somatic mutation phylogenies from physical architecture. Together, our modeling framework provides insights into how genetic mosaicism is shaped within tropical trees and reveals the stem cell dynamics underlying their long-term growth and accumulation of somatic mutations. (236 words) Highlights- We built mathematical models to predict the genetic differences between branch tips by somatic mutations. - The model considers the varying dynamics of stem cells in shoot meristem during shoot elongation and branching. - We compared the model prediction with empirical data from tropical trees, Dipterocarpaceae, and estimated the dynamics of stem cells and mutation rate. - Somatic mutation dynamics were shaped by somatic genetic drift arising from stem cell lineage replacement during shoot elongation and branching. - Accounting for stem cell dynamics led to slightly smaller estimates of mutation rates compared with previous estimates that ignored the dynamics. - Our models offer insights into how genetic variability is shaped in the tropical trees and the stem cell dynamics underlying their long-term growth.

Population genetic theory predicts that natural selection will be more efficient in large than small populations because genetic drift reduces the efficiency of selection in small populations. Small populations adapting to new environments can also be expected to evolve higher recombination rates to facilitate adaptation as well as to dissociate and purge harmful mutations. We tested these hypotheses (1) by investigating differences in the strength of association between nucleotide diversity ({pi}) and recombination rate across the genomes of nine-spined sticklebacks (Pungitius pungitius) from four small freshwater (mean Ne {approx} 2 578) and four large marine (mean Ne = 86 742) populations, as well as (2) by comparing recombination rates between small and large populations using population specific linkage maps. We found the predicted positive correlation of{pi} with recombination rate from all but the smallest freshwater populations, suggesting prevalent linked selection even after accounting for variation in GC/CpG content, and gene density. Mean recombination rates did not differ between freshwater and marine populations, except that the smallest Ne freshwater population exhibited significantly elevated recombination rate. GWAS analyses suggested a polygenic basis for recombination rates. These results suggest an important role for linked selection in reducing{pi} in low recombination regions especially in large populations. Moreover, as predicted by theory, at least one of the small freshwater populations appears to have evolved a higher recombination rate than its marine ancestors.

Premise of studyUnder increasingly frequent pollinator-limited environments, plants need to rely on modes of reproductive assurance such as selfing and cloning. However, few studies investigate the interplay between selfing and cloning in plants that can do both. Here, we explore mechanisms determining the relative expression of selfing and cloning throughout the European distribution of the wild woodland strawberry (Fragaria vesca) under a pollinator-free environment. MethodsWe established an outdoor common garden with 121 woodland strawberry genotypes from across Europe and excluded them from pollinators. For each genotype, we recorded reproductive traits and performed hand-pollination treatments. Key ResultsWe found a weak trade-off between cloning and selfing, driven by increased seed and fruit provisioning rather than flower production. The capacity to autonomously self-fertilize was determined by the lateral proximity of the anthers to the pistils (lateral herkogamy), but not by early inbreeding depression. Genotypes sampled at lower latitudes and altitudes were better at self-fertilizing and had smaller petals. The propensity to clone increased towards the east, where genotypes also had smaller petals, particularly at higher latitudes. ConclusionAt the species level, we detected a trade-off between the propensity for clonal reproduction and the capacity for self-fertilization. At a continental scale, the capacity to self-fertilize varied along a north-south gradient, whereas clonal propensity varied along an east-west gradient. Our results suggest that these two modes of reproductive assurance may compensate for reduced pollinator attractiveness (smaller petals) in regions where each mode is most strongly expressed.

Life history traits are often correlated, creating trade-offs that may impede the response to natural selection and be responsible for the evolution of senescence. These trade-offs may arise through pleiotropic effects, which can affect the response to selection in ways that resemble intra-locus sexual antagonism. Despite these hypothesized relationships, we lack clear connections between pleiotropy, sexual antagonism, and the evolution of life histories. Empirical tests for inter-sexual differences in life-history traits, including sex-specific aging, can be used to evaluate hypotheses about how pleiotropy and sexual conflict affect evolutionary trade-offs. To those ends, we measured lifespan, development time, and body size in Drosophila pseudoobscura males and females, each of which carried one of six third chromosome inversion genotypes. Temperature affected lifespan and development more than any other factor; higher temperatures increased mortality rate, decreased lifespan, and accelerated development. However, we also observed sex differences in mortality rates and development times that depended on genotype and temperature. Notably, temperature elevated the initial mortality rate across all flies, yet increasing temperatures reduced the rate of aging in some genotype-sex combinations. Similarly, direct effects of genotype on mortality rate and development time depended greatly on sex and temperature, but there was no genotype effect on body size. Despite these context-dependent genotype effects on life history traits, we failed to identify any correlations that would serve as clear evidence for sexual conflict or trade-offs. Our results therefore suggest that either historical conflicts have been resolved or any conflicts that may exist do not result in the correlations predicted by existing models.

Understanding relatedness in sharks is challenging due to uncertainty in distributions, low population densities and difficulties in sampling across life stages. In Fiji, bull sharks (Carcharhinus leucas), with an effective population size estimate of [~]258, aggregate at the Shark Reef Marine Reserve (SRMR), but gravid females disperse at the end of the year to give birth in adjacent rivers. Questions remain regarding reproductive connectivity, female returns across years, and kinship structure. Using population genomics on 296 bull sharks across age classes (neonates, young-of-the-year, juveniles, and adults) collected over a decade at the SRMR and in three adjacent rivers, we assessed familial connections. Direct genetic links, including first- and second-degree relationships, connected SRMR adults with young age classes in the Navua and Rewa rivers, providing evidence of reproductive connectivity. Within rivers, genetic similarities across cohorts revealed reproductive philopatry. Remarkably, several individuals sampled years apart were assigned to the same sire-dam pairs, indicating repeated pairings across breeding seasons. However, the few related links detected between the SRMR and the rivers may reflect incomplete sampling. Altogether, bull shark reproduction in Fiji seems influenced by reproductive philopatry and repeated pairings, suggesting added complexity in their reproductive behaviour.

Genetic evidence for fluctuating selection has begun to accumulate for different species over the past few decades, especially for the Drosophila genus where studies have reported hundreds of loci undergoing putatively adaptive oscillations across successive seasons. However, most theoretical and simulation studies of fluctuating selection have relied on abstract or weakly parameterized models, making it difficult to assess their relevance for natural populations. In this study, we simulate multilocus seasonally fluctuating selection under a recently developed model and examine its effect on the variance effective population size (Ne) at a genome-wide scale. By recapitulating genomic, demographic, and evolutionary parameters from natural Drosophila populations in our simulations, we were able to reproduce allele frequency oscillations reported in recent studies and show that these lead to [~]50% genome-wide reductions in Ne. We also demonstrate that Ne reductions are well predicted by the maximum frequency amplitude among all adaptively fluctuating loci, and that the frequency amplitudes are largely determined by the number of adaptively fluctuating loci and the strength of their epistatic interactions. Our results demonstrate that fluctuating selection can substantially reduce effective population size and underscore the importance of temporally variable selection in shaping genome-wide patterns of variation beyond classical models. Article SummaryGenetic studies of fluctuating selection in natural populations have grown steadily over the past decade, with reports suggesting that hundreds of loci undergo adaptive oscillations over seasonal timescales in cosmopolitan Drosophila populations. By simulating seasonally fluctuating selection under a recently developed model and ecological scenarios informed by published studies, the authors show that this mode of selection can reduce effective population size by [~]50%, with the magnitude of the reduction correlated with the locus exhibiting the largest allele frequency fluctuations. These findings highlight fluctuating selection as an important factor shaping genome-wide patterns of genetic variation and effective population size.

Individual phenotypes often depend on the genotypes of other individuals within a group. These phenomena are termed indirect genetic effects (IGEs) and have been distinguished from direct genetic effects (DGEs) using quantitative genetic models. Recent studies have utilized high-resolution polymorphism data to enable genomic prediction (GP) and genome-wide association study (GWAS) of IGEs, but unified methods remain limited. Here we integrate polygenic and oligogenic IGEs using a multi-kernel mixed model incorporating two random effects with a single covariance parameter. Underlying this implementation, the Ising model of ferromagnetics enabled us to simplify locus-wise and background IGEs for GWAS and GP, respectively. Our simulations demonstrated that, while the previous and present models exhibited similar performance, the present model can infer a trade-off between DGEs and IGEs. By applying this method to three species of woody plants, we found evidence for intergenotypic competition in aspen and apple trees, but limited evidence in climbing grapevines. Based on GWAS, we also detected significant variants associated with the competitive IGEs on the apple trunk growth. Our study offers a flexible implementation for GWAS/GP of IGEs, thereby providing an effective tool to dissect the genetic architecture of group performance.

The measurement of inbreeding has gained significance across diverse fields, including population and conservation genetics, agricultural genetics, breeding programs for animals and plants, and wildlife management. This is due to the fact that inbreeding leads to increased homozygosity and results in lower genetic diversity, rendering populations more vulnerable to environmental changes, diseases, and other stressors. High or mid-coverage whole genome sequencing (WGS) has been widely used for inbreeding estimation, but it is resource-intensive. We aimed to investigate the use of ultra low-coverage whole genome sequencing (ulcWGS) as a cost-effective alternative for inbreeding analysis. Domestic dogs were used for our study as their extensive breeding histories lead to populations with a wide range of inbreeding levels. We constructed a multi-breed reference panel from high-coverage WGS samples. Inbreeding in independent ulcWGS samples was then estimated using runs of homozygosity (RoH) and inbreeding coefficients (F). We modeled the relationship between these measures and sequencing depth using nonlinear regression, to generate inbreeding estimates relative to sequencing depth. Resulting relative RoH and F measurements were significantly correlated, with purebred dogs exhibiting more runs of homozygosity and higher inbreeding coefficients compared to mixed-breed dogs. Our findings demonstrate that ulcWGS can provide reliable and economical estimations of inbreeding, expanding accessibility to genetic monitoring.

Iron is an essential nutrient for all types of organisms, including insects and the microbes that infect them. We predicted that insects fed an iron-supplemented diet would accumulate more iron in their hemolymph, and, because infectious microbes acquire iron from their hosts, that this extra iron would increase the severity of bacterial infections. To test this hypothesis, we studied the effects of dietary iron supplementation on infection outcomes in Manduca sexta (tobacco hornworm). Larvae were fed an artificial diet, with or without antibiotics, or the same diets supplemented with 10 mM iron. Control and iron-treated larvae were inoculated with non-pathogenic Escherichia coli or the entomopathogenic Enterococcus faecalis, and bacterial load and larval survival were measured. We found that dietary iron supplementation increased the iron content of hemolymph by approximately 20 fold; however, contrary to our prediction, this increase in iron did not result in an increase in the bacterial load of either E. coli or E. faecalis. The effect of iron supplementation on survival was more complicated. As expected, for larvae inoculated with nonpathogenic E. coli, iron supplementation had no effect. For larvae inoculated with E. faecalis, the effect of iron supplementation depended on whether antibiotics were present in the diet. Without antibiotics, iron supplementation prolonged larval survival; with antibiotics, iron supplementation decreased larval survival. The results of this study do not support the hypothesis that dietary iron supplementation increases infection severity in M. sexta. Instead, the results support the viewpoint that the relationship between dietary iron and infection outcome is complex.

Article summaryGene interactions are common, yet additive genetic models often predict short-term evolution and breeding response. This study argues that additivity can arise because populations sample only a small neighbourhood of a curved fitness landscape. In additive channels, genetic variation is small enough that local curvature contributes little to heritable fitness differences. The study defines an additivity index ([A]g) that compares variance from the local slope of log-fitness with variance from curvature, and links this ratio to expected prediction accuracy under Gaussian assumptions. A selection-inheritance framework shows when additive channels persist and when populations leave them. It yields testable predictions.

The Allee effect is a phenomenon where individual fitness is reduced in small populations, for example because of mate-finding difficulties or increased predation. Allee effects matter in conservation biology because they can drive small populations to extinction. The severity of Allee effects can depend on traits such as mate-search rate and defense against predators. Many natural populations exhibit considerable intraspecific trait variation (ITV) in such traits, but most studies so far assume these traits to be constant. Thus the impact of ITV on populations with Allee effect is largely unknown. Here we create two individual-based stochastic models that simulate a small population experiencing either a mate-finding Allee effect or a predator-driven Allee effect. We analyze how ITV, trait inheritance, and mutation affect the proportion of surviving populations. Under the mate-finding Allee effect, higher ITV hindered population survival and increased Allee thresholds. This can be explained by Jensens inequality and the negative curvature of the mate-finding function. Under the predator-driven Allee effect, ITV effects were weak, but higher mutation standard deviations were beneficial, likely because they provided more substrate for selection to act on. We thus recommend to take into account ITV when dealing with threatened populations with an Allee effect.

We study one of the simplest scenarios of polygenic selection that can be imagined: a subdivided population of diploid individuals expressing an additive trait under spatially homogeneous stabilizing selection. We are interested in the amounts of variation that can be maintained at mutation-selection-migration-drift equilibrium, at individual loci and at the level of the trait, within and among subpopulations. We derive analytical approximations for variance components and summary statistics such as FST and QST under the assumptions of the infinite-island model and compare these with individual-based simulations. We find that: (i) There is a critical migration threshold (which depends on effect sizes of trait loci) below which population structure strongly inflates genic variance in the subdivided population to levels well above those in a panmictic population. Variation within each subpopulation is maximized close to the critical migration rate. (ii) The genetic basis of trait variation across subpopulations is most similar close to this migration threshold and (counter-intuitively) decreases for higher migration rates. This has consequences for the portability of Genome-Wide Association Studies (GWAS) between subpopulations, i.e, the extent to which loci with large contributions to variance in one subpopulation explain variance in other subpopulations. (iii) An analytical mean-field approach based on the single-locus diffusion approximation, together with effective migration and selection parameters (to account for associations between loci), very accurately predicts various quantities.

Parthenogenesis is relatively rare and often regarded as an evolutionary dead end. Despite this, certain parthenogenetic animal species have endured for millions of years, but it is unclear what enables the persistence of some parthenogenetic lineages. Transitions from sexual to parthenogenetic reproduction can occur through different evolutionary processes that give rise to diverse cytological reproductive mechanisms. These mechanisms are likely to influence genetic diversity, especially in the early stages after the transition to parthenogenesis and may thus affect lineage persistence. To understand such evolutionary transitions, we used experimental crosses to investigate the mechanism of parthenogenesis and the immediate genetic consequences of switching from sexual to parthenogenetic reproduction in the facultatively parthenogenetic phasmid Megacrania batesii. We obtained DNA sequence data from multiple lineages propagated over three generations via sex, parthenogenesis, or transitions between reproductive modes. We quantified heterozygosity and within-family genetic variation and compared the genetic patterns with predictions for known mechanisms of parthenogenesis. We found that a single generation of parthenogenesis typically resulted in (near-)complete loss of heterozygosity and an absence of within-family genetic variation, consistent with automixis with gamete duplication or terminal fusion and little/no recombination. However, we also found evidence of variation in the mechanism of parthenogenesis among lineages and even within the same individual, associated with drastic differences in the amount of heterozygosity and within-family genetic variation maintained across generations. Our findings show that considerable variation in parthenogenetic mechanisms can exist within populations and suggest that such variation could influence the persistence and evolution of parthenogenetic lineages.

Global networks of crop breeding programs leverage diverse germplasm, but diversity increases the complexity of maintaining stability in their elite genepools. To characterize genetic heterogeneity in breeding metapopulations and develop insights on how to manage it, we simulated the evolution of breeding populations on fitness landscapes. We revealed the geometric decrease in the average effect size of alleles segregating as standing variation that become fixed along an adaptive walk. We also demonstrated how independent adaptive walks of subpopulations are influenced by genetic drift, leading to cryptic genetic heterogeneity among elite genepools. This variation is released when elite lines derived from independent subpopulations are crossed, leading to segregation for 2-4X more major QTL in admixed families as in unadmixed families, and 2-4X more epistatic interactions. The emergent property of fitness epistasis for traits under stabilizing selection is well-understood in evolutionary genetics, but under-appreciated in crop quantitative genetics. To highlight the importance of this phenomenon, we constructed an empirical genotype-to-fitness landscape from the sorghum NAM, a global admixed prebreeding resource, demonstrating the utility of fitness landscapes for inferring genetic compatibilities within metapopulations. Our findings suggest that in breeding networks, strategies for effective germplasm exchange must account for epistasis in the oligogenic component of the genetic architecture of locally-adapted traits. Article summaryModern public sector crop improvement happens in networks of breeding programs that routinely exchange genetic information. Traditional models for understanding quantitative traits have limited predictiveness in situations with such genetic heterogeneity. This study uses breeding simulations and empirical data to show the utility of the fitness landscape framework for characterizing the genetic architecture of complex traits in breeding metapopulations. By simulating the evolution of breeding programs and integration into networks, it demonstrates how epistatic interactions between large-effect alleles are a fundamental property that must be accounted for when exchanging germplasm. Graphical Abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=102 SRC="FIGDIR/small/712732v1_ufig1.gif" ALT="Figure 1"> View larger version (25K): org.highwire.dtl.DTLVardef@1541326org.highwire.dtl.DTLVardef@b553a8org.highwire.dtl.DTLVardef@8758b4org.highwire.dtl.DTLVardef@1d0bdcd_HPS_FORMAT_FIGEXP M_FIG C_FIG

Transitions from sexual to asexual reproduction are well-documented across different taxa. However, despite extensive efforts, the regulatory changes underlying the emergence of asexuality remain largely undiscovered in the majority of species studied. Artemia brine shrimp have multiple closely related sexual and obligate parthenogenetic lineages, making them a promising model for addressing this question. While earlier work suggested that asexuals use a modified meiosis, and inferred a likely role for the Z-chromosome in its transmission, no master regulator or genetic changes have been put forward as the root causes for the shift. Here, we generate single-nucleus RNAseq data of the female reproductive system of individuals from the Aibi lake population of Artemia parthenogenetica and its closely related obligate sexual species Artemia sp. Kazakhstan. We identify the germline cell clusters in the female reproductive system and perform differential expression analysis to infer substantial transcriptional differences at genes putatively involved in cell cycle and oocyte development between the meiotic cells of the two species. Additionally, we use whole-genome sequencing of 32 individuals from two backcrossing experiments to narrow down the genomic regions associated with the transmission of asexuality to an 8 megabase region of the Z chromosome. Within the identified regions, two adjacent genes with known functions in oogenesis, ITPR and USP8, show differential expression and genetic differentiation between sexuals and asexuals, making them promising candidate drivers of asexuality in this species. Significance statementWhile most animals reproduce sexually, many do not, and why and how these shifts occur remains an open question. This paper presents a systematic investigation of the molecular changes that underlie the transition from sexual to asexual reproduction in brine shrimp. We combine multiple computational and experimental approaches to look for differences between close sexual and asexual lineages. We find that a subset of meiotic germ cells is regulated differently in the two, and that two important oogenesis genes are the likely drivers of asexuality. This work is unique in providing an in-depth characterization of the combined genetic and regulatory changes underlying this key transition in reproductive modes.

Understanding how mutations evolve on Y chromosomes is central to explaining the origin, diversity and persistence of sex chromosomes. Mutations occurring on the Y chromosome in sexual populations experience selective dynamics that differ markedly from those on autosomes, due to a reduced effective population size and the presence of large non-recombining regions containing alleles maintained in a permanently heterozygous state. These specific features alter gene transmission in the Y chromosome population compared to autosomes, even within the same pedigree. Here, we provide a two-sex diploid Wright-Fisher model that explicitly incorporates both sex chromosomes and autosomes within a unified population framework, in order to capture the influence of these specificities on the fate of mutations, not only considering fixation probabilities but also segregation times. We use diffusion approximations and provide analytical and numerical tools to compute these quantities across a wide range of parameters and selection regimes. We recover classical results on fixation probabilities in various scenarios, including purely beneficial, deleterious or overdominant mutations, and extend them in the light of mean segregation time, a key but often overlooked determinant of evolutionary outcomes over finite timescales. In particular, our analyses show that overdominant mutations are overall more likely to fix in observable time windows on the Y chromosome than on autosomes. Individual-based simulations corroborate our approximations and highlight parameter regimes where the theoretical approach is particularly useful, especially for parameter values inducing long segregation times or small fixation probabilities, for which simulations are impractical. Our results provide a comprehensive and tractable framework for clarifying how chromosome-specific features shape evolutionary dynamics beyond fixation probabilities alone.

BackgroundAlthough strict maternal transmission of mitochondria is a general feature of animals and humans for ensuring homogeneity in mitochondrial DNA (mtDNA) across generations, exceptions were reported in the recent past. For example, some extremely rare but spectacular cases of heteroplasmy and paternal transmission in humans have questioned the universal evolutionary principle. Hence, as an alternative, the Mega-NUMT concept was coined to explain this discovery and was thereafter partly proven to exist. This concept expands on the quite common transfer of mtDNA fragments to the nucleus (NUMTs) by considering the existence of multicopy mitochondrial nuclear insertions. Mega-NUMT reports are currently restricted to a few cases in animals, including humans. However, even in humans, their detailed genomic organization, natural prevalence, and potential biological functions remain unclear. Methodology/Principal FindingsHere, we discovered that up to 60 full-sized mitochondrial genomes are integrated into the nuclear genome of the neotropical fruit fly Drosophila paulistorum using long-read sequencing and confirmed their presence by in situ hybridization. The copies are organized in one cluster on chromosome 3, which we, due to its similarity with the Mega-NUMT concept, designated the "Dpau Mega-NUMT". Contrary to the rarity in humans, this Mega-NUMT is found at high prevalence (40%) in both long-term laboratory lines and natural D. paulistorum populations of different semispecies. Additionally, the mitochondrial copies in the Mega-NUMT cluster are phylogenetically separated from the current mitotypes of D. paulistorum. Together, these observations suggest long-term maintenance of the Mega-NUMT in nature. Hence, we propose that the Dpau Mega-NUMT may have been transferred to the nuclear genome before D. paulistorum semispecies radiation and maintained at relatively high prevalence in nature by balancing selection due to yet undetermined functions. Conclusions/SignificanceTo our knowledge, this is the first verified existence and detailed dissection of a Mega-NUMT outside cats and humans. We show that Mega-NUMTs can be persistent in nature, even at high prevalence, potentially due to balancing selection. Our findings strengthen the importance of high-quality long-read sequencing technologies for deciphering complex repeat-rich genomic regions to deepen our understanding of the dynamics of genome evolution within genomic "dark matter".