Understanding the evolutionary history of a species is essential for effective conservation management. Malus sieversii, a relict broad-leaf forest tree found in arid Central Asian mountains, has a narrow and fragmented distribution and is classified as an endangered species in China. This species is considered one of the ancestors of the domesticated apple trees. In the present study, we sampled five populations of M. sieversii and its wide-ranging congener M. baccata from China. Through deep whole-genome resequencing, we analyzed the population's genetic diversity, genetic structure, demographic history, fixation of deleterious mutations, and genomic divergence. Our results revealed that M. baccata exhibits a higher level of genetic diversity than M. sieversii. The effective population size of M. sieversii decreased, whereas that of M. baccata recovered after the bottleneck effect. In M. sieversii, the genetic structure of the Yili region was distinct from that of the Tacheng region. Populations at the rear edge of the Tacheng region showed a stronger fixation of deleterious mutations than those in the Yili region. Genomic divergence indicated that the positively selected genes were associated with physiological processes within the genomic islands between the Yili and Tacheng regions. Based on these findings, we recommend the establishment of two separate conservation units for the Yili and Tacheng lineages to preserve their genetic resources. Given the limited distribution range and high fixation rate of deleterious mutations, urgent protective measures are recommended for the Tacheng lineage.
{"title":"Evolutionary Genomics Provides Insights Into Endangerment and Conservation of a Wild Apple Tree Species, Malus sieversii","authors":"Jian Zhang, Fang-Yuan Zhao, Hong-Xiang Zhang","doi":"10.1111/eva.70048","DOIUrl":"https://doi.org/10.1111/eva.70048","url":null,"abstract":"<p>Understanding the evolutionary history of a species is essential for effective conservation management. <i>Malus sieversii</i>, a relict broad-leaf forest tree found in arid Central Asian mountains, has a narrow and fragmented distribution and is classified as an endangered species in China. This species is considered one of the ancestors of the domesticated apple trees. In the present study, we sampled five populations of <i>M. sieversii</i> and its wide-ranging congener <i>M. baccata</i> from China. Through deep whole-genome resequencing, we analyzed the population's genetic diversity, genetic structure, demographic history, fixation of deleterious mutations, and genomic divergence. Our results revealed that <i>M. baccata</i> exhibits a higher level of genetic diversity than <i>M. sieversii</i>. The effective population size of <i>M. sieversii</i> decreased, whereas that of <i>M. baccata</i> recovered after the bottleneck effect. In <i>M. sieversii</i>, the genetic structure of the Yili region was distinct from that of the Tacheng region. Populations at the rear edge of the Tacheng region showed a stronger fixation of deleterious mutations than those in the Yili region. Genomic divergence indicated that the positively selected genes were associated with physiological processes within the genomic islands between the Yili and Tacheng regions. Based on these findings, we recommend the establishment of two separate conservation units for the Yili and Tacheng lineages to preserve their genetic resources. Given the limited distribution range and high fixation rate of deleterious mutations, urgent protective measures are recommended for the Tacheng lineage.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 12","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-12-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70048","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142762390","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}
J. L. Dimond, J. V. Bouma, F. Lafarga-De la Cruz, K. J. Supernault, T. White, D. A. Witting
Connectivity is integral to the dynamics of metapopulations through dispersal and gene flow, and understanding these processes is essential for guiding conservation efforts. Abalone, broadcast-spawning marine snails associated with shallow rocky habitats, have experienced widespread declines, and all seven North American species are threatened. We investigated the connectivity and population genomics of pinto/northern abalone (Haliotis kamtschatkana), the widest-ranging of abalone species. We employed reduced representation sequencing (RADseq) to generate single nucleotide polymorphism (SNP) data, assessing population connectivity and potential adaptive variation at 12 locations across the full range from Alaska to Mexico. Despite depleted populations, our analysis of over 6000 SNPs across nearly 300 individuals revealed that pinto abalone maintains a high genetic diversity with no evidence of a genetic bottleneck. Neutral population structure and isolation by distance were extremely weak, indicating panmixia across the species' range (global FST = 0.0021). Phylogenetic analysis, principal components analysis, and unsupervised clustering methods all supported a single genetic population. However, slight population differentiation was noted in the Salish Sea and Inside Passage regions, with evidence for higher barriers to dispersal relative to outer coastal areas. This north-central region may also represent the species' ancestral range based on relatively low population-specific FST values; the northern and southern extremes of the range likely represent range expansions. Outlier analysis did not identify consensus loci implicated in adaptive variation, suggesting limited adaptive differentiation. Our study sheds light on the evolutionary history and contemporary gene flow of this threatened species, providing key insights for conservation strategies, particularly in sourcing broodstock for ongoing restoration efforts.
{"title":"Endangered Pinto/Northern Abalone (Haliotis kamtschatkana) are Panmictic Across Their 3700 km Range Along the Pacific Coast of North America","authors":"J. L. Dimond, J. V. Bouma, F. Lafarga-De la Cruz, K. J. Supernault, T. White, D. A. Witting","doi":"10.1111/eva.70040","DOIUrl":"https://doi.org/10.1111/eva.70040","url":null,"abstract":"<p>Connectivity is integral to the dynamics of metapopulations through dispersal and gene flow, and understanding these processes is essential for guiding conservation efforts. Abalone, broadcast-spawning marine snails associated with shallow rocky habitats, have experienced widespread declines, and all seven North American species are threatened. We investigated the connectivity and population genomics of pinto/northern abalone (<i>Haliotis kamtschatkana</i>), the widest-ranging of abalone species. We employed reduced representation sequencing (RADseq) to generate single nucleotide polymorphism (SNP) data, assessing population connectivity and potential adaptive variation at 12 locations across the full range from Alaska to Mexico. Despite depleted populations, our analysis of over 6000 SNPs across nearly 300 individuals revealed that pinto abalone maintains a high genetic diversity with no evidence of a genetic bottleneck. Neutral population structure and isolation by distance were extremely weak, indicating panmixia across the species' range (global <i>F</i><sub>ST</sub> = 0.0021). Phylogenetic analysis, principal components analysis, and unsupervised clustering methods all supported a single genetic population. However, slight population differentiation was noted in the Salish Sea and Inside Passage regions, with evidence for higher barriers to dispersal relative to outer coastal areas. This north-central region may also represent the species' ancestral range based on relatively low population-specific <i>F</i><sub>ST</sub> values; the northern and southern extremes of the range likely represent range expansions. Outlier analysis did not identify consensus loci implicated in adaptive variation, suggesting limited adaptive differentiation. Our study sheds light on the evolutionary history and contemporary gene flow of this threatened species, providing key insights for conservation strategies, particularly in sourcing broodstock for ongoing restoration efforts.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 12","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-12-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70040","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142762525","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}
Pia Guadalupe Dominguez, Angela Veronica Gutierrez, Monica Irina Fass, Carla Valeria Filippi, Pablo Vera, Andrea Puebla, Raquel Alicia Defacio, Norma Beatriz Paniego, Veronica Viviana Lia
Maize (Zea mays ssp. mays L.) landraces are traditional American crops with high genetic variability that conform a source of original alleles for conventional maize breeding. Northern Argentina, one the southernmost regions of traditional maize cultivation in the Americas, harbours around 57 races traditionally grown in two regions with contrasting environmental conditions, namely, the Andean mountains in the Northwest and the tropical grasslands and Atlantic Forest in the Northeast. These races encounter diverse threats to their genetic diversity and persistence in their regions of origin, with climate change standing out as one of the major challenges. In this work, we use genome-wide SNPs derived from ddRADseq to study the genetic diversity of individuals representing the five groups previously described for this area. This allowed us to distinguish two clearly differentiated gene pools, the highland northwestern maize (HNWA) and the floury northeastern maize (FNEA). Subsequently, we employed essential biodiversity variables at the genetic level, as proposed by the Group on Earth Observations Biodiversity Observation Network (GEO BON), to evaluate the conservation status of these two groups. This assessment encompassed genetic diversity (Pi), inbreeding coefficient (F) and effective population size (Ne). FNEA showed low Ne values and high F values, while HNWA showed low Ne values and low Pi values, indicating that further genetic erosion is imminent for these landraces. Outlier detection methods allowed identification of putative adaptive genomic regions, consistent with previously reported flowering-time loci and chromosomal regions displaying introgression from the teosinte Zea mays ssp. mexicana. Finally, species distribution models were obtained for two future climate scenarios, showing a notable reduction in the potential planting area of HNWA and a shift in the cultivation areas of FNEA. These results suggest that maize landraces from Northern Argentina may be unable to cope with climate change. Therefore, active conservation policies are advisable.
{"title":"Genome-Wide Diversity in Lowland and Highland Maize Landraces From Southern South America: Population Genetics Insights to Assist Conservation","authors":"Pia Guadalupe Dominguez, Angela Veronica Gutierrez, Monica Irina Fass, Carla Valeria Filippi, Pablo Vera, Andrea Puebla, Raquel Alicia Defacio, Norma Beatriz Paniego, Veronica Viviana Lia","doi":"10.1111/eva.70047","DOIUrl":"https://doi.org/10.1111/eva.70047","url":null,"abstract":"<p>Maize (<i>Zea mays</i> ssp. <i>mays</i> L.) landraces are traditional American crops with high genetic variability that conform a source of original alleles for conventional maize breeding. Northern Argentina, one the southernmost regions of traditional maize cultivation in the Americas, harbours around 57 races traditionally grown in two regions with contrasting environmental conditions, namely, the Andean mountains in the Northwest and the tropical grasslands and Atlantic Forest in the Northeast. These races encounter diverse threats to their genetic diversity and persistence in their regions of origin, with climate change standing out as one of the major challenges. In this work, we use genome-wide SNPs derived from ddRADseq to study the genetic diversity of individuals representing the five groups previously described for this area. This allowed us to distinguish two clearly differentiated gene pools, the highland northwestern maize (HNWA) and the floury northeastern maize (FNEA). Subsequently, we employed essential biodiversity variables at the genetic level, as proposed by the Group on Earth Observations Biodiversity Observation Network (GEO BON), to evaluate the conservation status of these two groups. This assessment encompassed genetic diversity (Pi), inbreeding coefficient (F) and effective population size (Ne). FNEA showed low Ne values and high F values, while HNWA showed low Ne values and low Pi values, indicating that further genetic erosion is imminent for these landraces. Outlier detection methods allowed identification of putative adaptive genomic regions, consistent with previously reported flowering-time loci and chromosomal regions displaying introgression from the teosinte <i>Zea mays</i> ssp. <i>mexicana</i>. Finally, species distribution models were obtained for two future climate scenarios, showing a notable reduction in the potential planting area of HNWA and a shift in the cultivation areas of FNEA. These results suggest that maize landraces from Northern Argentina may be unable to cope with climate change. Therefore, active conservation policies are advisable.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 12","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70047","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142762496","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}
Melina Campos, Gordana Rašić, João Viegas, Anthony J. Cornel, João Pinto, Gregory C. Lanzaro
The malaria vector Anopheles coluzzii is widespread across West Africa and is the sole vector species on the islands of São Tomé and Príncipe. Our interest in the population genetics of this species on these islands is part of an assessment of their suitability for a field trial involving the release of genetically engineered A. coluzzii. The engineered construct includes two genes that encode anti-Plasmodium peptides, along with a Cas9-based gene drive. We investigated gene flow among A. coluzzii subpopulations on each island to estimate dispersal rates between sites. Sampling covered the known range of A. coluzzii on both islands. Spatial autocorrelation suggests 7 km to be the likely extent of dispersal of this species, whereas estimates based on a convolutional neural network were roughly 3 km. This difference highlights the complexity of dispersal dynamics and the value of using multiple approaches. Our analysis also revealed weak heterogeneity among populations within each island but did identify areas weakly resistant or permissive of gene flow. Overall, A. coluzzii on each of the two islands exist as single Mendelian populations. We expect that a gene construct that includes a low-threshold gene drive and has minimal fitness impact should, once introduced, spread relatively unimpeded across each island.
疟疾病媒按蚊广泛分布于西非,是圣多美和普林西比群岛上唯一的病媒物种。我们之所以对这些岛屿上这一物种的种群遗传学感兴趣,是为了评估这些岛屿是否适合进行释放基因工程疟蚊的实地试验。该工程构建体包括两个编码抗疟原虫肽的基因,以及一个基于 Cas9 的基因驱动。我们调查了每个岛屿上 A. coluzzii 亚群之间的基因流动情况,以估计不同地点之间的扩散率。取样范围覆盖了两座岛屿上 A. coluzzii 的已知分布区。空间自相关性表明,该物种的扩散范围可能为 7 公里,而基于卷积神经网络的估计值约为 3 公里。这一差异凸显了扩散动态的复杂性和使用多种方法的价值。我们的分析还显示,每个岛屿上的种群之间存在微弱的异质性,但也确定了基因流动的微弱阻力区或容许区。总体而言,两个岛上的 A. coluzzii 都是单一的孟德尔种群。我们预计,包含低阈值基因驱动且对适应性影响最小的基因构建体一旦被引入,就会相对不受阻碍地在每个岛上传播。
{"title":"Patterns of Gene Flow in Anopheles coluzzii Populations From Two African Oceanic Islands","authors":"Melina Campos, Gordana Rašić, João Viegas, Anthony J. Cornel, João Pinto, Gregory C. Lanzaro","doi":"10.1111/eva.70044","DOIUrl":"10.1111/eva.70044","url":null,"abstract":"<p>The malaria vector <i>Anopheles coluzzii</i> is widespread across West Africa and is the sole vector species on the islands of São Tomé and Príncipe. Our interest in the population genetics of this species on these islands is part of an assessment of their suitability for a field trial involving the release of genetically engineered <i>A. coluzzii</i>. The engineered construct includes two genes that encode anti-Plasmodium peptides, along with a Cas9-based gene drive. We investigated gene flow among <i>A. coluzzii</i> subpopulations on each island to estimate dispersal rates between sites. Sampling covered the known range of <i>A. coluzzii</i> on both islands. Spatial autocorrelation suggests 7 km to be the likely extent of dispersal of this species, whereas estimates based on a convolutional neural network were roughly 3 km. This difference highlights the complexity of dispersal dynamics and the value of using multiple approaches. Our analysis also revealed weak heterogeneity among populations within each island but did identify areas weakly resistant or permissive of gene flow. Overall, <i>A. coluzzii</i> on each of the two islands exist as single Mendelian populations. We expect that a gene construct that includes a low-threshold gene drive and has minimal fitness impact should, once introduced, spread relatively unimpeded across each island.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 11","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-11-26","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11589655/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142724363","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}
Mingming Cui, Amanda D. Roe, Brian Boyle, Melody Keena, Yunke Wu, W. Evan Braswell, Michael T. Smith, Ben Gasman, Juan Shi, Marion Javal, Geraldine Roux, Jean J. Turgeon, Richard Hamelin, Ilga Porth
Biological invasions pose significant threats to ecological and economic stability, with invasive pests like the Asian longhorned beetle (Anoplophora glabripennis Motschulsky, ALB) causing substantial damage to forest ecosystems. Effective pest management relies on comprehensive knowledge of the insect's biology and invasion history. This study uses genomics to address these knowledge gaps and inform existing biosurveillance frameworks. We used 2768 genome-wide single nucleotide polymorphisms to compare invasive A. glabripennis populations in North America, using genomic variation to trace their sources of invasion and spread patterns, thereby refining our understanding of this species' invasion history. We found that most North American A. glabripennis infestations were distinct, resulting from multiple independent introductions from the native range. Following their introduction, all invasive populations experienced a genetic bottleneck which was followed by a population expansion, with a few also showing secondary spread to satellite infestations. Our study provides a foundation for a genome-based biosurveillance tool that can be used to clarify the origin of intercepted individuals, allowing regulatory agencies to strengthen biosecurity measures against this invasive beetle.
{"title":"Tracking the North American Asian Longhorned Beetle Invasion With Genomics","authors":"Mingming Cui, Amanda D. Roe, Brian Boyle, Melody Keena, Yunke Wu, W. Evan Braswell, Michael T. Smith, Ben Gasman, Juan Shi, Marion Javal, Geraldine Roux, Jean J. Turgeon, Richard Hamelin, Ilga Porth","doi":"10.1111/eva.70036","DOIUrl":"https://doi.org/10.1111/eva.70036","url":null,"abstract":"<p>Biological invasions pose significant threats to ecological and economic stability, with invasive pests like the Asian longhorned beetle (<i>Anoplophora glabripennis</i> Motschulsky, ALB) causing substantial damage to forest ecosystems. Effective pest management relies on comprehensive knowledge of the insect's biology and invasion history. This study uses genomics to address these knowledge gaps and inform existing biosurveillance frameworks. We used 2768 genome-wide single nucleotide polymorphisms to compare invasive <i>A. glabripennis</i> populations in North America, using genomic variation to trace their sources of invasion and spread patterns, thereby refining our understanding of this species' invasion history. We found that most North American <i>A. glabripennis</i> infestations were distinct, resulting from multiple independent introductions from the native range. Following their introduction, all invasive populations experienced a genetic bottleneck which was followed by a population expansion, with a few also showing secondary spread to satellite infestations. Our study provides a foundation for a genome-based biosurveillance tool that can be used to clarify the origin of intercepted individuals, allowing regulatory agencies to strengthen biosecurity measures against this invasive beetle.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 11","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-11-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70036","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142674211","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}
Sibelle Torres Vilaça, Jeronymo Dalapicolla, Renata Soares, Neiva Maria Robaldo Guedes, Cristina Y. Miyaki, Alexandre Aleixo
Estimates of current genetic diversity and population connectivity are especially important for endangered species that are subject to illegal harvesting and trafficking. Genetic monitoring can also ensure that management units are sustaining viable populations, while estimating genetic structure and population dynamics can influence genetic rescue efforts and reintroduction from captive breeding and confiscated animals. The Hyacinth Macaw (Anodorhynchus hyacinthinus) is a charismatic endangered species with a fragmented (allopatric) distribution. Using low coverage genomes, we aimed to investigate the dynamics across the remaining three large disjunct populations of Hyacinth Macaws in Brazil to inform conservation strategies. We obtained low coverage DNA data for 54 individuals from seven sampling sites. Our results showed that Hyacinth Macaws have four genetically structured clusters with relatively high levels of diversity. The Pantanal biome had two genetically distinct populations, with no obvious physical barriers that might explain this differentiation. We detected signs of gene flow between populations, with some geographical regions being more connected than others. Estimates of effective population size in the past million years of the species' evolutionary history showed a decline trend with the lowest Ne in all populations reached within the last few thousand years. Our findings suggest that populations from the Pantanal biome are key to connecting sites across its distribution, and maintaining the integrity of this habitat is important for protecting the species. Given the genetic structure found, we also highlight the need of conserving all wild populations to ensure the protection of the species' evolutionary potential.
对于遭受非法捕猎和贩运的濒危物种来说,当前遗传多样性和种群连通性的估计尤为重要。遗传监测还可以确保管理单位维持着可生存的种群,而对遗传结构和种群动态的估计则可以影响遗传拯救工作以及从人工繁殖和没收的动物中重新引入物种。风信子金刚鹦鹉(Anodorhynchus hyacinthinus)是一种极具魅力的濒危物种,分布零散(异地分布)。利用低覆盖率基因组,我们旨在调查巴西剩余的三个大型风信子金刚鹦鹉离散种群的动态,为保护策略提供信息。我们从七个采样点获得了 54 个个体的低覆盖率 DNA 数据。我们的研究结果表明,风信子金刚鹦鹉有四个具有相对较高多样性的基因结构群。潘塔纳尔生物群落有两个基因不同的种群,没有明显的物理障碍可以解释这种分化。我们发现了种群间基因流动的迹象,一些地理区域的联系比其他区域更紧密。在物种进化史的过去一百万年中,对有效种群数量的估计显示出下降趋势,所有种群的最低Ne值都是在过去几千年中达到的。我们的研究结果表明,来自潘塔纳尔生物群落的种群是连接其分布地的关键,保持这一栖息地的完整性对保护该物种非常重要。鉴于所发现的遗传结构,我们还强调了保护所有野生种群的必要性,以确保保护该物种的进化潜力。
{"title":"Prioritizing Conservation Areas for the Hyacinth Macaw (Anodorhynchus hyacinthinus) in Brazil From Low-Coverage Genomic Data","authors":"Sibelle Torres Vilaça, Jeronymo Dalapicolla, Renata Soares, Neiva Maria Robaldo Guedes, Cristina Y. Miyaki, Alexandre Aleixo","doi":"10.1111/eva.70039","DOIUrl":"https://doi.org/10.1111/eva.70039","url":null,"abstract":"<p>Estimates of current genetic diversity and population connectivity are especially important for endangered species that are subject to illegal harvesting and trafficking. Genetic monitoring can also ensure that management units are sustaining viable populations, while estimating genetic structure and population dynamics can influence genetic rescue efforts and reintroduction from captive breeding and confiscated animals. The Hyacinth Macaw (<i>Anodorhynchus hyacinthinus</i>) is a charismatic endangered species with a fragmented (allopatric) distribution. Using low coverage genomes, we aimed to investigate the dynamics across the remaining three large disjunct populations of Hyacinth Macaws in Brazil to inform conservation strategies. We obtained low coverage DNA data for 54 individuals from seven sampling sites. Our results showed that Hyacinth Macaws have four genetically structured clusters with relatively high levels of diversity. The Pantanal biome had two genetically distinct populations, with no obvious physical barriers that might explain this differentiation. We detected signs of gene flow between populations, with some geographical regions being more connected than others. Estimates of effective population size in the past million years of the species' evolutionary history showed a decline trend with the lowest <i>Ne</i> in all populations reached within the last few thousand years. Our findings suggest that populations from the Pantanal biome are key to connecting sites across its distribution, and maintaining the integrity of this habitat is important for protecting the species. Given the genetic structure found, we also highlight the need of conserving all wild populations to ensure the protection of the species' evolutionary potential.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 11","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-11-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/eva.70039","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142674308","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}
Martyna Lasek, Julia Zaborowska, Bartosz Łabiszak, Daniel J. Chmura, Witold Wachowiak
Scots pine is a crucial component of ecosystems in Europe and Asia and a major utility species that comprises more than 60% of total forest production in Poland. Despite its importance, the genetic relationships between key conservation and the commercial value of Scots pine ecotypes in Poland remain unclear. To address this problem, we analyzed 27 populations (841 trees) of the most valuable Polish Scots pine ecotypes, including the oldest natural stands in all 24 regions of provenance established for the species in the country. By examining maternally inherited mitochondrial markers, nuclear microsatellite loci, and thousands of SNP markers from a genotyping array, we evaluated the genetic structure between and within them. These multilevel genomic data revealed high genetic similarity and a homogeneous structure in most populations, suggesting a common historical origin and admixture of populations after the postglacial recolonization of Central Europe. This research presents novel data on existing genomic resources among local ecotypes defined within strictly managed Polish regions of provenance, challenging their validity. Formal tests of the progeny of seed stands are needed to check whether the diversity in adaptation and quantitative traits still supports the delineation of provenance regions. In parallel, the health status of selected populations and the viability of seeds from these regions should be monitored to detect early-stage symptoms of their environmental stress. It seems reasonable that periodic shortages of forest reproductive material (FRM) in a given region of provenance could be supplemented with the one from other regions that match their climatic envelope. Together, our results have important implications for the management of native Scots pine stands, particularly elite breeding populations, as they contribute to the discussion of the boundaries of provenance regions and the transfers of FRM that face increasing climate change.
苏格兰松是欧洲和亚洲生态系统的重要组成部分,也是波兰森林总产量 60% 以上的主要实用树种。尽管它非常重要,但波兰苏格兰松树生态型的关键保护和商业价值之间的遗传关系仍不清楚。为了解决这个问题,我们分析了波兰最有价值的苏格兰松树生态型的 27 个种群(841 棵树),其中包括波兰为该物种建立的所有 24 个产地区域中最古老的自然林分。通过研究母系遗传的线粒体标记、核微卫星位点以及基因分型阵列中的数千个 SNP 标记,我们评估了这些种群之间以及种群内部的遗传结构。这些多层次基因组数据揭示了大多数种群的高度遗传相似性和同质结构,表明中欧在冰川期后被重新殖民后,存在共同的历史起源和种群混杂。这项研究提供了在严格管理的波兰原产地区域内定义的当地生态型之间现有基因组资源的新数据,对其有效性提出了质疑。需要对种子群的后代进行正式测试,以检查适应性和数量性状的多样性是否仍然支持原产地区域的划分。与此同时,还应对这些地区所选种群的健康状况和种子的存活率进行监测,以发现其环境压力的早期症状。在某一特定产地,森林繁殖材料(FRM)的周期性短缺似乎是合理的,可以用符合其气候环境的其他地区的森林繁殖材料来补充。总之,我们的研究结果对本土苏格兰松林的管理,尤其是精英繁殖种群的管理具有重要意义,因为它们有助于讨论面临日益严重的气候变化的原产地区域边界和森林生殖材料的转移。
{"title":"Genomic Data Support the Revision of Provenance Regions Delimitation for Scots Pine","authors":"Martyna Lasek, Julia Zaborowska, Bartosz Łabiszak, Daniel J. Chmura, Witold Wachowiak","doi":"10.1111/eva.70038","DOIUrl":"10.1111/eva.70038","url":null,"abstract":"<p>Scots pine is a crucial component of ecosystems in Europe and Asia and a major utility species that comprises more than 60% of total forest production in Poland. Despite its importance, the genetic relationships between key conservation and the commercial value of Scots pine ecotypes in Poland remain unclear. To address this problem, we analyzed 27 populations (841 trees) of the most valuable Polish Scots pine ecotypes, including the oldest natural stands in all 24 regions of provenance established for the species in the country. By examining maternally inherited mitochondrial markers, nuclear microsatellite loci, and thousands of SNP markers from a genotyping array, we evaluated the genetic structure between and within them. These multilevel genomic data revealed high genetic similarity and a homogeneous structure in most populations, suggesting a common historical origin and admixture of populations after the postglacial recolonization of Central Europe. This research presents novel data on existing genomic resources among local ecotypes defined within strictly managed Polish regions of provenance, challenging their validity. Formal tests of the progeny of seed stands are needed to check whether the diversity in adaptation and quantitative traits still supports the delineation of provenance regions. In parallel, the health status of selected populations and the viability of seeds from these regions should be monitored to detect early-stage symptoms of their environmental stress. It seems reasonable that periodic shortages of forest reproductive material (FRM) in a given region of provenance could be supplemented with the one from other regions that match their climatic envelope. Together, our results have important implications for the management of native Scots pine stands, particularly elite breeding populations, as they contribute to the discussion of the boundaries of provenance regions and the transfers of FRM that face increasing climate change.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 11","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-11-15","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11568063/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142646285","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}
Charles A. Kwadha, Guillermo Rehermann, Deni Tasso, Simon Fellous, Marie Bengtsson, Erika A. Wallin, Adam Flöhr, Peter Witzgall, Paul G. Becher
The spotted-wing drosophila, Drosophila suzukii and the cosmopolitan vinegar fly D. melanogaster feed on soft fruit and berries and widely overlap in geographic range. The presence of D. melanogaster reduces egg-laying in D. suzukii, possibly because D. melanogaster outcompetes D. suzukii larvae feeding in the same fruit substrate. Flies use pheromones to communicate for mating, but pheromones also serve a role in reproductive isolation between related species. We asked whether a D. melanogaster pheromone also modulates oviposition behaviour in D. suzukii. A dual-choice oviposition assay confirms that D. suzukii lays fewer eggs on blueberries exposed to D. melanogaster flies and further shows that female flies have a stronger effect than male flies. This was corroborated by treating berries with synthetic pheromones. Avoidance of D. suzukii oviposition is mediated by the female D. melanogaster pheromone (Z)-4-undecenal (Z4-11Al). Significantly fewer eggs were laid on berries treated with synthetic Z4-11Al. In comparison, the male pheromone (Z)-11-octadecenyl acetate (cVA) had no effect on D. suzukii oviposition. Z4-11Al is a highly volatile compound that is perceived via olfaction and it is accordingly behaviourally active at a distance from the source. D. suzukii is known to engage in mutual niche construction with the yeast Hanseniaspora uvarum, which strongly attracts flies. Adding Z4-11Al to fermenting H. uvarum significantly decreased D. suzukii flight attraction in a laboratory wind tunnel and a field trapping assay. That a D. melanogaster pheromone regulates oviposition in D. suzukii demonstrates that heterospecific pheromone communication contributes to reproductive isolation and resource partitioning in cognate species. Stimulo-deterrent diversion or push-pull methods, building on combined use of attractant and deterrent compounds, have shown promise for control of D. suzukii. A pheromone that specifically reduces D. suzukii attraction and oviposition adds to the toolbox for D. suzukii integrated management.
斑翅果蝇(Drosophila suzukii)和世界性醋蝇(D. melanogaster)以软果和浆果为食,在地理分布上广泛重叠。D. melanogaster 的存在减少了 D. suzukii 的产卵量,这可能是因为 D. melanogaster 比在同一水果基质中取食的 D. suzukii 幼虫更具竞争力。苍蝇利用信息素进行交配交流,但信息素也在相关物种之间的生殖隔离中发挥作用。我们想知道一种 D. melanogaster 费洛蒙是否也能调节 D. suzukii 的产卵行为。一个双选择产卵试验证实,D. suzukii在暴露于D. melanogaster苍蝇的蓝莓上产卵较少,并进一步表明雌蝇比雄蝇有更强的影响。用合成信息素处理浆果也证实了这一点。雌性黑腹滨蝇信息素(Z)-4-十一烯醛(Z4-11Al)可促进避开铃木虫产卵。经合成 Z4-11Al 处理的浆果产卵量明显减少。相比之下,雄性信息素 (Z)-11- 十八烯基醋酸酯 (cVA) 对铃虫产卵没有影响。Z4-11Al 是一种高挥发性化合物,可通过嗅觉感知,因此在距离来源较远的地方也具有行为活性。众所周知,苏木蝇会与酵母菌 Hanseniaspora uvarum 共同构建生态位,后者能强烈吸引苍蝇。在实验室风洞和野外诱捕试验中,向发酵的 H. uvarum 中添加 Z4-11Al 能显著降低铃木蝇的飞行吸引力。一种D. melanogaster信息素能调节D. suzukii的产卵,这表明异种信息素交流有助于同源物种的生殖隔离和资源分配。结合使用引诱剂和威慑化合物的刺激-威慑转移或推拉方法已显示出控制铃木害虫的前景。一种信息素能专门减少苏云金蝇的引诱和产卵,为苏云金蝇的综合防治增添了新的手段。
{"title":"Sex Pheromone Mediates Resource Partitioning Between Drosophila melanogaster and D. suzukii","authors":"Charles A. Kwadha, Guillermo Rehermann, Deni Tasso, Simon Fellous, Marie Bengtsson, Erika A. Wallin, Adam Flöhr, Peter Witzgall, Paul G. Becher","doi":"10.1111/eva.70042","DOIUrl":"10.1111/eva.70042","url":null,"abstract":"<p>The spotted-wing drosophila, <i>Drosophila suzukii</i> and the cosmopolitan vinegar fly <i>D. melanogaster</i> feed on soft fruit and berries and widely overlap in geographic range. The presence of <i>D. melanogaster</i> reduces egg-laying in <i>D. suzukii</i>, possibly because <i>D. melanogaster</i> outcompetes <i>D. suzukii</i> larvae feeding in the same fruit substrate. Flies use pheromones to communicate for mating, but pheromones also serve a role in reproductive isolation between related species. We asked whether a <i>D. melanogaster</i> pheromone also modulates oviposition behaviour in <i>D. suzukii</i>. A dual-choice oviposition assay confirms that <i>D. suzukii</i> lays fewer eggs on blueberries exposed to <i>D. melanogaster</i> flies and further shows that female flies have a stronger effect than male flies. This was corroborated by treating berries with synthetic pheromones. Avoidance of <i>D. suzukii</i> oviposition is mediated by the female <i>D. melanogaster</i> pheromone (<i>Z</i>)-4-undecenal (Z4-11Al). Significantly fewer eggs were laid on berries treated with synthetic Z4-11Al. In comparison, the male pheromone (<i>Z</i>)-11-octadecenyl acetate (cVA) had no effect on <i>D. suzukii</i> oviposition. Z4-11Al is a highly volatile compound that is perceived via olfaction and it is accordingly behaviourally active at a distance from the source. <i>D. suzukii</i> is known to engage in mutual niche construction with the yeast <i>Hanseniaspora uvarum</i>, which strongly attracts flies. Adding Z4-11Al to fermenting <i>H. uvarum</i> significantly decreased <i>D. suzukii</i> flight attraction in a laboratory wind tunnel and a field trapping assay. That a <i>D. melanogaster</i> pheromone regulates oviposition in <i>D. suzukii</i> demonstrates that heterospecific pheromone communication contributes to reproductive isolation and resource partitioning in cognate species. Stimulo-deterrent diversion or push-pull methods, building on combined use of attractant and deterrent compounds, have shown promise for control of <i>D. suzukii</i>. A pheromone that specifically reduces <i>D. suzukii</i> attraction and oviposition adds to the toolbox for <i>D. suzukii</i> integrated management.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 11","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-11-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11555161/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142613207","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}
Brian D. Taras, Paul B. Conn, Mark V. Bravington, Andrzej Kilian, Aimée R. Lang, Anna Bryan, Raphaela Stimmelmayr, Lori Quakenbush
Reliable estimates of population abundance and demographics are essential for managing harvested species. Ice-associated phocids, “ice seals,” are a vital resource for subsistence-dependent coastal Native communities in western and northern Alaska, USA. In 2012, the Beringia distinct population segment of the bearded seal, Erignathus barbatus nauticus, was listed as “threatened” under the US Endangered Species Act requiring greater scrutiny for management assessments. We sought to estimate requisite population parameters from harvested seals by using close-kin mark-recapture (CKMR) methods, the first such application for marine mammals. Samples from 1758 bearded seals harvested by Bering, Chukchi, and Beaufort Sea communities during 1998–2020 were genotyped, genetically sexed, and aged by tooth annuli. After rigorous quality control, kin relationships were established for 1484 seals including two parent–offspring pairs (POPs) and 25 potential second-order kin pairs. Most of the second-order kin were half-sibling pairs (HSPs), but four were potential grandparent-grandchild pairs (GGPs). There were no full sibling pairs, suggesting a lack of mate fidelity. Mitochondrial DNA analysis identified 17 potential HSPs as paternally related, providing substantial evidence of persistent heterogeneity in reproductive success among adult males. The statistical CKMR model incorporates probabilities associated with POPs, HSPs, and GGPs and assumes known ages and a stable population. Our top model accommodates heterogeneity in adult male breeding success and yields an abundance estimate of ~409,000 with a coefficient of variation (CV) = 0.35, which is substantially greater than the “non-heterogeneity” model estimate of ~232,000 (CV = 0.21), an important difference for managing a harvested species. Using CKMR methods with harvested species provides estimates of abundance with the added opportunity to acquire information about adult survival, fecundity, and breeding success that could be applied to other species of concern, marine and terrestrial.
{"title":"Estimating Demographic Parameters for Bearded Seals, Erignathus barbatus, in Alaska Using Close-Kin Mark-Recapture Methods","authors":"Brian D. Taras, Paul B. Conn, Mark V. Bravington, Andrzej Kilian, Aimée R. Lang, Anna Bryan, Raphaela Stimmelmayr, Lori Quakenbush","doi":"10.1111/eva.70035","DOIUrl":"10.1111/eva.70035","url":null,"abstract":"<p>Reliable estimates of population abundance and demographics are essential for managing harvested species. Ice-associated phocids, “ice seals,” are a vital resource for subsistence-dependent coastal Native communities in western and northern Alaska, USA. In 2012, the Beringia distinct population segment of the bearded seal, <i>Erignathus barbatus nauticus</i>, was listed as “threatened” under the US Endangered Species Act requiring greater scrutiny for management assessments. We sought to estimate requisite population parameters from harvested seals by using close-kin mark-recapture (CKMR) methods, the first such application for marine mammals. Samples from 1758 bearded seals harvested by Bering, Chukchi, and Beaufort Sea communities during 1998–2020 were genotyped, genetically sexed, and aged by tooth annuli. After rigorous quality control, kin relationships were established for 1484 seals including two parent–offspring pairs (POPs) and 25 potential second-order kin pairs. Most of the second-order kin were half-sibling pairs (HSPs), but four were potential grandparent-grandchild pairs (GGPs). There were no full sibling pairs, suggesting a lack of mate fidelity. Mitochondrial DNA analysis identified 17 potential HSPs as paternally related, providing substantial evidence of persistent heterogeneity in reproductive success among adult males. The statistical CKMR model incorporates probabilities associated with POPs, HSPs, and GGPs and assumes known ages and a stable population. Our top model accommodates heterogeneity in adult male breeding success and yields an abundance estimate of ~409,000 with a coefficient of variation (CV) = 0.35, which is substantially greater than the “non-heterogeneity” model estimate of ~232,000 (CV = 0.21), an important difference for managing a harvested species. Using CKMR methods with harvested species provides estimates of abundance with the added opportunity to acquire information about adult survival, fecundity, and breeding success that could be applied to other species of concern, marine and terrestrial.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 11","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-11-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11549065/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142613198","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}
Francisco Encinas-Viso, Peter H. Thrall, Andrew G. Young
Habitat fragmentation and the acceleration of environmental change threaten the survival of many plant species. The problem is especially pronounced for plant species with self-incompatibility mating systems, which are obligate outcrossers, thus requiring high mate availability to persist. In such situations, plant populations suffering decreased fitness could be rescued by: (a) improving local habitat conditions (habitat rescue), (b) increasing the number of individuals (demographic rescue), or (c) introducing new genetic variation (genetic rescue). In this study, we used a spatially and genetically explicit individual-based model to approximate the demography of a small (N = 250) isolated self-incompatible population using a timescale of 500 years. Using this model, we quantified the effectiveness of the different types of rescues described above, singly and in combination. Our results show that individual genetic rescue is the most effective type of rescue with respect to improving fitness and population viability. However, we found that introducing a high number of individuals (N > 30) to a small population (N = 50) at the brink of extinction through demographic rescue can also have a positive effect on viability, improving average fitness by 55% compared to introducing a low number of individuals (N = 10) over a long timescale (> 500 years). By itself, habitat rescue showed the lowest effects on viability. However, combining genetic and habitat rescue provided the best results overall, increasing both persistence (> 30%) and mate availability (> 50%). Interestingly, we found that the addition of even a small number of new S alleles (20%) can be highly beneficial to increase mate availability and persistence. We conclude that genetic rescue through the introduction of new S alleles and an increase in habitat suitability is the best management strategy to improve mate availability and population viability of small isolated SI plant populations to overcome the effects of demographic stochasticity and positive density dependence.
栖息地的破碎化和环境变化的加速威胁着许多植物物种的生存。对于具有自交不亲和交配系统的植物物种来说,这个问题尤为突出,因为这些物种是强制性外交动物,因此需要有大量的配偶才能生存下去。在这种情况下,可以通过以下方法拯救健康状况下降的植物种群:(a) 改善当地的生境条件(生境拯救),(b) 增加个体数量(人口拯救),或 (c) 引入新的遗传变异(遗传拯救)。在这项研究中,我们使用了一个基于个体的空间和遗传显式模型,以 500 年的时间尺度来近似计算一个小型(N = 250)孤立自相容种群的人口统计。利用该模型,我们对上述不同类型的拯救措施(单独或组合)的有效性进行了量化。我们的研究结果表明,就提高适应性和种群存活率而言,个体基因拯救是最有效的拯救类型。然而,我们发现,通过人口救援为一个濒临灭绝的小种群(N = 50)引入大量个体(N > 30)也能对生存能力产生积极影响,与引入少量个体(N = 10)相比,在较长的时间尺度内(> 500 年),平均适应性提高了 55%。栖息地拯救本身对生存能力的影响最小。然而,将基因拯救和栖息地拯救结合在一起,总体效果最好,持续性(> 30%)和配偶可用性(> 50%)都有所提高。有趣的是,我们发现,即使增加少量新的 S 等位基因(20%),对提高交配率和持续性也非常有益。我们的结论是,通过引入新的 S 等位基因和提高栖息地适宜性来进行遗传拯救,是提高小型孤立 SI 植物种群的配偶可得性和种群存活率以克服人口随机性和正密度依赖性影响的最佳管理策略。
{"title":"Genetic and Habitat Rescue Improve Population Viability in Self-Incompatible Plants","authors":"Francisco Encinas-Viso, Peter H. Thrall, Andrew G. Young","doi":"10.1111/eva.70037","DOIUrl":"10.1111/eva.70037","url":null,"abstract":"<p>Habitat fragmentation and the acceleration of environmental change threaten the survival of many plant species. The problem is especially pronounced for plant species with self-incompatibility mating systems, which are obligate outcrossers, thus requiring high mate availability to persist. In such situations, plant populations suffering decreased fitness could be rescued by: (a) improving local habitat conditions (habitat rescue), (b) increasing the number of individuals (demographic rescue), or (c) introducing new genetic variation (genetic rescue). In this study, we used a spatially and genetically explicit individual-based model to approximate the demography of a small (<i>N</i> = 250) isolated self-incompatible population using a timescale of 500 years. Using this model, we quantified the effectiveness of the different types of rescues described above, singly and in combination. Our results show that individual genetic rescue is the most effective type of rescue with respect to improving fitness and population viability. However, we found that introducing a high number of individuals (<i>N</i> > 30) to a small population (<i>N</i> = 50) at the brink of extinction through demographic rescue can also have a positive effect on viability, improving average fitness by 55% compared to introducing a low number of individuals (<i>N</i> = 10) over a long timescale (> 500 years). By itself, habitat rescue showed the lowest effects on viability. However, combining genetic and habitat rescue provided the best results overall, increasing both persistence (> 30%) and mate availability (> 50%). Interestingly, we found that the addition of even a small number of new S alleles (20%) can be highly beneficial to increase mate availability and persistence. We conclude that genetic rescue through the introduction of new S alleles and an increase in habitat suitability is the best management strategy to improve mate availability and population viability of small isolated SI plant populations to overcome the effects of demographic stochasticity and positive density dependence.</p>","PeriodicalId":168,"journal":{"name":"Evolutionary Applications","volume":"17 11","pages":""},"PeriodicalIF":3.5,"publicationDate":"2024-11-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11549066/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142613203","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}