Abstract
Spiders, scorpions, mites and ticks (chelicerates) form one of the most diverse groups of arthropods on land, but their origin and times of diversification are not yet established. We estimated, for the first time, the molecular divergence times for these chelicerates using complete mitochondrial sequences from 25 taxa. All mitochondrial genes were evaluated individually or after concatenation. Sequences belonging to three missing genes (ND3, 6, and tRNA-Asp) from three taxa, as well as the faster-evolving ribosomal RNAs (12S and 16S), tRNAs, and the third base of each codon from 11 protein-coding genes (PCGs) (COI-III, CYTB, ATP8, 6, ND1-2, 4L, and 4-5), were identified and removed. The remaining concatenated sequences from 11 PCGs produced a completely resolved phylogenetic tree and confirmed that all chelicerates are monophyletic. Removing the third base from each codon was essential to resolve the phylogeny, which allowed deep divergence times to be calculated using three nodes calibrated with upper and lower priors. Our estimates indicate that the orders and classes of spiders, scorpions, mites, and ticks diversified in the late Paleozoic, much earlier than previously reported from fossil date estimates. The divergence time estimated for ticks suggests that their first land hosts could have been amphibians rather than reptiles. Using molecular data, we separated the spider-scorpion clades and estimated their divergence times at 397 ± 23 million years ago. Algae, fungi, plants, and animals, including insects, were well established on land when these chelicerates diversified. Future analyses, involving mitochondrial sequences from additional chelicerate taxa and the inclusion of nuclear genes (or entire genomes) will provide a more complete picture of the evolution of the Chelicerata, the second most abundant group of animals on earth.
Similar content being viewed by others
References
Black-IV WC, Roehrdanz RL (1998) Mitochondrial gene order is not conserved in arthropods: prostriate and metastriate tick mitochondrial genomes. Mol Biol Evol 15:1772–1785
Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27:1767–1780. doi:10.1093/nar/27.8.1767
Choi EH, Park SJ, Jang KH, Hwang W (2007) Complete mitochondrial genome of a Chinese scorpion Mesobuthus martensii (Chelicerata, Scorpiones, Buthidae). DNA Seq 18:459–471. doi:10.1080/10425170701289883
Crease TJ (1999) The complete sequence of the mitochondrial genome of Daphnia pulex (Cladocera: Crustacea). Gene 233:89–99. doi:10.1016/S0378-1119(99)00151-1
Davila S, Pinero D, Bustos P, Cevallos MA, Davila G (2005) The mitochondrial genome sequence of the scorpion Centruroides limpidus (Karsch 1879) (Chelicerata: Arachnida). Gene 360:92–102. doi:10.1016/j.gene.2005.06.008
Donoghue PCJ, Benton MJ (2007) Rocks and clocks: calibrating the tree of life using fossils and molecules. Trends Ecol Evol 22:424–431. doi:10.1016/j.tree.2007.05.005
Dunlop JA, Selden PA (1998) Early history and phylogeny of the chelicerates. In: Fortey RA, Thomas RH (eds) Arthropod relationships. Chapman & Hall, London, pp 221–237
Evans GO (1992) Principles of Acarology. C.A.B. International, Wallingford
Evans JD, Lopez DL (2002) Complete mitochondrial DNA sequence of the important honey bee pest, Varroa destructor (Acari: Varroidae). Exp Appl Acarol 27:69–78. doi:10.1023/A:1021574306010
Flook PK, Rowell CH, Gellissen G (1995) The sequence, organization, and evolution of the Locusta migratoria mitochondrial genome. J Mol Evol 41:928–941. doi:10.1007/BF00173173
Gantenbein B, Fet V, Ganteinbein-Ritter IA, Balloux F (2005) Evidence for recombination in scorpion mitochondrial DNA (Scorpiones: Buthidae). Proc R Soc Lond B Biol Sci 272:697–704. doi:10.1098/rspb.2004.3017
Hall BG (2001) Phylogenetic trees made easy. Sinauer Associates, Inc., Sunderland
Hall BG (2004) CodonAlign Version 2.0. Sinauer Associates, Inc., Sunderland
Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB (2001) Molecular evidence for the early colonization of land by fungi and plants. Science 293:1129–1133. doi:10.1126/science.1061457
Hedges SB, Kumar S (2003) Genomic clocks and evolutionary timescales. Trends Genet 19:200–206. doi:10.1016/S0168-9525(03)00053-2
Hoogstraal H (1978) Biology of ticks. In: Wilde JKH (ed) Tick-borne diseases and their vectors. Edinburg University Press, Edinburg, pp 3–14
Huelsenbeck JP, Ronquist F (2001) MrBayes: Bayesian inference of phylogeny. Bioinformatics 17:754–755. doi:10.1093/bioinformatics/17.8.754
Inoue JG, Miya M, Venkatesh B, Nishida M (2005) The mitochondrial genome of Indonesian coelacanth Latimeria menadoensis (Sarcopterygii: Coelacanthiformes) and divergence time estimation between the two coelacanths. Gene 349:227–235. doi:10.1016/j.gene.2005.01.008
Jeyaprakash A, Hoy MA (2007) The mitochondrial genome of the predatory mite Metaseiulus occidentalis (Arthropoda: Chelicerata: Acari: Phytoseiidae) is unexpectedly large and contains several novel features. Gene 391:264–274. doi:10.1016/j.gene.2007.01.012
Klompen H, Grimaldi D (2001) First record of a parasitiform mite: a larval argasid tick in Cretaceous amber (Acari: Ixodida: Argasidae). Ann Entomol Soc Am 94:10–15. doi:10.1603/0013-8746(2001)094[0010:FMROAP]2.0.CO;2
Klompen JSH, Black-IV WC, Keirans JE, Oliver JH Jr (1996) Evolution of ticks. Annu Rev Entomol 41:141–161. doi:10.1146/annurev.en.41.010196.001041
Klompen H, Lekveishvili M, Black-IV WC (2007) Phylogeny of parasitiform mites (Acari) based on rRNA. Mol Phylogenet Evol 43:936–951. doi:10.1016/j.ympev.2006.10.024
Kumar S, Hedges SB (1998) A molecular timescale for vertebrate evolution. Nature 392:917–920. doi:10.1038/31927
Lavrov DV, Boore JL, Brown WM (2000a) The complete mitochondrial DNA sequence of the horseshoe crab Limulus polyphemus. Mol Biol Evol 17:813–824
Lavrov DV, Boore JL, Brown WM (2000b) A novel RNA editing occurs in the mitochondrial tRNAs of the centipede Lithobius forficatus. Proc Natl Acad Sci USA 97:13738–13742. doi:10.1073/pnas.250402997
Lavrov DV, Boore JL, Brown WM (2002) Complete mtDNA sequences of two millipedes suggest a new model for mitochondrial gene rearrangements: duplication and nonrandom loss. Mol Biol Evol 19:163–169
Lewis DL, Farr CL, Kaguni LS (1995) Drosophila melanogaster mitochondrial DNA: completion of the nucleotide sequence and evolutionary comparisons. Insect Mol Biol 4:263–278. doi:10.1111/j.1365-2583.1995.tb00032.x
Lourenco WR, Gall JC (2004) Fossil scorpion from the Buntsandstein (Early Triassic) of France. C R Palevol 3:369–378. doi:10.1016/j.crpv.2004.06.006
Loytynoja Q, Goldman N (2008) Phylogeny-aware gap placement prevents errors in sequence alignment and evolutionary analysis. Science 320:1632–1635. doi:10.1126/science.1158395
Maddison WP, Maddison DR (1992) MacClade analysis of phylogeny and character evolution. Sinauer Associates, Inc., Sunderland
Manuel M, Jager M, Murienne J, Clabaut C, Guyader HL (2006) Hox genes in sea spiders (Pycnogonida) and the homology of arthropod head segments. Dev Genes Evol 216:481–491. doi:10.1007/s00427-006-0095-2
Masta SE, Boore JL (2004) The complete mitochondrial genome sequence of the spider Habronattus oregonensis reveals rearranged and extremely truncated tRNAs. Mol Biol Evol 21:893–902. doi:10.1093/molbev/msh096
Mitani H, Talbert A, Fukunaga M (2004) New world relapsing fever Borrelia found in Ornithodoros porcinus ticks in central Tanzania. Microbiol Immunol 48:501–505
Navajas M, le Conte Y, Solignac M, Cros-Arteil S, Cornuet J-M (2002) The complete sequence of the mitochondrial genome of the honeybee ectoparasite mite Varroa destructor (Acari: Mesostigmata). Mol Biol Evol 19:2313–2317
Negrisolo E, Minelli A, Valle G (2004a) Extensive gene order rearrangement in the mitochondrial genome of the centipede Scutigera coleoptrata. J Mol Evol 58:413–423. doi:10.1007/s00239-003-2563-x
Negrisolo E, Minelli A, Valle G (2004b) The mitochondrial genome of the house centipede Scutigera and the monophyly versus paraphyly of myriapods. Mol Biol Evol 21:770–780. doi:10.1093/molbev/msh078
Norton RA, Bonamo PM, Grierson JD, Shear WM (1988) Oribatid mite fossils from a Devonian deposit near Gilboa, New York State. J Paleontol 62:259–269
Pennisi E (2008) Building the tree of life, genome by genome. Science 320:1716–1717. doi:10.1126/science.320.5884.1716
Penny D, Selden PA (2002) The oldest linyphiid spider, in lower Cretaceous Lebanese amber (Araneae, Linyphiidae, Linyphiinae). J Arachnol 30:487–493. doi:10.1636/0161-8202(2002)030[0487:TOLSIL]2.0.CO;2
Perez ML, Valverde JR, Batuecas B, Amat F, Marco R, Garesse R (1994) Speciation in the Artemia genus: mitochondrial DNA analysis of bisexual and parthenogenetic brine shrimps. J Mol Evol 38:156–168. doi:10.1007/BF00166162
Pisani D, Poling LL, Lyons-Weiler M, Hedges SB (2004) The colonization of land by animals: molecular phylogeny and divergence times among arthropods. BMC Biol 2:1–10. http://www.biomedcentral.com/1741-7007/2/1. doi:10.1186/1741-7007-2-1
Podsiadlowski L, Braband A (2006) The complete mitochondrial genome of the sea spider Nymphon gracile (Arthropoda: Pycnogonida). BMC Genomics 7:1–13. http://www.biomedcentral.com/1471-2164/7/284. doi:10.1186/1471-2164-7-284
Podsiadlowski L, Kohlhagen H, Koch M (2007) The complete mitochondrial genome of Scutigerella causeyae (Myriapoda: Symphyla) and the phylogenetic position of Symphyla. Mol Phylogenet Evol 45:251–260. doi:10.1016/j.ympev.2007.07.017
Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818. doi:10.1093/bioinformatics/14.9.817
Qiu Y, Song D, Zhou K, Sun H (2005) The mitochondrial sequences of Heptathela hangzhouensis and Ornithoctonus huwena reveal unique gene arrangements and atypical tRNAs. J Mol Evol 60:57–71. doi:10.1007/s00239-004-0010-2
Sanderson MJ (2003) r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19:301–302. doi:10.1093/bioinformatics/19.2.301
Sanderson MJ (2008) Phylogenetic signal in the eukaryotic tree of life. Science 321:121–123. doi:10.1126/science.1154449
Shao R, Aoki Y, Mitani H, Tabuchi N, Barker SC, Fukunaga M (2004) The mitochondrial genomes of soft ticks have an arrangement of genes that has remained unchanged for over 400 million years. Insect Mol Biol 13:219–224. doi:10.1111/j.0962-1075.2004.00447.x
Shao R, Barker SC, Mitani H, Aoki Y, Fukunaga M (2005a) Evolution of duplicate control regions in the mitochondrial genomes of Metazoa: a case study with Australian Ixodes ticks. Mol Biol Evol 22:620–629. doi:10.1093/molbev/msi047
Shao R, Mitani H, Barker SC, Takahashi M, Fukunaga M (2005b) Novel mitochondrial gene content and gene arrangement indicate illegitimate inter-mtDNA recombination in the chigger mite, Leptotrombidium pallidum. J Mol Evol 60:764–773. doi:10.1007/s00239-004-0226-1
Shao R, Barker SC, Mitani H, Takahashi M, Fukunaga M (2006) Molecular mechanisms for the variation of mitochondrial gene content and gene arrangement among chigger mites of the genus Leptotrombidium (Acari: Acariformes). J Mol Biol 63:251–261
Shultz JW, Regier JC (2000) Phylogenetic analysis of arthropods using two nuclear protein-encoding genes supports a crustacean + hexapod clade. Proc R Soc Lond B Biol Sci 267:1011–1019. doi:10.1098/rspb.2000.1104
Swofford DL (2002) PAUP* phylogenetic analysis using parsimony, version 4. Sinauer Associates, Inc., Sunderland
Thorne JL, Kishino H, Painter IS (1998) Estimating the rate of evolution of the rate of molecular evolution. Mol Biol Evol 15:1647–1657
Waloszek D, Dunlop JA (2002) A larval sea spider (Arthropoda: Pycnogonida) from the Upper Cambrian ‘Orsten’ of Sweden and the phylogenetic position of pycnogonids. Palaentol 45:421–436. doi:10.1111/1475-4983.00244
Webster BL, Copley RR, Jenner RA, Mackenzie-Dodds JA, Bourlat SJ, Rota-Stabelli O et al (2006) Mitogenomics and phylogenomics reveal priapulid worms as extant models of the ancestral ecdysozoan. Evol Dev 8:502–510. doi:10.1111/j.1525-142X.2006.00123.x
Webster BL, Mackenzie-Dodds JA, Telford MJ, Littlewood DTJ (2007) The mitochondrial genome of Priapulus caudatus Lamarck (Priapulida: Priapulidae). Gene 389:96–105. doi:10.1016/j.gene.2006.10.005
Yang Z (1997) PAML: a program package for phylogenetics analysis by maximum likelihood. Comput Appl Biosci 13:555–556
Yang Z, Yoder AD (2003) Comparison of likelihood and Bayesian methods for estimating divergence times using multiple gene loci and calibration points, with application to a radiation of cute-looking mouse lemur species. Syst Biol 52:705–716. doi:10.1080/10635150390235557
Acknowledgment
The research was supported in part by the Davies, Fisher, and Eckes endowment in biological control to Marjorie A. Hoy.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Jeyaprakash, A., Hoy, M.A. First divergence time estimate of spiders, scorpions, mites and ticks (subphylum: Chelicerata) inferred from mitochondrial phylogeny. Exp Appl Acarol 47, 1–18 (2009). https://doi.org/10.1007/s10493-008-9203-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10493-008-9203-5