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Sexual selection, genomic evolution and population fitness in Drosophila pseudoobscura.

Sexual selection shapes the genome in unique ways. It is also likely to have significant fitness consequences, such as purging deleterious mutations from the genome or conversely maintaining genetic load in a population via sexual conflict. Here, we examined what the influence of sexual selection has on genomic variation potentially underlying population fitness using experimentally evolved Drosophila pseudoobscura populations. Sexual selection was manipulated by keeping replicate lines in elevated polyandry or strict monogamy for approximately 200 generations followed by individual-based sequencing. Using pi (π), fixation index (Fst)and recombination rate measures, we confirmed signatures of selection were not dispersed but mainly localized to the third and X chromosome. Overall mutational load was similar between lines but our analysis of the distribution of fitness effects revealed considerable variation between lines and chromosomes. Furthermore, we found that the distribution of transposable elements differs between the lines, with a higher load in monogamous lines. Our results suggest that complex interactions between purifying selection and sexual conflict are shaping the genome, particularly on chromosome 3 and the sex chromosome; sexual selection influences divergence across chromosomes but in a more complex way than proposed by simple 'purging' of deleterious loci.

Animals

Sexual selection purges mutation load, but not overall genetic diversity, decreasing vulnerability to extinction.

Theory suggests sexual selection will enhance population viability by purging deleterious alleles. However, direct genomic evidence for this fundamental idea is scarce and contradictory. We combined long-term experimental evolution with whole-genome resequencing to directly test how sexual selection affects mutation load, genomic divergence, and extinction risk in small populations (maximum Ne = 40) of Tribolium castaneum. After 156 generations, populations evolving under strong sexual selection carried substantially fewer deleterious alleles than populations under weak sexual selection, based on both individual-level estimates of missense and nonsense variants and population-level Rxy analyses, indicating more efficient purging of deleterious alleles. In contrast, nucleotide diversity and runs of homozygosity were similar across treatments, indicating that purging acted most strongly on deleterious variation, and that reduced mutation load in these small populations under strong sexual selection was not explained by demographic effects. Importantly, population-level mutation load estimates best explained extinction risk under inbreeding, directly linking sexual selection to purging and population viability. Genome scans of high and low sexual selection populations revealed peaks of divergence, which included genes involved in courtship, sex discrimination, and seminal fluid proteins. Our results provide direct genomic evidence that sexual selection can reduce mutation load without eroding standing genetic diversity and thus adaptive potential, while driving adaptive divergence in reproductive traits. This beneficial purging may help explain the widespread prevalence of sexual reproduction in nature despite inherent costs and have important ramifications as to how we manage populations of conservation concern.

Animals

The Genetic Basis of Elongated Tails in Birds: Evidence for Sexual Selection as a Driver of Convergent Evolution.

Elongated tails are exaggerated ornaments observed in various bird species, and their functional and evolutionary dynamics have attracted considerable attention. Empirical studies consistently show that sexual selection is a major drive of tail elongation. However, the genetic basis of this trait remains poorly understood. To address this gap, we performed comparative genomic analyses of 23 bird species, including 7 with extremely long tails and 16 with relative short tails. Genes related to feather development exhibited amino acid convergence replacement (e.g., APC) or displayed faster evolutionary rates (e.g., LEF1, WISP3) in the long-tailed species. Importantly, we identified convergence replacements of amino acids and rapid evolution in genes related to reproductive functions (e.g., PAQR7) and immunity (e.g., ADA), suggesting that elongated tails may serve as honest signals of genetic quality. In conclusion, this study provides genomic evidence supporting the role of sexual selection in the evolution of elongated tails, revealing an intricate interplay between sexually selected traits, fitness, and immune competence.

Animals

Accounting for recombination rate variation improves inference of barrier loci and reveals the role of both natural and sexual selection in an incipient bird radiation.

Examining genomic patterns of differentiation across lineage pairs at different stages of the speciation continuum, in combination with recombination maps, can help disentangle the effects of linked and divergent selection and identify lineage-specific targets of selection that may act as barrier loci during speciation. Here, we apply this framework to genomic data from African and Indian Ocean bird species of the genus Zosterops (Zosteropidae) to identify candidate barrier loci between ecologically, phenotypically, and genetically distinct Reunion gray white-eye (Zosterops borbonicus) parapatric geographic forms. Using analyses that account for recombination rate variation, we show that putative targets of divergent selection are primarily located on the Z chromosome, except in comparisons between geographic forms that differ in their ecologies. Functional annotation revealed that candidate barrier loci between forms with similar environmental niches are associated with genes involved in song formation and immune function, whereas those between forms with different environmental niches are associated with adaptation to altitude, morphology, and song behavior. Our results highlight the combined roles of natural and sexual selection in the evolution of reproductive barriers in this incipient species radiation.

Animals

Positive selection and relaxed purifying selection contribute to rapid evolution of sex-biased genes in green seaweed Ulva.

BACKGROUND: The evolution of differences in gamete size and number between sexes is a cornerstone of sexual selection theories. The green macroalga Ulva, with incipient anisogamy and parthenogenetic gametes, provides a unique system to investigate theoretical predictions regarding the evolutionary pressures that drive the transition from isogamy to anisogamy, particularly in relation to gamete size differentiation and sexual selection. Its minimal gamete dimorphism and facultative parthenogenesis enable a rare window into early evolutionary steps toward anisogamy. RESULTS: By analyzing the expression profiles of sex-biased genes (SBGs) during gametogenesis, we found that SBGs evolve faster than unbiased genes, driven by higher rates of non-synonymous substitution (dN), indicating that SBGs are under stronger selective pressures. Mating type minus-biased genes (mt-BGs) exhibit higher dN/dS values than mating type plus-biased genes (mt+BGs), suggesting stronger selective pressures on mt-BGs, although this difference was not statistically significant (P = 0.08). Using branch-site and RELAX models, we found positive selection and relaxed purifying selection acting on a significant proportion of SBGs, particularly those associated with flagella function. CONCLUSIONS: This study highlights the selective pressures shaping anisogamy and provides insights into the molecular mechanisms underlying its evolution. The faster evolution of SBGs, particularly mt-BGs, and the positive selection on genes associated with motility, such as those related to flagella function, suggest the importance of enhanced gamete motility in the transition to anisogamy. These findings contribute to our understanding of sexual selection and the evolutionary forces that drive the differentiation of gamete size and number between sexes.

Selection, Genetic

Latent preference for red ornamentation drives interspecific mating in nascent jumping spider species (Habronattus americanus group, F. Salticidae).

Heterospecific interactions between nascent species offer insights into how sexual selection shapes novel traits, illuminating patterns in species interactions and diversification. We tested female preferences between two recently diverged, allopatric species of jumping spiders: Habronattus americanus PLC, with red-coloured males performing short multimodal displays, and Habronattus sansoni CC, with brown-coloured males performing long multimodal displays. Mate choice experiments showed that females of both species preferred H. americanus PLC males. To examine the role of red coloration, we manipulated male coloration in both species. Results indicated that red-painted H. sansoni CC males experienced an increase in mating success, whereas brown-painted H. americanus PLCmales did not show reduced success. Our study suggests that (i) strong latent female preferences can drive unidirectional introgression across species boundaries, potentially leading to genomic homogenization; (ii) latent preferences may override preferences for existing traits; and (iii) the geographical distribution of colour morphs is consistent with a hypothesis of strong latent preferences across populations. Overall, our study demonstrates the role that mating interactions can play in speciation dynamics.

Animals

Improved Genomic Resources for the swordtail cricket, Laupala kohalensis Otte 1994.

Advances in genetic tools such as next and third generation sequencing, paired with a focus on representative clades, provide insight into how processes including adaptation, admixture, and genome structure shape the evolution and maintenance of species. However, our understanding of the genomics of speciation is dominated by systems where ecological adaptations are thought to cause initial barriers to gene exchange. In contrast to other model systems, the 38 species of the genus Laupala constitute a very rapid radiation, where evolution of reproductive barriers and speciation is thought to be driven by sexual selection. Here, with novel PacBio HiFi reads and RNA- and Iso-Seq data, we provide a highly contiguous, chromosome-level genome and markedly improved annotation of the endemic Hawaiian cricket, Laupala kohalensis Otte, 1994. Our new resources advance previous efforts, placing 99% of 47 scaffolds on 7 autosomes and 1 sex chromosome in the 1.67 Gb assembly, with a 98.8% BUSCO score (insecta_db10), N50 of ~268 Mb, and L50 of 3. Using a custom repeat library, we estimate the genome to have 46.09% repeat content, and the new annotation includes an increased estimate of 17,670 genes, which coincides with that known from other Orthopterans. Notably, we find a large nuclear DNA segment of mitochondrial origin on chromosome 7. This new resource provides a powerful tool to identify and compare genomic causes of phenotypic diversification in a system characterized by strong signatures of sexual differentiation, representing an underappreciated but potentially widespread cause of speciation.

Hawaii

Rapid vertebrate speciation via isolation, bottlenecks, and drift.

Speciation is often driven by selective processes like those associated with viability, mate choice, or local adaptation, and "speciation genes" have been identified in many eukaryotic lineages. In contrast, neutral processes are rarely considered as the primary drivers of speciation, especially over short evolutionary timeframes. Here, we describe a rapid vertebrate speciation event driven primarily by genetic drift. The White Sands pupfish (Cyprinodon tularosa) is endemic to New Mexico's Tularosa Basin where the species is currently managed as two Evolutionarily significant units (ESUs) and is of international conservation concern (Endangered). Whole-genome resequencing data from each ESU showed remarkably high and uniform levels of differentiation across the entire genome (global FST ≈ 0.40). Despite inhabiting ecologically dissimilar springs and streams, our whole-genome analysis revealed no discrete islands of divergence indicative of strong selection, even when we focused on an array of candidate genes. Demographic modeling of the joint allele frequency spectrum indicates the two ESUs split only ~4 to 5 kya and that both ESUs have undergone major bottlenecks within the last 2.5 millennia. Our results indicate the genome-wide disparities between the two ESUs are not driven by divergent selection but by neutral drift due to small population sizes, geographic isolation, and repeated bottlenecks. While rapid speciation is often driven by natural or sexual selection, here we show that isolation and drift have led to speciation within a few thousand generations. We discuss these evolutionary insights in light of the conservation management challenges they pose.

Animals

A telomere-to-telomere gap-free genome assembly of the endangered humphead wrasse (Cheilinus undulatus).

Humphead wrasse, Cheilinus undulatus, is an endangered fish species with high economic and ecological value as well as natural sex change from female to male, while sexual selection occurs in breeding aggregations. In our present study, we constructed the first gap-free telomere-to-telomere (T2T) genome assembly for humphead wrasse, by integration of PacBio HiFi, ONT Ultra-long and Hi-C sequencing techniques. With 99% of the entire sequences anchored into 24 chromosomes, this haplotypic genome assembly spans approximately 1.25 Gb and presents a complete set of 48 telomeres and 24 centromeres. In terms of correctness (quality value QV: 53.447) and completeness (BUSCO score: 99.3%), this chromosome-scale assembly is indeed of high quality. We predicted 658.03 Mb of repetitive sequences and annotated 26,609 protein-coding genes in the assembled genome. This high-quality T2T genome assembly not only facilitates the genetic conservation of humphead wrasse, but also offers fundamental genomic data for supporting in-depth investigations on functional genomics, genetic diversity, and selective breeding for this economically important teleost.

Animals

The metabolic costs of meiotic drive.

Selfish genetic elements, such as meiotic drive genes, disrupt Mendel's law of equal segregation by biasing their own transmission, often at a detriment to the rest of the genome. Metabolic costs of the X-linked sex ratio (SR) meiotic drive were investigated in stalk-eyed flies (Teleopsis dalmanni). The experiments demonstrate that individuals with SR have reduced capacity for ATP synthesis. The disruption in mitochondrial function leads to compensation exhibited in increased basal metabolic rate and greater food consumption across a range of diets. The range of metabolic costs of drive was evident in males and females at a similar magnitude. The likely cause lies in the accumulation of deleterious mutations within the series of large inversions on the drive X chromosome, subject to low recombination and weak natural selection. In females, the drive chromosome had a dominant effect, with a single copy causing substantial metabolic compromise. There was little evidence of male-specific metabolic costs, nor evidence of greater effects of drive chromosomes on female metabolism. This suggests that direct metabolic costs from meiotic drive on spermatogenesis and from sexually antagonistic selection are relatively weak. Our results underscore the broad physiological impacts that selfish genetic elements have on host metabolism and fitness.

Animals

Multivariate genetic architecture reveals testosterone-driven sexual antagonism in contemporary humans.

Sex difference (SD) is ubiquitous in humans despite shared genetic architecture (SGA) between the sexes. A univariate approach, i.e., studying SD in single traits by estimating genetic correlation, does not provide a complete biological overview, because traits are not independent and are genetically correlated. The multivariate genetic architecture between the sexes can be summarized by estimating the additive genetic (co)variance across shared traits, which, apart from the cross-trait and cross-sex covariances, also includes the cross-sex-cross-trait covariances, e.g., between height in males and weight in females. Using such a multivariate approach, we investigated SD in the genetic architecture of 12 anthropometric, fat depositional, and sex-hormonal phenotypes. We uncovered sexual antagonism (SA) in the cross-sex-cross-trait covariances in humans, most prominently between testosterone and the anthropometric traits - a trend similar to phenotypic correlations. 27% of such cross-sex-cross-trait covariances were of opposite sign, contributing to asymmetry in the SGA. Intriguingly, using multivariate evolutionary simulations, we observed that the SGA acts as a genetic constraint to the evolution of SD in humans only when selection is sexually antagonistic and not concordant. Remarkably, we found that the lifetime reproductive success in both the sexes shows a positive genetic correlation with anthropometric traits, but not with testosterone. Moreover, we demonstrated that genetic variance is depleted along multivariate trait combinations in both the sexes but in different directions, suggesting absolute genetic constraint to evolution. Our results indicate that testosterone drives SA in contemporary humans and emphasize the necessity and significance of using a multivariate framework in studying SD.

Humans

Biochemical and Genomic Underpinnings of Carotenoid Colour Variation Across a Hybrid Zone Between South Asian Flameback Woodpeckers.

Colouration and patterning have been implicated in lineage diversification across various taxa, as colour traits are heavily influenced by sexual and natural selection. Investigating the biochemical and genomic foundations of these traits therefore provides deeper insights into the interplay between genetics, ecology and social interactions in shaping the diversity of life. In this study, we assessed the pigment chemistries and genomic underpinnings of carotenoid colour variation in naturally hybridising Dinopium flamebacks in tropical South Asia. We employed reflectance spectrometric analysis to quantify species-specific plumage colouration, High-Performance Liquid Chromatography (HPLC) to elucidate the feather carotenoids of flamebacks across the hybrid zone, and Genome-Wide Association Study (GWAS) using next-generation sequencing data to uncover the genetic factors underlying carotenoid colour variation in flamebacks. Our analysis revealed that the red mantle feathers of D. psarodes primarily contained astaxanthin, with small amounts of other 4-keto-carotenoids. In contrast, the yellow mantle feathers of D. benghalense predominantly contained lutein and 3'-dehydro-lutein, alongside minor amounts of zeaxanthin, β-cryptoxanthin and canary-xanthophylls A and B. Hybrids with an intermediate, orange colouration deposited all of these pigments in their mantle feathers, with notably higher concentrations of carotenoids with ε-end rings. The GWAS analysis identified the CYP2J2 gene, which plays a role in carotenoid ketolation, as associated with the expression of carotenoid colouration. Read depth data suggested variation in copy number of this gene in flamebacks. These findings contribute to the growing knowledge of avian carotenoid metabolism and highlight how genomic architecture can influence phenotypic diversity.

Animals

Genomic response to sex-separated gene pools.

Males and females experience differences in the strength and direction of selection but discerning the type of genes that are targets of sex differences in selection is complicated by their shared genome. We used experimental evolution in Drosophila melanogaster to partially separate the gene pools of males and females for 130 generations. In six replicate populations, we forced one pool of genetically variable Chromosome 2s to experience patrilinear inheritance (segregating like a Y-chromosome) and male-limited selection. The alternative pool segregated like an X-chromosome and experienced female-biased selection. This allowed alleles which are differentially selected for between the sexes to diverge between these pools, enabling us to gain insight into the type of genes subject to such selection. We find that genes which diverge between these pools have an elevated intersexual genetic correlation(rMF) for expression on average, consistent with the idea that high genetic correlations may hinder sex-specific adaptation under normal inheritance. Diverged genes were also enriched for moderately male-biased genes whereas female-biased genes were underrepresented. At the SNP level, we find an overrepresentation of diverged SNPs involved in splicing or occurring in the 5'UTR and an underrepresentation of missense or synonymous SNPs, suggesting sex differences in selection for isoform usage.

intersexual genetic correlation

Sexually dimorphic expression and hormonal responsiveness of steroidogenic Cyp genes during gonadal differentiation in mandarin fish.

Steroid hormones play a pivotal role in fish sex differentiation, yet the dynamic expression patterns of key steroidogenic enzymes during this process remain incompletely characterized. Here, we combined genome-wide identification, time series transcriptomes spanning gonadal development (5-360 days post-hatch), and multiple hormone treatment experiments (17α-methyltestosterone, estrone, and etonogestrel) to investigate the Cyp11, Cyp17, Cyp19, and Cyp21 subfamilies in mandarin fish (Siniperca chuatsi). Seven steroidogenic Cyp genes were identified, showing teleost-specific expansion, with one duplicated pair (cyp17a2 and cyp2u1) exhibiting strong purifying selection. Expression profiling revealed pronounced sexually dimorphic and stage-specific patterns: During female differentiation (20-30 days), cyp19a1a and associated genes were highly expressed, coinciding with ovarian differentiation; during male differentiation (30-60 days), cyp17a2 and related genes were upregulated, aligning with testicular development. Exogenous hormone treatments further demonstrated that these genes are dynamically responsive: cyp19a1a and cyp17a2 were highly responsive to androgenic and progestogenic treatments, and their expression changes correlated closely with gonadal sex reversal phenotypes observed histologically. Collectively, this study provides a comprehensive expression atlas of steroidogenic Cyp genes during gonadal differentiation and identifies key hormonally responsive candidates for sex control in aquaculture.

Animals

The release of sexual conflict after sex loss is associated with evolutionary changes in gene expression.

Sexual conflict can arise because males and females, while sharing most of their genome, can have different phenotypic optima. Sexually dimorphic gene expression may help reduce conflict, but the expression of many genes may remain sub-optimal owing to unresolved tensions between the sexes. Asexual lineages lack such conflict, making them relevant models for understanding the extent to which sexual conflict influences gene expression. We investigate the evolution of sexual conflict subsequent to sex loss by contrasting the gene expression patterns of sexual and asexual lineages in the pea aphid Acyrthosiphon pisum. Although asexual lineages of this aphid produce a small number of males in autumn, their mating opportunities are limited because of geographic isolation between sexual and asexual lineages. Therefore, gene expression in parthenogenetic females of asexual lineages is no longer constrained by that of other morphs. We found that the expression of genes in males from asexual lineages tended towards the parthenogenetic female optimum, in agreement with theoretical predictions. Surprisingly, males and parthenogenetic females of asexual lineages overexpressed genes normally found in the ovaries and testes of sexual morphs. These changes in gene expression in asexual lineages may arise from the relaxation of selection or the dysregulation of gene networks otherwise used in sexual lineages.

Animals

High-variance phenome database reveals important roles of WD40 proteins in the plant pathogenic fungus Fusarium graminearum.

WD40 is a highly conserved protein domain in eukaryotes that functions as a versatile platform for protein-protein interactions and participates in diverse biological processes. We performed a genome-wide functional analysis of WD40 domain-containing proteins in Fusarium graminearum, a phytopathogenic fungus that causes severe yield losses and mycotoxin contamination in major cereal crops. Comprehensive phenotypic profiling of 119 WD40 gene deletion mutants across 22 phenotypic traits established a systematic WD40 phenome dataset, revealing the broad functional involvement of WD40 proteins and a strong correlation between sexual reproduction and virulence. Protein interaction analyses of selected WD40 proteins revealed diverse WD40-mediated interaction patterns and provided further insights into WD40-mediated protein interactions and their roles in protein complex formation. This study provides a foundation for further characterization of WD40 proteins in filamentous fungi.

Fusarium graminearum

Sex without crossovers mimics clonal reproduction in Rhynchospora tenuis.

Meiotic recombination ensures accurate chromosome segregation and promotes genetic diversity by generating crossovers between homologous chromosomes1. Although essential in most sexually reproducing organisms, recombination is variably regulated and can be absent in some lineages, a condition known as achiasmy2. However, obligate achiasmy in both sexes of a sexual species has not been documented. Here we investigate Rhynchospora tenuis, a flowering plant with the lowest known chromosome number and inverted meiosis3. Combining genomics with molecular experiments, we show that R. tenuis undergoes obligate, genome-wide achiasmy in both male and female meiosis. Despite normal early meiotic axis formation, synapsis fails, crossovers are undetectable cytologically and genetically, and univalents persist at metaphase I. Haplotype-specific accumulation of transposable elements generates segregation distortion favouring the transmission of larger, repeat-rich chromosomes. Sexual reproduction is nevertheless retained: fertilization yields viable seeds only when translocation-compatible gametes meet, indicating strong post-meiotic selection against incompatible homozygous combinations. As a result, all surviving offspring are genetically identical, effectively maintaining heterozygosity by sexual reproduction with parental genotype restitution mimicking clonal reproduction. We propose that recombination loss, a low chromosome number, inverted meiosis and selection for compatible gamete combinations together enable faithful segregation and clonal-like inheritance despite sexual reproduction. These findings blur the boundary between sex and clonality, linking genome architecture, recombination loss and transmission bias.

Journal Article

Response to divergent selection on meiotic recombination in Saccharomyces cerevisiae.

Meiotic recombination is a key driver of evolution in sexually reproducing species, reshaping genetic diversity by generating novel allelic combinations. The rate of recombination varies substantially across living organisms depending on cis- or trans-acting genetic elements, as seen in many species, including the yeast Saccharomyces cerevisiae. Here, we report on an experimental evolution-based study to better understand the factors shaping this natural variation. Starting with a genetically diverse population of S. cerevisiae, we have carried out recurrent divergent selection on recombination rate using a fluorescence-based sorting approach in four independent lineages. After ten generations, we observed an average response of recombination rate of +28% after positive selection and -24% after negative selection, within the interval used for selection. In the adjacent region, however, we observed a weaker response in the opposite direction, and no response in four other unlinked genomic regions. Whole-genome sequencing of individuals selected for high recombination revealed mixed outcomes in the four independently evolved lineages for high genome-wide recombination rates. However, all four lineages showed selection for high recombination locally, with particular haplotypes heavily favored and sequence- or structural variation-based heterozygosity selected against within the selection interval. Overall, this experimental evolution approach provides original and useful insights into the evolvability of the meiotic recombination rate and the associated genetic determinants.

Meiotic recombination