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Evolution of Satellite DNAs in a Radiation of Endemic Hawaiian Spiders: Does Concerted Evolution of Highly Repetitive Sequences Reflect Evolutionary History?

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Abstract

Satellite DNAs are known for an unusual and nonuniform evolution characterized by rapid evolutionary change between species and concerted evolution leading to molecular homogeneity within species. In this paper we use satellite DNAs for phylogenetic analysis of a rapidly evolving lineage of spiders and compare the phylogeny with a hypothesis previously generated based on mitochondrial DNA and allozymes. The spiders examined include almost all species within a monophyletic clade of endemic Hawaiian Tetragnatha species, the spiny-leg clade. The phylogeny based on satellite sequences is largely congruent to those produced by mtDNA and allozymes, except that the satellite DNA yields much longer branches, with higher levels of support for any given node. Closely related species that have differentiated ecologically within an island are well resolved with satellite DNA but much less so with mtDNA. These results suggest that Tetragnatha stDNA repeats seem to be evolving gradually and cohesively during the diversification of these endemic Hawaiian spiders. The study also reveals gain–loss of satellite DNA copies during species diversification. We conclude that satellite DNA sequences may potentially be very useful for resolving relationships between rapidly evolving taxa within an adaptive radiation. In addition, satellite DNA as a nuclear marker suggests that hybridization or peripatry could play a possible role in species formation that cannot be revealed by mitochondrial markers due to its maternal inheritance.

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References

  • I A’lvarez JF Wendel (2003) ArticleTitleRibosomal ITS sequences and plant phylogenetic inference Mol Phylogenet Evol 29 417–434

    Google Scholar 

  • U Arnason S Gretarsdottir B Widegren (1992) ArticleTitleMysticetae (baleen whale) relationships based upon the sequence of the common cetacean DNA satellite Mol Biol Evol 9 1018–1028

    Google Scholar 

  • L Bachmann D Sperlich (1993) ArticleTitleGradual evolution of a specific satellite DNA family in Drosophila ambigua, D. tristis, and D. obscura Mol Biol Evol 10 647–659

    Google Scholar 

  • DL Brutlag (1980) ArticleTitleMolecular arrangement and evolution of heterochromatin DNA Annu Rev Genet 14 121–144

    Google Scholar 

  • HL Carson DA Clague (1995) Geology and biogeography of the Hawaiian Islands WL Wagner V Funk (Eds) Hawaiian biogeography: Evolution on a hot spot archipelago Smithsonian Institution Press Washington, DC 14–29

    Google Scholar 

  • R la Herran Particlede CR Rejon MR Rejon MA Garrido-Ramos (2001) ArticleTitleThe molecular phylogeny of the Sparidae (Pisces, Perciformes) based on two satellite DNA families Heredity 87 691–697

    Google Scholar 

  • GA Dover (2002) ArticleTitleMolecular drive Trends Genet 18 587–589

    Google Scholar 

  • JF Elder BJ Turner (1995) ArticleTitleConcerted evolution of repetitive DNA sequences in eukaryotes Q Rev Biol 70 297–323 Occurrence Handle10.1086/419073 Occurrence Handle1:CAS:528:DyaK2sXksFGrurY%3D Occurrence Handle7568673

    Article  CAS  PubMed  Google Scholar 

  • RG Gillespie (1991) ArticleTitleHawaiian spiders of the genus Tetragnatha. I. Spiny leg clade J Arachnol 19 174–209

    Google Scholar 

  • RG Gillespie (1999) ArticleTitleComparison of rates of speciation in web-building and non-web-building groups within a Hawaiian spider radiation J Arachnol 27 79–85

    Google Scholar 

  • RG Gillespie (2002) ArticleTitleHawaiian spiders of the genus Tetragnatha. IV: New, small species in the spiny leg clade J Arachnol 30 159–172

    Google Scholar 

  • R Gillespie (2004) ArticleTitleCommunity assembly through adaptive radiation in Hawaiian spiders Science 303 356–359

    Google Scholar 

  • RG Gillespie SR Palumbi HB Groom (1994) ArticleTitleMultiple origins of a spider radiation in Hawaii Proc Natl Acad Sci USA 91 2290–2294

    Google Scholar 

  • RG Gillespie HB Croom GL Hasty (1997) ArticleTitlePhylogenetic relationships and adaptive shifts among major clades of Tetragnatha spiders (Araneae: Tetragnathidae) in Hawai’i Pacif Sci 51 380–394

    Google Scholar 

  • DS Gladstein WC Wheeler (1997) POY: The optimization of alignment characters American Museum of Natural History New York

    Google Scholar 

  • DM Hillis C Moritz CA Porter RJ Baker (1991) ArticleTitleEvidence for biased gene conversion in concerted evolution of ribosomal DNA Science 251 308–310

    Google Scholar 

  • G Hormiga MA Arnedo RG Gillespie (2003) ArticleTitleSpeciation on a conveyor belt: sequential colonization of the Hawaiian Islands by Orsonwelles spiders (Araneae: Linyphiidae) Syst Biol 52 70–88

    Google Scholar 

  • JP Huelsenbeck F Ronquist (2001) ArticleTitleMRBAYES: Bayesian inference of phylogenetic trees Bioinformatics 17 754–755 Occurrence Handle10.1093/bioinformatics/17.8.754 Occurrence Handle1:STN:280:DC%2BD3MvotV2isw%3D%3D Occurrence Handle11524383

    Article  CAS  PubMed  Google Scholar 

  • S Jordan C Simon D Polhemus (2003) ArticleTitleMolecular systematics and adaptive radiation of Hawaii’s endemic damselfly genus Megalagrion (Odonata: Coenagrionidae) Syst Biol 52 89–109

    Google Scholar 

  • R Kalendar J Tanskanen S Immonen E Nevo AH Schulman (2000) ArticleTitleGenome evolution of wild barley (Hordeum spontaneum) by BARE-1 retrotransposon dynamics in response to sharp microclimatic divergence Proc Natl Acad Sci USA 97 6603–6607 Occurrence Handle10.1073/pnas.110587497 Occurrence Handle1:CAS:528:DC%2BD3cXktFaju7Y%3D Occurrence Handle10823912

    Article  CAS  PubMed  Google Scholar 

  • N Mestrovic M Plohl B Mravinac D Ugarkovic (1998) ArticleTitleEvolution of satellite DNAs from the genus Palorus—Experimental evidence for the “library” hypothesis Mol Biol Evol 15 1062–1068

    Google Scholar 

  • GL Miklos AC Gill (1981) ArticleTitleThe DNA sequences of cloned complex satellite DNAs from Hawaiian Drosophila and their bearing on satellite DNA sequence conservation Chromosoma 82 409–427

    Google Scholar 

  • T Ohta GA Dover (1984) ArticleTitleThe cohesive population genetics of molecular drive Genetics 108 501–521

    Google Scholar 

  • F Panzera R Perez Y Panzera F A’lvarez E Scvortzoff R Salvatella (1995) ArticleTitleKaryotype evolution in holocentric chromosomes of three related species of triatomines (Hemiptera–Reduviidae) Chromosome Res 3 143–150

    Google Scholar 

  • J Pons RG Gillespie (2003) ArticleTitleCommon origin of the satellite DNAs of Hawaiian spiders of the genus Tetragnatha: Evolutionary constraints on the length and nucleotide composition of the repeats Gene 313 169–177

    Google Scholar 

  • J Pons E Petitpierre C Juan (2002) ArticleTitleEvolutionary dynamics of satellite DNA family PIM357 in species of the genus Pimelia (Tenebrionidae, Coleoptera) Mol Biol Evol 19 1329–1340

    Google Scholar 

  • J Pons B Bruvo E Petitpierre M Plohl D Ugarkovic C Juan (2004) ArticleTitleComplex structural features of satellite DNA sequences in the genus Pimelia (Coleoptera: Tenebrionidae): Random differential amplification from a common satellite DNA library Heredity 92 418–427

    Google Scholar 

  • D Posada KA Crandall (1998) ArticleTitleModeltest: testing the model of DNA substitution Bioinformatics 14 817–818 Occurrence Handle10.1093/bioinformatics/14.9.817 Occurrence Handle1:CAS:528:DyaK1MXktlCltw%3D%3D Occurrence Handle9918953

    Article  CAS  PubMed  Google Scholar 

  • J Rozas R Rozas (1997) ArticleTitleDnaSP version 2.0, a novel software package for extensive molecular population genetic analysis Comput Applic Biosci 13 307–311

    Google Scholar 

  • T Strachan D Webb GA Dover (1985) ArticleTitleTransition stages of molecular drive in multiple-copy DNA families in Drosophila EMBO J 4 1701–1708

    Google Scholar 

  • DL Swofford (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and other methods) Sinauer Associates Sunderland, MA

    Google Scholar 

  • M Trick GA Dover (1984) ArticleTitleUnexpectedly slow homogenization within a repetitive DNA family shared between two subspecies of tsetse fly J Mol Evol 20 322–329

    Google Scholar 

  • D Ugarkovic M Plohl (2002) ArticleTitleVariation in satellite DNA profiles—causes and effects EMBO J 21 5955–5959 Occurrence Handle10.1093/emboj/cdf612 Occurrence Handle1:CAS:528:DC%2BD38XptFOrt7w%3D Occurrence Handle12426367

    Article  CAS  PubMed  Google Scholar 

  • WL Wagner V Funk (1995) Hawaiian biogeography: Evolution on a hot spot archipelago Smithsonian Institution Press Washington, DC

    Google Scholar 

  • WC Wheeler (1996) ArticleTitleOptimization alignment: The end of multiple sequence alignment in phylogenetics? Cladistics 12 1–9

    Google Scholar 

  • WC Wheeler (2002) Optimization alignment: down, up, error, and improvements R DeSalle G Giribet WC Wheeler (Eds) Techniques in molecular systematics and evolution Birkhäuser Basel 55–69

    Google Scholar 

  • WC Wheeler (2003) ArticleTitleImplied alignment: A synapomorphy-based multiple-sequence alignment method and its use in cladogram search Cladistics 19 261–268

    Google Scholar 

Download references

Acknowledgments

This work was funded by a grant from the Obra Cultural i Social Sa Nostra Fundation (Spain) to J.P., with additional funds from the Schlinger Foundation, and a National Science Foundation (DEB 9726573) grant to R.G.G. For help with fieldwork, we are indebted to Haleakala National Park, the Nature Conservancy of Hawaii, Maui Pineapple Company, the State Department of Land and Natural Resources, and the Hawaii Natural Areas Reserve System. For help with collecting we owe particular thanks to M.A. Arnedo, R. Bartlett, C.F. Davenport, J. Giffin, A.C. Medeiros, D. Preston, and G.K. Roderick. We also thank M.A. Arnedo for help with the POY analysis.

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Correspondence to Joan Pons.

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Reviewing Editor: Dr. Rafael Zardoya

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Pons, J., Gillespie, R.G. Evolution of Satellite DNAs in a Radiation of Endemic Hawaiian Spiders: Does Concerted Evolution of Highly Repetitive Sequences Reflect Evolutionary History?. J Mol Evol 59, 632–641 (2004). https://doi.org/10.1007/s00239-004-2655-2

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