Spider phylogenomics: untangling the Spider Tree of Life
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 a...
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PeerJ Inc.
2016-02-01
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author | Nicole L. Garrison Juanita Rodriguez Ingi Agnarsson Jonathan A. Coddington Charles E. Griswold Christopher A. Hamilton Marshal Hedin Kevin M. Kocot Joel M. Ledford Jason E. Bond |
author_facet | Nicole L. Garrison Juanita Rodriguez Ingi Agnarsson Jonathan A. Coddington Charles E. Griswold Christopher A. Hamilton Marshal Hedin Kevin M. Kocot Joel M. Ledford Jason E. Bond |
author_sort | Nicole L. Garrison |
collection | DOAJ |
description | 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. |
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spelling | doaj.art-43b94023af044a4aa143acd8304a6ef92023-12-03T09:52:29ZengPeerJ Inc.PeerJ2167-83592016-02-014e171910.7717/peerj.1719Spider phylogenomics: untangling the Spider Tree of LifeNicole L. Garrison0Juanita Rodriguez1Ingi Agnarsson2Jonathan A. Coddington3Charles E. Griswold4Christopher A. Hamilton5Marshal Hedin6Kevin M. Kocot7Joel M. Ledford8Jason E. Bond9Department of Biological Sciences and Auburn University Museum of Natural History, Auburn University, Auburn, AL, United StatesDepartment of Biological Sciences and Auburn University Museum of Natural History, Auburn University, Auburn, AL, United StatesDepartment of Biology, University of Vermont, Burlington, VT, United StatesDepartment of Entomology, National Museum of Natural History, Smithsonian Institution, Washingtion, DC, United StatesArachnology, California Academy of Sciences, San Francisco, CA, United StatesDepartment of Biological Sciences and Auburn University Museum of Natural History, Auburn University, Auburn, AL, United StatesDepartment of Biology, San Diego State University, San Diego, CA, United StatesDepartment of Biological Sciences and Alabama Museum of Natural History, University of Alabama—Tuscaloosa, Tuscaloosa, AL, United StatesDepartment of Plant Biology, University of California, Davis, Davis, CA, United StatesDepartment of Biological Sciences and Auburn University Museum of Natural History, Auburn University, Auburn, AL, United StatesSpiders (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.https://peerj.com/articles/1719.pdfArachnidaMolecular systematicsAraneaeSpider phylogenyWeb evolution |
spellingShingle | Nicole L. Garrison Juanita Rodriguez Ingi Agnarsson Jonathan A. Coddington Charles E. Griswold Christopher A. Hamilton Marshal Hedin Kevin M. Kocot Joel M. Ledford Jason E. Bond Spider phylogenomics: untangling the Spider Tree of Life PeerJ Arachnida Molecular systematics Araneae Spider phylogeny Web evolution |
title | Spider phylogenomics: untangling the Spider Tree of Life |
title_full | Spider phylogenomics: untangling the Spider Tree of Life |
title_fullStr | Spider phylogenomics: untangling the Spider Tree of Life |
title_full_unstemmed | Spider phylogenomics: untangling the Spider Tree of Life |
title_short | Spider phylogenomics: untangling the Spider Tree of Life |
title_sort | spider phylogenomics untangling the spider tree of life |
topic | Arachnida Molecular systematics Araneae Spider phylogeny Web evolution |
url | https://peerj.com/articles/1719.pdf |
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