Phenotypic plasticity is widespread and evolutionarily important, but genomic consequences of new plastic traits remain unclear. Here, we explore patterns of molecular evolution linked to the repeated evolution of Cephalotes turtle ant worker plasticity, in which smaller minor workers and distinct larger soldiers are produced from a single genomic blueprint through developmentally plastic mechanisms. We integrate developmental transcriptomics with comparative genomic approaches to test the relative relationships of selection on genes, selection on regulatory sequences, and the emergence of lineage-specific genes with the repeated evolution of the soldier morph. We find that phenotypic plasticity shields protein-coding genes from selection, whereas it imposes a strong selective constraint on the evolution of gene regulatory loci. The development of a soldier morph disproportionately involves the activity of evolutionarily ancient genes. Moreover, our data link three pathways- nutrition via insulin signaling, imaginal disc development, and for the first time Hippo signaling- which allow for the differential development of soldiers and workers from a single genomic background in turtle ants. Taken together, our results provide evidence that plasticity leads to relaxed selection on genes, but imposes selective constraint on regulatory elements, during the repeated evolution of the turtle ant soldier morph.
{"title":"Phenotypic plasticity in turtle ants has opposing evolutionary consequences for genes and regulatory loci.","authors":"Megan Barkdull, Corrie S Moreau","doi":"10.1093/evolut/qpaf237","DOIUrl":"https://doi.org/10.1093/evolut/qpaf237","url":null,"abstract":"<p><p>Phenotypic plasticity is widespread and evolutionarily important, but genomic consequences of new plastic traits remain unclear. Here, we explore patterns of molecular evolution linked to the repeated evolution of Cephalotes turtle ant worker plasticity, in which smaller minor workers and distinct larger soldiers are produced from a single genomic blueprint through developmentally plastic mechanisms. We integrate developmental transcriptomics with comparative genomic approaches to test the relative relationships of selection on genes, selection on regulatory sequences, and the emergence of lineage-specific genes with the repeated evolution of the soldier morph. We find that phenotypic plasticity shields protein-coding genes from selection, whereas it imposes a strong selective constraint on the evolution of gene regulatory loci. The development of a soldier morph disproportionately involves the activity of evolutionarily ancient genes. Moreover, our data link three pathways- nutrition via insulin signaling, imaginal disc development, and for the first time Hippo signaling- which allow for the differential development of soldiers and workers from a single genomic background in turtle ants. Taken together, our results provide evidence that plasticity leads to relaxed selection on genes, but imposes selective constraint on regulatory elements, during the repeated evolution of the turtle ant soldier morph.</p>","PeriodicalId":12082,"journal":{"name":"Evolution","volume":" ","pages":""},"PeriodicalIF":2.6,"publicationDate":"2025-11-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145548630","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Jordan S Martin, David F Westneat, Shinichi Nakagawa, Julia Schroeder, Terry Burke
Plastic phenotypes may often be subject to conflicting demands, which should generate nonlinear selection favoring intermediate optima. However, investigating complex patterns of selection on reaction norms has been challenging. We leveraged data on clutch size from 2 long-term studies (25 and 19 years) of individually marked house sparrows (Passer domesticus). We used a novel multivariate technique for examining linear and nonlinear selection acting on clutch size reaction norms via the fitness components of hatchling number, nestling survival, and nestling body mass at the end of the main parental period. Reaction norm slopes were highly canalized and lacked sufficient among-female variation to detect selection. Stabilizing selection and opposing patterns of directional selection occurred on both intercepts and individual residual variation via hatchling counts and nestling body mass. We also observed changes in these gradients as a function of laying date. Our results support Lack's hypothesis that quantity-quality tradeoffs shape selection on both mean clutch size and the variability of clutch sizes across breeding seasons. Our findings are also consistent with models of adaptation on asymmetric fitness landscapes, where tradeoffs near a local fitness ridge or cliff favor distinct patterns of clutch size plasticity in response to unpredictable environmental variability.
{"title":"Measuring selection on reaction norms: Lack's principle and plasticity in clutch size.","authors":"Jordan S Martin, David F Westneat, Shinichi Nakagawa, Julia Schroeder, Terry Burke","doi":"10.1093/evolut/qpaf168","DOIUrl":"10.1093/evolut/qpaf168","url":null,"abstract":"<p><p>Plastic phenotypes may often be subject to conflicting demands, which should generate nonlinear selection favoring intermediate optima. However, investigating complex patterns of selection on reaction norms has been challenging. We leveraged data on clutch size from 2 long-term studies (25 and 19 years) of individually marked house sparrows (Passer domesticus). We used a novel multivariate technique for examining linear and nonlinear selection acting on clutch size reaction norms via the fitness components of hatchling number, nestling survival, and nestling body mass at the end of the main parental period. Reaction norm slopes were highly canalized and lacked sufficient among-female variation to detect selection. Stabilizing selection and opposing patterns of directional selection occurred on both intercepts and individual residual variation via hatchling counts and nestling body mass. We also observed changes in these gradients as a function of laying date. Our results support Lack's hypothesis that quantity-quality tradeoffs shape selection on both mean clutch size and the variability of clutch sizes across breeding seasons. Our findings are also consistent with models of adaptation on asymmetric fitness landscapes, where tradeoffs near a local fitness ridge or cliff favor distinct patterns of clutch size plasticity in response to unpredictable environmental variability.</p>","PeriodicalId":12082,"journal":{"name":"Evolution","volume":" ","pages":"2460-2473"},"PeriodicalIF":2.6,"publicationDate":"2025-11-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144845054","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sperm gigantism has evolved multiple times independently, raising the question of whether intracellular allocation strategies evolved in concert with cell size. Allocation to intracellular components might evolve from direct selection on specific subcellular constituents that affect cell size indirectly, or instead as a byproduct of selection on cell size per se. We used transmission electron microscopy of nematode spermatozoa to quantify investment in pseudopods, mitochondria, and membranous organelles (MOs) from Caenorhabditis macrosperma and C. nouraguensis, related species divergent in sperm size. We demonstrate that C. macrosperma allocates more to mitochondria, in both total and relative terms, consistent with larger sperm cells having greater energetic demands associated with longevity, adhesion, and motility functions. Similar relative pseudopod sizes between species, however, are consistent with an optimal pseudopod : cell body ratio. MO size and distribution patterns within cells implicate C. macrosperma having lower relative investment in MO contributions to seminal fluid, thus excluding increased investment in MOs and pseudopod as drivers of sperm gigantism in C. macrosperma. We conclude that cell size per se likely represents the primary target of selection in the evolution of sperm gigantism, with mitochondrial traits likely evolving as a consequence of increased energetic demands of giant sperm cells.
{"title":"Divergent organelle allocation in the evolution of sperm gigantism revealed from subcellular quantification of nematode sperm with electron microscopy.","authors":"Rebecca Schalkowski, Asher D Cutter","doi":"10.1093/evolut/qpaf172","DOIUrl":"10.1093/evolut/qpaf172","url":null,"abstract":"<p><p>Sperm gigantism has evolved multiple times independently, raising the question of whether intracellular allocation strategies evolved in concert with cell size. Allocation to intracellular components might evolve from direct selection on specific subcellular constituents that affect cell size indirectly, or instead as a byproduct of selection on cell size per se. We used transmission electron microscopy of nematode spermatozoa to quantify investment in pseudopods, mitochondria, and membranous organelles (MOs) from Caenorhabditis macrosperma and C. nouraguensis, related species divergent in sperm size. We demonstrate that C. macrosperma allocates more to mitochondria, in both total and relative terms, consistent with larger sperm cells having greater energetic demands associated with longevity, adhesion, and motility functions. Similar relative pseudopod sizes between species, however, are consistent with an optimal pseudopod : cell body ratio. MO size and distribution patterns within cells implicate C. macrosperma having lower relative investment in MO contributions to seminal fluid, thus excluding increased investment in MOs and pseudopod as drivers of sperm gigantism in C. macrosperma. We conclude that cell size per se likely represents the primary target of selection in the evolution of sperm gigantism, with mitochondrial traits likely evolving as a consequence of increased energetic demands of giant sperm cells.</p>","PeriodicalId":12082,"journal":{"name":"Evolution","volume":" ","pages":"2503-2515"},"PeriodicalIF":2.6,"publicationDate":"2025-11-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144948007","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Jan Laine, Jana Nickel, Anders Romundset, Andrew D Foote
The parallel evolution of traits and their underlying genetic basis is well studied; however, studies of the parallel chronology of adaptive genetic changes remain scarce. The probability of parallel genetic change should be increased by the clustering of adaptive alleles in regions of suppressed recombination, particularly for genes that have large fitness or phenotypic effects. The threespine stickleback is a model system for studying parallel evolution, here we present genomic data from nine subfossil stickleback bones dated to 14.8-0.7 KYR BP in age. Comparing the four highest coverage genomes, which represent different stages along the marine-freshwater divergence continuum, we find that the accumulation of freshwater ancestry is clustered rather than randomly distributed throughout the marine-freshwater divergent regions of the genome. We consistently find freshwater ancestry on chromosome IV at the early stages of freshwater adaptation. Regions of chromosome IV contain the greatest genetic differentiation between marine and freshwater ecotypes and among the highest density of quantitative trait loci. These include Ectodysplasin (EDA), a large-effect pleiotropic locus associated with defensive armor and variation in neurosensory and behavioral traits. Freshwater ancestry in the subfossils is also consistently found at inversions and X chromosome early in the adaptive process. Our findings add to emerging evidence that freshwater adaptation in threespine stickleback could have a staggered but predictable temporal dynamic.
{"title":"Ancient stickleback genomes reveal the early stages of parallel adaptation.","authors":"Jan Laine, Jana Nickel, Anders Romundset, Andrew D Foote","doi":"10.1093/evolut/qpaf164","DOIUrl":"10.1093/evolut/qpaf164","url":null,"abstract":"<p><p>The parallel evolution of traits and their underlying genetic basis is well studied; however, studies of the parallel chronology of adaptive genetic changes remain scarce. The probability of parallel genetic change should be increased by the clustering of adaptive alleles in regions of suppressed recombination, particularly for genes that have large fitness or phenotypic effects. The threespine stickleback is a model system for studying parallel evolution, here we present genomic data from nine subfossil stickleback bones dated to 14.8-0.7 KYR BP in age. Comparing the four highest coverage genomes, which represent different stages along the marine-freshwater divergence continuum, we find that the accumulation of freshwater ancestry is clustered rather than randomly distributed throughout the marine-freshwater divergent regions of the genome. We consistently find freshwater ancestry on chromosome IV at the early stages of freshwater adaptation. Regions of chromosome IV contain the greatest genetic differentiation between marine and freshwater ecotypes and among the highest density of quantitative trait loci. These include Ectodysplasin (EDA), a large-effect pleiotropic locus associated with defensive armor and variation in neurosensory and behavioral traits. Freshwater ancestry in the subfossils is also consistently found at inversions and X chromosome early in the adaptive process. Our findings add to emerging evidence that freshwater adaptation in threespine stickleback could have a staggered but predictable temporal dynamic.</p>","PeriodicalId":12082,"journal":{"name":"Evolution","volume":" ","pages":"2446-2459"},"PeriodicalIF":2.6,"publicationDate":"2025-11-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144845043","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Malagasy lemurs are diverse primates that underwent adaptive radiation. While this radiation promotes modifications in cranium for niche partitioning, evolutionary constraints impose common craniofacial patterns among smaller lemurs: they are predicted to be constrained to have a shorter upper jaw and laterally facing orbits to compensate for small masticatory muscles and accommodate relatively large orbits, regardless of niche. This study aims to elucidate how these evolutionary constraints operate during the adaptive radiation of lemurs. The results demonstrated that smaller species, such as dwarf/mouse lemurs (cheirogaleids) and sportive lemurs (lepilemurids), shared an overall cranial shape despite their diverse ecological niches, as predicted. However, under the constraints related to body size, these groups are adapted to their respective niches through modifications in specific parts of the cranium, such as the rostrum. These findings suggest that, even in the presence of constraints, morphological diversity can still be produced. In contrast, larger taxa, such as Megaladapis, exhibited more diverse overall cranial morphologies, reflecting fewer constraints, and suggested novel cranial functions through modifications of the entire skull. Thus, while evolutionary constraints may limit certain aspects of morphological evolution, they can also foster diversity by channeling distinct evolutionary trajectories based on body size in adaptive radiation.
{"title":"Distinct pathways for diversification of craniofacial morphology driven by size-related constraints in Madagascar primates.","authors":"Naoto Toyoda","doi":"10.1093/evolut/qpaf176","DOIUrl":"10.1093/evolut/qpaf176","url":null,"abstract":"<p><p>Malagasy lemurs are diverse primates that underwent adaptive radiation. While this radiation promotes modifications in cranium for niche partitioning, evolutionary constraints impose common craniofacial patterns among smaller lemurs: they are predicted to be constrained to have a shorter upper jaw and laterally facing orbits to compensate for small masticatory muscles and accommodate relatively large orbits, regardless of niche. This study aims to elucidate how these evolutionary constraints operate during the adaptive radiation of lemurs. The results demonstrated that smaller species, such as dwarf/mouse lemurs (cheirogaleids) and sportive lemurs (lepilemurids), shared an overall cranial shape despite their diverse ecological niches, as predicted. However, under the constraints related to body size, these groups are adapted to their respective niches through modifications in specific parts of the cranium, such as the rostrum. These findings suggest that, even in the presence of constraints, morphological diversity can still be produced. In contrast, larger taxa, such as Megaladapis, exhibited more diverse overall cranial morphologies, reflecting fewer constraints, and suggested novel cranial functions through modifications of the entire skull. Thus, while evolutionary constraints may limit certain aspects of morphological evolution, they can also foster diversity by channeling distinct evolutionary trajectories based on body size in adaptive radiation.</p>","PeriodicalId":12082,"journal":{"name":"Evolution","volume":" ","pages":"2530-2541"},"PeriodicalIF":2.6,"publicationDate":"2025-11-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145000062","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Gonçalo C Cardoso, Jakob Isager Friis, Joana Sabino, Pedro Santos, Torben Dabelsteen
Bird songs differ widely among species and can show peculiar phenotypes, such as extreme or unusual sound frequencies for a species' body size. Although birds modulate sound frequency, size-related limitations prevent vocalizing efficiently (i.e., with high amplitude) at any frequency. To understand how the evolution of unusual sound frequencies interacts with constraints on sound amplitude, we compared where peak amplitude is located within the frequency bandwidth of songs (hereafter PRRR: peak relative to realized range) across >1,000 passerine species. Consistent with constraints on sound amplitude increasing toward the song bandwidth fringes of each species, PRRR was usually close to the bandwidth midpoint, and very few species had PRRR close to their upper or lower bandwidth limits. We found that constraints on amplitude often evolved such as to facilitate singing extreme sound frequencies: on average, species using higher-frequency frequency ranges than expected for their body size had higher PRRR compared to species with lower-frequency frequency ranges than predicted for their size. This indicates that, despite constrained by size, the evolution of unusual or extreme sound frequencies is often accompanied by adaptations (e.g., morphology of the vocal organ or tract) that to some extent facilitate singing at those unusual frequencies.
{"title":"The evolution of extreme sound frequencies in bird songs.","authors":"Gonçalo C Cardoso, Jakob Isager Friis, Joana Sabino, Pedro Santos, Torben Dabelsteen","doi":"10.1093/evolut/qpaf178","DOIUrl":"10.1093/evolut/qpaf178","url":null,"abstract":"<p><p>Bird songs differ widely among species and can show peculiar phenotypes, such as extreme or unusual sound frequencies for a species' body size. Although birds modulate sound frequency, size-related limitations prevent vocalizing efficiently (i.e., with high amplitude) at any frequency. To understand how the evolution of unusual sound frequencies interacts with constraints on sound amplitude, we compared where peak amplitude is located within the frequency bandwidth of songs (hereafter PRRR: peak relative to realized range) across >1,000 passerine species. Consistent with constraints on sound amplitude increasing toward the song bandwidth fringes of each species, PRRR was usually close to the bandwidth midpoint, and very few species had PRRR close to their upper or lower bandwidth limits. We found that constraints on amplitude often evolved such as to facilitate singing extreme sound frequencies: on average, species using higher-frequency frequency ranges than expected for their body size had higher PRRR compared to species with lower-frequency frequency ranges than predicted for their size. This indicates that, despite constrained by size, the evolution of unusual or extreme sound frequencies is often accompanied by adaptations (e.g., morphology of the vocal organ or tract) that to some extent facilitate singing at those unusual frequencies.</p>","PeriodicalId":12082,"journal":{"name":"Evolution","volume":" ","pages":"2542-2551"},"PeriodicalIF":2.6,"publicationDate":"2025-11-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145029103","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Jonathan P Velotta, Maria Stager, Zachary A Cheviron, Nathan R Senner
Novel environments can induce fitness-reducing responses (i.e., maladaptive plasticity) that should be eliminated by selection via genetic compensation. Across an environmental gradient, genetic compensation may result in a cryptic form of trait variation known as countergradient variation, in which genetic changes oppose environmental effects on trait expression. We combined lab and field data to quantify maladaptive hematological responses to hypoxia and cold in deer mice (Peromyscus maniculatus) across their ∼4,000 m elevational range. In laboratory-raised mice native to low elevations, individuals increased their hemoglobin concentration and hematocrit in response to simulated high-elevation, a response that is maladaptive if unmitigated. In contrast, deer mice from high elevation increased hematocrit and hemoglobin to a lesser degree, consistent with genetic compensation. Unlike the predictions under complete genetic compensation, we observed a positive slope between hematological traits and elevation in the field, although this slope was lower than that observed in lowlanders in the lab. Our results suggest that deer mice have attenuated maladaptive hematological responses to high-elevation via genetic compensation that is incomplete, which has led to weak countergradient variation. We suggest this phenomenon is the result of a balance between positive selection for increased oxygen carrying capacity and antagonistic selection against elevated blood viscosity.
{"title":"Incomplete genetic compensation and countergradient variation of blood-oxygen transport in deer mice.","authors":"Jonathan P Velotta, Maria Stager, Zachary A Cheviron, Nathan R Senner","doi":"10.1093/evolut/qpaf186","DOIUrl":"10.1093/evolut/qpaf186","url":null,"abstract":"<p><p>Novel environments can induce fitness-reducing responses (i.e., maladaptive plasticity) that should be eliminated by selection via genetic compensation. Across an environmental gradient, genetic compensation may result in a cryptic form of trait variation known as countergradient variation, in which genetic changes oppose environmental effects on trait expression. We combined lab and field data to quantify maladaptive hematological responses to hypoxia and cold in deer mice (Peromyscus maniculatus) across their ∼4,000 m elevational range. In laboratory-raised mice native to low elevations, individuals increased their hemoglobin concentration and hematocrit in response to simulated high-elevation, a response that is maladaptive if unmitigated. In contrast, deer mice from high elevation increased hematocrit and hemoglobin to a lesser degree, consistent with genetic compensation. Unlike the predictions under complete genetic compensation, we observed a positive slope between hematological traits and elevation in the field, although this slope was lower than that observed in lowlanders in the lab. Our results suggest that deer mice have attenuated maladaptive hematological responses to high-elevation via genetic compensation that is incomplete, which has led to weak countergradient variation. We suggest this phenomenon is the result of a balance between positive selection for increased oxygen carrying capacity and antagonistic selection against elevated blood viscosity.</p>","PeriodicalId":12082,"journal":{"name":"Evolution","volume":" ","pages":"2552-2562"},"PeriodicalIF":2.6,"publicationDate":"2025-11-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12620655/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145130339","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Maria J Albo, Bert Foquet, Jack T McKermitt, John Hunt, Scott K Sakaluk, Ben M Sadd
In response to sexual conflict, males have evolved strategies manipulating female behavior and physiology to increase their paternity. One hypothesis posits that males of some insects use nuptial food gifts given to females at copulation to achieve this. In decorated crickets, Gryllodes sigillatus, the male's nuptial gift, the spermatophylax, is consumed by the female after mating, prior to her removing a sperm-containing ampulla. Spermatophylax feeding deters premature termination of sperm transfer, thereby enhancing male paternity. We hypothesized that spermatophylax proteins play a key role in sexual conflict and are a route through which males manipulate female future reproductive behavior to their own fitness benefit. We used RNA interference to knockdown gene expression of SPX1 and SPX2, the most abundant spermatophylax proteins, assessing focal male mating and female remating. Males with reduced SPX1/2 expression had lower mating success, and females fed for a shorter time on their spermatophylaxes. Moreover, females mated with SPX1/2 knockdown males had reduced latency to remate and fed longer on spermatophylaxes upon remating. Our results provide evidence that spermatophylax proteins play important roles in mediating sexual conflict, enhancing a male's paternity share by increasing his sperm transfer time, while decreasing that of competitors in subsequent matings.
{"title":"RNA interference reveals that male nuptial gift proteins affect female behavior to increase male paternity share in decorated crickets.","authors":"Maria J Albo, Bert Foquet, Jack T McKermitt, John Hunt, Scott K Sakaluk, Ben M Sadd","doi":"10.1093/evolut/qpaf161","DOIUrl":"10.1093/evolut/qpaf161","url":null,"abstract":"<p><p>In response to sexual conflict, males have evolved strategies manipulating female behavior and physiology to increase their paternity. One hypothesis posits that males of some insects use nuptial food gifts given to females at copulation to achieve this. In decorated crickets, Gryllodes sigillatus, the male's nuptial gift, the spermatophylax, is consumed by the female after mating, prior to her removing a sperm-containing ampulla. Spermatophylax feeding deters premature termination of sperm transfer, thereby enhancing male paternity. We hypothesized that spermatophylax proteins play a key role in sexual conflict and are a route through which males manipulate female future reproductive behavior to their own fitness benefit. We used RNA interference to knockdown gene expression of SPX1 and SPX2, the most abundant spermatophylax proteins, assessing focal male mating and female remating. Males with reduced SPX1/2 expression had lower mating success, and females fed for a shorter time on their spermatophylaxes. Moreover, females mated with SPX1/2 knockdown males had reduced latency to remate and fed longer on spermatophylaxes upon remating. Our results provide evidence that spermatophylax proteins play important roles in mediating sexual conflict, enhancing a male's paternity share by increasing his sperm transfer time, while decreasing that of competitors in subsequent matings.</p>","PeriodicalId":12082,"journal":{"name":"Evolution","volume":" ","pages":"2421-2432"},"PeriodicalIF":2.6,"publicationDate":"2025-11-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144783872","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sophie Lyth, Tom Gill, Andri Manser, Jolanta Tanianis, Gregory D D Hurst, Andrea J Betancourt, Thomas A R Price, Rudi L Verspoor
Selfish genetic elements enjoy an evolutionary advantage by enhancing their own transmission to offspring, and their genetic suppressors are favored when they re-establish fair inheritance patterns. Here, we study an X-linked sex ratio drive system (SR) in Drosophila subobscura, which kills Y-bearing sperm of SR males, resulting in the over-transmission of the SR chromosome and a strong female bias in their offspring. We surveyed D. subobscura populations in North Africa, which naturally harbor SR, and found that suppression occurs in ∼13.5% of wild-derived lines. We characterize this suppression phenotype through a series of crossing experiments, including multigenerational introgression of SR chromosomes into a suppressing genetic background. We show that introgression can restore normal offspring sex ratios or, in some cases, result in an excess of male offspring. This suppression appears to be a multilocus trait, involving autosomes and the Y chromosomes. Suppression of SR fails to ameliorate all costs of drive, with fully suppressed SR-carrying males having depressed fertility and low offspring egg hatch rates. Further examination of internal male reproductive organs using microscopy suggests that suppressed SR males also have abnormal testes. These factors may explain why the suppression fails to reach high frequencies, despite the strong advantage of suppressing SR.
{"title":"Suppression of sex-ratio drive in Drosophila subobscura.","authors":"Sophie Lyth, Tom Gill, Andri Manser, Jolanta Tanianis, Gregory D D Hurst, Andrea J Betancourt, Thomas A R Price, Rudi L Verspoor","doi":"10.1093/evolut/qpaf153","DOIUrl":"10.1093/evolut/qpaf153","url":null,"abstract":"<p><p>Selfish genetic elements enjoy an evolutionary advantage by enhancing their own transmission to offspring, and their genetic suppressors are favored when they re-establish fair inheritance patterns. Here, we study an X-linked sex ratio drive system (SR) in Drosophila subobscura, which kills Y-bearing sperm of SR males, resulting in the over-transmission of the SR chromosome and a strong female bias in their offspring. We surveyed D. subobscura populations in North Africa, which naturally harbor SR, and found that suppression occurs in ∼13.5% of wild-derived lines. We characterize this suppression phenotype through a series of crossing experiments, including multigenerational introgression of SR chromosomes into a suppressing genetic background. We show that introgression can restore normal offspring sex ratios or, in some cases, result in an excess of male offspring. This suppression appears to be a multilocus trait, involving autosomes and the Y chromosomes. Suppression of SR fails to ameliorate all costs of drive, with fully suppressed SR-carrying males having depressed fertility and low offspring egg hatch rates. Further examination of internal male reproductive organs using microscopy suggests that suppressed SR males also have abnormal testes. These factors may explain why the suppression fails to reach high frequencies, despite the strong advantage of suppressing SR.</p>","PeriodicalId":12082,"journal":{"name":"Evolution","volume":" ","pages":"2394-2405"},"PeriodicalIF":2.6,"publicationDate":"2025-11-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144741677","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Thyago Vanderlinde, Fabiana Uno, Gabriel Goldstein, François Sabot, Claudia M A Carareto, Cristina Vieira, Therese A Markow, Antonio Bernardo Carvalho
Y chromosomes play important roles in sex determination, male fertility, and, in some cases, hybrid male sterility. Nearly 40 years ago, Zouros and co-workers found that Drosophila mojavensis males carrying a Y chromosome from the sibling species D. arizonae are sterile, with fertility restored by chromosome 4 from D. arizonae. While these findings could result from gene interactions, they may also suggest the movement of an essential male fertility gene from the Y to chromosome 4 in the D. arizonae lineage. To test this, we analyzed the Y-linked gene content of D. mojavensis, D. arizonae, and the closely related D. navojoa. We identified 5 previously unreported Y-linked genes, bringing the total to 14. These genes fit the pattern observed in other Drosophila species: they originated from autosomal, testis-specific genes that duplicated onto the Y chromosome. All Y-linked genes are shared between D. arizonae and D. mojavensis, ruling out the movement of a protein-coding gene as the cause of sterility. However, we found a huge difference in the copy number of GI26128, an HP1 gene family member, with ∼1,400 Y-linked copies in D. arizonae but only 6 in D. mojavensis, making it a candidate to explain the hybrid male sterility.
Y染色体在性别决定,男性生育能力,以及在某些情况下,杂交男性不育中起着重要作用。大约40年前,Zouros和他的同事发现,携带兄弟种亚利桑那果蝇Y染色体的莫贾果蝇雄性不育,通过亚利桑那果蝇的4号染色体恢复生育能力。虽然这可能是基因相互作用的结果,但它们也可能表明,在亚利桑那龙谱系中,一个重要的雄性生育基因从Y染色体转移到了4号染色体。为了验证这一点,我们分析了D. mojavensis, D. arizonae和近亲D. navojoa的y连锁基因含量。我们确定了5个以前未报道的y连锁基因,使总数达到14个。这些基因符合在其他果蝇物种中观察到的模式:它们起源于常染色体,睾丸特异性基因复制到Y染色体上。所有的y连锁基因在D. arizonae和D. mojavensis之间都是共享的,这就排除了一个蛋白质编码基因的移动是不育的原因。然而,我们发现HP1基因家族成员GI26128的拷贝数存在巨大差异,在D. arizonae中有~ 1400个y连锁拷贝,而在D. mojavensis中只有6个,这使其成为解释杂交雄性不育的候选基因。
{"title":"Male sterility in Drosophila mojavensis × D. arizonae hybrids is not caused by gene movements in the Y chromosome.","authors":"Thyago Vanderlinde, Fabiana Uno, Gabriel Goldstein, François Sabot, Claudia M A Carareto, Cristina Vieira, Therese A Markow, Antonio Bernardo Carvalho","doi":"10.1093/evolut/qpaf163","DOIUrl":"10.1093/evolut/qpaf163","url":null,"abstract":"<p><p>Y chromosomes play important roles in sex determination, male fertility, and, in some cases, hybrid male sterility. Nearly 40 years ago, Zouros and co-workers found that Drosophila mojavensis males carrying a Y chromosome from the sibling species D. arizonae are sterile, with fertility restored by chromosome 4 from D. arizonae. While these findings could result from gene interactions, they may also suggest the movement of an essential male fertility gene from the Y to chromosome 4 in the D. arizonae lineage. To test this, we analyzed the Y-linked gene content of D. mojavensis, D. arizonae, and the closely related D. navojoa. We identified 5 previously unreported Y-linked genes, bringing the total to 14. These genes fit the pattern observed in other Drosophila species: they originated from autosomal, testis-specific genes that duplicated onto the Y chromosome. All Y-linked genes are shared between D. arizonae and D. mojavensis, ruling out the movement of a protein-coding gene as the cause of sterility. However, we found a huge difference in the copy number of GI26128, an HP1 gene family member, with ∼1,400 Y-linked copies in D. arizonae but only 6 in D. mojavensis, making it a candidate to explain the hybrid male sterility.</p>","PeriodicalId":12082,"journal":{"name":"Evolution","volume":" ","pages":"2433-2445"},"PeriodicalIF":2.6,"publicationDate":"2025-11-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12620656/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144834662","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"环境科学与生态学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}