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}
Einar Eg Nielsen, Kim Birnie-Gauvin, Henrik Baktoft, Haritz Arrizabalaga, Tomas Brodin, Massimiliano Cardinale, Michele Casini, Gustav Helström, Teunis Jansen, Anders Koed, Petter Lundberg, Brian R. MacKenzie, Antonio Medina, Søren Post, Naiara Rodriguez-Ezpeleta, Andreas Sundelöf, José Luis Varela, Kim Aarestrup
Knowledge about sex-specific difference in life-history traits—like growth, mortality, or behavior—is of key importance for management and conservation as these parameters are essential for predictive modeling of population sustainability. We applied a newly developed molecular sex identification method, in combination with a SNP (single nucleotide polymorphism) panel for inferring the population of origin, for more than 300 large Atlantic bluefin tuna (ABFT) collected over several years from newly reclaimed feeding grounds in the Northeast Atlantic. The vast majority (95%) of individuals were genetically assigned to the eastern Atlantic population, which migrates between spawning grounds in the Mediterranean and feeding grounds in the Northeast Atlantic. We found a consistent pattern of a male bias among the eastern Atlantic individuals, with a 4-year mean of 63% males (59%–65%). Males were most prominent within the smallest (< 230 cm) and largest (> 250 cm) length classes, while the sex ratio was close to 1:1 for intermediate sizes (230–250 cm). The results from this new, widely applicable, and noninvasive approach suggests differential occupancy or migration timing of ABFT males and females, which cannot be explained alone by sex-specific differences in growth. Our findings are corroborated by previous traditional studies of sex ratios in dead ABFT from the Atlantic, the Mediterranean, and the Gulf of Mexico. In concert with observed differences in growth and mortality rates between the sexes, these findings should be recognized in order to sustainably manage the resource, maintain productivity, and conserve diversity within the species.
{"title":"Genetic Sex and Origin Identification Suggests Differential Migration of Male and Female Atlantic Bluefin Tuna (Thunnus thynnus) in the Northeast Atlantic","authors":"Einar Eg Nielsen, Kim Birnie-Gauvin, Henrik Baktoft, Haritz Arrizabalaga, Tomas Brodin, Massimiliano Cardinale, Michele Casini, Gustav Helström, Teunis Jansen, Anders Koed, Petter Lundberg, Brian R. MacKenzie, Antonio Medina, Søren Post, Naiara Rodriguez-Ezpeleta, Andreas Sundelöf, José Luis Varela, Kim Aarestrup","doi":"10.1111/eva.70009","DOIUrl":"https://doi.org/10.1111/eva.70009","url":null,"abstract":"<p>Knowledge about sex-specific difference in life-history traits—like growth, mortality, or behavior—is of key importance for management and conservation as these parameters are essential for predictive modeling of population sustainability. We applied a newly developed molecular sex identification method, in combination with a SNP (single nucleotide polymorphism) panel for inferring the population of origin, for more than 300 large Atlantic bluefin tuna (ABFT) collected over several years from newly reclaimed feeding grounds in the Northeast Atlantic. The vast majority (95%) of individuals were genetically assigned to the eastern Atlantic population, which migrates between spawning grounds in the Mediterranean and feeding grounds in the Northeast Atlantic. We found a consistent pattern of a male bias among the eastern Atlantic individuals, with a 4-year mean of 63% males (59%–65%). Males were most prominent within the smallest (< 230 cm) and largest (> 250 cm) length classes, while the sex ratio was close to 1:1 for intermediate sizes (230–250 cm). The results from this new, widely applicable, and noninvasive approach suggests differential occupancy or migration timing of ABFT males and females, which cannot be explained alone by sex-specific differences in growth. Our findings are corroborated by previous traditional studies of sex ratios in dead ABFT from the Atlantic, the Mediterranean, and the Gulf of Mexico. In concert with observed differences in growth and mortality rates between the sexes, these findings should be recognized in order to sustainably manage the resource, maintain productivity, and conserve diversity within the species.</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.70009","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142273128","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}
Agostino Leone, Sophie Arnaud-Haond, Massimiliano Babbucci, Luca Bargelloni, Ilaria Coscia, Dimitrios Damalas, Chrystelle Delord, Rafaella Franch, Fulvio Garibaldi, David Macias, Stefano Mariani, Jann Martinsohn, Persefoni Megalofonou, Primo Micarelli, Natacha Nikolic, Paulo A. Prodöhl, Emilio Sperone, Marco Stagioni, Antonella Zanzi, Alessia Cariani, Fausto Tinti
Populations of marine top predators have been sharply declining during the past decades, and one-third of chondrichthyans are currently threatened with extinction. Sustainable management measures and conservation plans of large pelagic sharks require knowledge on population genetic differentiation and demographic connectivity. Here, we present the case of the Mediterranean blue shark (Prionace glauca, L. 1758), commonly found as bycatch in longline fisheries and classified by the IUCN as critically endangered. The management of this species suffers from a scarcity of data about population structure and connectivity within the Mediterranean Sea and between this basin and the adjacent Northeast Atlantic. Here, we assessed the genetic diversity and spatial structure of blue shark from different areas of the Mediterranean Sea and the Northeast Atlantic through genome scan analyses. Pairwise genetic differentiation estimates (FST) on 203 specimens genotyped at 14,713 ddRAD-derived SNPs revealed subtle, yet significant, genetic differences within the Mediterranean sampling locations, and between the Mediterranean Sea and the Northeast Atlantic Ocean. Genetic differentiation suggests some degree of demographic independence between the Western and Eastern Mediterranean blue shark populations. Furthermore, results show limited genetic connectivity between the Mediterranean and the Atlantic basins, supporting the hypothesis of two distinct populations of blue shark separated by the Strait of Gibraltar. Although reproductive interactions may be limited, the faint genetic signal of differentiation suggests a recent common history between these units. Therefore, Mediterranean blue sharks may function akin to a metapopulation relying upon local demographic processes and connectivity dynamics, whereby the limited contemporary gene flow replenishment from the Atlantic may interplay with currently poorly regulated commercial catches and large-scale ecosystem changes. Altogether, these results emphasise the need for revising management delineations applied to these critically endangered sharks.
{"title":"Population Genomics of the Blue Shark, Prionace glauca, Reveals Different Populations in the Mediterranean Sea and the Northeast Atlantic","authors":"Agostino Leone, Sophie Arnaud-Haond, Massimiliano Babbucci, Luca Bargelloni, Ilaria Coscia, Dimitrios Damalas, Chrystelle Delord, Rafaella Franch, Fulvio Garibaldi, David Macias, Stefano Mariani, Jann Martinsohn, Persefoni Megalofonou, Primo Micarelli, Natacha Nikolic, Paulo A. Prodöhl, Emilio Sperone, Marco Stagioni, Antonella Zanzi, Alessia Cariani, Fausto Tinti","doi":"10.1111/eva.70005","DOIUrl":"https://doi.org/10.1111/eva.70005","url":null,"abstract":"<p>Populations of marine top predators have been sharply declining during the past decades, and one-third of chondrichthyans are currently threatened with extinction. Sustainable management measures and conservation plans of large pelagic sharks require knowledge on population genetic differentiation and demographic connectivity. Here, we present the case of the Mediterranean blue shark (<i>Prionace glauca</i>, L. 1758), commonly found as bycatch in longline fisheries and classified by the IUCN as critically endangered. The management of this species suffers from a scarcity of data about population structure and connectivity within the Mediterranean Sea and between this basin and the adjacent Northeast Atlantic. Here, we assessed the genetic diversity and spatial structure of blue shark from different areas of the Mediterranean Sea and the Northeast Atlantic through genome scan analyses. Pairwise genetic differentiation estimates (<i>F</i><sub>ST</sub>) on 203 specimens genotyped at 14,713 ddRAD-derived SNPs revealed subtle, yet significant, genetic differences within the Mediterranean sampling locations, and between the Mediterranean Sea and the Northeast Atlantic Ocean. Genetic differentiation suggests some degree of demographic independence between the Western and Eastern Mediterranean blue shark populations. Furthermore, results show limited genetic connectivity between the Mediterranean and the Atlantic basins, supporting the hypothesis of two distinct populations of blue shark separated by the Strait of Gibraltar. Although reproductive interactions may be limited, the faint genetic signal of differentiation suggests a recent common history between these units. Therefore, Mediterranean blue sharks may function akin to a metapopulation relying upon local demographic processes and connectivity dynamics, whereby the limited contemporary gene flow replenishment from the Atlantic may interplay with currently poorly regulated commercial catches and large-scale ecosystem changes. Altogether, these results emphasise the need for revising management delineations applied to these critically endangered sharks.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 9","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-09-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70005","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142244529","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}
Chenqing Zheng, Qing Chen, Michelle Hang Gi Wong, Nick Marx, Thananh Khotpathoom, Hesheng Wang, Feng Yang, Xiaodong Rao, Bosco Pui Lok Chan, Yang Liu
Eld's deer Rucervus eldii (McClelland, 1842) is an ungulate that lives in tropical lowland forests in several countries of Indochina and Hainan Island of China. Its remaining population is small and scattered, and the species is listed as an Endangered species on the IUCN Red List. The debate over the taxonomic status of the Hainan population has persisted for over a century—as an island-endemic subspecies R. e. hainanus, or an insular population of the subspecies R. e. siamensis, would have significant conservation implications. And, given the Hainan population had experienced both population bottleneck and multiple translocations in the past, conservation genomics would be a powerful tool to evaluate the genetic impacts of these events. In this study, we used conservation genomics assessment to study population differentiation and genetic diversity of R. e. siamensis in Cambodia and three Eld's deer subpopulations on Hainan Island. Based on the unique genetic profile and demographic analysis, this study corroborated previous studies using genetic markers that the Hainan Eld's deer warrants the taxonomic status of a distinct subspecies. The Hainan population exhibits a reduction in genetic diversity and an increase in the level of inbreeding when compared to the population of Cambodia. The signs of purifying selection were found against homozygous loss-of-function mutations to decrease the deleterious burden in the Hainan population. However, there was an accumulation of more deleterious missense mutations. Furthermore, significant differences in genetic diversity and level of inbreeding found among the three Hainan subpopulations indicated population isolation and suboptimal translocation strategies, which calls for urgent, coordinated, and science-based genetic management to ensure the long-term viability of the endemic subspecies hainanus. This study provides guidance for the conservation and management of Eld's deer.
{"title":"Whole-Genome Analyses Reveal the Distinct Taxonomic Status of the Hainan Population of Endangered Rucervus eldii and Its Conservation Implications","authors":"Chenqing Zheng, Qing Chen, Michelle Hang Gi Wong, Nick Marx, Thananh Khotpathoom, Hesheng Wang, Feng Yang, Xiaodong Rao, Bosco Pui Lok Chan, Yang Liu","doi":"10.1111/eva.70010","DOIUrl":"https://doi.org/10.1111/eva.70010","url":null,"abstract":"<p>Eld's deer <i>Rucervus eldii</i> (McClelland, 1842) is an ungulate that lives in tropical lowland forests in several countries of Indochina and Hainan Island of China. Its remaining population is small and scattered, and the species is listed as an Endangered species on the IUCN Red List. The debate over the taxonomic status of the Hainan population has persisted for over a century—as an island-endemic subspecies <i>R. e. hainanus</i>, or an insular population of the subspecies <i>R. e. siamensis</i>, would have significant conservation implications. And, given the Hainan population had experienced both population bottleneck and multiple translocations in the past, conservation genomics would be a powerful tool to evaluate the genetic impacts of these events. In this study, we used conservation genomics assessment to study population differentiation and genetic diversity of <i>R. e. siamensis</i> in Cambodia and three Eld's deer subpopulations on Hainan Island. Based on the unique genetic profile and demographic analysis, this study corroborated previous studies using genetic markers that the Hainan Eld's deer warrants the taxonomic status of a distinct subspecies. The Hainan population exhibits a reduction in genetic diversity and an increase in the level of inbreeding when compared to the population of Cambodia. The signs of purifying selection were found against homozygous loss-of-function mutations to decrease the deleterious burden in the Hainan population. However, there was an accumulation of more deleterious missense mutations. Furthermore, significant differences in genetic diversity and level of inbreeding found among the three Hainan subpopulations indicated population isolation and suboptimal translocation strategies, which calls for urgent, coordinated, and science-based genetic management to ensure the long-term viability of the endemic subspecies <i>hainanus</i>. This study provides guidance for the conservation and management of Eld's deer.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 9","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-09-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70010","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142234849","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}
Nicole E. Adams, Jared J. Homola, Nicholas M. Sard, Lucas R. Nathan, Brian M. Roth, John D. Robinson, Kim T. Scribner
The establishment and spread of invasive species are directly related to intersexual interactions as dispersal and reproductive success are related to distribution, effective population size, and population growth. Accordingly, populations established by r-selected species are particularly difficult to suppress or eradicate. One such species, the red swamp crayfish (Procambarus clarkii) is established globally at considerable ecological and financial costs to natural and human communities. Here, we develop a single nucleotide polymorphism (SNP) loci panel for P. clarkii using restriction-associated DNA-sequencing data. We use the SNP panel to successfully genotype 1800 individuals at 930 SNPs in southeastern Michigan, USA. Genotypic data were used to reconstruct pedigrees, which enabled the characterization of P. clarkii's mating system and statistical tests for associations among environmental, demographic, and phenotypic predictors and adult reproductive success estimates. We identified juvenile cohorts using genotype-based pedigrees, body size, and sampling timing, which elucidated the breeding phenology of multiple introduced populations. We report a high prevalence of multiple paternity in each surveyed waterbody, indicating polyandry in this species. We highlight the use of newly developed rapid genomic assessment tools for monitoring population reproductive responses, effective population sizes, and dispersal during ongoing control efforts.
入侵物种的建立和扩散与性间相互作用直接相关,因为扩散和繁殖成功率与分布、有效种群规模和种群增长有关。因此,r-选择物种建立的种群尤其难以抑制或根除。红沼泽螯虾(Procambarus clarkii)就是这样一种物种,它在全球范围内建立种群,给自然和人类社区带来了巨大的生态和经济损失。在本文中,我们利用限制性相关 DNA 测序数据为克氏原螯虾开发了一个单核苷酸多态性(SNP)位点面板。我们利用 SNP 面板在美国密歇根州东南部成功地对 1800 个个体的 930 个 SNP 进行了基因分型。基因分型数据被用于重建血统,从而确定了克氏原鲤交配系统的特征,并对环境、人口和表型预测因子与成年繁殖成功率估计值之间的关联进行了统计检验。我们利用基于基因型的系谱、体型和取样时间确定了幼体群,从而阐明了多个引入种群的繁殖表型。我们报告了每个调查水体中多重父子关系的高发生率,表明该物种存在多雄现象。我们重点介绍了新开发的快速基因组评估工具在监测种群繁殖反应、有效种群规模和持续控制过程中的扩散情况方面的应用。
{"title":"Genomic Data Characterize Reproductive Ecology Patterns in Michigan Invasive Red Swamp Crayfish (Procambarus clarkii)","authors":"Nicole E. Adams, Jared J. Homola, Nicholas M. Sard, Lucas R. Nathan, Brian M. Roth, John D. Robinson, Kim T. Scribner","doi":"10.1111/eva.70007","DOIUrl":"https://doi.org/10.1111/eva.70007","url":null,"abstract":"<p>The establishment and spread of invasive species are directly related to intersexual interactions as dispersal and reproductive success are related to distribution, effective population size, and population growth. Accordingly, populations established by r-selected species are particularly difficult to suppress or eradicate. One such species, the red swamp crayfish (<i>Procambarus clarkii</i>) is established globally at considerable ecological and financial costs to natural and human communities. Here, we develop a single nucleotide polymorphism (SNP) loci panel for <i>P. clarkii</i> using restriction-associated DNA-sequencing data. We use the SNP panel to successfully genotype 1800 individuals at 930 SNPs in southeastern Michigan, USA. Genotypic data were used to reconstruct pedigrees, which enabled the characterization of <i>P. clarkii's</i> mating system and statistical tests for associations among environmental, demographic, and phenotypic predictors and adult reproductive success estimates. We identified juvenile cohorts using genotype-based pedigrees, body size, and sampling timing, which elucidated the breeding phenology of multiple introduced populations. We report a high prevalence of multiple paternity in each surveyed waterbody, indicating polyandry in this species. We highlight the use of newly developed rapid genomic assessment tools for monitoring population reproductive responses, effective population sizes, and dispersal during ongoing control efforts.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 9","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-09-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70007","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142234921","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}
Assisted migration provides a potential solution to mitigate the increasing risks of forest maladaptation under climate change. Western larch (Larix occidentalis Nutt.) is a deciduous conifer species undergoing assisted migration beyond its natural range in British Columbia into areas that have become suitable based on climatic niche modelling. We established a seedling common garden experiment in raised beds in a warm location outside the natural range for three growing seasons, with 52 natural populations from across the species range and 28 selectively bred families from British Columbia. Intraspecific genetic variation in growth, phenology and cold hardiness was analyzed to test for signals of local adaptation and the effects of selective breeding to better understand the implications for assisted migration and breeding for future climates. We found weak differentiation among populations in all traits, with the proportion of additive genetic variance (QST) ranging from 0.10 to 0.28. Cold hardiness had the weakest population differentiation and exhibited no clines with geographic or climatic variables. Selective breeding for faster growth has maintained genetic variation in bud flush phenology and cold hardiness despite delaying bud set. The weak signals of local adaptation we found in western larch seedlings highlights that assisted gene flow among populations is likely to have limited benefits and risks for mitigating maladaptation with climate change. Our findings suggest that assisted migration outside of the range and selective breeding may be important management strategies for western larch for future climates.
{"title":"Weak Local Adaptation to Climate in Seedlings of a Deciduous Conifer Suggests Limited Benefits and Risks of Assisted Gene Flow","authors":"Beth Roskilly, Sally Aitken","doi":"10.1111/eva.70001","DOIUrl":"https://doi.org/10.1111/eva.70001","url":null,"abstract":"<p>Assisted migration provides a potential solution to mitigate the increasing risks of forest maladaptation under climate change. Western larch (<i>Larix occidentalis</i> Nutt.) is a deciduous conifer species undergoing assisted migration beyond its natural range in British Columbia into areas that have become suitable based on climatic niche modelling. We established a seedling common garden experiment in raised beds in a warm location outside the natural range for three growing seasons, with 52 natural populations from across the species range and 28 selectively bred families from British Columbia. Intraspecific genetic variation in growth, phenology and cold hardiness was analyzed to test for signals of local adaptation and the effects of selective breeding to better understand the implications for assisted migration and breeding for future climates. We found weak differentiation among populations in all traits, with the proportion of additive genetic variance (<i>Q</i><sub>ST</sub>) ranging from 0.10 to 0.28. Cold hardiness had the weakest population differentiation and exhibited no clines with geographic or climatic variables. Selective breeding for faster growth has maintained genetic variation in bud flush phenology and cold hardiness despite delaying bud set. The weak signals of local adaptation we found in western larch seedlings highlights that assisted gene flow among populations is likely to have limited benefits and risks for mitigating maladaptation with climate change. Our findings suggest that assisted migration outside of the range and selective breeding may be important management strategies for western larch for future climates.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 9","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-09-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70001","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142234848","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}
Eugenie C. Yen, James D. Gilbert, Alice Balard, Inês O. Afonso, Kirsten Fairweather, Débora Newlands, Artur Lopes, Sandra M. Correia, Albert Taxonera, Stephen J. Rossiter, José M. Martín-Durán, Christophe Eizaguirre
To date, studies of the impacts of climate warming on individuals and populations have mostly focused on mortality and thermal tolerance. In contrast, much less is known about the consequences of sublethal effects, which are more challenging to detect, particularly in wild species with cryptic life histories. This necessitates the development of molecular tools to identify their signatures. In a split-clutch field experiment, we relocated clutches of wild, nesting loggerhead sea turtles (Caretta caretta) to an in situ hatchery. Eggs were then split into two sub-clutches and incubated under shallow or deep conditions, with those in the shallow treatment experiencing significantly higher temperatures in otherwise natural conditions. Although no difference in hatching success was observed between treatments, hatchlings from the shallow, warmer treatment had different length–mass relationships and were weaker at locomotion tests than their siblings incubated in the deep, cooler treatment. To characterise the molecular signatures of these thermal effects, we performed whole genome bisulfite sequencing on blood samples collected upon emergence. We identified 287 differentially methylated sites between hatchlings from different treatments, including on genes with neurodevelopmental, cytoskeletal, and lipid metabolism functions. Taken together, our results show that higher incubation temperatures induce sublethal effects in hatchlings, which are reflected in their DNA methylation status at identified sites. These sites could be used as biomarkers of thermal stress, especially if they are retained across life stages. Overall, this study suggests that global warming reduces hatchling fitness, which has implications for dispersal capacity and ultimately a population's adaptive potential. Conservation efforts for these endangered species and similar climate-threatened taxa will therefore benefit from strategies for monitoring and mitigating exposure to temperatures that induce sublethal effects.
{"title":"DNA Methylation Carries Signatures of Sublethal Effects Under Thermal Stress in Loggerhead Sea Turtles","authors":"Eugenie C. Yen, James D. Gilbert, Alice Balard, Inês O. Afonso, Kirsten Fairweather, Débora Newlands, Artur Lopes, Sandra M. Correia, Albert Taxonera, Stephen J. Rossiter, José M. Martín-Durán, Christophe Eizaguirre","doi":"10.1111/eva.70013","DOIUrl":"https://doi.org/10.1111/eva.70013","url":null,"abstract":"<p>To date, studies of the impacts of climate warming on individuals and populations have mostly focused on mortality and thermal tolerance. In contrast, much less is known about the consequences of sublethal effects, which are more challenging to detect, particularly in wild species with cryptic life histories. This necessitates the development of molecular tools to identify their signatures. In a split-clutch field experiment, we relocated clutches of wild, nesting loggerhead sea turtles (<i>Caretta caretta</i>) to an in situ hatchery. Eggs were then split into two sub-clutches and incubated under shallow or deep conditions, with those in the shallow treatment experiencing significantly higher temperatures in otherwise natural conditions. Although no difference in hatching success was observed between treatments, hatchlings from the shallow, warmer treatment had different length–mass relationships and were weaker at locomotion tests than their siblings incubated in the deep, cooler treatment. To characterise the molecular signatures of these thermal effects, we performed whole genome bisulfite sequencing on blood samples collected upon emergence. We identified 287 differentially methylated sites between hatchlings from different treatments, including on genes with neurodevelopmental, cytoskeletal, and lipid metabolism functions. Taken together, our results show that higher incubation temperatures induce sublethal effects in hatchlings, which are reflected in their DNA methylation status at identified sites. These sites could be used as biomarkers of thermal stress, especially if they are retained across life stages. Overall, this study suggests that global warming reduces hatchling fitness, which has implications for dispersal capacity and ultimately a population's adaptive potential. Conservation efforts for these endangered species and similar climate-threatened taxa will therefore benefit from strategies for monitoring and mitigating exposure to temperatures that induce sublethal effects.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 9","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-09-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70013","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142234750","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}