scholarly journals Spider phylogenomics: untangling the Spider Tree of Life

Author(s):  
Nicole L Garrison ◽  
Juanita Rodriguez ◽  
Ingi Agnarsson ◽  
Jonathan A Coddington ◽  
Charles E Griswold ◽  
...  

Spiders (Order Araneae) are massively abundant generalist arthropod predators that are found in nearly every ecosystem on the planet and have persisted for over 380 million years. Spiders have long served as evolutionary models for studying complex mating and web spinning behaviors, key innovation and adaptive radiation hypotheses, and have been inspiration for important theories like sexual selection by female choice. Unfortunately, past major attempts to reconstruct spider phylogeny typically employing the “usual suspect” genes have been unable to produce a well-supported phylogenetic framework for the entire order. To further resolve spider evolutionary relationships we have assembled a transcriptome-based data set comprising 70 ingroup spider taxa. Using maximum likelihood and shortcut coalescence-based approaches, we analyze eight data sets, the largest of which contains 3,398 gene regions and 696,652 amino acid sites forming the largest phylogenomic analysis of spider relationships produced to date. Contrary to long held beliefs that the orb web is the crowning achievement of spider evolution, ancestral state reconstructions of web type support a phylogenetically ancient origin of the orb web and diversification analyses show that the mostly ground-dwelling, web-less RTA clade diversified faster than orb weavers. Consistent with molecular dating estimates we report herein, this may reflect a major increase in biomass of non-flying insects during the Cretaceous Tertiary Revolution 125-90 million years ago favoring diversification of spiders that feed on cursorial rather than flying prey. Our results also have major implications for our understanding of spider systematics. Phylogenomic analyses corroborate several well-accepted high level groupings: Opisthothele, Mygalomorphae, Atypoidina, Aviculariodea, Theraphosidina, Araneomorphae, Entelygynae, Araneoidea, the RTA – clade, Dionycha and the Lycosoidea. Alternatively, our results challenge the monophyly of Eresoidea, Orbiculariae, and Deinopoidea. The composition of the major Paleocribellate and Neocribellate clades, the basal divisions of Araneomorphae, appear to be falsified. Traditional Haplogynae, and even the new concept of Synspermiata, need revision after the departure of Filistatidae and Leptonetidae from the haplogyne clade. The sister pairing of filistatids with hypochilids, implies that some peculiar features of each family may in fact be synapomorphic for the pair. Leptonetids now are seen as a possible sister group to the Entelegynae, illustrating possible intermediates in the evolution of the more complex entelegyne genitalic condition, spinning organs and respiratory organs.

PeerJ ◽  
2016 ◽  
Vol 4 ◽  
pp. e1719 ◽  
Author(s):  
Nicole L. Garrison ◽  
Juanita Rodriguez ◽  
Ingi Agnarsson ◽  
Jonathan A. Coddington ◽  
Charles E. Griswold ◽  
...  

Spiders (Order Araneae) are massively abundant generalist arthropod predators that are found in nearly every ecosystem on the planet and have persisted for over 380 million years. Spiders have long served as evolutionary models for studying complex mating and web spinning behaviors, key innovation and adaptive radiation hypotheses, and have been inspiration for important theories like sexual selection by female choice. Unfortunately, past major attempts to reconstruct spider phylogeny typically employing the “usual suspect” genes have been unable to produce a well-supported phylogenetic framework for the entire order. To further resolve spider evolutionary relationships we have assembled a transcriptome-based data set comprising 70 ingroup spider taxa. Using maximum likelihood and shortcut coalescence-based approaches, we analyze eight data sets, the largest of which contains 3,398 gene regions and 696,652 amino acid sites forming the largest phylogenomic analysis of spider relationships produced to date. Contrary to long held beliefs that the orb web is the crowning achievement of spider evolution, ancestral state reconstructions of web type support a phylogenetically ancient origin of the orb web, and diversification analyses show that the mostly ground-dwelling, web-less RTA clade diversified faster than orb weavers. Consistent with molecular dating estimates we report herein, this may reflect a major increase in biomass of non-flying insects during the Cretaceous Terrestrial Revolution 125–90 million years ago favoring diversification of spiders that feed on cursorial rather than flying prey. Our results also have major implications for our understanding of spider systematics. Phylogenomic analyses corroborate several well-accepted high level groupings: Opisthothele, Mygalomorphae, Atypoidina, Avicularoidea, Theraphosoidina, Araneomorphae, Entelegynae, Araneoidea, the RTA clade, Dionycha and the Lycosoidea. Alternatively, our results challenge the monophyly of Eresoidea, Orbiculariae, and Deinopoidea. The composition of the major paleocribellate and neocribellate clades, the basal divisions of Araneomorphae, appear to be falsified. Traditional Haplogynae is in need of revision, as our findings appear to support the newly conceived concept of Synspermiata. The sister pairing of filistatids with hypochilids implies that some peculiar features of each family may in fact be synapomorphic for the pair. Leptonetids now are seen as a possible sister group to the Entelegynae, illustrating possible intermediates in the evolution of the more complex entelegyne genitalic condition, spinning organs and respiratory organs.


Author(s):  
Nicole L Garrison ◽  
Juanita Rodriguez ◽  
Ingi Agnarsson ◽  
Jonathan A Coddington ◽  
Charles E Griswold ◽  
...  

Spiders (Order Araneae) are massively abundant generalist arthropod predators that are found in nearly every ecosystem on the planet and have persisted for over 380 million years. Spiders have long served as evolutionary models for studying complex mating and web spinning behaviors, key innovation and adaptive radiation hypotheses, and have been inspiration for important theories like sexual selection by female choice. Unfortunately, past major attempts to reconstruct spider phylogeny typically employing the “usual suspect” genes have been unable to produce a well-supported phylogenetic framework for the entire order. To further resolve spider evolutionary relationships we have assembled a transcriptome-based data set comprising 70 ingroup spider taxa. Using maximum likelihood and shortcut coalescence-based approaches, we analyze eight data sets, the largest of which contains 3,398 gene regions and 696,652 amino acid sites forming the largest phylogenomic analysis of spider relationships produced to date. Contrary to long held beliefs that the orb web is the crowning achievement of spider evolution, ancestral state reconstructions of web type support a phylogenetically ancient origin of the orb web and diversification analyses show that the mostly ground-dwelling, web-less RTA clade diversified faster than orb weavers. Consistent with molecular dating estimates we report herein, this may reflect a major increase in biomass of non-flying insects during the Cretaceous Tertiary Revolution 125-90 million years ago favoring diversification of spiders that feed on cursorial rather than flying prey. Our results also have major implications for our understanding of spider systematics. Phylogenomic analyses corroborate several well-accepted high level groupings: Opisthothele, Mygalomorphae, Atypoidina, Aviculariodea, Theraphosidina, Araneomorphae, Entelygynae, Araneoidea, the RTA – clade, Dionycha and the Lycosoidea. Alternatively, our results challenge the monophyly of Eresoidea, Orbiculariae, and Deinopoidea. The composition of the major Paleocribellate and Neocribellate clades, the basal divisions of Araneomorphae, appear to be falsified. Traditional Haplogynae, and even the new concept of Synspermiata, need revision after the departure of Filistatidae and Leptonetidae from the haplogyne clade. The sister pairing of filistatids with hypochilids, implies that some peculiar features of each family may in fact be synapomorphic for the pair. Leptonetids now are seen as a possible sister group to the Entelegynae, illustrating possible intermediates in the evolution of the more complex entelegyne genitalic condition, spinning organs and respiratory organs.


Author(s):  
Robert S de Moya ◽  
Kazunori Yoshizawa ◽  
Kimberly K O Walden ◽  
Andrew D Sweet ◽  
Christopher H Dietrich ◽  
...  

Abstract The insect order Psocodea is a diverse lineage comprising both parasitic (Phthiraptera) and non-parasitic members (Psocoptera). The extreme age and ecological diversity of the group may be associated with major genomic changes, such as base compositional biases expected to affect phylogenetic inference. Divergent morphology between parasitic and non-parasitic members has also obscured the origins of parasitism within the order. We conducted a phylogenomic analysis on the order Psocodea utilizing both transcriptome and genome sequencing to obtain a data set of 2,370 orthologous genes. All phylogenomic analyses, including both concatenated and coalescent methods suggest a single origin of parasitism within the order Psocodea, resolving conflicting results from previous studies. This phylogeny allows us to propose a stable ordinal level classification scheme that retains significant taxonomic names present in historical scientific literature and reflects the evolution of the group as a whole. A dating analysis, with internal nodes calibrated by fossil evidence, suggests an origin of parasitism that predates the K-Pg boundary. Nucleotide compositional biases are detected in third and first codon positions and result in the anomalous placement of the Amphientometae as sister to Psocomorpha when all nucleotide sites are analyzed. Likelihood-mapping and quartet sampling methods demonstrate that base compositional biases can also have an effect on quartet-based methods.


2020 ◽  
Vol 20 (1) ◽  
Author(s):  
Bonnie B. Blaimer ◽  
Dietrich Gotzek ◽  
Seán G. Brady ◽  
Matthew L. Buffington

Abstract Background Parasitoidism, a specialized life strategy in which a parasite eventually kills its host, is frequently found within the insect order Hymenoptera (wasps, ants and bees). A parasitoid lifestyle is one of two dominant life strategies within the hymenopteran superfamily Cynipoidea, with the other being an unusual plant-feeding behavior known as galling. Less commonly, cynipoid wasps exhibit inquilinism, a strategy where some species have adapted to usurp other species’ galls instead of inducing their own. Using a phylogenomic data set of ultraconserved elements from nearly all lineages of Cynipoidea, we here generate a robust phylogenetic framework and timescale to understand cynipoid systematics and the evolution of these life histories. Results Our reconstructed evolutionary history for Cynipoidea differs considerably from previous hypotheses. Rooting our analyses with non-cynipoid outgroups, the Paraulacini, a group of inquilines, emerged as sister-group to the rest of Cynipoidea, rendering the gall wasp family Cynipidae paraphyletic. The families Ibaliidae and Liopteridae, long considered archaic and early-branching parasitoid lineages, were found nested well within the Cynipoidea as sister-group to the parasitoid Figitidae. Cynipoidea originated in the early Jurassic around 190 Ma. Either inquilinism or parasitoidism is suggested as the ancestral and dominant strategy throughout the early evolution of cynipoids, depending on whether a simple (three states: parasitoidism, inquilinism and galling) or more complex (seven states: parasitoidism, inquilinism and galling split by host use) model is employed. Conclusions Our study has significant impact on understanding cynipoid evolution and highlights the importance of adequate outgroup sampling. We discuss the evolutionary timescale of the superfamily in relation to their insect hosts and host plants, and outline how phytophagous galling behavior may have evolved from entomophagous, parasitoid cynipoids. Our study has established the framework for further physiological and comparative genomic work between gall-making, inquiline and parasitoid lineages, which could also have significant implications for the evolution of diverse life histories in other Hymenoptera.


PeerJ ◽  
2017 ◽  
Vol 5 ◽  
pp. e3941 ◽  
Author(s):  
Alejandra Panzera ◽  
Adam D. Leaché ◽  
Guillermo D’Elía ◽  
Pedro F. Victoriano

The genusLiolaemusis one of the most ecologically diverse and species-rich genera of lizards worldwide. It currently includes more than 250 recognized species, which have been subject to many ecological and evolutionary studies. Nevertheless,Liolaemuslizards have a complex taxonomic history, mainly due to the incongruence between morphological and genetic data, incomplete taxon sampling, incomplete lineage sorting and hybridization. In addition, as many species have restricted and remote distributions, this has hampered their examination and inclusion in molecular systematic studies. The aims of this study are to infer a robust phylogeny for a subsample of lizards representing the Chilean clade (subgenusLiolaemus sensu stricto), and to test the monophyly of several of the major species groups. We use a phylogenomic approach, targeting 541 ultra-conserved elements (UCEs) and 44 protein-coding genes for 16 taxa. We conduct a comparison of phylogenetic analyses using maximum-likelihood and several species tree inference methods. The UCEs provide stronger support for phylogenetic relationships compared to the protein-coding genes; however, the UCEs outnumber the protein-coding genes by 10-fold. On average, the protein-coding genes contain over twice the number of informative sites. Based on our phylogenomic analyses, all the groups sampled are polyphyletic.Liolaemus tenuis tenuisis difficult to place in the phylogeny, because only a few loci (nine) were recovered for this species. Topologies or support values did not change dramatically upon exclusion ofL. t. tenuisfrom analyses, suggesting that missing data did not had a significant impact on phylogenetic inference in this data set. The phylogenomic analyses provide strong support for sister group relationships betweenL. fuscus,L. monticola,L. nigroviridisandL. nitidus, andL. plateiandL. velosoi. Despite our limited taxon sampling, we have provided a reliable starting hypothesis for the relationships among many major groups of the Chilean clade ofLiolaemusthat will help future work aimed at resolving theLiolaemusphylogeny.


2016 ◽  
Author(s):  
Scott V. Edwards ◽  
Alison Cloutier ◽  
Allan J. Baker

AbstractNoncoding markers have a particular appeal as tools for phylogenomic analysis because, at least in vertebrates, they appear less subject to strong variation in GC content among lineages. Thus far, ultraconserved elements (UCEs) and introns have been the most widely used noncoding markers. Here we analyze and study the evolutionary properties of a new type of noncoding marker, conserved non-exonic elements (CNEEs), which consists of noncoding elements that are estimated to evolve slower than the neutral rate across a set of species. Although they often include UCEs, CNEEs are distinct from UCEs because they are not ultraconserved, and, most importantly, the core region alone is analyzed, rather than both the core and its flanking regions. Using a data set of 16 birds plus an alligator outgroup, and ~3600 - ~3800 loci per marker type, we found that although CNEEs were less variable than UCEs or introns and in some cases exhibited a slower approach to branch resolution as determined by phylogenomic subsampling, the quality of CNEE alignments was superior to those of the other markers, with fewer gaps and missing species. Phylogenetic resolution using coalescent approaches was comparable among the three marker types, with most nodes being fully and congruently resolved. Comparison of phylogenetic results across the three marker types indicated that one branch, the sister group to the passerine+falcon clade, was resolved differently and with moderate (> 70%) bootstrap support between CNEEs and UCEs or introns. Overall, CNEEs appear to be promising as phylogenomic markers, yielding phylogenetic resolution as high as for UCEs and introns but with fewer gaps, less ambiguity in alignments and with patterns of nucleotide substitution more consistent with the assumptions of commonly used methods of phylogenetic analysis.


2020 ◽  
Vol 20 (1) ◽  
Author(s):  
Alexandros Vasilikopoulos ◽  
Bernhard Misof ◽  
Karen Meusemann ◽  
Doria Lieberz ◽  
Tomáš Flouri ◽  
...  

Abstract Background The latest advancements in DNA sequencing technologies have facilitated the resolution of the phylogeny of insects, yet parts of the tree of Holometabola remain unresolved. The phylogeny of Neuropterida has been extensively studied, but no strong consensus exists concerning the phylogenetic relationships within the order Neuroptera. Here, we assembled a novel transcriptomic dataset to address previously unresolved issues in the phylogeny of Neuropterida and to infer divergence times within the group. We tested the robustness of our phylogenetic estimates by comparing summary coalescent and concatenation-based phylogenetic approaches and by employing different quartet-based measures of phylogenomic incongruence, combined with data permutations. Results Our results suggest that the order Raphidioptera is sister to Neuroptera + Megaloptera. Coniopterygidae is inferred as sister to all remaining neuropteran families suggesting that larval cryptonephry could be a ground plan feature of Neuroptera. A clade that includes Nevrorthidae, Osmylidae, and Sisyridae (i.e. Osmyloidea) is inferred as sister to all other Neuroptera except Coniopterygidae, and Dilaridae is placed as sister to all remaining neuropteran families. Ithonidae is inferred as the sister group of monophyletic Myrmeleontiformia. The phylogenetic affinities of Chrysopidae and Hemerobiidae were dependent on the data type analyzed, and quartet-based analyses showed only weak support for the placement of Hemerobiidae as sister to Ithonidae + Myrmeleontiformia. Our molecular dating analyses suggest that most families of Neuropterida started to diversify in the Jurassic and our ancestral character state reconstructions suggest a primarily terrestrial environment of the larvae of Neuropterida and Neuroptera. Conclusion Our extensive phylogenomic analyses consolidate several key aspects in the backbone phylogeny of Neuropterida, such as the basal placement of Coniopterygidae within Neuroptera and the monophyly of Osmyloidea. Furthermore, they provide new insights into the timing of diversification of Neuropterida. Despite the vast amount of analyzed molecular data, we found that certain nodes in the tree of Neuroptera are not robustly resolved. Therefore, we emphasize the importance of integrating the results of morphological analyses with those of sequence-based phylogenomics. We also suggest that comparative analyses of genomic meta-characters should be incorporated into future phylogenomic studies of Neuropterida.


2018 ◽  
Vol 115 (50) ◽  
pp. 12775-12780 ◽  
Author(s):  
Kevin P. Johnson ◽  
Christopher H. Dietrich ◽  
Frank Friedrich ◽  
Rolf G. Beutel ◽  
Benjamin Wipfler ◽  
...  

Hemipteroid insects (Paraneoptera), with over 10% of all known insect diversity, are a major component of terrestrial and aquatic ecosystems. Previous phylogenetic analyses have not consistently resolved the relationships among major hemipteroid lineages. We provide maximum likelihood-based phylogenomic analyses of a taxonomically comprehensive dataset comprising sequences of 2,395 single-copy, protein-coding genes for 193 samples of hemipteroid insects and outgroups. These analyses yield a well-supported phylogeny for hemipteroid insects. Monophyly of each of the three hemipteroid orders (Psocodea, Thysanoptera, and Hemiptera) is strongly supported, as are most relationships among suborders and families. Thysanoptera (thrips) is strongly supported as sister to Hemiptera. However, as in a recent large-scale analysis sampling all insect orders, trees from our data matrices support Psocodea (bark lice and parasitic lice) as the sister group to the holometabolous insects (those with complete metamorphosis). In contrast, four-cluster likelihood mapping of these data does not support this result. A molecular dating analysis using 23 fossil calibration points suggests hemipteroid insects began diversifying before the Carboniferous, over 365 million years ago. We also explore implications for understanding the timing of diversification, the evolution of morphological traits, and the evolution of mitochondrial genome organization. These results provide a phylogenetic framework for future studies of the group.


2021 ◽  
Author(s):  
Yi-Kai Tea ◽  
Xin Xu ◽  
Joseph D DiBattista ◽  
Nathan Lo ◽  
Peter F Cowman ◽  
...  

Abstract The fairy wrasses (genus Cirrhilabrus) are among the most successful of the extant wrasse lineages (Teleostei: Labridae), with their 61 species accounting for nearly 10$\%$ of the family. Although species complexes within the genus have been diagnosed on the basis of coloration patterns and synapomorphies, attempts to resolve evolutionary relationships among these groups using molecular and morphological data have largely been unsuccessful. Here, we use a phylogenomic approach with a data set comprising 991 ultraconserved elements (UCEs) and mitochondrial COI to uncover the evolutionary history and patterns of temporal and spatial diversification of the fairy wrasses. Our analyses of phylogenetic signal suggest that most gene-tree incongruence is caused by estimation error, leading to poor resolution in a summary-coalescent analysis of the data. In contrast, analyses of concatenated sequences are able to resolve the major relationships of Cirrhilabrus. We determine the placements of species that were previously regarded as incertae sedis and find evidence for the nesting of Conniella, an unusual, monotypic genus, within Cirrhilabrus. Our relaxed-clock dating analysis indicates that the major divergences within the genus occurred around the Miocene–Pliocene boundary, followed by extensive cladogenesis of species complexes in the Pliocene–Pleistocene. Biogeographic reconstruction suggests that the fairy wrasses emerged within the Coral Triangle, with episodic fluctuations of sea levels during glacial cycles coinciding with shallow divergence events but providing few opportunities for more widespread dispersal. Our study demonstrates both the resolving power and limitations of UCEs across shallow timescales where there is substantial estimation error in individual gene trees.[Biogeography; concatenation; gene genealogy interrogation; gene trees; molecular dating; summary coalescent; UCEs.]


2019 ◽  
Vol 68 (6) ◽  
pp. 896-917 ◽  
Author(s):  
Jesús A Ballesteros ◽  
Prashant P Sharma

AbstractHorseshoe crabs (Xiphosura) are traditionally regarded as sister group to the clade of terrestrial chelicerates (Arachnida). This hypothesis has been challenged by recent phylogenomic analyses, but the non-monophyly of Arachnida has consistently been disregarded as artifactual. We re-evaluated the placement of Xiphosura among chelicerates using the most complete phylogenetic data set to date, expanding outgroup sampling, and including data from whole genome sequencing projects. In spite of uncertainty in the placement of some arachnid clades, all analyses show Xiphosura consistently nested within Arachnida as the sister group to Ricinulei (hooded tick spiders). It is apparent that the radiation of arachnids is an old one and occurred over a brief period of time, resulting in several consecutive short internodes, and thus is a potential case for the confounding effects of incomplete lineage sorting (ILS). We simulated coalescent gene trees to explore the effects of increasing levels of ILS on the placement of horseshoe crabs. In addition, common sources of systematic error were evaluated, as well as the effects of fast-evolving partitions and the dynamics of problematic long branch orders. Our results indicated that the placement of horseshoe crabs cannot be explained by missing data, compositional biases, saturation, or ILS. Interrogation of the phylogenetic signal showed that the majority of loci favor the derived placement of Xiphosura over a monophyletic Arachnida. Our analyses support the inference that horseshoe crabs represent a group of aquatic arachnids, comparable to aquatic mites, breaking a long-standing paradigm in chelicerate evolution and altering previous interpretations of the ancestral transition to the terrestrial habitat. Future studies testing chelicerate relationships should approach the task with a sampling strategy where the monophyly of Arachnida is not held as the premise.


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