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Improved robustness to gene tree incompleteness, estimation errors, and systematic homology errors with weighted TREE-QMC
IF 6.5 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2025-02-26 DOI: 10.1093/sysbio/syaf009
Yunheng Han, Erin K Molloy
Summary methods are widely used to reconstruct species trees from gene tres while accommodating discordance from incomplete lineage sorting; however, it is increasingly recognized that their accuracy can be negatively impacted by incomplete and/or error-ridden gene trees. To address the latter, Zhang and Mirarab (2022) updated the popular summary method ASTRAL so that it weights quartets based on gene tree branch lengths and support values. The implementation of these weighting schemes presented computational challenges, leading Zhang and Mirarab (2022) to replace ASTRAL’s original algorithm (i.e., computing an exact solution within a constrained search space) in favor of search heuristics based on phylogenetic placement. Here, we show that these weighting schemes can be effectively leveraged within the Quartet Max Cut framework of Snir and Rao (2010), introducing weighted TREE-QMC. The incorporation of weighting schemes into TREE-QMC required only a small increase in time complexity compared to the unweighted algorithm; fortunately, the increase in runtime was also small, behaving more like a constant factor in our simulation study. Moreover, weighted TREE-QMC was fast and highly competitive with weighted ASTRAL, even outperforming it in terms of species tree accuracy on some challenging simulation conditions, such as large numbers of taxa. In reanalyzing two avian data sets, we found that weighting quartets by gene tree branch lengths can improve robustness to systematic homology errors and can be as effective as removing the impacted taxa from individual gene trees or removing the impacted gene trees entirely. Lastly, our study revealed that TREE-QMC was robust to extreme rates of missing taxa, suggesting its utility as a supertree method. Source code for weighted TREE-QMC is available on Github: (https://github.com/molloy-lab/TREE-QMC)
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引用次数: 0
Repeated Evolution of Storage Root and Invasions of Alpine Biome Drove Replicated Radiations of the Megadiverse Corydalis (Papaveraceae) in the Qinghai-Tibet Plateau.
IF 6.1 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2025-02-20 DOI: 10.1093/sysbio/syaf014
Huan-Wen Peng, Yuan-Yuan Ling, Kun-Li Xiang, Andrey S Erst, Xiao-Qian Li, Lian Lian, Bing Liu, Tatyana V Erst, Rosa Del C Ortiz, Florian Jabbour, Wei Wang

The interplay of key innovation and ecological opportunity is commonly recognized to be the catalyst for rapid radiation. Underground storage organs (USOs), as a vital ecological trait, are advantageous for adaptation of plants to extreme environments, but receive less attention compared to aboveground organs. Repeated evolution of various USOs has occurred across the plant tree of life. However, whether repeated occurrences of a USO in different clades of a group can promote its replicated radiations in combination with the invasion of similar environments remains poorly known. Corydalis is a megadiverse genus in Papaveraceae and exhibits remarkable variations in USO morphology and biome occupancy. Here, we first generated a robust phylogeny for Corydalis with wide taxonomic and genomic coverage based on plastome and nuclear ribosomal DNA sequence data. By dating the branching events, reconstructing ancestral ranges, evaluating diversification dynamics, and inferring evolutionary patterns of USOs and biomes and their correlations, we then tested whether the interplay of USO evolution and biome shifts has driven rapid diversification of some Corydalis lineages. Our results indicate that Corydalis began to diversify in the Qinghai-Tibet Plateau (QTP) at ca. 41 Ma, and 88% of dispersals happened through forests, suggesting that forests served as important dispersal corridors for range expansion of the genus. The storage root has originated independently at least six times in Corydalis since the Miocene, and its acquisition could have operated as a key innovation towards the adaptation to the alpine biome in the QTP. Repeated evolution of this game-changing trait and invasions of alpine biome, in combination with geoclimatic changes, could have jointly driven independent radiations of the two clades of Corydalis in the QTP at ca. 6 Ma. Our study provides new insights into the joint contribution of USO repeated evolution and biome shifts to replicated radiations, hence increasing our ability to predict evolutionary trajectories in plants facing similar environmental pressures. [Biome shift; diversification rates; Papaveraceae; phylogenomics; Qinghai-Tibet Plateau; underground storage organs.].

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引用次数: 0
Recent, Intricate Speciation in Amazonia Uncovered by a Multilayered Genomic Analysis of Tree Squirrels
IF 6.5 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2025-02-18 DOI: 10.1093/sysbio/syaf013
Edson F Abreu, Joyce R Prado, Jesús E Maldonado, Don E Wilson, Alexandre R Percequillo, Silvia E Pavan
Accurate estimates of species diversity are essential for all biodiversity research. Delimiting species and understanding the underlying processes of speciation are also central components of systematic biology that frame our comprehension of the evolutionary mechanisms generating biodiversity. The South American tree squirrels (genus Guerlinguetus) are keystone mammals, widely distributed, that are critical in tree-seed predation and dispersal in one of the most fragile and threated ecosystems of the world, the tropical rainforests of South America. We obtained genomic data (ultraconserved elements and single nucleotide polymorphisms) to explore alternative hypotheses on species limits of this genus and to clarify recent and rapid speciation on continental-scale and dynamically evolving landscapes. Using a multilayered genomic approach that integrates fine-scale population genetic analyses with quantitative molecular species delimitation methods, we observed that (i) the most likely number of species within Guerlinguetus is six, contrasting with both classic morphological revision and mitochondrial species delimitation; (ii) incongruencies in species relationships still persist, which might be a response to population migration and gene flow taking place in the lowlands of eastern Amazonia and/or to the extremely rapid successive speciation events; and (iii) effective migration surfaces detected important geographic barriers associated with the major Amazonian riverine systems and the mountain ranges of the Guiana Shield. In conclusion, we uncovered unexpected and higher species diversity on Guerlinguetus and corroborate recent findings suggesting that much of the extant species-level diversity in Amazonia is young, dating back to the Quaternary. We also reinforce long-established hypotheses on the role of rivers and climate-driven forest dynamics in triggering Amazonian speciation. [gene flow; Guerlinguetus; migration; mito-nuclear discordance; Neotropics; quantitative species delimitation; Sciuridae; ultraconserved elements]
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引用次数: 0
Global Patterns of Taxonomic Uncertainty and its Impacts on Biodiversity Research
IF 6.5 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2025-02-15 DOI: 10.1093/sysbio/syaf010
Jhonny J M Guedes, Mario R Moura, Lucas Jardim, José Alexandre F Diniz-Filho
Over two million species have been named so far, but many will be invalidated due to redundant descriptions. Undetected invalid species (i.e., synonyms) can impair inferences we make in biodiversity research and hamper the implementation of effective conservation strategies. However, the processes leading to the accumulation of invalid names remain largely unknown. Using multi-model inferences, we investigated the patterns and potential drivers of species- and assemblage-level variation in synonym counts across terrestrial vertebrates globally. We also explored how taxonomic uncertainty (i.e., instability in species identities) can affect latitudinal variation of diversification rates. The average number of synonyms was higher for species described earlier, better represented in scientific collections, with larger geographic ranges, occurring in temperate regions, and in areas of high biodiversity attention. In assemblage-level models, a higher average number of synonyms was associated with temperate regions harbouring more early-described species. Areas of high endemism richness showed fewer synonyms across amphibians and reptiles but had an inverse effect for birds and mammals. Other predictor-response relationships varied across taxonomic groups, biogeographical realm, and spatial grain. Assuming that more synonyms indicate more stable species that have been thoroughly studied and reviewed, high synonym numbers in temperate species and assemblages support claims of a potential latitudinal taxonomy gradient, where geographic variation in taxonomic practice could hinder the proper recognition of tropical species. We show that the accumulation of invalid names is not random and discuss how invalid hidden names can affect biodiversity inferences. A potential approach to address this problem would be developing a taxonomic uncertainty metric that could be incorporated into models (i.e., as weights to account for varying degrees of uncertainty during the fitting process). Our study provides an initial approximation and highlights the often-neglected issue of uncertainty and instability in species identities from a macroecological perspective.
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引用次数: 0
UnFATE: A Comprehensive Probe Set and Bioinformatics Pipeline for Phylogeny Reconstruction and Multilocus Barcoding of Filamentous Ascomycetes (Ascomycota, Pezizomycotina)
IF 6.5 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2025-02-15 DOI: 10.1093/sysbio/syaf011
Claudio G Ametrano, Jacob Jensen, H Thorsten Lumbsch, Felix Grewe
The subphylum Pezizomycotina (filamentous ascomycetes) is the largest clade within Ascomycota. Despite the importance of this group of fungi, our understanding of their evolution is still limited due to insufficient taxon sampling. Although next-generation sequencing technology allows us to obtain complete genomes for phylogenetic analyses, generating complete genomes of fungal species can be challenging, especially when fungi occur in symbiotic relationships or when the DNA of rare herbarium specimens is degraded or contaminated. Additionally, assembly, annotation, and gene extraction of whole-genome sequencing data require bioinformatics skills and computational power, resulting in a substantial data burden. To overcome these obstacles, we designed a universal target enrichment probe set to reconstruct the phylogenetic relationships of filamentous ascomycetes at different phylogenetic levels. From a pool of single-copy orthologous genes extracted from available Pezizomycotina genomes, we identified the smallest subset of genetic markers that can reliably reconstruct a robust phylogeny. We used a clustering approach to identify a sequence set that could provide an optimal trade-off between potential missing data and probe set cost. We incorporated this probe set into a user-friendly wrapper script named UnFATE (https://github.com/claudioametrano/UnFATE) that allows phylogenomic inferences without requiring expert bioinformatics knowledge. In addition to phylogenetic results, the software provides a powerful multilocus alternative to ITS-based barcoding. Phylogeny and barcoding approaches can be complemented by an integrated, pre-processed, and periodically updated database of all publicly available Pezizomycotina genomes. The UnFATE pipeline, using the 195 selected marker genes, consistently performed well across various phylogenetic depths, generating trees consistent with the reference phylogenomic inferences. The topological distance between the reference trees from literature and the best tree produced by UnFATE ranged between 0.10 and 0.14 (nRF) for phylogenies from family to subphylum level. We also tested the in vitro success of the universal baits set in a target capture approach on 25 herbarium specimens from ten representative classes in Pezizomycotina, which recovered a topology congruent with recent phylogenomic inferences for this group of fungi. The discriminating power of our gene set was also assessed by the multilocus barcoding approach, which outperformed the barcoding approach based on ITS. With these tools, we aim to provide a framework for a collaborative approach to build robust, conclusive phylogenies of this important fungal clade.
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引用次数: 0
The consequences of budding speciation on trees
IF 6.5 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2025-02-12 DOI: 10.1093/sysbio/syaf012
C Tomomi Parins-Fukuchi, James G Saulsbury
Paleobiologists have long sought to explain how alternative modes of speciation, including budding and bifurcating cladogenesis, shape patterns of evolution. Methods introduced over the past decade have paved the way for a renewed enthusiasm for exploring modes of speciation in the fossil record. However, the field does not yet have a strong intuition for how ancestor-descendant relationships, especially those that arise from budding speciation, might influence the shape of trees reconstructed for fossil or living clades. We developed a simulation approach based on classic paleobiological theory to ask what proportion of ancestral nodes in paleontological phylogenies are expected to correspond to sampled taxa under a range of preservational regimes. We compared our simulated results to empirical estimates of absolute fossil record completeness gathered from the literature and found that many fossilized clades of marine invertebrates are likely to display upwards of 80% sampled ancestors. Under a primarily budding model, phylogenies where 100% of the internal nodes correspond to named species are very possible for well-sampled clades at local and regional scales. We also leveraged our simulation approach to ask how budding might shape extant clades. We found that the ancestral signature of budding causes rampant hard polytomies (i.e., multifurcations), greatly impacting the shape of extant clades. Our results highlight how budding can yield dramatic and unrecognized effects on phylogenetic reconstruction of clades of both living and extinct organisms.
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引用次数: 0
The Fossilized Birth-Death Model Is Identifiable. 化石化的出生-死亡模型是可识别的。
IF 6.1 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2025-02-10 DOI: 10.1093/sysbio/syae058
Kate Truman, Timothy G Vaughan, Alex Gavryushkin, Alexandra Sasha Gavryushkina

Time-dependent birth-death sampling models have been used in numerous studies to infer past evolutionary dynamics in different biological contexts, for example,  speciation and extinction rates in macroevolutionary studies, or effective reproductive number in epidemiological studies. These models are branching processes where lineages can bifurcate, die, or be sampled with time-dependent birth, death, and sampling rates, generating phylogenetic trees. It has been shown that in some subclasses of such models, different sets of rates can result in the same distributions of reconstructed phylogenetic trees, and therefore, the rates become unidentifiable from the trees regardless of their size. Here, we show that widely used time-dependent fossilized birth-death (FBD) models are identifiable. This subclass of models makes more realistic assumptions about the fossilization process and certain infectious disease transmission processes than the unidentifiable birth-death sampling models. Namely, FBD models assume that sampled lineages stay in the process rather than being immediately removed upon sampling. The identifiability of the time-dependent FBD model justifies using statistical methods that implement this model to infer the underlying temporal diversification or epidemiological dynamics from phylogenetic trees or directly from molecular or other comparative data. We further show that the time-dependent FBD model with an extra parameter, the removal after sampling probability, is unidentifiable. This implies that in scenarios where we do not know how sampling affects lineages, we are unable to infer this extra parameter together with birth, death, and sampling rates solely from trees.

依赖时间的出生-死亡采样模型已被大量研究用于推断不同生物背景下过去的进化动态,例如宏观进化研究中的物种分化和灭绝率,或流行病学研究中的有效繁殖数量。这些模型是一个分支过程,在这个过程中,世系可以分叉、死亡,或以随时间变化的出生率、死亡率和采样率进行采样,从而生成系统进化树。有研究表明,在这类模型的某些子类中,不同的速率集会导致重建的系统发生树分布相同,因此,无论系统发生树的大小如何,速率都无法从系统发生树中识别出来。在这里,我们证明了广泛使用的时间依赖化石出生-死亡(FBD)模型是可识别的。与无法识别的出生-死亡抽样模型相比,这一子类模型对化石化过程和某些传染病的传播过程做出了更现实的假设。也就是说,FBD 模型假定采样的世系会留在化石过程中,而不是在采样后立即消失。时间依赖性 FBD 模型的可识别性使我们有理由使用实现该模型的统计方法,从系统发生树或直接从分子或其他比较数据中推断潜在的时间多样化或流行病学动态。我们进一步证明,具有额外参数(取样后移除概率)的时间依赖性化石出生-死亡模型是不可识别的。这意味着,在我们不知道采样如何影响世系的情况下,我们无法仅从树中推断出这个额外参数以及出生率、死亡率和采样率。
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引用次数: 0
Complex Models of Sequence Evolution Improve Fit, But Not Gene Tree Discordance, for Tetrapod Mitogenomes. 序列进化的复杂模型改善了四足有丝分裂基因组的拟合度,但没有改善基因树的不一致性。
IF 6.1 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2025-02-10 DOI: 10.1093/sysbio/syae056
Benjamin S Toups, Robert C Thomson, Jeremy M Brown

Variation in gene tree estimates is widely observed in empirical phylogenomic data and is often assumed to be the result of biological processes. However, a recent study using tetrapod mitochondrial genomes to control for biological sources of variation due to their haploid, uniparentally inherited, and non-recombining nature found that levels of discordance among mitochondrial gene trees were comparable to those found in studies that assume only biological sources of variation. Additionally, they found that several of the models of sequence evolution chosen to infer gene trees were doing an inadequate job of fitting the sequence data. These results indicated that significant amounts of gene tree discordance in empirical data may be due to poor fit of sequence evolution models and that more complex and biologically realistic models may be needed. To test how the fit of sequence evolution models relates to gene tree discordance, we analyzed the same mitochondrial data sets as the previous study using 2 additional, more complex models of sequence evolution that each include a different biologically realistic aspect of the evolutionary process: A covarion model to incorporate site-specific rate variation across lineages (heterotachy), and a partitioned model to incorporate variable evolutionary patterns by codon position. Our results show that both additional models fit the data better than the models used in the previous study, with the covarion being consistently and strongly preferred as tree size increases. However, even these more preferred models still inferred highly discordant mitochondrial gene trees, thus deepening the mystery around what we label the "Mito-Phylo Paradox" and leading us to ask whether the observed variation could, in fact, be biological in nature after all.

在经验性的系统发生组数据中,基因树估计值的变异被广泛观察到,并且通常被认为是生物过程的结果。然而,最近一项使用四足动物线粒体基因组来控制生物变异来源的研究发现,线粒体基因树之间的不一致程度与仅假定生物变异来源的研究中发现的不一致程度相当。此外,他们还发现,用于推断基因树的几个序列进化模型与序列数据的拟合程度不够。这些结果表明,经验数据中存在的大量基因树不一致现象可能是由于序列进化模型的拟合效果不佳造成的,因此可能需要更复杂、更符合生物学实际的模型。为了检验序列进化模型的拟合度与基因树不一致性之间的关系,我们使用了两个额外的、更复杂的序列进化模型来分析与前一项研究相同的线粒体数据集,这两个模型分别包含了进化过程中不同的生物学现实方面:一个是科瓦里翁模型(covarion model),它包含了不同世系中特定位点的速率变化(heterotachy);另一个是分区模型(partitioned model),它包含了不同密码子位置的进化模式。我们的研究结果表明,这两个额外的模型都比之前研究中使用的模型更适合数据,随着树规模的增加,共线性模型一直是首选。然而,即使是这些更受青睐的模型,仍然推断出了高度不和谐的线粒体基因树,从而加深了我们所称的 "Mito-Phylo 悖论 "的神秘性,并使我们提出了这样一个问题:所观察到的变异实际上是否具有生物学性质?
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引用次数: 0
Phylogenomics of Bivalvia Using Ultraconserved Elements Reveal New Topologies for Pteriomorphia and Imparidentia. 使用超保守元素(UCEs)的双壳类系统发生组学揭示了翼手目和翼手目的新拓扑结构。
IF 6.1 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2025-02-10 DOI: 10.1093/sysbio/syae052
Yi-Xuan Li, Jack Chi-Ho Ip, Chong Chen, Ting Xu, Qian Zhang, Yanan Sun, Pei-Zhen Ma, Jian-Wen Qiu

Despite significant advances in phylogenetics over the past decades, the deep relationships within Bivalvia (phylum Mollusca) remain inconclusive. Previous efforts based on morphology or several genes have failed to resolve many key nodes in the phylogeny of Bivalvia. Advances have been made recently using transcriptome data, but the phylogenetic relationships within Bivalvia historically lacked consensus, especially within Pteriomorphia and Imparidentia. Here, we inferred the relationships of key lineages within Bivalvia using matrices generated from specifically designed ultraconserved elements (UCEs) with 16 available genomic resources and 85 newly sequenced specimens from 55 families. Our new probes (Bivalve UCE 2k v.1) for target sequencing captured an average of 849 UCEs with 1085 bp in mean length from in vitro experiments. Our results introduced novel schemes from 6 major clades (Protobranchina, Pteriomorphia, Palaeoheterodonta, Archiheterodonta, Anomalodesmata, and Imparidentia), though some inner nodes were poorly resolved, such as paraphyletic Heterodonta in some topologies potentially due to insufficient taxon sampling. The resolution increased when analyzing specific matrices for Pteriomorphia and Imparidentia. We recovered 3 Pteriomorphia topologies different from previously published trees, with the strongest support for ((Ostreida + (Arcida + Mytilida)) + (Pectinida + (Limida + Pectinida))). Limida were nested within Pectinida, warranting further studies. For Imparidentia, our results strongly supported the new hypothesis of (Galeommatida + (Adapedonta + Cardiida)), while the possible non-monophyly of Lucinida was inferred but poorly supported. Overall, our results provide important insights into the phylogeny of Bivalvia and show that target enrichment sequencing of UCEs can be broadly applied to study both deep and shallow phylogenetic relationships.

尽管过去几十年来系统发生学取得了重大进展,但双壳纲动物(软体动物门)内部的深层关系仍未确定。以前基于形态学或几个基因的研究未能解决双壳纲系统发育中的许多关键节点。最近,利用转录组数据的研究取得了进展,但双壳纲的系统发育关系历来缺乏共识,尤其是翼手目(Pteriomorphia)和栉水母目(Imparidentia)的系统发育关系。在此,我们利用专门设计的超保守元素(UCEs)矩阵,结合 16 个可用的基因组资源和 55 个科的 85 个新测序标本,推断了双壳纲内关键种系的关系。我们用于目标测序的新探针(Bivalve UCE 2k v.1)从体外实验中平均捕获了 849 个 UCE,平均长度为 1085-bp。我们的研究结果引入了来自六个主要支系(原枝目、翼手目、古翼手目、古翼手目、无尾目和无尾目)的新方案,但一些内部节点的解析度较低,如一些拓扑结构中的旁支系异齿目(Heterodonta),这可能是由于分类群取样不足造成的。在分析翼手目和翼手目的特定矩阵时,分辨率有所提高。我们发现了三种不同于以前发表的翼手目拓扑结构,其中((Ostreida + (Arcida + Mytilida)) + (Pectinida + (Limida + Pectinida))支持度最高。)Limida 嵌套在 Pectinida 中,值得进一步研究。对于无尾目(Imparidentia),我们的结果有力地支持了(Galeommatida + (Adapedonta + Cardiida))的新假说,而推断出了 Lucinida 的可能非单系,但支持度不高。总之,我们的研究结果为双壳纲的系统发育提供了重要的见解,并表明 UCEs 的目标富集测序可广泛应用于研究深层和浅层的系统发育关系。
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引用次数: 0
How to Validate a Bayesian Evolutionary Model. 如何验证贝叶斯进化模型。
IF 6.1 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2025-02-10 DOI: 10.1093/sysbio/syae064
Fábio K Mendes, Remco Bouckaert, Luiz M Carvalho, Alexei J Drummond

Biology has become a highly mathematical discipline in which probabilistic models play a central role. As a result, research in the biological sciences is now dependent on computational tools capable of carrying out complex analyses. These tools must be validated before they can be used, but what is understood as validation varies widely among methodological contributions. This may be a consequence of the still embryonic stage of the literature on statistical software validation for computational biology. Our manuscript aims to advance this literature. Here, we describe, illustrate, and introduce new good practices for assessing the correctness of a model implementation with an emphasis on Bayesian methods. We also introduce a suite of functionalities for automating validation protocols. It is our hope that the guidelines presented here help sharpen the focus of discussions on (as well as elevate) expected standards of statistical software for biology.

生物学已成为一门高度数学化的学科,其中概率模型发挥着核心作用。因此,生物科学研究现在依赖于能够进行复杂分析的计算工具。这些工具在使用之前必须经过验证,但对验证的理解却因方法论的不同而大相径庭。这可能是计算生物学统计软件验证文献仍处于萌芽阶段的结果。我们的手稿旨在推动这一文献的发展。在这里,我们描述、说明并介绍了评估模型实现正确性的新的良好实践,重点是贝叶斯方法。我们还介绍了一套用于自动验证协议的功能。我们希望这里介绍的指导原则有助于使生物学统计软件预期标准的讨论重点更加突出(以及提高)。
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引用次数: 0
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