Selina B. I. Schmidt, Tom Täschner, Niclas Nordholt, Frank Schreiber
Biocides are used to control microorganisms across different applications, but emerging resistance may pose risks for those applications. Resistance to biocides has commonly been studied using adaptive laboratory evolution (ALE) experiments with growth at subinhibitory concentrations linked to serial subculturing. It has been shown recently that Escherichia coli adapts to repeated lethal stress imposed by the biocide benzalkonium chloride (BAC) by increased survival (i.e., tolerance) and not by evolving the ability to grow at increased concentrations (i.e., resistance). Here, we investigate the contributions of evolution for tolerance as opposed to resistance for the outcome of ALE experiments with E. coli exposed to BAC. We find that BAC concentrations close to the half maximal effective concentration (EC50, 4.36 μg mL−1) show initial killing (~40%) before the population resumes growth. This indicates that cells face a two-fold selection pressure: for increased survival and for increased growth. To disentangle the effects of both selection pressures, we conducted two ALE experiments: (i) one with initial killing and continued stress close to the EC50 during growth and (ii) another with initial killing and no stress during growth. Phenotypic characterization of adapted populations showed that growth at higher BAC concentrations was only selected for when BAC was present during growth. Whole genome sequencing revealed distinct differences in mutated genes across treatments. Treatments selecting for survival-only led to mutations in genes for metabolic regulation (cyaA) and cellular structure (flagella fliJ), while treatments selecting for growth and survival led to mutations in genes related to stress response (hslO and tufA). Our results demonstrate that serial subculture ALE experiments with an antimicrobial at subinhibitory concentrations can select for increased growth and survival. This finding has implications for the design of ALE experiments to assess resistance risks of antimicrobials in different scenarios such as disinfection, preservation, and environmental pollution.
杀菌剂用于控制不同应用领域的微生物,但新出现的抗药性可能会给这些应用带来风险。对杀菌剂抗药性的研究通常采用适应性实验室进化(ALE)实验,在亚抑制浓度下生长,并进行连续的亚培养。最近的研究表明,大肠杆菌通过提高存活率(即耐受性)而不是进化出在更高浓度下生长的能力(即抗性)来适应杀菌剂苯扎氯铵(BAC)反复施加的致死压力。在此,我们研究了耐受性进化相对于抗性进化对暴露于 BAC 的大肠杆菌的 ALE 实验结果的贡献。我们发现,BAC 浓度接近半数最大有效浓度(EC50,4.36 μg mL-1)时,在种群恢复生长之前会出现初始杀灭(约 40%)。这表明细胞面临着双重选择压力:提高存活率和提高生长率。为了区分这两种选择压力的影响,我们进行了两次 ALE 实验:(i)一个是初始杀灭,在生长过程中持续施加接近 EC50 的压力;(ii)另一个是初始杀灭,在生长过程中不施加压力。适应种群的表型特征显示,只有在生长过程中出现 BAC 时,才会选择在较高 BAC 浓度下生长。全基因组测序显示,不同处理的突变基因存在明显差异。只选择存活的处理导致代谢调节(cyaA)和细胞结构(鞭毛 fliJ)基因突变,而选择生长和存活的处理导致与应激反应有关的基因突变(hslO 和 tufA)。我们的研究结果表明,用亚抑制浓度的抗菌剂进行连续亚培养 ALE 实验可以选择性地提高生长和存活率。这一发现对设计 ALE 实验以评估消毒、保存和环境污染等不同情况下抗菌素的耐药性风险具有重要意义。
{"title":"Differential Selection for Survival and for Growth in Adaptive Laboratory Evolution Experiments With Benzalkonium Chloride","authors":"Selina B. I. Schmidt, Tom Täschner, Niclas Nordholt, Frank Schreiber","doi":"10.1111/eva.70017","DOIUrl":"https://doi.org/10.1111/eva.70017","url":null,"abstract":"<p>Biocides are used to control microorganisms across different applications, but emerging resistance may pose risks for those applications. Resistance to biocides has commonly been studied using adaptive laboratory evolution (ALE) experiments with growth at subinhibitory concentrations linked to serial subculturing. It has been shown recently that <i>Escherichia coli</i> adapts to repeated lethal stress imposed by the biocide benzalkonium chloride (BAC) by increased survival (i.e., tolerance) and not by evolving the ability to grow at increased concentrations (i.e., resistance). Here, we investigate the contributions of evolution for tolerance as opposed to resistance for the outcome of ALE experiments with <i>E. coli</i> exposed to BAC. We find that BAC concentrations close to the half maximal effective concentration (EC<sub>50</sub>, 4.36 μg mL<sup>−1</sup>) show initial killing (~40%) before the population resumes growth. This indicates that cells face a two-fold selection pressure: for increased survival and for increased growth. To disentangle the effects of both selection pressures, we conducted two ALE experiments: (i) one with initial killing and continued stress close to the EC<sub>50</sub> during growth and (ii) another with initial killing and no stress during growth. Phenotypic characterization of adapted populations showed that growth at higher BAC concentrations was only selected for when BAC was present during growth. Whole genome sequencing revealed distinct differences in mutated genes across treatments. Treatments selecting for survival-only led to mutations in genes for metabolic regulation (<i>cyaA</i>) and cellular structure (flagella <i>fliJ</i>), while treatments selecting for growth and survival led to mutations in genes related to stress response (<i>hslO</i> and <i>tufA</i>). Our results demonstrate that serial subculture ALE experiments with an antimicrobial at subinhibitory concentrations can select for increased growth and survival. This finding has implications for the design of ALE experiments to assess resistance risks of antimicrobials in different scenarios such as disinfection, preservation, and environmental pollution.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 10","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-10-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70017","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142429986","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Alexandra Pavlova, Luke Pearce, Felicity Sturgiss, Erin Lake, Paul Sunnucks, Mark Lintermans
Genetic diversity is rapidly lost from small, isolated populations by genetic drift. Measuring the level of genetic drift using effective population size (Ne) is highly useful for management. Single-cohort genetic Ne estimators approximate the number of breeders in one season (Nb): a value < 100 signals likely inbreeding depression. Per-generation Ne < 1000 estimated from multiple cohort signals reduced adaptive potential. Natural populations rarely meet assumptions of Ne-estimation, so interpreting estimates is challenging. Macquarie perch is an endangered Australian freshwater fish threatened by severely reduced range, habitat loss, and fragmentation. To counteract low Ne, augmented gene flow is being implemented in several populations. In the Murrumbidgee River, unknown effects of water management on among-site connectivity impede the design of effective interventions. Using DArT SNPs for 328 Murrumbidgee individuals sampled across several sites and years with different flow conditions, we assessed population structure, site isolation, heterozygosity, inbreeding, and Ne. We tested for inbreeding depression, assessed genetic diversity and dispersal, and evaluated whether individuals translocated from Cataract Reservoir to the Murrumbidgee River bred, and interbred with local fish. We found strong genetic structure, indicating complete or partial isolation of river fragments. This structure violates assumptions of Ne estimation, resulting in strongly downwardly biased Nb estimates unless assessed per-site, highlighting the necessity to account for population structure while estimating Ne. Inbreeding depression was not detected, but with low Nb at each site, inbreeding and inbreeding depression are likely. These results flagged the necessity to address within-river population connectivity through flow management and genetic mixing through translocations among sites and from other populations. Three detected genetically diverse offspring of a translocated Cataract fish and a local parent indicated that genetic mixing is in progress. Including admixed individuals in estimates yielded lower Ne but higher heterozygosity, suggesting heterozygosity is a preferable indicator of genetic augmentation.
遗传多样性会因遗传漂变而迅速从孤立的小种群中消失。用有效种群大小(Ne)来衡量遗传漂变的程度对管理非常有用。单群遗传 Ne 估计值近似于一季中繁殖者的数量(Nb):数值大于等于 100 表示可能存在近交抑郁。根据多队列估计的每代 Ne 值为 1000,表明适应潜力降低。自然种群很少符合Ne估计的假设,因此解释估计值具有挑战性。麦格理鲈是一种濒临灭绝的澳大利亚淡水鱼,受到栖息地严重减少和破碎化的威胁。为了应对低Ne值问题,一些种群正在实施基因流增强措施。在墨伦比奇河(Murrumbidgee River),水管理对不同地点之间连通性的未知影响阻碍了有效干预措施的设计。利用在不同水流条件下的多个地点和年份采样的 328 个 Murrumbidgee 个体的 DArT SNPs,我们评估了种群结构、地点隔离、杂合度、近亲繁殖和 Ne。我们检测了近亲繁殖抑制,评估了遗传多样性和扩散,并评估了从卡塔拉克水库迁移到墨伦比奇河的个体是否繁殖,以及是否与当地鱼类杂交。我们发现了很强的遗传结构,表明河流片段完全或部分隔离。这种结构违反了Ne估计的假设,导致Nb估计值严重向下偏移,除非对每个地点进行评估,这突出了在估计Ne时考虑种群结构的必要性。虽然没有检测到近交抑郁,但由于每个地点的 Nb 值较低,近亲繁殖和近交抑郁很有可能发生。这些结果表明,有必要通过水流管理来解决河内种群的连通性问题,并通过在不同地点之间以及从其他种群进行易位来实现基因混合。三条检测到的基因不同的后代是由一条移植的白内障鱼和一条本地亲鱼组成的,这表明基因混合正在进行中。将混血个体纳入估计值会降低 Ne 值,但会提高杂合度,这表明杂合度是遗传增殖的首选指标。
{"title":"Immediate Genetic Augmentation and Enhanced Habitat Connectivity Are Required to Secure the Future of an Iconic Endangered Freshwater Fish Population","authors":"Alexandra Pavlova, Luke Pearce, Felicity Sturgiss, Erin Lake, Paul Sunnucks, Mark Lintermans","doi":"10.1111/eva.70019","DOIUrl":"https://doi.org/10.1111/eva.70019","url":null,"abstract":"<p>Genetic diversity is rapidly lost from small, isolated populations by genetic drift. Measuring the level of genetic drift using effective population size (<i>N</i><sub>e</sub>) is highly useful for management. Single-cohort genetic <i>N</i><sub>e</sub> estimators approximate the number of breeders in one season (<i>N</i><sub>b</sub>): a value < 100 signals likely inbreeding depression. Per-generation <i>N</i><sub>e</sub> < 1000 estimated from multiple cohort signals reduced adaptive potential. Natural populations rarely meet assumptions of <i>N</i><sub>e</sub>-estimation, so interpreting estimates is challenging. Macquarie perch is an endangered Australian freshwater fish threatened by severely reduced range, habitat loss, and fragmentation. To counteract low <i>N</i><sub>e</sub>, augmented gene flow is being implemented in several populations. In the Murrumbidgee River, unknown effects of water management on among-site connectivity impede the design of effective interventions. Using DArT SNPs for 328 Murrumbidgee individuals sampled across several sites and years with different flow conditions, we assessed population structure, site isolation, heterozygosity, inbreeding, and <i>N</i><sub>e</sub>. We tested for inbreeding depression, assessed genetic diversity and dispersal, and evaluated whether individuals translocated from Cataract Reservoir to the Murrumbidgee River bred, and interbred with local fish. We found strong genetic structure, indicating complete or partial isolation of river fragments. This structure violates assumptions of <i>N</i><sub>e</sub> estimation, resulting in strongly downwardly biased <i>N</i><sub>b</sub> estimates unless assessed per-site, highlighting the necessity to account for population structure while estimating <i>N</i><sub>e</sub>. Inbreeding depression was not detected, but with low <i>N</i><sub>b</sub> at each site, inbreeding and inbreeding depression are likely. These results flagged the necessity to address within-river population connectivity through flow management and genetic mixing through translocations among sites and from other populations. Three detected genetically diverse offspring of a translocated Cataract fish and a local parent indicated that genetic mixing is in progress. Including admixed individuals in estimates yielded lower <i>N</i><sub>e</sub> but higher heterozygosity, suggesting heterozygosity is a preferable indicator of genetic augmentation.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 10","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-10-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70019","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142429957","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Chrystelle Delord, Sophie Arnaud-Haond, Agostino Leone, Jonathan Rolland, Natacha Nikolic
Estimating and understanding the ratio between effective population size (Ne) and census population size (Nc) are pivotal in the conservation of large marine pelagic fish species, including bony fish such as tunas and cartilaginous fish such as sharks, given the challenges associated with obtaining accurate estimates of their abundance. The difficulties inherent in capturing and monitoring these species in vast and dynamic marine environments often make direct estimation of their population size challenging. By focusing on Ne, it is conceivable in certain cases to approximate census size once the Ne/Nc ratio is known, although this ratio can vary and does not always increase linearly, as it is influenced by various ecological and evolutionary factors. Thus, this ratio presents challenges and complexities in the context of pelagic species conservation. To delve deeper into these challenges, firstly, we recall the diverse types of effective population sizes, including contemporary and historical sizes, and their implications in conservation biology. Secondly, we outline current knowledge about the influence of life history traits on the Ne/Nc ratio in the light of examples drawn from large and abundant pelagic fish species. Despite efforts to document an increasing number of marine species using recent technologies and statistical methods, establishing general rules to predict Ne/Nc remains elusive, necessitating further research and investment. Finally, we recall statistical challenges in relating Ne and Nc emphasizing the necessity of aligning temporal and spatial scales. This last part discusses the roles of generation and reproductive cycle effective population sizes to predict genetic erosion and guiding management strategies. Collectively, these sections underscore the multifaceted nature of effective population size estimation, crucial for preserving genetic diversity and ensuring the long-term viability of populations. By navigating statistical and theoretical complexities, and addressing methodological challenges, scientists should be able to advance our understanding of the Ne/Nc ratio.
估算和了解有效种群数量(N e)和普查种群数量(N c)之间的比率,对于保护大型海洋中上层鱼类物种(包括金枪鱼等硬骨鱼类和鲨鱼等软骨鱼类)至关重要,因为要准确估算它们的丰度是一项挑战。在广阔而多变的海洋环境中捕捉和监测这些物种本身就存在困难,因此直接估算其种群数量往往具有挑战性。通过关注 N e,可以设想在某些情况下,一旦知道 N e/N c 的比率,就能大致估算出普查规模,尽管这一比率会受到各种生态和进化因素的影响而变化,而且并不总是呈线性增长。因此,这一比率给远洋物种保护带来了挑战和复杂性。为了深入探讨这些挑战,首先,我们回顾了有效种群规模的不同类型,包括当代和历史规模,以及它们在保护生物学中的意义。其次,我们根据大型丰富中上层鱼类的实例,概述了目前有关生活史特征对 N e/N c 比率影响的知识。尽管利用最新技术和统计方法记录了越来越多的海洋物种,但建立预测 N e/N c 的一般规则仍然遥遥无期,需要进一步的研究和投资。最后,我们回顾了将 N e 和 N c 联系起来所面临的统计挑战,强调了调整时间和空间尺度的必要性。最后一部分讨论了世代和繁殖周期有效种群数量在预测遗传侵蚀和指导管理策略方面的作用。总之,这些部分强调了有效种群数量估计的多面性,这对于保护遗传多样性和确保种群的长期生存能力至关重要。通过克服统计和理论上的复杂性以及应对方法上的挑战,科学家们应该能够推进我们对 N e/N c 比率的理解。
{"title":"Unraveling the Complexity of the Ne/Nc Ratio for Conservation of Large and Widespread Pelagic Fish Species: Current Status and Challenges","authors":"Chrystelle Delord, Sophie Arnaud-Haond, Agostino Leone, Jonathan Rolland, Natacha Nikolic","doi":"10.1111/eva.70020","DOIUrl":"10.1111/eva.70020","url":null,"abstract":"<p>Estimating and understanding the ratio between effective population size (<i>N</i><sub>e</sub>) and census population size (<i>N</i><sub>c</sub>) are pivotal in the conservation of large marine pelagic fish species, including bony fish such as tunas and cartilaginous fish such as sharks, given the challenges associated with obtaining accurate estimates of their abundance. The difficulties inherent in capturing and monitoring these species in vast and dynamic marine environments often make direct estimation of their population size challenging. By focusing on <i>N</i><sub>e</sub>, it is conceivable in certain cases to approximate census size once the <i>N</i><sub>e</sub>/<i>N</i><sub>c</sub> ratio is known, although this ratio can vary and does not always increase linearly, as it is influenced by various ecological and evolutionary factors. Thus, this ratio presents challenges and complexities in the context of pelagic species conservation. To delve deeper into these challenges, firstly, we recall the diverse types of effective population sizes, including contemporary and historical sizes, and their implications in conservation biology. Secondly, we outline current knowledge about the influence of life history traits on the <i>N</i><sub>e</sub>/<i>N</i><sub>c</sub> ratio in the light of examples drawn from large and abundant pelagic fish species. Despite efforts to document an increasing number of marine species using recent technologies and statistical methods, establishing general rules to predict <i>N</i><sub>e</sub>/<i>N</i><sub>c</sub> remains elusive, necessitating further research and investment. Finally, we recall statistical challenges in relating <i>N</i><sub>e</sub> and <i>N</i><sub>c</sub> emphasizing the necessity of aligning temporal and spatial scales. This last part discusses the roles of generation and reproductive cycle effective population sizes to predict genetic erosion and guiding management strategies. Collectively, these sections underscore the multifaceted nature of effective population size estimation, crucial for preserving genetic diversity and ensuring the long-term viability of populations. By navigating statistical and theoretical complexities, and addressing methodological challenges, scientists should be able to advance our understanding of the <i>N</i><sub>e</sub>/<i>N</i><sub>c</sub> ratio.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 10","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-10-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11464753/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142398841","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Garazi Martin Bideguren, Orly Razgour, Antton Alberdi
Microorganisms associated with animals harbour a unique set of functional traits pivotal for the normal functioning of their hosts. This realisation has led researchers to hypothesise that animal-associated microbial communities may boost the capacity of their hosts to acclimatise and adapt to environmental changes, two eco-evolutionary processes with significant applied relevance. Aiming to assess the importance of microorganisms for wild vertebrate conservation, we conducted a quantitative systematic review to evaluate the scientific evidence for the contribution of gut microorganisms to the acclimation and adaptation capacity of wild vertebrate hosts. After screening 1974 publications, we scrutinised the 109 studies that met the inclusion criteria based on 10 metrics encompassing study design, methodology and reproducibility. We found that the studies published so far were not able to resolve the contribution of gut microorganisms due to insufficient study design and research methods for addressing the hypothesis. Our findings underscore the limited application to date of microbiome knowledge in vertebrate conservation and management, highlighting the need for a paradigm shift in research approaches. Considering these results, we advocate for a shift from observational studies to experimental manipulations, where fitness or related indicators are measured, coupled with an update in molecular techniques used to analyse microbial functions. In addition, closer collaboration with conservation managers and practitioners from the inception of the project is needed to encourage meaningful application of microbiome knowledge in adaptive wildlife conservation management.
{"title":"Quantitative Synthesis of Microbe-Driven Acclimation and Adaptation in Wild Vertebrates","authors":"Garazi Martin Bideguren, Orly Razgour, Antton Alberdi","doi":"10.1111/eva.70025","DOIUrl":"10.1111/eva.70025","url":null,"abstract":"<p>Microorganisms associated with animals harbour a unique set of functional traits pivotal for the normal functioning of their hosts. This realisation has led researchers to hypothesise that animal-associated microbial communities may boost the capacity of their hosts to acclimatise and adapt to environmental changes, two eco-evolutionary processes with significant applied relevance. Aiming to assess the importance of microorganisms for wild vertebrate conservation, we conducted a quantitative systematic review to evaluate the scientific evidence for the contribution of gut microorganisms to the acclimation and adaptation capacity of wild vertebrate hosts. After screening 1974 publications, we scrutinised the 109 studies that met the inclusion criteria based on 10 metrics encompassing study design, methodology and reproducibility. We found that the studies published so far were not able to resolve the contribution of gut microorganisms due to insufficient study design and research methods for addressing the hypothesis. Our findings underscore the limited application to date of microbiome knowledge in vertebrate conservation and management, highlighting the need for a paradigm shift in research approaches. Considering these results, we advocate for a shift from observational studies to experimental manipulations, where fitness or related indicators are measured, coupled with an update in molecular techniques used to analyse microbial functions. In addition, closer collaboration with conservation managers and practitioners from the inception of the project is needed to encourage meaningful application of microbiome knowledge in adaptive wildlife conservation management.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 10","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-10-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11464772/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142398827","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Thaïs A. Bernos, Zdenek Lajbner, Petr Kotlík, Jacklyn M. Hill, Silvia Marková, Jonah Yick, Nicholas E. Mandrak, Ken M. Jeffries
Species invading non-native habitats can cause irreversible environmental damage and economic harm. Yet, how introduced species become widespread invaders remains poorly understood. Adaptation within native-range habitats and rapid adaptation to new environments may both influence invasion success. Here, we examine these hypotheses using 7058 SNPs from 36 native, 40 introduced and 19 farmed populations of tench, a fish native to Eurasia. We examined genetic structure among these populations and accounted for long-term evolutionary history within the native range to assess whether introduced populations exhibited lower genetic diversity than native populations. Subsequent to infer genotype–environment correlations within native-range habitats, we assessed whether adaptation to native environments may have shaped the success of some introduced populations. At the broad scale, two glacial refugia contributed to the ancestry and genomic diversity of tench. However, native, introduced and farmed populations of admixed origin exhibited up to 10-fold more genetic diversity (i.e., observed heterozygosity, expected heterozygosity and allelic richness) compared to populations with predominantly single-source ancestry. The effects of introduction to a new location were also apparent as introduced populations exhibited fewer private alleles (mean = 9.9 and 18.9 private alleles in introduced and native populations, respectively) and higher population-specific Fst compared to native populations, highlighting their distinctiveness relative to the pool of allelic frequencies across tench populations. Finally, introduced populations with varying levels of genetic variation and similar genetic compositions have become established and persisted under strikingly different climatic and ecological conditions. Our results suggest that lack of prior adaptation and low genetic variation may not consistently hinder the success of introduced populations for species with a demonstrated ability to expand their native range.
{"title":"Assessing the Impacts of Adaptation to Native-Range Habitats and Contemporary Founder Effects on Genetic Diversity in an Invasive Fish","authors":"Thaïs A. Bernos, Zdenek Lajbner, Petr Kotlík, Jacklyn M. Hill, Silvia Marková, Jonah Yick, Nicholas E. Mandrak, Ken M. Jeffries","doi":"10.1111/eva.70006","DOIUrl":"10.1111/eva.70006","url":null,"abstract":"<p>Species invading non-native habitats can cause irreversible environmental damage and economic harm. Yet, how introduced species become widespread invaders remains poorly understood. Adaptation within native-range habitats and rapid adaptation to new environments may both influence invasion success. Here, we examine these hypotheses using 7058 SNPs from 36 native, 40 introduced and 19 farmed populations of tench, a fish native to Eurasia. We examined genetic structure among these populations and accounted for long-term evolutionary history within the native range to assess whether introduced populations exhibited lower genetic diversity than native populations. Subsequent to infer genotype–environment correlations within native-range habitats, we assessed whether adaptation to native environments may have shaped the success of some introduced populations. At the broad scale, two glacial refugia contributed to the ancestry and genomic diversity of tench. However, native, introduced and farmed populations of admixed origin exhibited up to 10-fold more genetic diversity (i.e., observed heterozygosity, expected heterozygosity and allelic richness) compared to populations with predominantly single-source ancestry. The effects of introduction to a new location were also apparent as introduced populations exhibited fewer private alleles (mean = 9.9 and 18.9 private alleles in introduced and native populations, respectively) and higher population-specific <i>Fst</i> compared to native populations, highlighting their distinctiveness relative to the pool of allelic frequencies across tench populations. Finally, introduced populations with varying levels of genetic variation and similar genetic compositions have become established and persisted under strikingly different climatic and ecological conditions. Our results suggest that lack of prior adaptation and low genetic variation may not consistently hinder the success of introduced populations for species with a demonstrated ability to expand their native range.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 10","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11450252/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142379664","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Zachary L. Robinson, Jason A. Coombs, Mark Hudy, Keith H. Nislow, Andrew R. Whiteley
Brook Trout (Salvelinus fontinalis) populations have experienced marked declines throughout their native range and are presently threatened due to isolation in small habitat fragments, land use changes, and climate change. The existence of numerous, spatially distinct populations poses substantial challenges for monitoring population status (e.g., abundance, recruitment, or occupancy). Genetic monitoring with estimates of effective number of breeders (Nb) provides a potentially powerful metric to complement existing population monitoring, assessment, and prioritization. We estimated Nb for 71 Brook Trout habitat units in mid-Atlantic region of the United States and obtained a mean Nb of 73.2 (range 6.90–493). Our modeling approach tested whether Nb estimates were sensitive to differences in habitat size, presence of non-native salmonids, base flow index, temperature, acidic precipitation, and indices of anthropogenic disturbance. We found significant support for three of our hypotheses including the positive influences of available habitat and base flow index and negative effect of temperature. Our results are consistent with presently observed and predicted future impacts of climate change on populations of this cold-water fish. Importantly, these findings support the use of Nb in population assessments as an index of relative population status.
布鲁克鳟(Salvelinus fontinalis)种群在其整个原生地都经历了明显的衰退,由于被隔离在狭小的栖息地片段、土地利用变化和气候变化,目前已濒临灭绝。由于存在众多在空间上截然不同的种群,这给监测种群状况(如丰度、招募或占有率)带来了巨大挑战。通过估算有效繁殖者数量(N b)来进行遗传监测,为补充现有的种群监测、评估和优先排序提供了一个潜在的有力指标。我们估算了美国大西洋中部地区 71 个布鲁克鳟栖息地单元的 N b,得到的平均 N b 为 73.2(范围为 6.90-493)。我们的建模方法测试了 N b 估计值是否对栖息地大小、是否存在非本地鲑鱼、基流指数、温度、酸性降水和人为干扰指数的差异敏感。我们发现,我们的三个假设得到了明显的支持,包括可用栖息地和基流指数的积极影响以及温度的消极影响。我们的研究结果与目前观察到的和预测的未来气候变化对这种冷水鱼类种群的影响是一致的。重要的是,这些发现支持在种群评估中使用 N b 作为相对种群状况的指标。
{"title":"Estimates of Effective Number of Breeders Identify Drivers of Decline in Mid-Atlantic Brook Trout Populations","authors":"Zachary L. Robinson, Jason A. Coombs, Mark Hudy, Keith H. Nislow, Andrew R. Whiteley","doi":"10.1111/eva.13769","DOIUrl":"10.1111/eva.13769","url":null,"abstract":"<p>Brook Trout (<i>Salvelinus fontinalis</i>) populations have experienced marked declines throughout their native range and are presently threatened due to isolation in small habitat fragments, land use changes, and climate change. The existence of numerous, spatially distinct populations poses substantial challenges for monitoring population status (e.g., abundance, recruitment, or occupancy). Genetic monitoring with estimates of effective number of breeders (<i>N</i><sub>b</sub>) provides a potentially powerful metric to complement existing population monitoring, assessment, and prioritization. We estimated <i>N</i><sub>b</sub> for 71 Brook Trout habitat units in mid-Atlantic region of the United States and obtained a mean <i>N</i><sub>b</sub> of 73.2 (range 6.90–493). Our modeling approach tested whether <i>N</i><sub>b</sub> estimates were sensitive to differences in habitat size, presence of non-native salmonids, base flow index, temperature, acidic precipitation, and indices of anthropogenic disturbance. We found significant support for three of our hypotheses including the positive influences of available habitat and base flow index and negative effect of temperature. Our results are consistent with presently observed and predicted future impacts of climate change on populations of this cold-water fish. Importantly, these findings support the use of <i>N</i><sub>b</sub> in population assessments as an index of relative population status.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 10","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-09-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11442137/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142363608","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sofia G. Costa, Sara Magalhães, Inês Santos, Flore Zélé, Leonor R. Rodrigues
Current pest management relies extensively on pesticide application worldwide, despite the frequent rise of pesticide resistance in crop pests. This is particularly worrisome because resistance is often not costly enough to be lost in populations after pesticide application, resulting in increased dependency on pesticide application. As climate warming increases, effort should be put into understanding how heat tolerance will affect the persistence of pesticide resistance in populations. To address this, we measured heat tolerance in two populations of the spider mite crop pest Tetranychus urticae that differ in the presence or absence of a target-site mutation conferring resistance to etoxazole pesticide. We found that developmental time and fertility, but not survival, were negatively affected by increasing temperatures in the susceptible population. Furthermore, we found no difference between resistant and susceptible populations in all life-history traits when both sexes developed at control temperature, nor when females developed at high temperature. Resistant heat-stressed males, in contrast, showed lower fertility than susceptible ones, indicating a sex-specific trade-off between heat tolerance and pesticide resistance. This suggests that global warming could lead to reduced pesticide resistance in natural populations. However, resistant females, being as affected by high temperature as susceptible individuals, may buffer the toll in resistant male fertility, and the shorter developmental time at high temperatures may accelerate adaptation to temperature, the pesticide or the cost thereof. Ultimately, the complex dynamic between these two factors will determine whether resistant populations can persist under climate warming.
{"title":"A Sex-Specific Trade-Off Between Pesticide Resistance and Tolerance to Heat-Induced Sterility in Tetranychus urticae","authors":"Sofia G. Costa, Sara Magalhães, Inês Santos, Flore Zélé, Leonor R. Rodrigues","doi":"10.1111/eva.70014","DOIUrl":"https://doi.org/10.1111/eva.70014","url":null,"abstract":"<p>Current pest management relies extensively on pesticide application worldwide, despite the frequent rise of pesticide resistance in crop pests. This is particularly worrisome because resistance is often not costly enough to be lost in populations after pesticide application, resulting in increased dependency on pesticide application. As climate warming increases, effort should be put into understanding how heat tolerance will affect the persistence of pesticide resistance in populations. To address this, we measured heat tolerance in two populations of the spider mite crop pest <i>Tetranychus urticae</i> that differ in the presence or absence of a target-site mutation conferring resistance to etoxazole pesticide. We found that developmental time and fertility, but not survival, were negatively affected by increasing temperatures in the susceptible population. Furthermore, we found no difference between resistant and susceptible populations in all life-history traits when both sexes developed at control temperature, nor when females developed at high temperature. Resistant heat-stressed males, in contrast, showed lower fertility than susceptible ones, indicating a sex-specific trade-off between heat tolerance and pesticide resistance. This suggests that global warming could lead to reduced pesticide resistance in natural populations. However, resistant females, being as affected by high temperature as susceptible individuals, may buffer the toll in resistant male fertility, and the shorter developmental time at high temperatures may accelerate adaptation to temperature, the pesticide or the cost thereof. Ultimately, the complex dynamic between these two factors will determine whether resistant populations can persist under climate warming.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 9","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-09-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70014","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142324522","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sonja Lečić, Thomas M. Wolfe, Animesh Ghosh, Serdar Satar, Camilla Souza Beraldo, Emily Smith, Jason J. Dombroskie, Emily Jernigan, Glen Ray Hood, Hannes Schuler, Christian Stauffer
The introduction of non-native species across the world represents a major global challenge. Retracing invasion origin is an important first step in understanding the invasion process, often requiring detailed sampling within the native range. Insect species frequently host Wolbachia, a widespread endosymbiotic bacterium that manipulates host reproduction to increase infected female fitness. Here, we draw on the spatial variation in infection frequencies of an actively spreading Wolbachia strain wCer2 to investigate the invasion origin of the European cherry fruit fly, Rhagoletis cerasi. This pest of cherries was introduced from Europe to North America within the last decade. First, we screen the introduced fly population for the presence of Wolbachia. The introduced populations lack the wCer2 strain and the strongly associated mitochondrial haplotype, suggesting strain absence due to founder effects with invading individuals originating from wCer2-uninfected native population(s). To narrow down geographic regions of invasion origin, we perform spatial interpolation of the wCer2 infection frequency across the native range and predict the infection frequency in unsampled regions. For this, we use an extensive dataset of R. cerasi infection covering 238 populations across Europe over 25 years, complemented with 14 additional populations analyzed for this study. We find that R. cerasi was unlikely introduced from wCer2-infected populations in Central and Western Europe. We propose wCer2-uninfected populations from Eastern Europe and the Mediterranean region as the most likely candidates for the invasion origin. This work utilizes Wolbachia as an indirect instrument to provide insights into the invasion source of R. cerasi in North America, revealing yet another application for this multifaceted heritable endosymbiont. Given the prevalence of biological invasions, rapidly uncovering invasion origins gives fundamental insights into how invasive species adapt to new environments.
{"title":"Spatially Varying Wolbachia Frequencies Reveal the Invasion Origin of an Agricultural Pest Recently Introduced From Europe to North America","authors":"Sonja Lečić, Thomas M. Wolfe, Animesh Ghosh, Serdar Satar, Camilla Souza Beraldo, Emily Smith, Jason J. Dombroskie, Emily Jernigan, Glen Ray Hood, Hannes Schuler, Christian Stauffer","doi":"10.1111/eva.70016","DOIUrl":"https://doi.org/10.1111/eva.70016","url":null,"abstract":"<p>The introduction of non-native species across the world represents a major global challenge. Retracing invasion origin is an important first step in understanding the invasion process, often requiring detailed sampling within the native range. Insect species frequently host <i>Wolbachia</i>, a widespread endosymbiotic bacterium that manipulates host reproduction to increase infected female fitness. Here, we draw on the spatial variation in infection frequencies of an actively spreading <i>Wolbachia</i> strain <i>w</i>Cer2 to investigate the invasion origin of the European cherry fruit fly, <i>Rhagoletis cerasi.</i> This pest of cherries was introduced from Europe to North America within the last decade. First, we screen the introduced fly population for the presence of <i>Wolbachia</i>. The introduced populations lack the <i>w</i>Cer2 strain and the strongly associated mitochondrial haplotype, suggesting strain absence due to founder effects with invading individuals originating from <i>w</i>Cer2-uninfected native population(s). To narrow down geographic regions of invasion origin, we perform spatial interpolation of the <i>w</i>Cer2 infection frequency across the native range and predict the infection frequency in unsampled regions. For this, we use an extensive dataset of <i>R. cerasi</i> infection covering 238 populations across Europe over 25 years, complemented with 14 additional populations analyzed for this study. We find that <i>R. cerasi</i> was unlikely introduced from <i>w</i>Cer2-infected populations in Central and Western Europe. We propose <i>w</i>Cer2-uninfected populations from Eastern Europe and the Mediterranean region as the most likely candidates for the invasion origin. This work utilizes <i>Wolbachia</i> as an indirect instrument to provide insights into the invasion source of <i>R. cerasi</i> in North America, revealing yet another application for this multifaceted heritable endosymbiont. Given the prevalence of biological invasions, rapidly uncovering invasion origins gives fundamental insights into how invasive species adapt to new environments.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 9","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-09-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70016","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142273213","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Robert Kwait, Malin L. Pinsky, Sarah Gignoux-Wolfsohn, Evan A. Eskew, Kathleen Kerwin, Brooke Maslo
Genome-wide scans for selection have become a popular tool for investigating evolutionary responses in wildlife to emerging diseases. However, genome scans are susceptible to false positives and do little to demonstrate specific mechanisms by which loci impact survival. Linking putatively resistant genotypes to observable phenotypes increases confidence in genome scan results and provides evidence of survival mechanisms that can guide conservation and management efforts. Here we used an expression quantitative trait loci (eQTL) analysis to uncover relationships between gene expression and alleles associated with the survival of little brown bats (Myotis lucifugus) despite infection with the causative agent of white-nose syndrome. We found that 25 of the 63 single-nucleotide polymorphisms (SNPs) associated with survival were related to gene expression in wing tissue. The differentially expressed genes have functional annotations associated with the innate immune system, metabolism, circadian rhythms, and the cellular response to stress. In addition, we observed differential expression of multiple genes with survival implications related to loci in linkage disequilibrium with focal SNPs. Together, these findings support the selective function of these loci and suggest that part of the mechanism driving survival may be the alteration of immune and other responses in epithelial tissue.
全基因组选择扫描已成为研究野生动物对新出现疾病的进化反应的常用工具。然而,基因组扫描很容易出现假阳性,而且几乎无法证明基因位点影响生存的具体机制。将假定的抗性基因型与可观察到的表型联系起来,可增加对基因组扫描结果的信心,并提供生存机制的证据,从而指导保护和管理工作。在这里,我们使用表达量性状位点(eQTL)分析来揭示基因表达与小棕蝠(Myotis lucifugus)在感染白鼻综合征致病因子后仍能存活的等位基因之间的关系。我们发现,在与存活率相关的 63 个单核苷酸多态性(SNPs)中,有 25 个与翅膀组织中的基因表达有关。差异表达基因的功能注释与先天免疫系统、新陈代谢、昼夜节律和细胞对应激的反应有关。此外,我们还观察到多个对生存有影响的基因的差异表达,这些基因与病灶 SNP 的连锁不平衡位点有关。这些发现共同支持了这些基因座的选择性功能,并表明驱动生存的部分机制可能是上皮组织中免疫和其他反应的改变。
{"title":"Impact of putatively beneficial genomic loci on gene expression in little brown bats (Myotis lucifugus, Le Conte, 1831) affected by white-nose syndrome","authors":"Robert Kwait, Malin L. Pinsky, Sarah Gignoux-Wolfsohn, Evan A. Eskew, Kathleen Kerwin, Brooke Maslo","doi":"10.1111/eva.13748","DOIUrl":"https://doi.org/10.1111/eva.13748","url":null,"abstract":"<p>Genome-wide scans for selection have become a popular tool for investigating evolutionary responses in wildlife to emerging diseases. However, genome scans are susceptible to false positives and do little to demonstrate specific mechanisms by which loci impact survival. Linking putatively resistant genotypes to observable phenotypes increases confidence in genome scan results and provides evidence of survival mechanisms that can guide conservation and management efforts. Here we used an expression quantitative trait loci (eQTL) analysis to uncover relationships between gene expression and alleles associated with the survival of little brown bats (<i>Myotis lucifugus</i>) despite infection with the causative agent of white-nose syndrome. We found that 25 of the 63 single-nucleotide polymorphisms (SNPs) associated with survival were related to gene expression in wing tissue. The differentially expressed genes have functional annotations associated with the innate immune system, metabolism, circadian rhythms, and the cellular response to stress. In addition, we observed differential expression of multiple genes with survival implications related to loci in linkage disequilibrium with focal SNPs. Together, these findings support the selective function of these loci and suggest that part of the mechanism driving survival may be the alteration of immune and other responses in epithelial tissue.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 9","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.13748","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142275083","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Israël Tankam Chedjou, Josselin Montarry, Sylvain Fournet, Frédéric M. Hamelin
The pale cyst nematode, Globodera pallida, is a pest that poses a significant threat to potato crops worldwide. The most effective chemical nematicides are toxic to nontarget organisms and are now banned. Alternative control methods are therefore required. Crop rotation and biological control methods have limitations for effectively managing nematodes. The use of genetically resistant cultivars is a promising alternative, but nematode populations evolve, and virulent mutants can break resistance after just a few years. Masculinizing resistances, preventing avirulent nematodes from producing females, might be more durable than blocking resistances, preventing infection. Our demo-genetic model, tracking both nematode population densities and virulence allele frequencies, shows that virulence against masculinizing resistance may not be fixed in the pest population under realistic agricultural conditions. Avirulence may persist despite the uniform use of resistance. This is because avirulent male nematodes may transmit avirulent alleles to their progeny by mating with virulent females. Additionally, because avirulent nematodes do not produce females themselves, they weaken the reproductive rate of the nematode population, leading to a reduction in its density by at least 20%. This avirulence load can even lead to the collapse of the nematode population in theory. Overall, our model showed that combining masculinizing resistance, rotation, and biocontrol may achieve durable suppression of G. pallida in a reasonable time frame. Our work is supported by an online interactive interface allowing users (i.e., growers, plant health authorities, researchers) to test their own control combinations.
苍白囊线虫(Globodera pallida)是一种对全球马铃薯作物构成重大威胁的害虫。最有效的化学杀线虫剂对非目标生物有毒,现已被禁用。因此需要采用替代控制方法。轮作和生物防治方法在有效控制线虫方面存在局限性。使用具有基因抗性的栽培品种是一种很有前景的替代方法,但线虫种群会不断进化,毒性突变体在短短几年后就会打破抗性。与阻止线虫感染的阻断抗性相比,阻止无毒线虫产生雌性线虫的雄性化抗性可能更持久。我们的人口遗传学模型同时跟踪线虫种群密度和毒力等位基因频率,结果表明,在现实的农业条件下,针对男性化抗性的毒力可能不会在害虫种群中固定下来。尽管统一使用抗性,但无毒性可能会持续存在。这是因为无毒雄性线虫可能会通过与有毒雌性线虫交配,将无毒等位基因传给后代。此外,由于无毒线虫本身不产生雌虫,它们会削弱线虫种群的繁殖率,导致其密度至少降低 20%。理论上,这种无毒负荷甚至会导致线虫种群的崩溃。总之,我们的模型表明,将抗药性、轮作和生物防治结合起来,可以在合理的时间范围内实现对 G. pallida 的持久抑制。我们的工作得到了在线互动界面的支持,允许用户(即种植者、植物健康机构、研究人员)测试自己的防治组合。
{"title":"Combining Masculinizing Resistance, Rotation, and Biocontrol to Achieve Durable Suppression of the Potato Pale Cyst Nematode: A Model","authors":"Israël Tankam Chedjou, Josselin Montarry, Sylvain Fournet, Frédéric M. Hamelin","doi":"10.1111/eva.70012","DOIUrl":"https://doi.org/10.1111/eva.70012","url":null,"abstract":"<p>The pale cyst nematode, <i>Globodera pallida</i>, is a pest that poses a significant threat to potato crops worldwide. The most effective chemical nematicides are toxic to nontarget organisms and are now banned. Alternative control methods are therefore required. Crop rotation and biological control methods have limitations for effectively managing nematodes. The use of genetically resistant cultivars is a promising alternative, but nematode populations evolve, and virulent mutants can break resistance after just a few years. Masculinizing resistances, preventing avirulent nematodes from producing females, might be more durable than blocking resistances, preventing infection. Our demo-genetic model, tracking both nematode population densities and virulence allele frequencies, shows that virulence against masculinizing resistance may not be fixed in the pest population under realistic agricultural conditions. Avirulence may persist despite the uniform use of resistance. This is because avirulent male nematodes may transmit avirulent alleles to their progeny by mating with virulent females. Additionally, because avirulent nematodes do not produce females themselves, they weaken the reproductive rate of the nematode population, leading to a reduction in its density by at least 20%. This avirulence load can even lead to the collapse of the nematode population in theory. Overall, our model showed that combining masculinizing resistance, rotation, and biocontrol may achieve durable suppression of <i>G. pallida</i> in a reasonable time frame. Our work is supported by an online interactive interface allowing users (i.e., growers, plant health authorities, researchers) to test their own control combinations.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 9","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-09-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70012","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142273129","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}