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Integrating Deep Learning Derived Morphological Traits and Molecular Data for Total-Evidence Phylogenetics: Lessons from Digitized Collections.
IF 6.5 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2025-01-18 DOI: 10.1093/sysbio/syae072
Roberta Hunt,José L Reyes-Hernández,Josh Jenkins Shaw,Alexey Solodovnikov,Kim Steenstrup Pedersen
Deep learning has previously shown success in automatically generating morphological traits which carry a phylogenetic signal. In this paper we explore combining molecular data with deep learning derived morphological traits from images of pinned insects to generate total-evidence phylogenies and we reveal challenges. Deep learning derived morphological traits, while informative, underperform when used in isolation compared to molecular analyses. However, they can improve molecular results in total evidence settings. We use a dataset of rove beetle images to compare the effect of different dataset splits and deep metric loss functions on morphological and total evidence results. We find a slight preference for the cladistic dataset split and contrastive loss function. Additionally, we explore the effect of varying the number of genes used in inference and find that different gene combinations provide the best results when used on their own vs in total evidence analysis. Despite the promising nature of integrating deep learning techniques with molecular data, challenges remain regarding the strength of the phylogenetic signal and the resource demands of data acquisition. We suggest that future work focus on improved trait extraction and the development of disentangled networks to better interpret the derived traits, thus expanding the applicability of these methods in phylogenetic studies.
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引用次数: 0
Inference of multiple mergers while dating a pathogen phylogeny
IF 6.5 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2025-01-18 DOI: 10.1093/sysbio/syaf003
David Helekal, Jere Koskela, Xavier Didelot
The vast majority of pathogen phylogenetic studies do not consider the possibility of multiple merger events being present, where a single node of the tree leads to more than two descendent branches. These events are however likely to occur when studying a relatively small population or if there is high variability in the reproductive chances. Here we consider the problem of detecting the presence of multiple mergers in the context of dating a phylogeny, that is determining the date of each of the nodes. We use the Lambda-coalescent theory as a modelling framework and show how Bayesian inference can be efficiently performed using a Billera-Holmes- Vogtmann space embedding and a customised Markov Chain Monte Carlo sampling scheme. We applied this new analysis methodology to a large number of simulated datasets to show that it is possible to infer if and when multiple merger events occurred, and that the phylogenetic dating is improved as a result of taking this information into account. We also analysed real datasets of Vibrio cholerae and Mycobacterium tuberculosis to demonstrate the relevance of our approach to real pathogen evolutionary epidemiology. We have implemented our new methodology in a R package which is freely available at https://github.com/dhelekal/MMCTime.
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引用次数: 0
Punctuated versus gradual shifts in the multivariate evolutionary process: a test with paired radiations of scincid lizards
IF 6.5 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2025-01-16 DOI: 10.1093/sysbio/syaf002
Natasha Stepanova, James D Boyko, Jada Lin, Alison R Davis Rabosky, Daniel L Rabosky
As lineages become separated in time, they are expected to accumulate mutational (or developmental-genetic) differences that influence the macroevolutionary trajectories of those lineages even under similar environmental conditions. Here, we compare the dynamics of phenotypic evolution in radiations of scincid lizards from Australia and Madagascar that are separated by more than 100 million years of independent evolution and show rampant phenotypic parallelism. We collected linear measurements of the skull, limbs, and limb girdles from micro-CT scans of 94 Australian and 29 Malagasy species. Using multivariate comparative methods, we tested whether the underlying evolutionary covariance structure for this superficial parallelism was conserved and whether these patterns were consistent across distinct functional modules. Malagasy and most Australian skinks have similar covariance matrices for skull evolution. Results are ambiguous for limbs and limb girdles, as some trait subsets support different evolutionary processes and for other subsets, a shared covariance matrix could not be rejected. However, across most trait sets, the extremely speciose Australian genus Ctenotus exhibits a radically different covariance structure from all other lizards in these groups, including several closely related genera. The shift in Ctenotus demonstrates that the architecture of trait correlations can change at relatively shallow timescales and may explain the unique position of this clade in morphospace relative to other scincid lizards from both geographic regions. More generally, our results demonstrate that the multivariate evolutionary process can change dramatically in a relatively short period of time.
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引用次数: 0
Evaluating UCE Data Adequacy and Integrating Uncertainty in a Comprehensive Phylogeny of Ants
IF 6.5 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2025-01-08 DOI: 10.1093/sysbio/syaf001
Marek L Borowiec, Y Miles Zhang, Karen Neves, Manuela O Ramalho, Brian L Fisher, Andrea Lucky, Corrie S Moreau
While some relationships in phylogenomic studies have remained stable since the Sanger sequencing era, many challenging nodes remain, even with genome-scale data. Incongruence or lack of resolution in the phylogenomic era is frequently attributed to inadequate data modeling and analytical issues that lead to systematic biases. However, few studies investigate the potential for random error or establish expectations for the level of resolution achievable with a given empirical dataset and integrate uncertainties across methods when faced with conflicting results. Ants are the most species-rich lineage of social insects and one of the most ecologically important terrestrial animals. Consequently, ants have garnered significant research attention, including their systematics. Despite this, there has been no comprehensive genus-level phylogeny of the ants inferred using genomic data that thoroughly evaluates both signal strength and incongruence. In this study, we provide insight into and quantify uncertainty across the ant tree of life by utilizing the most taxonomically comprehensive Ultraconserved Elements dataset of ants to date, including 277 (81%) of recognized ant genera from all 16 extant subfamilies, and representing over 98% of described species. We use simulations to establish expectations for resolution, identify branches with less-than-expected concordance, and dissect the effects of data and model selection on recalcitrant nodes. Simulations show that hundreds of loci are needed to resolve recalcitrant nodes on our genus-level ant phylogeny. This demonstrates the continued role of random error in phylogenomic studies. Our analyses provide a comprehensive picture of support and incongruence across the ant phylogeny, while offering a more nuanced depiction of uncertainty and significantly expanding generic sampling. We use a consensus approach to integrate uncertainty across different analyses and find that assumptions about root age exert substantial influence on divergence dating. Our results suggest that advancing the understanding of ant phylogeny will require not only more data but also more refined phylogenetic models. We also provide a workflow for identifying under-supported nodes in concatenation analyses, outline a pragmatic way to reconcile conflicting results in phylogenomics, and introduce a user-friendly locus selection tool for divergence dating.
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引用次数: 0
Phylogenomic Insights into the Evolution and Origin of Nematoda
IF 6.5 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2024-12-30 DOI: 10.1093/sysbio/syae073
Xue Qing, Y Miles Zhang, Sidi Sun, Mohammed Ahmed, Wen-Sui Lo, Wim Bert, Oleksandr Holovachov, Hongmei Li
The phylum Nematoda represents one of the most cosmopolitan and abundant metazoan groups on Earth. In this study, we reconstructed the phylogenomic tree for phylum Nematoda. A total of 60 genomes, belonging to eight nematode orders, were newly sequenced, providing the first low-coverage genomes for the orders Dorylaimida, Mononchida, Monhysterida, Chromadorida, Triplonchida, and Enoplida. The resulting phylogeny is well-resolved across most clades, with topologies remaining consistent across various reconstruction parameters. The subclass Enoplia is placed as a sister group to the rest of Nematoda, agreeing with previous published phylogenies. While the order Triplonchida is monophyletic, it is not well-supported, and the order Enoplida is paraphyletic. Taxa possessing a stomatostylet form a monophyletic group; however, the superfamily Aphelenchoidea does not constitute a monophyletic clade. The genera Trichinella and Trichuris are inferred to have shared a common ancestor approximately 202 millions of years ago (Ma), a considerably later period than previously suggested. All stomatostylet-bearing nematodes are proposed to have originated ~305 Ma, corresponding to the transition from the Devonian to the Permian period. The genus Thornia is placed outside of Dorylaimina and Nygolaimina, disagreeing with its position in previous studies. Additionally, we tested the whole genome amplification method and demonstrated that it is a promising strategy for obtaining sufficient DNA for phylogenomic studies of microscopic eukaryotes. This study significantly expanded the current nematode genome dataset, and the well-resolved phylogeny enhances our understanding of the evolution of Nematoda.
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引用次数: 0
Evolutionary timelines help explain the evolution of parental care strategies
IF 6.5 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2024-12-12 DOI: 10.1093/sysbio/syae069
Zackary A Graham, Zachary J Loughman, Alexandre V Palaoro
Comparative research on the evolution of parental care has followed a general trend in recent years, with researchers gathering data on clutch size or egg size and correlating these traits with ecological variables across a phylogeny. The goal of these studies is to shed light on how and why certain strategies evolve. However, results vary across studies, and we rarely have results explaining why the observed pattern occurred, leaving us with further hypotheses to test. By using a combination of comparative methods, we provide an explanation of how such patterns emerge based on the evolutionary timeline of constructing burrows and the energy invested into egg size and egg number; this combination also allowed us to pinpoint why the pattern occurred. We do so with data on freshwater crayfish, which are ideal for such investigations because they vary in their reliance on burrows, their body size, and their investment into their offspring. Specifically, we tested whether a strong dependence on burrows is related to investment in eggs (i.e., larger eggs or more eggs) given the body size of the species. Surprisingly, we found no correlation between burrowing and the size or number of eggs crayfish lay; instead, body size was the best predictor of the number of eggs (but not the size of eggs) that each species lays. Interestingly, our analysis suggests that crayfish ancestors had a small clutch size, relatively large eggs, and a weak connection to burrows. Thus, the shift to heavily relying on burrows appeared after this lineage was already investing in large eggs, which gives insights into the colonization of freshwater by an ancestral astacidean ancestor. While other studies show that the evolution of parental care strategies is not straightforward, our study provides a clear evolutionary timeline of the interplay between the evolution of burrowing behavior and shifts in the evolution of egg investment. Furthermore, our work showcases how merging multiple phylogenetically informed approaches can disentangle the origin and evolution of life history traits.
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引用次数: 0
Discordance Down Under: Combining phylogenomics & fungal symbioses to detangle difficult nodes in a diverse tribe of Australian terrestrial orchids
IF 6.5 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2024-12-10 DOI: 10.1093/sysbio/syae070
Ryan P O’Donnell, Darren C J Wong, Ryan D Phillips, Rod Peakall, Celeste C Linde
Orchid mycorrhizal fungi (OMF) associations in the Orchidaceae are thought to have been a major driver of diversification in the family. In the terrestrial orchid tribe Diurideae, it has long been hypothesised that OMF symbiont associations may reflect evolutionary relationships among orchid hosts. Given that recent phylogenomic efforts have been unable to fully resolve relationships among subtribes in the Diurideae, we sought to ascertain whether orchid OMF preferences may lend support to certain phylogenetic hypotheses. First, we used phylogenomic methods and Bayesian divergence time estimation to produce a genus-level tree for the Diurideae. Next, we synthesised decades of published fungal sequences and morphological/germination data to identify dominant fungal partners at the genus scale and perform ancestral state reconstruction to estimate the evolutionary trajectory of fungal symbiont shifts. Across the tribe, we found phylogenomic discordance stemming from incomplete lineage sorting. However, our results also revealed unprecedented phylogenetic niche conservatism of fungal symbionts within the tribe: entire genera, subtribes, and even groups of related subtribes associate with only a single fungal family, suggesting that fungal symbiont preferences in the Diurideae do indeed reflect phylogenetic relationships among orchid hosts. Moreover, we show that these relationships have evolved directionally from generalist associations with multiple fungal families towards more specific partnerships with only one fungal family. Orchid symbiont preferences here provide new insights into the placement of several groups with longstanding phylogenetic uncertainty. In spite of complex evolutionary histories, host-symbiont relationships can be used to help detangle alternative phylogenetic hypotheses.
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引用次数: 0
Persistent Gene Flow Suggests an Absence of Reproductive Isolation in an African Antelope Speciation Model. 基因持续流动表明非洲羚羊物种模式中不存在生殖隔离
IF 6.1 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2024-11-29 DOI: 10.1093/sysbio/syae037
Xi Wang, Casper-Emil Tingskov Pedersen, Georgios Athanasiadis, Genís Garcia-Erill, Kristian Hanghøj, Laura D Bertola, Malthe Sebro Rasmussen, Mikkel Schubert, Xiaodong Liu, Zilong Li, Long Lin, Renzo F Balboa, Emil Jørsboe, Casia Nursyifa, Shanlin Liu, Vincent Muwanika, Charles Masembe, Lei Chen, Wen Wang, Ida Moltke, Hans R Siegismund, Anders Albrechtsen, Rasmus Heller

African antelope diversity is a globally unique vestige of a much richer world-wide Pleistocene megafauna. Despite this, the evolutionary processes leading to the prolific radiation of African antelopes are not well understood. Here, we sequenced 145 whole genomes from both subspecies of the waterbuck (Kobus ellipsiprymnus), an African antelope believed to be in the process of speciation. We investigated genetic structure and population divergence and found evidence of a mid-Pleistocene separation on either side of the eastern Great Rift Valley, consistent with vicariance caused by a rain shadow along the so-called "Kingdon's Line." However, we also found pervasive evidence of both recent and widespread historical gene flow across the Rift Valley barrier. By inferring the genome-wide landscape of variation among subspecies, we found 14 genomic regions of elevated differentiation, including a locus that may be related to each subspecies' distinctive coat pigmentation pattern. We investigated these regions as candidate speciation islands. However, we observed no significant reduction in gene flow in these regions, nor any indications of selection against hybrids. Altogether, these results suggest a pattern whereby climatically driven vicariance is the most important process driving the African antelope radiation and suggest that reproductive isolation may not set in until very late in the divergence process. This has a significant impact on taxonomic inference, as many taxa will be in a gray area of ambiguous systematic status, possibly explaining why it has been hard to achieve consensus regarding the species status of many African antelopes. Our analyses demonstrate how population genetics based on low-depth whole genome sequencing can provide new insights that can help resolve how far lineages have gone along the path to speciation.

非洲羚羊的多样性是全球独一无二的遗存,它是世界上更丰富的更新世巨型动物的遗存。尽管如此,人们对导致非洲羚羊大量辐射的进化过程仍不甚了解。在这里,我们对水鹿(Kobus ellipsiprymnus)两个亚种的 145 个全基因组进行了测序。我们对遗传结构和种群分化进行了研究,发现了早在始新世中期大裂谷东部两侧出现分离的证据,这与所谓的 "金顿线 "沿线雨影造成的沧桑变化是一致的。不过,我们也发现了近期和历史上跨越大裂谷屏障广泛基因流动的普遍证据。通过推断亚种间的全基因组变异景观,我们发现了 14 个基因组分化加剧的区域,其中包括一个可能与每个亚种独特的皮毛色素模式有关的位点。我们将这些区域作为候选物种岛进行了研究。然而,我们在这些区域没有观察到基因流的明显减少,也没有观察到针对杂交的选择迹象。总之,这些结果表明,气候驱动的沧海桑田是推动非洲羚羊辐射的最重要过程,并表明生殖隔离可能要到分化过程的后期才会出现。这对分类推断有重大影响,因为许多类群将处于系统地位不明确的灰色区域,这可能解释了为什么许多非洲羚羊的物种地位难以达成共识。我们的分析表明,基于低深度全基因组测序的种群遗传学可以提供新的见解,帮助确定各系在物种形成的道路上已经走了多远。
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引用次数: 0
Phylogenomics and Pervasive Genome-Wide Phylogenetic Discordance Among Fin Whales (Balaenoptera physalus). 长须鲸(Balaenoptera physalus)的系统发生组学和普遍的全基因组系统发生不一致。
IF 6.1 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2024-11-29 DOI: 10.1093/sysbio/syae049
Fabricio Furni, Eduardo R Secchi, Camilla Speller, Daniel DenDanto, Christian Ramp, Finn Larsen, Sally Mizroch, Jooke Robbins, Richard Sears, Jorge Urbán R, Martine Bérubé, Per J Palsbøll

Phylogenomics has the power to uncover complex phylogenetic scenarios across the genome. In most cases, no single topology is reflected across the entire genome as the phylogenetic signal differs among genomic regions due to processes, such as introgression and incomplete lineage sorting. Baleen whales are among the largest vertebrates on Earth with a high dispersal potential in a relatively unrestricted habitat, the oceans. The fin whale (Balaenoptera physalus) is one of the most enigmatic baleen whale species, currently divided into four subspecies. It has been a matter of debate whether phylogeographic patterns explain taxonomic variation in fin whales. Here we present a chromosome-level whole genome analysis of the phylogenetic relationships among fin whales from multiple ocean basins. First, we estimated concatenated and consensus phylogenies for both the mitochondrial and nuclear genomes. The consensus phylogenies based upon the autosomal genome uncovered monophyletic clades associated with each ocean basin, aligning with the current understanding of subspecies division. Nevertheless, discordances were detected in the phylogenies based on the Y chromosome, mitochondrial genome, autosomal genome and X chromosome. Furthermore, we detected signs of introgression and pervasive phylogenetic discordance across the autosomal genome. This complex phylogenetic scenario could be explained by a puzzle of introgressive events, not yet documented in fin whales. Similarly, incomplete lineage sorting and low phylogenetic signal could lead to such phylogenetic discordances. Our study reinforces the pitfalls of relying on concatenated or single locus phylogenies to determine taxonomic relationships below the species level by illustrating the underlying nuances that some phylogenetic approaches may fail to capture. We emphasize the significance of accurate taxonomic delineation in fin whales by exploring crucial information revealed through genome-wide assessments.

系统发生组学能够揭示整个基因组的复杂系统发生情况。在大多数情况下,没有一种拓扑结构能反映整个基因组的情况,因为基因组区域之间的系统发育信号因引入和不完全世系分类等过程而有所不同。须鲸是地球上最大的脊椎动物之一,在相对不受限制的栖息地--海洋中具有很高的扩散潜力。长须鲸(Balaenoptera physalus)是最神秘的须鲸物种之一,目前分为四个亚种。系统地理学模式是否能解释长须鲸的分类变异一直是一个争论不休的问题。在此,我们对来自多个大洋盆地的长须鲸之间的系统发育关系进行了染色体水平的全基因组分析。首先,我们估算了线粒体和核基因组的连接系统进化和共识系统进化。基于常染色体基因组的共识系统发生发现了与各大洋盆地相关的单系支系,这与目前对亚种划分的理解一致。然而,在基于 Y 染色体、线粒体基因组、常染色体基因组和 X 染色体的系统发生中发现了不一致。此外,我们还在常染色体基因组中发现了引入的迹象和普遍的系统发育不协调。这种复杂的系统发育情况可以用长须鲸中还没有记录到的内传事件来解释。同样,不完全的世系分类和较低的系统发育信号也可能导致这种系统发育不一致。我们的研究通过说明一些系统发育方法可能无法捕捉到的潜在细微差别,强化了依靠连接或单位点系统发育来确定物种水平以下分类学关系的缺陷。我们通过探讨全基因组评估所揭示的关键信息,强调了准确划分长须鲸分类的重要性。
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引用次数: 0
Blouch: Bayesian Linear Ornstein-Uhlenbeck Models for Comparative Hypotheses. Blouch:比较假设的贝叶斯线性奥恩斯坦-乌伦贝克模型。
IF 6.1 1区 生物学 Q1 EVOLUTIONARY BIOLOGY Pub Date : 2024-11-29 DOI: 10.1093/sysbio/syae044
Mark Grabowski

Relationships among species in the tree of life can complicate comparative methods and testing adaptive hypotheses. Models based on the Ornstein-Uhlenbeck process permit hypotheses about adaptation to be tested by allowing traits to either evolve toward fixed adaptive optima (e.g., regimes or niches) or track continuously changing optima that can be influenced by other traits. These models allow estimation of the effects of both adaptation and phylogenetic inertia-resistance to adaptation due to any source-on trait evolution, an approach known as the "adaptation-inertia" framework. However, previous applications of this framework, and most approaches suggested to deal with the issue of species non-independence, are based on a maximum likelihood approach, and thus it is difficult to include information based on prior biological knowledge in the analysis, which can affect resulting inferences. Here, I present Blouch, (Bayesian Linear Ornstein-Uhlenbeck Models for Comparative Hypotheses), which fits allometric and adaptive models of continuous trait evolution in a Bayesian framework based on fixed or continuous predictors and incorporates measurement error. I first briefly discuss the models implemented in Blouch, and then the new applications for these models provided by a Bayesian framework. This includes the advantages of assigning biologically meaningful priors when compared to non-Bayesian approaches, allowing for varying effects (intercepts and slopes), and multilevel modeling. Validations on simulated data show good performance in recovering the true evolutionary parameters for all models. To demonstrate the workflow of Blouch on an empirical dataset, I test the hypothesis that the relatively larger antlers of larger-bodied deer are the result of more intense sexual selection that comes along with their tendency to live in larger breeding groups. While results show that larger-bodied deer that live in larger breeding groups have relatively larger antlers, deer living in the smallest groups appear to have a different and steeper scaling pattern of antler size to body size than other groups. These results are contrary to previous findings and may argue that a different type of sexual selection or other selective pressures govern optimum antler size in the smallest breeding groups.

生命树中物种之间的关系会使比较方法和适应性假设检验变得复杂。基于奥恩斯坦-乌伦贝克过程(Ornstein-Uhlenbeck process)的模型允许性状向固定的适应性最佳值(如制度或龛位)演化,或追踪可受其他性状影响的持续变化的最佳值,从而对适应性假说进行检验。这些模型可以估算适应性和系统发育惯性(任何原因导致的适应阻力)对性状进化的影响,这种方法被称为 "适应-惯性 "框架。然而,以往对这一框架的应用,以及为处理物种非独立性问题而提出的大多数方法,都是基于最大似然法,因此很难在分析中纳入基于先验生物学知识的信息,这可能会影响推论结果。在此,我将介绍Blouch(用于比较假设的贝叶斯线性奥恩斯坦-乌伦贝克模型),它在贝叶斯框架内基于固定或连续预测因子拟合连续性状进化的异速和适应模型,并纳入测量误差。我首先简要讨论了 Blouch 中实现的模型,然后讨论了贝叶斯框架为这些模型提供的新应用。与非贝叶斯方法相比,这包括分配有生物意义的先验、允许不同效应(截距和斜率)以及多层次建模等优势。模拟数据的验证结果表明,该方法在恢复所有模型的真实进化参数方面性能良好。为了展示 Blouch 在经验数据集上的工作流程,我检验了这样一个假设:体型较大的鹿的鹿角相对较大,这是由于它们倾向于生活在较大的繁殖群体中,因而性选择更为强烈。结果表明,生活在较大繁殖群体中的体型较大的鹿的鹿角相对较大,但生活在最小群体中的鹿的鹿角大小与体型的比例模式似乎与其他群体不同,而且更陡峭。这些结果与之前的研究结果相反,可能说明在最小的繁殖群体中,不同类型的性选择或其他选择压力会影响鹿角的最佳尺寸。
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引用次数: 0
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