The house spider genome reveals an ancient whole-genome duplication during arachnid evolution

Evelyn E. Schwager1, Prashant P. Sharma2, Thomas H. Clarke3, Daniel J. Leite1, Torsten Wierschin4, Matthias Pechmann5, Yasuko Akiyama-Oda6, Lauren A. Esposito7, Jesper Bechsgaard8, Trine Bilde8, Alexandra D. Buffry1, Hsu Chao9, Huyen Dinh9, Harshavardhan Doddapaneni9, Shannon Dugan9, Cornelius Eibner10, Cassandra G. Extavour11, Peter Funch8, Jessica E. Garb12, Luis Baudouin Gonzalez1, Vanessa L. González13, Sam Griffiths-Jones14, Yi Han9, Cheryl Y. Hayashi15, Maarten Hilbrant16, Daniel Hughes9, Ralf Janßen17, Sandra L. Lee9, Ignacio Maeso18, Shwetha C. Murali9, Donna M. Muzny9, Rodrigo Nunes da Fonseca19, Christian Louis Bonatto Paese1, Jiaxin Qu9, Matthew Ronshaugen14, Christoph Schomburg5, Anna Schönauer1, Angelika Stollewerk20, Montserrat Torres-Oliva5, Natascha Turetzek5, Bram Vanthournout8, John H. Werren21, Carsten Wolff22, Kim C. Worley9, Gregor Bucher23, Richard A. Gibbs9, Jonathan A. Coddington13, Hiroki Oda24, Mario Stanke4, Nadia A. Ayoub3, Nikola‐Michael Prpic5, Jean‐François Flot25, Nico Posnien5, Stephen Richards9, Alistair P. McGregor1
1Department of Biological and Medical Sciences, Oxford Brookes University, Gipsy Lane, Oxford, OX3 0BP, UK
2Department of Zoology, University of Wisconsin-Madison, 430 Lincoln Drive, Madison, WI 53706, USA
3Department of Biology, Washington and Lee University, 204 West Washington Street, Lexington, VA, 24450, USA
4Ernst Moritz Arndt University Greifswald, Institute for Mathematics and Computer Science, Walther-Rathenau-Str. 47, 17487, Greifswald, Germany
5Department for Developmental Biology, University Goettingen, Johann-Friedrich-Blumenbach-Institut for Zoology and Anthropology, GZMB Ernst-Caspari-Haus, Justus-von-Liebig-Weg 11, 37077, Goettingen, Germany
6JT Biohistory Research Hall, 1-1 Murasaki-cho, Takatsuki, Osaka 569-1125, Japan
7Institute for Biodiversity Science and Sustainability, California Academy of Sciences, 55 Music Concourse Drive, San Francisco, CA, 94118, USA
8Department of Bioscience, Aarhus University, Ny Munkegade 116, Building 1540, 8000 Aarhus C, Denmark
9Human Genome Sequencing Center, Department of Molecular and Human Genetics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA
10Department of Genetics, Friedrich-Schiller-University Jena, Philosophenweg 12, 07743, Jena, Germany
11Department of Organismic and Evolutionary Biology, Harvard University, 16 Divinity Avenue, Cambridge, MA 02138, USA
12Department of Biological Sciences, University of Massachusetts Lowell, 198 Riverside Street, Lowell, MA, 01854, USA
13Smithsonian National Museum of Natural History, MRC-163, P.O. Box 37012, Washington, DC, 20013-7012, USA
14Faculty of Biology Medicine and Health, University of Manchester, D.1416 Michael Smith Building, Oxford Road, Manchester, M13 9PT, UK
15Department of Biology, University of California – Riverside, Riverside, CA 92521, USA
16Department of Developmental Biology, University of Cologne, Cologne Biocenter, Institute of Zoology, Zuelpicher Straße 47b, 50674, Cologne, Germany
17Department of Earth Sciences, Palaeobiology, Uppsala University, Villavägen 16, 75236, Uppsala, Sweden
18Centro Andaluz de Biología del Desarrollo (CABD), Consejo Superior de Investigaciones Científicas/Universidad Pablo de Olavide, Sevilla, Spain
19Nucleo em Ecologia e Desenvolvimento SocioAmbiental de Macaé (NUPEM), Campus Macaé, Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro, 27941-222, Brazil
20School of Biological and Chemical Sciences, Queen Mary University of London, Mile End Road, E1 4NS London, UK
21Biology Department, University of Rochester, Rochester, NY 14627, USA
22Humboldt-Universität of Berlin, Institut für Biologie, Philippstr.13, 10115, Berlin, Germany
23Department of Evolutionary Developmental Genetics, Johann-Friedrich-Blumenbach-Institute, GZMB, Georg-August-University, Göttingen Campus, Justus von Liebig Weg 11, 37077, Göttingen, Germany
24Department of Biological Sciences, Graduate School of Science, Osaka University, Osaka, Japan
25Université libre de Bruxelles (ULB), Evolutionary Biology & Ecology, C.P. 160/12, Avenue F.D. Roosevelt 50, 1050, Brussels, Belgium

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Tài liệu tham khảo

Ohno S. Evolution by Gene Duplication. Berlin: Springer; 1970.

Semon M, Wolfe KH. Consequences of genome duplication. Curr Opin Genet Dev. 2007;17(6):505–12.

Yun S, Furlong M, Sim M, Cho M, Park S, Cho EB, Reyes-Alcaraz A, Hwang JI, Kim J, Seong JY. Prevertebrate local gene duplication facilitated expansion of the neuropeptide GPCR superfamily. Mol Biol Evol. 2015;32(11):2803–17.

Chipman AD, Ferrier DE, Brena C, Qu J, Hughes DS, Schroder R, Torres-Oliva M, Znassi N, Jiang H, Almeida FC, et al. The first myriapod genome sequence reveals conservative arthropod gene content and genome organisation in the centipede Strigamia maritima. PLoS Biol. 2014;12(11), e1002005.

Fawcett JA, Maere S, Van de Peer Y. Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. Proc Natl Acad Sci U S A. 2009;106(14):5737–42.

Li Z, Baniaga AE, Sessa EB, Scascitelli M, Graham SW, Rieseberg LH, Barker MS. Early genome duplications in conifers and other seed plants. Sci Adv. 2015;1(10), e1501084.

Wolfe KH, Shields DC. Molecular evidence for an ancient duplication of the entire yeast genome. Nature. 1997;387(6634):708–13.

Ma LJ, Ibrahim AS, Skory C, Grabherr MG, Burger G, Butler M, Elias M, Idnurm A, Lang BF, Sone T, et al. Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genet. 2009;5(7), e1000549.

Aury JM, Jaillon O, Duret L, Noel B, Jubin C, Porcel BM, Segurens B, Daubin V, Anthouard V, Aiach N, et al. Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature. 2006;444(7116):171–8.

Martens C, Van de Peer Y. The hidden duplication past of the plant pathogen Phytophthora and its consequences for infection. BMC Genomics. 2010;11:353.

Nossa CW, Havlak P, Yue JX, Lv J, Vincent KY, Brockmann HJ, Putnam NH. Joint assembly and genetic mapping of the Atlantic horseshoe crab genome reveals ancient whole genome duplication. GigaScience. 2014;3:9.

Bisbee CA, Baker MA, Wilson AC, Haji-Azimi I, Fischberg M. Albumin phylogeny for clawed frogs (Xenopus). Science. 1977;195(4280):785–7.

Amores A, Force A, Yan YL, Joly L, Amemiya C, Fritz A, Ho RK, Langeland J, Prince V, Wang YL, et al. Zebrafish hox clusters and vertebrate genome evolution. Science. 1998;282(5394):1711–4.

Flot JF, Hespeels B, Li X, Noel B, Arkhipova I, Danchin EG, Hejnol A, Henrissat B, Koszul R, Aury JM, et al. Genomic evidence for ameiotic evolution in the bdelloid rotifer Adineta vaga. Nature. 2013;500(7463):453–7.

Edger PP, Pires JC. Gene and genome duplications: the impact of dosage-sensitivity on the fate of nuclear genes. Chromosome Res. 2009;17(5):699–717.

Session AM, Uno Y, Kwon T, Chapman JA, Toyoda A, Takahashi S, Fukui A, Hikosaka A, Suzuki A, Kondo M, et al. Genome evolution in the allotetraploid frog Xenopus laevis. Nature. 2016;538(7625):336–43.

Jaillon O, Aury JM, Brunet F, Petit JL, Stange-Thomann N, Mauceli E, Bouneau L, Fischer C, Ozouf-Costaz C, Bernot A, et al. Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype. Nature. 2004;431(7011):946–57.

Davis JC, Petrov DA. Do disparate mechanisms of duplication add similar genes to the genome? Trends Genet. 2005;21(10):548–51.

Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics. 1999;151(4):1531–45.

Lynch M, Force A. The probability of duplicate gene preservation by subfunctionalization. Genetics. 2000;154(1):459–73.

Lynch M, O’Hely M, Walsh B, Force A. The probability of preservation of a newly arisen gene duplicate. Genetics. 2001;159(4):1789–804.

Lynch M, Conery JS. The evolutionary fate and consequences of duplicate genes. Science. 2000;290(5494):1151–5.

Kellis M, Birren BW, Lander ES. Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature. 2004;428(6983):617–24.

Putnam NH, Butts T, Ferrier DE, Furlong RF, Hellsten U, Kawashima T, Robinson-Rechavi M, Shoguchi E, Terry A, Yu JK, et al. The amphioxus genome and the evolution of the chordate karyotype. Nature. 2008;453(7198):1064–71.

Hakes L, Pinney JW, Lovell SC, Oliver SG, Robertson DL. All duplicates are not equal: the difference between small-scale and genome duplication. Genome Biol. 2007;8(10):R209.

Hurley IA, Mueller RL, Dunn KA, Schmidt EJ, Friedman M, Ho RK, Prince VE, Yang Z, Thomas MG, Coates MI. A new time-scale for ray-finned fish evolution. Proc Biol Sci. 2007;274(1609):489–98.

Furlong RF, Holland PW. Were vertebrates octoploid? Philos Trans R Soc Lond B Biol Sci. 2002;357(1420):531–44.

Donoghue PC, Purnell MA. Genome duplication, extinction and vertebrate evolution. Trends Ecol Evol. 2005;20(6):312–9.

McGinnis W, Krumlauf R. Homeobox genes and axial patterning. Cell. 1992;68(2):283–302.

Dehal P, Boore JL. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 2005;3(10), e314.

Kenny NJ, Chan KW, Nong W, Qu Z, Maeso I, Yip HY, Chan TF, Kwan HS, Holland PW, Chu KH, et al. Ancestral whole-genome duplication in the marine chelicerate horseshoe crabs. Heredity. 2016;116(2):190–9.

Ricci CN. Ecology of bdelloids: how to be successful. Hydrobiologia. 1987;147:117–27.

Rudkin DM, Young GA. Horseshoe crabs – an ancient ancestry revealed. In: Tanacredi JT, Botton ML, Smith DR, editors. Biology and Conservation of Horseshoe Crabs. Boston: Springer; 2009. p. 25–44.

Clarke TH, Garb JE, Hayashi CY, Arensburger P, Ayoub NA. Spider transcriptomes identify ancient large-scale gene duplication event potentially important in silk gland evolution. Genome Biol Evol. 2015;7(7):1856–70.

Clarke TH, Garb JE, Hayashi CY, Haney RA, Lancaster AK, Corbett S, Ayoub NA. Multi-tissue transcriptomics of the black widow spider reveals expansions, co-options, and functional processes of the silk gland gene toolkit. BMC Genomics. 2014;15:365.

Di Z, Yu Y, Wu Y, Hao P, He Y, Zhao H, Li Y, Zhao G, Li X, Li W, et al. Genome-wide analysis of homeobox genes from Mesobuthus martensii reveals Hox gene duplication in scorpions. Insect Biochem Mol Biol. 2015;61:25–33.

Janssen R, Le Gouar M, Pechmann M, Poulin F, Bolognesi R, Schwager EE, Hopfen C, Colbourne JK, Budd GE, Brown SJ, et al. Conservation, loss, and redeployment of Wnt ligands in protostomes: implications for understanding the evolution of segment formation. BMC Evol Biol. 2010;10:374.

Schwager EE, Schoppmeier M, Pechmann M, Damen WG. Duplicated Hox genes in the spider Cupiennius salei. Front Zool. 2007;4:10.

Sharma PP, Santiago MA, Gonzalez-Santillan E, Monod L, Wheeler WC. Evidence of duplicated Hox genes in the most recent common ancestor of extant scorpions. Evol Dev. 2015;17(6):347–55.

Sharma PP, Schwager EE, Extavour CG, Wheeler WC. Hox gene duplications correlate with posterior heteronomy in scorpions. Proc Biol Sci. 2014;281(1792).

Turetzek N, Pechmann M, Schomburg C, Schneider J, Prpic NM. Neofunctionalization of a duplicate dachshund gene underlies the evolution of a novel leg segment in arachnids. Mol Biol Evol. 2016;33(1):109–21.

Fuzita FJ, Pinkse MW, Patane JS, Juliano MA, Verhaert PD, Lopes AR. Biochemical, transcriptomic and proteomic analyses of digestion in the scorpion Tityus serrulatus: insights into function and evolution of digestion in an ancient arthropod. PLoS One. 2015;10(4), e0123841.

Fuzita FJ, Pinkse MW, Patane JS, Verhaert PD, Lopes AR. High throughput techniques to reveal the molecular physiology and evolution of digestion in spiders. BMC Genomics. 2016;17:716.

Leite DJ, Ninova M, Hilbrant M, Arif S, Griffiths-Jones S, Ronshaugen M, McGregor AP. Pervasive microRNA duplication in Chelicerates: insights from the embryonic microRNA repertoire of the spider Parasteatoda tepidariorum. Genome Biol Evol. 2016;8(7):2133–44.

Lawson D, Arensburger P, Atkinson P, Besansky NJ, Bruggner RV, Butler R, Campbell KS, Christophides GK, Christley S, Dialynas E, et al. VectorBase: a data resource for invertebrate vector genomics. Nucleic Acids Res. 2009;37(Database issue):D583–7.

Gulia-Nuss M, Nuss AB, Meyer JM, Sonenshine DE, Roe RM, Waterhouse RM, Sattelle DB, de la Fuente J, Ribeiro JM, Megy K, et al. Genomic insights into the Ixodes scapularis tick vector of Lyme disease. Nat Commun. 2016;7:10507.

Grbic M, Van Leeuwen T, Clark RM, Rombauts S, Rouze P, Grbic V, Osborne EJ, Dermauw W, Ngoc PC, Ortego F, et al. The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature. 2011;479(7374):487–92.

Cao Z, Yu Y, Wu Y, Hao P, Di Z, He Y, Chen Z, Yang W, Shen Z, He X, et al. The genome of Mesobuthus martensii reveals a unique adaptation model of arthropods. Nat Commun. 2013;4:2602.

Sanggaard KW, Bechsgaard JS, Fang X, Duan J, Dyrlund TF, Gupta V, Jiang X, Cheng L, Fan D, Feng Y, et al. Spider genomes provide insight into composition and evolution of venom and silk. Nat Commun. 2014;5:3765.

Babb PL, Lahens NF, Correa-Garhwal SM, Nicholson DN, Kim EJ, Hogenesch JB, Kuntner M, Higgins L, Hayashi CY, Agnarsson I, et al. The Nephila clavipes genome highlights the diversity of spider silk genes and their complex expression. Nat Genet. 2017;49(6):895–903.

Schwager EE, Schoenauer A, Leite DJ, Sharma PP, McGregor AP. Chelicerata. In: Wanninger A, editor. Evolutionary Developmental Biology of Invertebrates, vol. 3. Berlin: Spinger; 2015.

Yoshida H. A revision of the genus Achaearanea (Araneae: Theridiidae). Acta Arachnologica. 2008;57(1):37–40.

Sharma PP, Kaluziak ST, Pérez-Porro AR, González VL, Hormiga G, Wheeler WC, Giribet G. Phylogenomic interrogation of Arachnida reveals systemic conflicts in phylogenetic signal. Mol Biol Evol. 2014;31:2963–84.

Simao FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31(19):3210–2.

Altenhoff AM, Skunca N, Glover N, Train CM, Sueki A, Pilizota I, Gori K, Tomiczek B, Muller S, Redestig H, et al. The OMA orthology database in 2015: function predictions, better plant support, synteny view and other improvements. Nucleic Acids Res. 2015;43(Database issue):D240–9.

Colbourne JK, Pfrender ME, Gilbert D, Thomas WK, Tucker A, Oakley TH, Tokishita S, Aerts A, Arnold GJ, Basu MK, et al. The ecoresponsive genome of Daphnia pulex. Science. 2011;331(6017):555–61.

Schomburg C, Turetzek N, Schacht MI, Schneider J, Kirfel P, Prpic NM, Posnien N. Molecular characterization and embryonic origin of the eyes in the common house spider Parasteatoda tepidariorum. EvoDevo. 2015;6:15.

Samadi L, Schmid A, Eriksson BJ. Differential expression of retinal determination genes in the principal and secondary eyes of Cupiennius salei Keyserling (1877). EvoDevo. 2015;6:16.

Janssen R, Schönauer A, Weber M, Turetzek N, Hogvall M, Goss GE, Patel NH, McGregor AP, Hilbrant M. The evolution and expression of panarthropod frizzled genes. Front Ecol Evol. 2015;3:96.

Grabherr MG, Russell P, Meyer M, Mauceli E, Alfoldi J, Di Palma F, Lindblad-Toh K. Genome-wide synteny through highly sensitive sequence alignment: Satsuma. Bioinformatics. 2010;26(9):1145–51.

Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 2012;40(Database issue):D1178–86.

Hasegawa M, Kishino H, Yano T. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol. 1985;22(2):160–74.

Kagale S, Robinson SJ, Nixon J, Xiao R, Huebert T, Condie J, Kessler D, Clarke WE, Edger PP, Links MG, et al. Polyploid evolution of the Brassicaceae during the Cenozoic era. Plant Cell. 2014;26(7):2777–91.

Schaeper ND, Prpic NM, Wimmer EA. A clustered set of three Sp-family genes is ancestral in the Metazoa: evidence from sequence analysis, protein domain structure, developmental expression patterns and chromosomal location. BMC Evol Biol. 2010;10:88.

Akiyama-Oda Y, Oda H. Cell migration that orients the dorsoventral axis is coordinated with anteroposterior patterning mediated by Hedgehog signaling in the early spider embryo. Development. 2010;137(8):1263–73.

Pechmann M, Schwager EE, Turetzek N, Prpic NM. Regressive evolution of the arthropod tritocerebral segment linked to functional divergence of the Hox gene labial. Proc Biol Sci. 2015;282(1814):20151162.

Waddington J, Rudkin DM, Dunlop JA. A new mid-Silurian aquatic scorpion-one step closer to land? Biol Lett. 2015;11(1):20140815.

Dunlop JA. Geological history and phylogeny of Chelicerata. Arthropod Struct Dev. 2010;39(2-3):124–42.

Papp B, Pal C, Hurst LD. Dosage sensitivity and the evolution of gene families in yeast. Nature. 2003;424(6945):194–7.

Papp B, Pal C, Hurst LD. Evolution of cis-regulatory elements in duplicated genes of yeast. Trends Genet. 2003;19(8):417–22.

Abzhanov A, Popadic A, Kaufman TC. Chelicerate Hox genes and the homology of arthropod segments. Evol Dev. 1999;1(2):77–89.

Damen WG, Hausdorf M, Seyfarth EA, Tautz D. A conserved mode of head segmentation in arthropods revealed by the expression pattern of Hox genes in a spider. Proc Natl Acad Sci U S A. 1998;95(18):10665–70.

Regier JC, Shultz JW, Zwick A, Hussey A, Ball B, Wetzer R, Martin JW, Cunningham CW. Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences. Nature. 2010;463(7284):1079–83.

Scholtz G, Kamenz C. The book lungs of Scorpiones and Tetrapulmonata (Chelicerata, Arachnida): evidence for homology and a single terrestrialisation event of a common arachnid ancestor. Zoology. 2006;109(1):2–13.

Rota-Stabelli O, Daley AC, Pisani D. Molecular timetrees reveal a Cambrian colonization of land and a new scenario for ecdysozoan evolution. Curr Biol. 2013;23(5):392–8.

Lozano-Fernandez J, Carton R, Tanner AR, Puttick MN, Blaxter M, Vinther J, Olesen J, Giribet G, Edgecombe GD, Pisani D. A molecular palaeobiological exploration of arthropod terrestrialization. Philos Trans R Soc Lond B Biol Sci. 2016;371(1699): pii: 20150133.

Sharma PP, Wheeler WC. Cross-bracing uncalibrated nodes in molecular dating improves congruence of fossil and molecular age estimates. Front Zool. 2014;11:57.

Selden PA, Shear WA, Sutton MD. Fossil evidence for the origin of spider spinnerets, and a proposed arachnid order. Proc Natl Acad Sci U S A. 2008;105(52):20781–5.

Freeling M, Scanlon MJ, Fowler JE. Fractionation and subfunctionalization following genome duplications: mechanisms that drive gene content and their consequences. Curr Opin Genet Dev. 2015;35:110–8.

Glasauer SM, Neuhauss SC. Whole-genome duplication in teleost fishes and its evolutionary consequences. Mol Genet Genomics. 2014;289(6):1045–60.

Holland LZ. Evolution of new characters after whole genome duplications: insights from amphioxus. Semin Cell Dev Biol. 2013;24(2):101–9.

Clarke JT, Lloyd GT, Friedman M. Little evidence for enhanced phenotypic evolution in early teleosts relative to their living fossil sister group. Proc Natl Acad Sci U S A. 2016;113(41):11531–6.

Hilbrant M, Damen WG, McGregor AP. Evolutionary crossroads in developmental biology: the spider Parasteatoda tepidariorum. Development. 2012;139(15):2655–62.

McGregor AP, Hilbrant M, Pechmann M, Schwager EE, Prpic NM, Damen WG. Cupiennius salei and Achaearanea tepidariorum: Spider models for investigating evolution and development. Bioessays. 2008;30(5):487–98.

Oda H, Akiyama-Oda Y. Differing strategies for forming the arthropod body plan: lessons from Dpp, Sog and Delta in the fly Drosophila and spider Achaearanea. Develop Growth Differ. 2008;50(4):203–14.

Posnien N, Zeng V, Schwager EE, Pechmann M, Hilbrant M, Keefe JD, Damen WGM, Prpic N-M, McGregor AP, Extavour CG. A comprehensive reference transcriptome resource for the common house spider Parasteatoda tepidariorum. PLoS ONE. 2014;9(8), e104885.

Gnerre S, Maccallum I, Przybylski D, Ribeiro FJ, Burton JN, Walker BJ, Sharpe T, Hall G, Shea TP, Sykes S, et al. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci U S A. 2011;108(4):1513–8.

BCM-HGSC Software. https://www.hgsc.bcm.edu/software/ .

Flot JF, Marie-Nelly H, Koszul R. Contact genomics: scaffolding and phasing (meta)genomes using chromosome 3D physical signatures. FEBS Lett. 2015;589(20 Pt A):2966–74.

Putnam NH, O’Connell BL, Stites JC, Rice BJ, Blanchette M, Calef R, Troll CJ, Fields A, Hartley PD, Sugnet CW, et al. Chromosome-scale shotgun assembly using an in vitro method for long-range linkage. Genome Res. 2016;26(3):342–50.

Scalable Nucleotide Alignment Program. http://snap.cs.berkeley.edu .

Stanke M, Diekhans M, Baertsch R, Haussler D. Using native and syntenically mapped cDNA alignments to improve de novo gene finding. Bioinformatics. 2008;24(5):637–44.

Oda H, Nishimura O, Hirao Y, Tarui H, Agata K, Akiyama-Oda Y. Progressive activation of Delta-Notch signaling from around the blastopore is required to set up a functional caudal lobe in the spider Achaearanea tepidariorum. Development. 2007;134(12):2195–205.

Smit A, Hubley R, Green P. Repeatmasker open-3.0. 1996-2010. http://www.repeatmasker.org .

Benson G. Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res. 1999;27(2):573–80.

Price AL, Jones NC, Pevzner PA. De novo identification of repeat families in large genomes. Bioinformatics. 2005;21 Suppl 1:i351–8.

Haas BJ, Salzberg SL, Zhu W, Pertea M, Allen JE, Orvis J, White O, Buell CR, Wortman JR. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol. 2008;9(1):R7.

Parra G, Bradnam K, Korf I. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics. 2007;23(9):1061–7.

Wu TD, Nacu S. Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics. 2010;26(7):873–81.

UniProtConsortium. Activities at the Universal Protein Resource (UniProt). Nucleic Acids Res. 2014;42(Database issue):D191–8.

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10.

Kent WJ. BLAT--the BLAST-like alignment tool. Genome Res. 2002;12(4):656–64.

Roberts A, Pachter L. Streaming fragment assignment for real-time analysis of sequencing experiments. Nat Methods. 2013;10(1):71–3.

Slater GS, Birney E. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics. 2005;6:31.

Trinotate: Transcriptome Functional Annotation and Analysis. https://trinotate.github.io/ .

HMMER: biosequence analysis using profile hidden Markov models. http://hmmer.org/ .

HPC GridRunner. http://hpcgridrunner.github.io/ .

SQLite. https://www.sqlite.org/ .

JBrowse/Web Apollo Parasteatoda tepidariorum. https://i5k.nal.usda.gov/JBrowse-partep .

Campbell MS, Holt C, Moore B, Yandell M. Genome Annotation and Curation Using MAKER and MAKER-P. Curr Protoc Bioinformatics. 2014;48:4.11.11–39.

RNA sequencing of Centruroides exilicauda whole organism sample CEXI.00-juvenile. http://www.ncbi.nlm.nih.gov/sra/SRX911075 .

RNA sequencing of Centruroides exilicauda whole organism sample CEXI.00-female. http://www.ncbi.nlm.nih.gov/sra/SRX911064 .

RNA sequencing of Centruroides exilicauda whole organism sample CEXI.00-male. http://www.ncbi.nlm.nih.gov/sra/SRX911079 .

Centruroides Genome Browser. https://apollo.nal.usda.gov/cenexi/jbrowse .

Centruroides sculpturatus MAKER annotation. ftp://ftp.hgsc.bcm.edu/I5K-pilot/Bark_scorpion/ .

Battelle BA, Ryan JF, Kempler KE, Saraf SR, Marten CE, Warren WC, Minx P, Montague MJ, Green PJ, Schmidt SA, Fulton L, Patel NH, Protas ME, Wilson RK, Porter ML. Opsin repertoire and expression patterns in horseshoe crabs: evidence from the genome of Limulus polyphemus (Arthropoda: Chelicerata). Genome Biol Evol. 2016;8(5):1571-89. doi: 10.1093/gbe/evw100 .

Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012;40(7), e49.

Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics. 2012;28(23):3150–2.

Altenhoff AM, Gil M, Gonnet GH, Dessimoz C. Inferring hierarchical orthologous groups from orthologous gene pairs. PLoS One. 2013;8(1), e53786.

Altenhoff AM, Schneider A, Gonnet GH, Dessimoz C. OMA 2011: orthology inference among 1000 complete genomes. Nucleic Acids Res. 2011;39(Database issue):D289–94.

Waterhouse RM, Tegenfeldt F, Li J, Zdobnov EM, Kriventseva EV. OrthoDB: a hierarchical catalog of animal, fungal and bacterial orthologs. Nucleic Acids Res. 2013;41(Database issue):D358–65.

Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32(5):1792–7.

Castresana J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol. 2000;17(4):540–52.

Le SQ, Dang CC, Gascuel O. Modeling protein evolution with several amino acid replacement matrices depending on site rates. Mol Biol Evol. 2012;29(10):2921–36.

Yang Z. Among-site rate variation and its impact on phylogenetic analyses. Trends Ecol Evol. 1996;11(9):367–72.

Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22(21):2688–90.

Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol. 2011;29(7):644–52.

Capella-Gutierrez S, Silla-Martinez JM, Gabaldon T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25(15):1972–3.

TreeSoft: Softwares for Phylogenetic Trees. http://treesoft.sourceforge.net/treebest.shtml .

McCarthy FM, Wang N, Magee GB, Nanduri B, Lawrence ML, Camon EB, Barrell DG, Hill DP, Dolan ME, Williams WP, et al. AgBase: a functional genomics resource for agriculture. BMC Genomics. 2006;7:229.

Edwards JH. The Oxford Grid. Ann Hum Genet. 1991;55(Pt 1):17–31.

Orthodotter. http://www.genoscope.cns.fr/orthodotter .

Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. Circos: an information aesthetic for comparative genomics. Genome Res. 2009;19(9):1639–45.

Zhong Y-F, Butts T, Holland PWH. HomeoDB: a database of homeobox gene diversity. Evol Dev. 2008;10(5):516–8.

Zhong Y-F, Holland PWH. HomeoDB2: functional expansion of a comparative homeobox gene database for evolutionary developmental biology. Evol Dev. 2011;13(6):567–8.

Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. BLAST+: architecture and applications. BMC Bioinformatics. 2009;10:421.

Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, et al. CDD: NCBI’s conserved domain database. Nucleic Acids Res. 2015;43(Database issue):D222–6.

Holland PW, Booth HA, Bruford EA. Classification and nomenclature of all human homeobox genes. BMC Biol. 2007;5:47.

Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28(12):1647–9.

Sharma PP, Schwager EE, Extavour CG, Giribet G. Hox gene expression in the harvestman Phalangium opilio reveals divergent patterning of the chelicerate opisthosoma. Evol Dev. 2012;14(5):450–63.

Akiyama-Oda Y, Oda H. Early patterning of the spider embryo: a cluster of mesenchymal cells at the cumulus produces Dpp signals received by germ disc epithelial cells. Development. 2003;130(9):1735–47.

Prpic NM, Schoppmeier M, Damen WG. The American Wandering Spider Cupiennius salei. Cold Spring Harb Protoc. 2008. doi: 10.1101/pdb.emo103 .

Mittmann B, Wolff C. Embryonic development and staging of the cobweb spider Parasteatoda tepidariorum C. L. Koch, 1841 (syn.: Achaearanea tepidariorum; Araneomorphae; Theridiidae). Dev Genes Evol. 2012;222(4):189–216.

Bond JE, Garrison NL, Hamilton CA, Godwin RL, Hedin M, Agnarsson I. Phylogenomics resolves a spider backbone phylogeny and rejects a prevailing paradigm for orb web evolution. Curr Biol. 2014;24(15):1765–71.

Sharma PP, Giribet G. A revised dated phylogeny of the arachnid order Opiliones. Front Genet. 2014;5:255.