Marisa A Rodrigues, Chantal Dauphin-Villemant, Margot Paris, M. Kapun, Esra Durmaz Mitchell, Envel Kerdaffrec, T. Flatt
Little is known about the metabolic basis of life-history trade-offs but lipid stores seem to play a pivotal role. During reproduction, an energetically highly costly process, animals mobilize fat reserves. Conversely, reduced or curtailed reproduction promotes lipid storage in many animals. Systemic signals from the gonad seem to be involved: Caenorhabditis elegans lacking germline stem cells display endocrine changes, have increased fat stores and are long-lived. Similarly, germline-ablated Drosophila melanogaster exhibit major somatic physiological changes, but whether and how germline loss affects lipid metabolism remains largely unclear. Here we show that germline-ablated flies have profoundly altered energy metabolism at the transcriptional level and store excess fat as compared to fertile flies. Germline activity thus constrains or represses fat accumulation, and this effect is conserved between flies and worms. More broadly, our findings confirm that lipids represent a major energetic currency in which costs of reproduction are paid.
{"title":"Germline proliferation trades off with lipid metabolism in Drosophila","authors":"Marisa A Rodrigues, Chantal Dauphin-Villemant, Margot Paris, M. Kapun, Esra Durmaz Mitchell, Envel Kerdaffrec, T. Flatt","doi":"10.1093/evlett/qrad059","DOIUrl":"https://doi.org/10.1093/evlett/qrad059","url":null,"abstract":"Little is known about the metabolic basis of life-history trade-offs but lipid stores seem to play a pivotal role. During reproduction, an energetically highly costly process, animals mobilize fat reserves. Conversely, reduced or curtailed reproduction promotes lipid storage in many animals. Systemic signals from the gonad seem to be involved: Caenorhabditis elegans lacking germline stem cells display endocrine changes, have increased fat stores and are long-lived. Similarly, germline-ablated Drosophila melanogaster exhibit major somatic physiological changes, but whether and how germline loss affects lipid metabolism remains largely unclear. Here we show that germline-ablated flies have profoundly altered energy metabolism at the transcriptional level and store excess fat as compared to fertile flies. Germline activity thus constrains or represses fat accumulation, and this effect is conserved between flies and worms. More broadly, our findings confirm that lipids represent a major energetic currency in which costs of reproduction are paid.","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":"82 2","pages":""},"PeriodicalIF":5.0,"publicationDate":"2023-11-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"139253024","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Abstract While temperature has been shown to affect the survival and growth of bacteria and their phage parasites, it is unclear if trade-offs between phage resistance and other bacterial traits depend on the temperature. Here, we experimentally compared the evolution of phage resistance–virulence trade-offs and underlying molecular mechanisms in phytopathogenic Ralstonia solanacearum bacterium at 25 °C and 35 °C temperature environments. We found that while phages reduced R. solanacearum densities relatively more at 25 °C, no difference in the final level of phage resistance was observed between temperature treatments. Instead, small colony variants (SCVs) with increased growth rate and mutations in the quorum-sensing (QS) signaling receptor gene, phcS, evolved in both temperature treatments. Interestingly, SCVs were also phage-resistant and reached higher frequencies in the presence of phages. Evolving phage resistance was costly, resulting in reduced carrying capacity, biofilm formation, and virulence in planta, possibly due to loss of QS-mediated expression of key virulence genes. We also observed mucoid phage-resistant colonies that showed loss of virulence and reduced twitching motility likely due to parallel mutations in prepilin peptidase gene, pilD. Moreover, phage-resistant SCVs from 35 °C-phage treatment had parallel mutations in type II secretion system (T2SS) genes (gspE and gspF). Adsorption assays confirmed the role of pilD as a phage receptor, while no loss of adsorption was found with phcS or T2SS mutants, indicative of other downstream phage resistance mechanisms. Additional transcriptomic analysis revealed upregulation of CBASS and type I restriction-modification phage defense systems in response to phage exposure, which coincided with reduced expression of motility and virulence-associated genes, including pilD and type II and III secretion systems. Together, these results suggest that while phage resistance–virulence trade-offs are not affected by the growth temperature, they could be mediated through both pre- and postinfection phage resistance mechanisms.
{"title":"Phage selection drives resistance–virulence trade-offs in <i>Ralstonia solanacearum</i> plant-pathogenic bacterium irrespective of the growth temperature","authors":"Jianing Wang, Xiaofang Wang, Keming Yang, Chunxia Lu, Bryden Fields, Yangchun Xu, Qirong Shen, Zhong Wei, Ville-Petri Friman","doi":"10.1093/evlett/qrad056","DOIUrl":"https://doi.org/10.1093/evlett/qrad056","url":null,"abstract":"Abstract While temperature has been shown to affect the survival and growth of bacteria and their phage parasites, it is unclear if trade-offs between phage resistance and other bacterial traits depend on the temperature. Here, we experimentally compared the evolution of phage resistance–virulence trade-offs and underlying molecular mechanisms in phytopathogenic Ralstonia solanacearum bacterium at 25 °C and 35 °C temperature environments. We found that while phages reduced R. solanacearum densities relatively more at 25 °C, no difference in the final level of phage resistance was observed between temperature treatments. Instead, small colony variants (SCVs) with increased growth rate and mutations in the quorum-sensing (QS) signaling receptor gene, phcS, evolved in both temperature treatments. Interestingly, SCVs were also phage-resistant and reached higher frequencies in the presence of phages. Evolving phage resistance was costly, resulting in reduced carrying capacity, biofilm formation, and virulence in planta, possibly due to loss of QS-mediated expression of key virulence genes. We also observed mucoid phage-resistant colonies that showed loss of virulence and reduced twitching motility likely due to parallel mutations in prepilin peptidase gene, pilD. Moreover, phage-resistant SCVs from 35 °C-phage treatment had parallel mutations in type II secretion system (T2SS) genes (gspE and gspF). Adsorption assays confirmed the role of pilD as a phage receptor, while no loss of adsorption was found with phcS or T2SS mutants, indicative of other downstream phage resistance mechanisms. Additional transcriptomic analysis revealed upregulation of CBASS and type I restriction-modification phage defense systems in response to phage exposure, which coincided with reduced expression of motility and virulence-associated genes, including pilD and type II and III secretion systems. Together, these results suggest that while phage resistance–virulence trade-offs are not affected by the growth temperature, they could be mediated through both pre- and postinfection phage resistance mechanisms.","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":"5 3","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-11-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"135086972","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Vincent J Fasanello, Ping Liu, Justin C Fay, Carlos A Botero
Abstract Evolutionary compromises are thought to be common under fluctuating selection because the mutations that best enable adaptation to one environmental context can often be detrimental to others. Yet, prior experimental work has shown that generalists can sometimes perform as well as specialists in their own environments. Here we use a highly replicated evolutionary experiment (N = 448 asexual lineages of the brewer’s yeast) to show that even though fluctuation between two environmental conditions often induces evolutionary compromises (at least early on), it can also help reveal difficult to reach adaptive outcomes that ultimately improve performance in both environments. Specifically, we begin by showing that yeast adaptation to chemical stress can involve fitness trade-offs with stress-free environments and that, accordingly, lineages that are repeatedly exposed to occasional stress tend to respond by trading performance for breadth of adaptation. We then show that on rare occasions, fluctuating selection leads to the evolution of no-cost generalists that can even outcompete constant selection specialists in their own environments. We propose that the discovery of these broader and more effective adaptive outcomes under fluctuating selection could be partially facilitated by changes in the adaptive landscape that result from having to deal with fitness trade-offs across different environmental conditions. Overall, our findings indicate that reconciling the short- and long-term evolutionary consequences of fluctuating selection could significantly improve our understanding of the evolution of specialization and generalism.
{"title":"Fluctuating selection facilitates the discovery of broadly effective but difficult to reach adaptive outcomes in yeast","authors":"Vincent J Fasanello, Ping Liu, Justin C Fay, Carlos A Botero","doi":"10.1093/evlett/qrad055","DOIUrl":"https://doi.org/10.1093/evlett/qrad055","url":null,"abstract":"Abstract Evolutionary compromises are thought to be common under fluctuating selection because the mutations that best enable adaptation to one environmental context can often be detrimental to others. Yet, prior experimental work has shown that generalists can sometimes perform as well as specialists in their own environments. Here we use a highly replicated evolutionary experiment (N = 448 asexual lineages of the brewer’s yeast) to show that even though fluctuation between two environmental conditions often induces evolutionary compromises (at least early on), it can also help reveal difficult to reach adaptive outcomes that ultimately improve performance in both environments. Specifically, we begin by showing that yeast adaptation to chemical stress can involve fitness trade-offs with stress-free environments and that, accordingly, lineages that are repeatedly exposed to occasional stress tend to respond by trading performance for breadth of adaptation. We then show that on rare occasions, fluctuating selection leads to the evolution of no-cost generalists that can even outcompete constant selection specialists in their own environments. We propose that the discovery of these broader and more effective adaptive outcomes under fluctuating selection could be partially facilitated by changes in the adaptive landscape that result from having to deal with fitness trade-offs across different environmental conditions. Overall, our findings indicate that reconciling the short- and long-term evolutionary consequences of fluctuating selection could significantly improve our understanding of the evolution of specialization and generalism.","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":" 511","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-11-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"135186628","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Jesús Martínez-Gómez, Michael J Song, Carrie M Tribble, Bjørn T Kopperud, William A Freyman, Sebastian Höhna, Chelsea D Specht, Carl J Rothfels
Abstract Identifying along which lineages shifts in diversification rates occur is a central goal of comparative phylogenetics; these shifts may coincide with key evolutionary events such as the development of novel morphological characters, the acquisition of adaptive traits, polyploidization or other structural genomic changes, or dispersal to a new habitat and subsequent increase in environmental niche space. However, while multiple methods now exist to estimate diversification rates and identify shifts using phylogenetic topologies, the appropriate use and accuracy of these methods are hotly debated. Here we test whether five Bayesian methods—Bayesian Analysis of Macroevolutionary Mixtures (BAMM), two implementations of the Lineage-Specific Birth–Death–Shift model (LSBDS and PESTO), the approximate Multi-Type Birth–Death model (MTBD; implemented in BEAST2), and the Cladogenetic Diversification Rate Shift model (ClaDS2)—produce comparable results. We apply each of these methods to a set of 65 empirical time-calibrated phylogenies and compare inferences of speciation rate, extinction rate, and net diversification rate. We find that the five methods often infer different speciation, extinction, and net-diversification rates. Consequently, these different estimates may lead to different interpretations of the macroevolutionary dynamics. The different estimates can be attributed to fundamental differences among the compared models. Therefore, the inference of shifts in diversification rates is strongly method dependent. We advise biologists to apply multiple methods to test the robustness of the conclusions or to carefully select the method based on the validity of the underlying model assumptions to their particular empirical system.
{"title":"Commonly used Bayesian diversification methods lead to biologically meaningful differences in branch-specific rates on empirical phylogenies","authors":"Jesús Martínez-Gómez, Michael J Song, Carrie M Tribble, Bjørn T Kopperud, William A Freyman, Sebastian Höhna, Chelsea D Specht, Carl J Rothfels","doi":"10.1093/evlett/qrad044","DOIUrl":"https://doi.org/10.1093/evlett/qrad044","url":null,"abstract":"Abstract Identifying along which lineages shifts in diversification rates occur is a central goal of comparative phylogenetics; these shifts may coincide with key evolutionary events such as the development of novel morphological characters, the acquisition of adaptive traits, polyploidization or other structural genomic changes, or dispersal to a new habitat and subsequent increase in environmental niche space. However, while multiple methods now exist to estimate diversification rates and identify shifts using phylogenetic topologies, the appropriate use and accuracy of these methods are hotly debated. Here we test whether five Bayesian methods—Bayesian Analysis of Macroevolutionary Mixtures (BAMM), two implementations of the Lineage-Specific Birth–Death–Shift model (LSBDS and PESTO), the approximate Multi-Type Birth–Death model (MTBD; implemented in BEAST2), and the Cladogenetic Diversification Rate Shift model (ClaDS2)—produce comparable results. We apply each of these methods to a set of 65 empirical time-calibrated phylogenies and compare inferences of speciation rate, extinction rate, and net diversification rate. We find that the five methods often infer different speciation, extinction, and net-diversification rates. Consequently, these different estimates may lead to different interpretations of the macroevolutionary dynamics. The different estimates can be attributed to fundamental differences among the compared models. Therefore, the inference of shifts in diversification rates is strongly method dependent. We advise biologists to apply multiple methods to test the robustness of the conclusions or to carefully select the method based on the validity of the underlying model assumptions to their particular empirical system.","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":"65 1","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-10-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"135976419","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Martin A Stoffel, Susan E Johnston, Jill G Pilkington, Josephine M Pemberton
Abstract Embryonic lethal mutations are arguably the earliest and most severe manifestation of inbreeding depression, but their impact on wild populations is not well understood. Here, we combined genomic, fitness, and life-history data from 5,925 wild Soay sheep sampled over nearly three decades to explore the impact of embryonic lethal mutations and their evolutionary dynamics. We searched for haplotypes that in their homozygous state are unusually rare in the offspring of known carrier parents and found three putatively semi-lethal haplotypes with 27%–46% fewer homozygous offspring than expected. Two of these haplotypes are decreasing in frequency, and gene-dropping simulations through the pedigree suggest that this is partially due to purifying selection. In contrast, the frequency of the third semi-lethal haplotype remains relatively stable over time. We show that the haplotype could be maintained by balancing selection because it is also associated with increased postnatal survival and body weight and because its cumulative frequency change is lower than in most drift-only simulations. Our study highlights embryonic mutations as a largely neglected contributor to inbreeding depression and provides a rare example of how harmful genetic variation can be maintained through balancing selection in a wild mammal population.
{"title":"Purifying and balancing selection on embryonic semi-lethal haplotypes in a wild mammal","authors":"Martin A Stoffel, Susan E Johnston, Jill G Pilkington, Josephine M Pemberton","doi":"10.1093/evlett/qrad053","DOIUrl":"https://doi.org/10.1093/evlett/qrad053","url":null,"abstract":"Abstract Embryonic lethal mutations are arguably the earliest and most severe manifestation of inbreeding depression, but their impact on wild populations is not well understood. Here, we combined genomic, fitness, and life-history data from 5,925 wild Soay sheep sampled over nearly three decades to explore the impact of embryonic lethal mutations and their evolutionary dynamics. We searched for haplotypes that in their homozygous state are unusually rare in the offspring of known carrier parents and found three putatively semi-lethal haplotypes with 27%–46% fewer homozygous offspring than expected. Two of these haplotypes are decreasing in frequency, and gene-dropping simulations through the pedigree suggest that this is partially due to purifying selection. In contrast, the frequency of the third semi-lethal haplotype remains relatively stable over time. We show that the haplotype could be maintained by balancing selection because it is also associated with increased postnatal survival and body weight and because its cumulative frequency change is lower than in most drift-only simulations. Our study highlights embryonic mutations as a largely neglected contributor to inbreeding depression and provides a rare example of how harmful genetic variation can be maintained through balancing selection in a wild mammal population.","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":"11 8","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"135367042","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Erik I Svensson, Mads F Schou, Julian Melgar, John Waller, Anel Engelbrecht, Zanell Brand, Schalk Cloete, Charlie K Cornwallis
Abstract Organisms inhabiting extreme thermal environments, such as desert birds, have evolved spectacular adaptations to thermoregulate during hot and cold conditions. However, our knowledge of selection for thermoregulation and the potential for evolutionary responses is limited, particularly for large organisms experiencing extreme temperature fluctuations. Here we use thermal imaging to quantify selection and genetic variation in thermoregulation in ostriches (Struthio camelus), the world’s largest bird species that is experiencing increasingly volatile temperatures. We found that females who are better at regulating their head temperatures (“thermoregulatory capacity”) had higher egg-laying rates under hotter conditions. Thermoregulatory capacity was both heritable and showed signatures of local adaptation: females originating from more unpredictable climates were better at regulating their head temperatures in response to temperature fluctuations. Together these results reveal that past and present evolutionary processes have shaped genetic variation in thermoregulatory capacity, which appears to protect critical organs, such as the brain, from extreme temperatures during reproduction.
{"title":"Heritable variation in thermal profiles is associated with reproductive success in the world’s largest bird","authors":"Erik I Svensson, Mads F Schou, Julian Melgar, John Waller, Anel Engelbrecht, Zanell Brand, Schalk Cloete, Charlie K Cornwallis","doi":"10.1093/evlett/qrad049","DOIUrl":"https://doi.org/10.1093/evlett/qrad049","url":null,"abstract":"Abstract Organisms inhabiting extreme thermal environments, such as desert birds, have evolved spectacular adaptations to thermoregulate during hot and cold conditions. However, our knowledge of selection for thermoregulation and the potential for evolutionary responses is limited, particularly for large organisms experiencing extreme temperature fluctuations. Here we use thermal imaging to quantify selection and genetic variation in thermoregulation in ostriches (Struthio camelus), the world’s largest bird species that is experiencing increasingly volatile temperatures. We found that females who are better at regulating their head temperatures (“thermoregulatory capacity”) had higher egg-laying rates under hotter conditions. Thermoregulatory capacity was both heritable and showed signatures of local adaptation: females originating from more unpredictable climates were better at regulating their head temperatures in response to temperature fluctuations. Together these results reveal that past and present evolutionary processes have shaped genetic variation in thermoregulatory capacity, which appears to protect critical organs, such as the brain, from extreme temperatures during reproduction.","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":"157 1","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-10-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"135567957","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Abstract The genetic covariance between traits can affect the evolution of a population through selection, drift, and migration. Conversely, research has demonstrated the reciprocal effect of evolutionary processes on changing genetic covariances, in part through mutational covariance, correlational selection, and plasticity. In this article, we propose that correlated changes in selective optima over generations can cause the evolution of genetic covariance and the G-matrix in such a way that the population can, in the future, evolve faster. We use individual-based simulations of populations exposed to three types of changing environments that differ in the correlation of the change between selective pressures. Our simulation experiments demonstrate that selection pressures for different traits changing in a correlated pattern over generations can lead to stronger trait correlations compared to the case with independently changing selective optima. Our findings show that correlated selective pressures result in significantly higher genetic trait covariance and that pleiotropy accounts for the majority of the difference in covariance between treatments. We also observe that the mutational variance evolves according to the environment that the populations were exposed to. Moreover, we show that clustered patterns of changes in selection can allow the evolution of genetic modularity. We show that the pattern of change in the selective environment affects the pace at which fitness evolves, with populations experiencing correlated change in optima having on average higher mean fitness than those experiencing uncorrelated environment change.
{"title":"The evolution of genetic covariance and modularity as a result of multigenerational environmental fluctuation","authors":"Isabela do O, Michael C Whitlock","doi":"10.1093/evlett/qrad048","DOIUrl":"https://doi.org/10.1093/evlett/qrad048","url":null,"abstract":"Abstract The genetic covariance between traits can affect the evolution of a population through selection, drift, and migration. Conversely, research has demonstrated the reciprocal effect of evolutionary processes on changing genetic covariances, in part through mutational covariance, correlational selection, and plasticity. In this article, we propose that correlated changes in selective optima over generations can cause the evolution of genetic covariance and the G-matrix in such a way that the population can, in the future, evolve faster. We use individual-based simulations of populations exposed to three types of changing environments that differ in the correlation of the change between selective pressures. Our simulation experiments demonstrate that selection pressures for different traits changing in a correlated pattern over generations can lead to stronger trait correlations compared to the case with independently changing selective optima. Our findings show that correlated selective pressures result in significantly higher genetic trait covariance and that pleiotropy accounts for the majority of the difference in covariance between treatments. We also observe that the mutational variance evolves according to the environment that the populations were exposed to. Moreover, we show that clustered patterns of changes in selection can allow the evolution of genetic modularity. We show that the pattern of change in the selective environment affects the pace at which fitness evolves, with populations experiencing correlated change in optima having on average higher mean fitness than those experiencing uncorrelated environment change.","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":"13 1","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-10-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"135993805","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Hwei-yen Chen, Therese Krieg, Brian Mautz, Cécile Jolly, Douglas Scofield, Alexei A Maklakov, Simone Immler
Abstract The effect of parental age on germline mutation rate across generations is not fully understood. While some studies report a positive linear relationship of mutation rate with increasing age, others suggest that mutation rate varies with age but not in a linear fashion. We investigated the effect of parental age on germline mutations by generating replicated mutation accumulation lines in Caenorhabditis remanei at three parental ages (“Young T1” [Day 1], “Peak T2” [Day 2], and “Old T5” [Day 5] parents). We conducted whole-genome resequencing and variant calling to compare differences in mutation rates after three generations of mutation accumulation. We found that Peak T2 lines had an overall reduced mutation rate compared to Young T1 and Old T5 lines, but this pattern of the effect varied depending on the variant impact. Specifically, we found no high-impact variants in Peak T2 lines, and modifiers and up- and downstream gene variants were less frequent in these lines. These results suggest that animals at the peak of reproduction have better DNA maintenance and repair compared to young and old animals. We propose that C. remanei start to reproduce before they optimize their DNA maintenance and repair, trading the benefits of earlier onset of reproduction against offspring mutation load. The increase in offspring mutation load with age likely represents germline senescence.
{"title":"Germline mutation rate is elevated in young and old parents in <i>Caenorhabditis remanei</i>","authors":"Hwei-yen Chen, Therese Krieg, Brian Mautz, Cécile Jolly, Douglas Scofield, Alexei A Maklakov, Simone Immler","doi":"10.1093/evlett/qrad052","DOIUrl":"https://doi.org/10.1093/evlett/qrad052","url":null,"abstract":"Abstract The effect of parental age on germline mutation rate across generations is not fully understood. While some studies report a positive linear relationship of mutation rate with increasing age, others suggest that mutation rate varies with age but not in a linear fashion. We investigated the effect of parental age on germline mutations by generating replicated mutation accumulation lines in Caenorhabditis remanei at three parental ages (“Young T1” [Day 1], “Peak T2” [Day 2], and “Old T5” [Day 5] parents). We conducted whole-genome resequencing and variant calling to compare differences in mutation rates after three generations of mutation accumulation. We found that Peak T2 lines had an overall reduced mutation rate compared to Young T1 and Old T5 lines, but this pattern of the effect varied depending on the variant impact. Specifically, we found no high-impact variants in Peak T2 lines, and modifiers and up- and downstream gene variants were less frequent in these lines. These results suggest that animals at the peak of reproduction have better DNA maintenance and repair compared to young and old animals. We propose that C. remanei start to reproduce before they optimize their DNA maintenance and repair, trading the benefits of earlier onset of reproduction against offspring mutation load. The increase in offspring mutation load with age likely represents germline senescence.","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":"138 1","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-10-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"135994809","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Samuel V Hulse, Janis Antonovics, Michael E Hood, Emily L Bruns
Abstract Genetic variation for disease resistance within host populations can strongly impact the spread of endemic pathogens. In plants, recent work has shown that within-population variation in resistance can also affect the transmission of foreign spillover pathogens if that resistance is general. However, most hosts also possess specific resistance mechanisms that provide strong defenses against coevolved endemic pathogens. Here we use a modeling approach to ask how antagonistic coevolution between hosts and their endemic pathogen at the specific resistance locus can affect the frequency of general resistance, and therefore a host’s vulnerability to foreign pathogens. We develop a two-locus model with variable recombination that incorporates both general resistance (effective against all pathogens) and specific resistance (effective against endemic pathogens only). With coevolution, when pathogens can evolve to evade specific resistance, we find that the regions where general resistance can evolve are greatly expanded, decreasing the risk of foreign pathogen invasion. Furthermore, coevolution greatly expands the conditions that maintain polymorphisms at both resistance loci, thereby driving greater genetic diversity within host populations. This genetic diversity often leads to positive correlations between host resistance to foreign and endemic pathogens, similar to those observed in natural populations. However, if resistance loci become linked, the resistance correlations can shift to negative. If we include a third linkage-modifying locus in our model, we find that selection often favors complete linkage. Our model demonstrates how coevolutionary dynamics with an endemic pathogen can mold the resistance structure of host populations in ways that affect its susceptibility to foreign pathogen spillovers, and that the nature of these outcomes depends on resistance costs, as well as the degree of linkage between resistance genes.
{"title":"Host–pathogen coevolution promotes the evolution of general, broad-spectrum resistance and reduces foreign pathogen spillover risk","authors":"Samuel V Hulse, Janis Antonovics, Michael E Hood, Emily L Bruns","doi":"10.1093/evlett/qrad051","DOIUrl":"https://doi.org/10.1093/evlett/qrad051","url":null,"abstract":"Abstract Genetic variation for disease resistance within host populations can strongly impact the spread of endemic pathogens. In plants, recent work has shown that within-population variation in resistance can also affect the transmission of foreign spillover pathogens if that resistance is general. However, most hosts also possess specific resistance mechanisms that provide strong defenses against coevolved endemic pathogens. Here we use a modeling approach to ask how antagonistic coevolution between hosts and their endemic pathogen at the specific resistance locus can affect the frequency of general resistance, and therefore a host’s vulnerability to foreign pathogens. We develop a two-locus model with variable recombination that incorporates both general resistance (effective against all pathogens) and specific resistance (effective against endemic pathogens only). With coevolution, when pathogens can evolve to evade specific resistance, we find that the regions where general resistance can evolve are greatly expanded, decreasing the risk of foreign pathogen invasion. Furthermore, coevolution greatly expands the conditions that maintain polymorphisms at both resistance loci, thereby driving greater genetic diversity within host populations. This genetic diversity often leads to positive correlations between host resistance to foreign and endemic pathogens, similar to those observed in natural populations. However, if resistance loci become linked, the resistance correlations can shift to negative. If we include a third linkage-modifying locus in our model, we find that selection often favors complete linkage. Our model demonstrates how coevolutionary dynamics with an endemic pathogen can mold the resistance structure of host populations in ways that affect its susceptibility to foreign pathogen spillovers, and that the nature of these outcomes depends on resistance costs, as well as the degree of linkage between resistance genes.","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":"34 1","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-10-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"136078794","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Abstract Rapid evolutionary adaptation could reduce the negative impacts of climate change if sufficient heritability of key traits exists under future climate conditions. Plastic responses to climate change could also reduce negative impacts. Understanding which populations are likely to respond via evolution or plasticity could therefore improve estimates of extinction risk. A large body of research suggests that the evolutionary and plastic potential of a population can be predicted by the degree of spatial and temporal climatic variation it experiences. However, we know little about the scale at which these relationships apply. Here, we test if spatial and temporal variation in temperature affects genetic variation and plasticity of fitness and a key thermal tolerance trait (critical thermal maximum; CTmax) at microgeographic scales using a metapopulation of Daphnia magna in freshwater rock pools. Specifically, we ask if (a) there is a microgeographic adaptation of CTmax and fitness to differences in temperature among the pools, (b) pools with greater temporal temperature variation have more genetic variation or plasticity in CTmax or fitness, and (c) increases in temperature affect the heritability of CTmax and fitness. Although we observed genetic variation and plasticity in CTmax and fitness, and differences in fitness among pools, we did not find support for the predicted relationships between temperature variation and genetic variation or plasticity. Furthermore, the genetic variation and plasticity we observed in CTmax are unlikely sufficient to reduce the impacts of climate change. CTmax plasticity was minimal and heritability was 72% lower when D. magna developed at the higher temperatures predicted under climate change. In contrast, the heritability of fitness increased by 53% under warmer temperatures, suggesting an increase in overall evolutionary potential unrelated to CTmax under climate change. More research is needed to understand the evolutionary and plastic potential under climate change and how that potential will be altered in future climates.
{"title":"Macroecological predictors of evolutionary and plastic potential do not apply at microgeographic scales for a freshwater cladoceran under climate change","authors":"Christopher P Nadeau, Mark C Urban","doi":"10.1093/evlett/qrad042","DOIUrl":"https://doi.org/10.1093/evlett/qrad042","url":null,"abstract":"Abstract Rapid evolutionary adaptation could reduce the negative impacts of climate change if sufficient heritability of key traits exists under future climate conditions. Plastic responses to climate change could also reduce negative impacts. Understanding which populations are likely to respond via evolution or plasticity could therefore improve estimates of extinction risk. A large body of research suggests that the evolutionary and plastic potential of a population can be predicted by the degree of spatial and temporal climatic variation it experiences. However, we know little about the scale at which these relationships apply. Here, we test if spatial and temporal variation in temperature affects genetic variation and plasticity of fitness and a key thermal tolerance trait (critical thermal maximum; CTmax) at microgeographic scales using a metapopulation of Daphnia magna in freshwater rock pools. Specifically, we ask if (a) there is a microgeographic adaptation of CTmax and fitness to differences in temperature among the pools, (b) pools with greater temporal temperature variation have more genetic variation or plasticity in CTmax or fitness, and (c) increases in temperature affect the heritability of CTmax and fitness. Although we observed genetic variation and plasticity in CTmax and fitness, and differences in fitness among pools, we did not find support for the predicted relationships between temperature variation and genetic variation or plasticity. Furthermore, the genetic variation and plasticity we observed in CTmax are unlikely sufficient to reduce the impacts of climate change. CTmax plasticity was minimal and heritability was 72% lower when D. magna developed at the higher temperatures predicted under climate change. In contrast, the heritability of fitness increased by 53% under warmer temperatures, suggesting an increase in overall evolutionary potential unrelated to CTmax under climate change. More research is needed to understand the evolutionary and plastic potential under climate change and how that potential will be altered in future climates.","PeriodicalId":48629,"journal":{"name":"Evolution Letters","volume":"174 1","pages":"0"},"PeriodicalIF":0.0,"publicationDate":"2023-10-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"136012905","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
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