Jake Galvin, Sevan Yedigarian, Mohammad Rahman, Kirill Borziak, Michael DeNieu, Erica L Larson, Mollie K Manier
{"title":"Sperm length and seminal fluid proteins promote male reproductive success in D. melanogaster.","authors":"Jake Galvin, Sevan Yedigarian, Mohammad Rahman, Kirill Borziak, Michael DeNieu, Erica L Larson, Mollie K Manier","doi":"10.1093/jeb/voaf065","DOIUrl":"https://doi.org/10.1093/jeb/voaf065","url":null,"abstract":"<p><p>Spermatozoal morphology is highly variable both within and among species, often corresponding to variation in the shape of the female sperm storage organs in ways that can significantly impact fertilization success. In an effort to understand genetic mechanisms of sperm length variation, we compared gene expression patterns in the testes of Drosophila melanogaster males that produce either long or short sperm. We found that genes upregulated in long sperm testes are enriched for long noncoding RNAs (lncRNAs) and seminal fluid proteins (Sfps). Transferred in seminal fluid to the female during mating, Sfps are secreted by the male accessory glands and affect female remating rate, physiology, and behavior with concomitant advantages for male reproductive success. While sperm and Sfps are both critical for male reproductive success, they are largely considered to be functionally, genetically, and developmentally independent and despite being upregulated in long sperm testes, Sfps have no known function in testis tissue. We found that knockouts of two Sfps upregulated in long sperm males, Sex Peptide (SP) and ovulin (Acp26Aa) resulted in shorter sperm, which altogether suggests that Sfps may play a role in the development of sperm length during spermatogenesis. Consistent with this, knockout of accessory gland function did not affect sperm length, suggesting that accessory gland expression had no influence on spermatogenic processes. We also found that long sperm males were better able to delay female remating. These results might suggest that long sperm males have a double advantage in sperm competition by both delaying female remating, likely through transfer of more Sfps, and by resisting sperm displacement. However, we found that the delay in female remating does not necessarily translate to more progeny or higher paternity success. Thus, we found that multiple components of the ejaculate promote male reproductive success at different stages of reproduction, but the realized fitness advantages in sperm competition are uncertain.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":""},"PeriodicalIF":2.1,"publicationDate":"2025-05-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144174554","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Surviving in the fast lane: No increased mortality, but faster growth for pathogen-exposed larvae of a family living beetle.","authors":"Leon Müller, Sandra Steiger, Maximilian Körner","doi":"10.1093/jeb/voaf068","DOIUrl":"https://doi.org/10.1093/jeb/voaf068","url":null,"abstract":"<p><p>Animal taxa exhibiting post-hatching care can be found throughout the animal kingdom. During this period, parents aggregate with their offspring and allow them to invest their resources into growth and development as parents take over energy consuming tasks. For instance, studies show that food provisioning and social immunity by parents can alleviate the costs of an offspring's immune response to pathogen exposure. However, this issue has rarely been explored in offspring of species showing plasticity in their dependency on parental care. Here, we raise the question of how offspring are affected by pathogen exposure if they have access to social immunity through a caring parent. Parents of Nicrophorus vespilloides, a species exhibiting facultative post-hatching care, control the carcass microbiome by coating it with their antimicrobial exudates, stopping further decay and protecting their offspring from potential pathogens. We exposed N. vespilloides offspring to a generalist entomopathogenic fungus, Beauveria bassiana, while manipulating presence or absence of post-hatching parental care. We monitored offspring performance parameters throughout their development and found, curiously, larvae showed an increase in mean weight and growth rate after being exposed to the pathogen, while their survival and adult immunity were unaffected. These effects of pathogen exposure occurred regardless of parental care. Simultaneously, our results indicate that females invest fewer resources into their offspring if they have been exposed to the pathogen. Overall, we show that offspring of facultative subsocial species may not respond differently to pathogen exposure depending on their parents' aid. Additionally, our results indicate that offspring of facultatively subsocial species may adjust their growth rate in response to pathogen exposure in the nest.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":""},"PeriodicalIF":2.1,"publicationDate":"2025-05-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144174887","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"The evolution of sex-specific gene expression in polygenic traits.","authors":"Ewan Flintham","doi":"10.1093/jeb/voaf050","DOIUrl":"https://doi.org/10.1093/jeb/voaf050","url":null,"abstract":"<p><p>Selection often favours different phenotypes in males and females, driving the evolu- tion of sex-specific genetic architectures that facilitate sexual dimorphism. Previous theory based on single-locus models has shown how such architecture can evolve through modifiers of gene expres- sion and allelic dominance in males and females. Here I consider the evolution of gene expression in polygenic traits experiencing sex-specific selection. In such traits, I find that sexual dimorphism evolves more readily through sex-specific gene amplification, whereby genes differ in their absolute expression levels between the sexes, than through the evolution of sex-specific dominance across loci, which requires strong sexual antagonism. Furthermore, I show that the type of genetic architecture that evolves through sex-specific amplification, namely the number and nature of sex-biased genes, is highly sensitive to the distance between optimal male and female trait values relative to the number of loci contributing to a trait, i.e, to the level of genetic redundancy for sexual dimor- phism. Together these results indicate that genetic architectures resulting from sex-specific selection are highly dependent on the genetic basis of the trait of interest, and that this creates challenges when interpreting current metrics of sexual antagonism.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":""},"PeriodicalIF":2.1,"publicationDate":"2025-05-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144175144","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Hector Pacheco-Fuentes, Riccardo Ton, Ondi L Crino, Federico Ferraccioli, Christine E Cooper, Daniel M Hooper, Simon C Griffith
{"title":"Experimental demonstration of functional divergence in mitochondrial metabolism between two finch subspecies subjected to a thermal challenge.","authors":"Hector Pacheco-Fuentes, Riccardo Ton, Ondi L Crino, Federico Ferraccioli, Christine E Cooper, Daniel M Hooper, Simon C Griffith","doi":"10.1093/jeb/voaf070","DOIUrl":"https://doi.org/10.1093/jeb/voaf070","url":null,"abstract":"<p><p>Whilst there is a growing appreciation that mitochondrial divergence across lineages is not selectively neutral, less work has examined the functional differences that may exist in closely divergent taxa. We measured mitochondrial oxygen consumption in the blood of two subspecies of an Australian songbird-the long-tailed finch, Poephila acuticauda-before and after ten days of heat treatment at 40°C to explore mitochondrial metabolic plasticity in response to thermal stress. There were significant differences between subspecies in the efficiency of oxidative phosphorylation, with P. a. hecki having higher energy production efficiency than P. a. acuticauda independent of heat treatment. Mitochondrial metabolism increased significantly after the treatment in four out of six variables in both subspecies, with P. a. hecki showing higher oxygen consumption rates in acclimating to 40°C. In the same experiment, we also measured circulating levels of corticosterone to assess the effect of the treatment on stress and to explore a possible mechanistic link with mitochondrial metabolism. The heat significantly increased baseline corticosterone, but at an individual level, corticosterone and mitochondrial metabolism were unrelated, indicating that functional plasticity in response to the thermal challenge was not mechanistically determined by corticosterone. Whilst the geographic ranges of the two subspecies differ in climate, the extent to which the functional divergence in mitochondrial efficiency reflects selectively neutral or adaptive divergence requires further research. Nonetheless, the reduced metabolic flexibility of P. a. acuticauda after heat suggests that future increases in the frequency and intensity of heatwaves may impose asymmetric effects on the two subspecies.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":""},"PeriodicalIF":2.1,"publicationDate":"2025-05-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144175706","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Trends in loss and retention of vision-related genes are similar between two trechine beetles independently colonizing caves.","authors":"Takuma Niida, Hisashi Ashida, Shigeyuki Koshikawa","doi":"10.1093/jeb/voaf071","DOIUrl":"https://doi.org/10.1093/jeb/voaf071","url":null,"abstract":"<p><p>Whether evolution is predictable has been tested in evolutionary biology by comparing lineages that experienced parallel evolution. For example, the repeatability of gene expression between strains was examined in the experimental evolution of bacteria. However, whether it is possible to predict the evolutionary fate of a gene (i.e., loss or retention) after an organism colonizes a new habitat and experiences a long period is not sufficiently clear. Here, we investigate a visual gene set in two species of eyeless trechine beetles (Coleoptera: Carabidae: Trechinae), which are thought to have colonized caves independently, and show that many of the lost genes and retained genes are common between them. We also estimate the pleiotropy which represents the extent to which these genes act in several tissues, using gene expression data in a model organism, and show that commonly lost genes have low pleiotropy. Our results suggest that the loss and retention of a visual gene set are relatively easy to predict in cave-dwelling trechine beetles. Furthermore, this study supports the possibility that even evolutionary fates of genes, which occur after a long period, are influenced by the functional constraints of these genes.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":""},"PeriodicalIF":2.1,"publicationDate":"2025-05-27","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144163648","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Embryonic life histories in annual killifish: adapted to what?","authors":"Tom J M Van Dooren","doi":"10.1093/jeb/voaf067","DOIUrl":"https://doi.org/10.1093/jeb/voaf067","url":null,"abstract":"<p><p>Adaptation requires an evolving strategy and an environment. Starting from environmental patterns, we predict which strategies are adapted. Given a strategy, we want to know in which environments it might be adapted. Annual killifish embryos can arrest development, survive desiccation of temporary ponds in the soil and hatch when they are rewetted. They might implement diversified bet-hedging. However, an association between magnitudes of environmental and developmental variability across populations or species has not yet been found. Their environments also have a strongly seasonal character and small-scale variation between pond centre and edge. Using data on embryonic life histories of Austrolebias annual killifish, parameter estimates and parsimonious assumptions, a population dynamical model is constructed with explicit developmental stages. For different simulated seasonal pond filling regimes with gradual filling and drying, it is used to estimate survival in the egg bank across a year and recruitment. Survival in the egg bank is small and variable, contrary to a standard assumption of most seed bank models. Calculations aiming to determine seasonal regimes where embryonic life histories could be adapted are presented. Invasion fitness gradients of rates of development and hatching probabilities are used to search for evolutionarily singular environments ESE, where none of the traits experience directional selection. Among the seasonal annual cycles investigated, no ESE occurred. Faster development rates were always favoured. For hatching probabilities, seasonal regimes were found which made their invasion fitness sensitivities zero. However, the observed trait values did not have long-term evolutionary stability in these regimes. It is argued that tests for adaptation to uncertain environments in annual fish should focus on associations between variability in pond filling and hatching probabilities.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":""},"PeriodicalIF":2.1,"publicationDate":"2025-05-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144135951","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Genital behavior in crane flies (Diptera: Tipuloidea): testing hypotheses for genital evolution.","authors":"William G Eberhard","doi":"10.1093/jeb/voaf069","DOIUrl":"https://doi.org/10.1093/jeb/voaf069","url":null,"abstract":"<p><p>The tendency for the genital morphology of animals to diverge more rapidly than other traits is one of the most pervasive evolutionary patterns in animal form. Current controversy regarding explanations of this pattern stems in part from the difficulty of observing the behavior of male genitalia during copulation. This limitation is reduced in tipuloid crane flies, because most of the male's elaborate, divergent genital structures remain outside the female during copulation. Observations of genital behavior during copulation in 45 species in 21 genera and subgenera, the most extensive sample of genital behavior in any comparable group of animals, show a combination of trends that fits better with the stimulation version of the cryptic female choice hypothesis than with any of the other hypotheses commonly cited to explain rapid divergent genital evolution: sustained, rhythmic male genital movements such as brushing and tapping; frequent female facilitation of stimulation; lack of consistent morphological coevolution between corresponding male and female structures; lack of forceful male manipulations of females; lack of female \"defenses\" that impede male stimulation; and lack of direct male interference with other males' sperm. Tipuloids are atypical among Diptera in generally lacking rhythmic, forceful genital thrusting and squeezing.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":""},"PeriodicalIF":2.1,"publicationDate":"2025-05-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144133263","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Antton Alberdi, Morten T Limborg, Mathieu Groussin, Ostaizka Aizpurua, M Thomas P Gilbert
{"title":"Metagenomic spaces: a framework to study the effect of microbiome variation on animal ecology and evolution.","authors":"Antton Alberdi, Morten T Limborg, Mathieu Groussin, Ostaizka Aizpurua, M Thomas P Gilbert","doi":"10.1093/jeb/voaf063","DOIUrl":"https://doi.org/10.1093/jeb/voaf063","url":null,"abstract":"<p><p>Microorganisms are essential for the normal functioning of most vertebrates. Hence, identifying and measuring the factors that shape host-associated microbial communities is necessary to understand ecological and evolutionary implications of host-microbiota associations. We propose a framework, built on the so-called 'metagenomic space' concept, which incorporates multiple definitions and quantifiable features relating to the variation of microbial communities that are associated with vertebrate hosts. By drawing on diverse theories and concepts developed in different fields of biology, our framework sets a conceptual landscape that transcends the mere characterisation of microbial communities. This provides the basis to study more complex attributes, such as 'potential' and 'fundamental metagenomic spaces', 'metagenomic plasticity' and 'metagenomic evolvability', which we argue are essential for understanding the microbial contribution to vertebrate host ecology and evolution-and hold considerable promise for advancing applied research and innovation. In doing so, we hope to contribute to an improved understanding of the impact of spatio-temporal variation of vertebrate host-microbiota associations, and inspire new approaches to address testable hypotheses related to ecological, evolutionary and applied processes.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":""},"PeriodicalIF":2.1,"publicationDate":"2025-05-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144129272","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Why does the target-recognition site in PRDM9 have unusually high mutation rates?","authors":"Frédéric Fyon, Francisco Úbeda","doi":"10.1093/jeb/voaf056","DOIUrl":"https://doi.org/10.1093/jeb/voaf056","url":null,"abstract":"<p><p>Gene PRDM9, responsible for the location of recombination hotspots in mammals (including humans), exhibits one of the highest mutation rate in the human genome. This high mutation rate has a direct impact on the life expectancy of recombination hotspots and the variability of the recombination landscape in mammals. Why would PRDM9 evolve such a high mutation rate? Why is PRDM9 one of the fastest evolving genes in the human genome? While the evolution of PRDM9-guided recombination hotspots has received much attention, the evolution of mutation rates at PRDM9 has received little attention. Here we explore the evolution of mutation rates at PRDM9. We formulate and analyse population genetics models for modifiers of mutation rates at PRDM9 and modifiers of mutation rates at PRDM9's target sites. By letting mutation rates evolve we find that natural selection favours the evolution of high mutation rates at PRDM9 and low mutation rates at PRDM9's target sites. However, considerations about linkage disequilibrium and genetic drift suggest that only high mutation rates at PRDM9 are likely to evolve. Our predictions match observations, with mutation rates at PRDM9 being two orders of magnitude higher than the average for the genome. Our modifiers of mutations at PRDM9 are most likely to evolve in close linkage with the PRDM9 locus. This is consistent with the binding domain in PRDM9 adopting a zinc-finger structure -molecular structure with high intrinsic mutation rates. Interestingly, our results are an exception of the reduction principle in modifier theory. We draw parallels between our results and another exception to the reduction principle: when genes are evolving in fluctuating environments. We suggest that the red-queen dynamics that characterise the co-evolution between PRDM9 and its target can generate a fluctuating genomic environment that drives the evolution of our modifier of mutation rates at PRDM9.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":""},"PeriodicalIF":2.1,"publicationDate":"2025-05-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144129371","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Reduced signatures of gene organization and duplication in shaping stage-specific patterns of expression across the C. elegans life cycle.","authors":"James G DuBose, Levi T Morran","doi":"10.1093/jeb/voaf061","DOIUrl":"https://doi.org/10.1093/jeb/voaf061","url":null,"abstract":"<p><p>Complex eukaryotes generally express different traits as they grow and develop to facilitate their function in different ecological niches. Theory suggests the evolution of differentiation between life stages is facilitated by the expression of different genes at different points throughout ontogeny, which alleviates evolutionary constraints. Therefore, ascertaining what contributes to specialized patterns of gene expression across ontogeny is fundamental to understanding the evolution of ontogenetic complexity. Expression divergence between duplicate genes and gene organization have been identified as important features of relatively complex ontogenies. Therefore, one could predict that their link to transcriptional specialization may be weaker across relatively simpler ontogenies. Here, we investigated the links between gene duplication, gene organization, and stage-specific patterns of expression across the relatively simple Caenorhabditis elegans life cycle. We found that signatures of stage-biased chromosomal regions were weaker in C. elegans than what has been previously described in organisms with more complex ontogenies. Furthermore, we found the extent that duplicate genes varied in ontogenetic expression pattern was more constrained in C. elegans. Overall, these findings help generalize our understanding of the association between gene duplication, gene organization, and the evolution of complex ontogenies.</p>","PeriodicalId":50198,"journal":{"name":"Journal of Evolutionary Biology","volume":" ","pages":""},"PeriodicalIF":2.1,"publicationDate":"2025-05-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"144129351","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}