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Mitochondrial markers reveal deep population subdivision in the European protected spider Macrothele calpeiana (Walckenaer, 1805) (Araneae, Hexathelidae)

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Abstract

The funnel-web spider genus Macrothele is the only representative of the mygalomorph family Hexathelidae not found in Australia or New Zealand. Its 26 species occur in Central Africa and the Oriental region. Two Macrothele species are found in Europe: M. cretica Kulczynski, 1903 from Crete, and M. calpeiana (Walckenaer, 1805) type species of the genus and the largest European spider, whose distribution extends across the south-eastern Iberian Peninsula, and in two localities of North Africa. Macrothele calpeiana is the only spider protected under European legislation. The fragmentation and destruction of the cork oak forest, with which M. calpeiana was thought to be closely associated, prompted the inclusion of this species in the Bern Convention. Some authors, however, have challenged this view and consider M. calpeiana to be neither a cork oak forest bioindicator nor an endangered species. By contrast, other observations suggest that the distribution of the species is extremely fragmented and that most local populations should be considered as threatened. In this paper, we examine aspects of the conservation status of M. calpeiana in the light of molecular phylogenetic analyses based on mitochondrial markers of sample specimens from major populations. Our data confirm the fragmented distribution of M. calpeiana and reveal high levels of genetic differentiation across its populations. Local population growth cannot be ruled out, though the lineage as a whole has apparently not undergone population growth. Lineage age estimates suggest that M. calpeiana colonized the Iberian Peninsula during the Messinian salinity crisis and that the current population fragmentation originates from the Pliocene and Pleistocene. We argue that the fragmentation and deep genetic divergence across populations, along with evolutionary singularity and endemicity in one of Europe’s main biodiversity hotspots, support the preservation of its legally protected status.

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References

  • Arntzen JW, García-París M (1995) Morphological and allozyme studies of midwife toads (genus Alytes) including the description of two new taxa from Spain. Contrib Zool 65:5–34

    Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge, Mass

    Google Scholar 

  • Ballard JW, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744

    Article  PubMed  Google Scholar 

  • Barea-Azcón JM, Ferrández MA, Ballesteros-Duperón E, Irurita JM (2005) Factores ambientales condicionantes de la distribución de Macrothele calpeiana (Walkenaer, 1805) a nivel de macrohábitat: implicaciones para su conservación. In: VI Jornadas del Grupo Ibérico de Aracnología. http://www.aracnologia.ennor.org/docs/actas_GIA_2005.pdf, Madrid

  • Blasco A, Ferrández MA (1986) El género Macrothele Ausserer, 1871 (Araneae: Dipluridae) en la Península Ibérica. In: X International Congress of Arachnology, Jaca, Spain, pp 311–320

  • Blondel J, Aronson J (1999) Biology and wildlife of the Mediterranean region. Oxford University Press, Oxford, New York

    Google Scholar 

  • Bond JE (2004) Systematics of the Californian euctenizine spider genus Apomastus (Araneae : Mygalomorphae : Cyrtaucheniidae): the relationship between molecular and morphological taxonomy. Invertebr Syst 18:361–376

    Article  CAS  Google Scholar 

  • Bond JE, Beamer DA, Lamb T, Hedin M (2006) Combining genetic and geospatial analyses to infer population extinction in mygalomorph spiders endemic to the Los Angeles region. Anim Conserv 9:145–157

    Article  Google Scholar 

  • Bond JE, Hedin MC, Ramirez MG, Opell BD (2001) Deep molecular divergence in the absence of morphological and ecological change in the Californian coastal dune endemic trapdoor spider Aptostichus simus. Mol Ecol 10:899–910

    Article  PubMed  CAS  Google Scholar 

  • Brandley MC, Schmitz A, Reeder TW (2005) Partitioned Bayesian analyses, partition choice, and the phylogenetic relationships of Scincid lizards. Syst Biol 54:373–390

    Article  PubMed  Google Scholar 

  • Bremer K (1994) Branch support and tree stability. Cladistics 10:295–304

    Article  Google Scholar 

  • Brower AVZ (1994) Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc Natl Acad Sci USA 91:6491–6495

    Article  PubMed  CAS  Google Scholar 

  • Calvo-Hernández D, Santos-Lobatón MC (2001) Variabilidad morfológica de las poblaciones de Macrothele calpeiana (Walckenaer, 1805) (Araneae, Hexathelidae) en la provincia de Cádiz (España). Rev iber Aracnol 3:43–45

    Google Scholar 

  • Carranza S, Arnold EN (2003) History of West Mediterranean newts, Pleurodeles (Amphibia: Salamandridae), inferred from old and recent DNA sequences. Syst Biodivers 1:327–338

    Article  Google Scholar 

  • Carranza S, Wade E (2004) Taxonomic revision of Algero-Tunisian Pleurodeles (Caudata: Salamandridae) using molecular and morphological data. Revalidation of the taxon Pleurodeles nebulosus (Guichenot, 1850). Zootaxa 488:1–24

    Google Scholar 

  • Collins NM, Wells S (1987) Invertebrates in need of special protection in Europe. Augier H. Nature & Environment Series No. 35. Council of Europe, Strasbourg, pp 162

  • Corzo G, Escoubas P (2003) Pharmacologically active spider peptide toxins. Cell Mol Life Sci 60:2409–2426

    Article  PubMed  CAS  Google Scholar 

  • Crandall K, Bininda-Emonds O, Mace G, Wayne R (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295

    Article  PubMed  Google Scholar 

  • Drummond AJ, Rambaut A (2003) BEAST. Available from http://www.evolve.zoo.ox.ac.uk/beast/

  • Duggen S, Hoernle K, van den Bogaard P, Rüpke L, Morgan JP (2003) Deep roots of the Messinian salinity crisis. Nature 422:602–606

    Article  PubMed  CAS  Google Scholar 

  • Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2582

    Article  PubMed  CAS  Google Scholar 

  • Emerson B, Paradis E, Thebaud C (2001) Revealing the demographic histories of species using DNA sequences. Trends Ecol Evol 16:707–716

    Article  Google Scholar 

  • Emerson BC, Oromi P, Hewitt GM (2000) Colonization and diversification of the species Brachyderes rugatus (Coleoptera) on the Canary Islands: evidence from mitochondrial DNA COII gene sequences. Evolution 54:911–923

    PubMed  CAS  Google Scholar 

  • Farris JS, Albert VA, Kallersjo M, Lipscomb D, Kluge AG (1996) Parsimony jackknifing outperforms neighbor-joining. Cladistics 12:99–124

    Article  Google Scholar 

  • Ferrández MA, Ferrández de Céspedes H (1996) Macrothele calpeiana. In: Inventario de los invertebrados incluidos en los Anejos de la directiva 92/43/CEE del Consejo. Icona, Madrid

  • Ferrández MA, Ferrández de Céspedes H (2001) Arachnida. In: Ramos MA, Bragado D, Fernández J (eds) Los Invertebrados no insectos de la “Directiva Hábitat” en España, Ministerio de Medio Ambiente, Dirección Genaral de la Conservación de la naturaleza, pp 133–144

  • Ferrández MA, Ferrández de Céspedes H, Perucho A (1998) Macrothele calpeiana, la araña negra de los alcornocales. Quercus 146:14–18

    Google Scholar 

  • Foelix RF (1996) Biology of spiders. Oxford University Press, New York

    Google Scholar 

  • Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annu Rev Ecol Evol Syst 34:397–423

    Article  Google Scholar 

  • Gallon RC (1994) Observations on Macrothele calpeiana (Walckenaer, 1805) in southern Iberia. J Br Tarantula Soc 1:1–12

    Google Scholar 

  • Gantenbein B, Largiader CR (2003) The phylogeographic importance of the Strait of Gibraltar as a gene flow barrier in terrestrial arthropods: a case study with the scorpion Buthus occitanus as model organism. Mol Phylogenet Evol 28:119–130

    Article  PubMed  CAS  Google Scholar 

  • García-París M, Alcobendas P, Alberch P (1998) Influence of the Guadalquivir River basin on mitochondrial DNA evolution of Salamandra salamandra (Caudata: Salamandridae) from Southern Spain. Copeia 1:173–176

    Article  Google Scholar 

  • Giribet G, Wheeler W, Muona J (2002) DNA multiple sequence alignments. In: DeSalle R, Giribet G, Wheeler W (eds) Molecular systematics and evolution: theory and practice. Birkhaüser Verlag, Switzerland, pp 107–114

    Google Scholar 

  • Goloboff PA, Farris JS, Nixon KC (2003) TNT: tree analysis using new technologies

  • Gómez A, Lunt DH (2004) Refugia within refugia: patterns of phylogeographic concordance in the Iberian Peninsula. In: Weiss S, Ferrand N (eds) Phylogeography in Southern European refugia: evolutionary perspectives on the origins and conservation of European biodiversity. Kluwer Academic Publishers, Dordrecht

  • Gómez-Zurita J, Petitpierre E, Juan C (2000) Nested cladistic analysis, phylogeography and speciation in the Timarcha goettingensis complex (Coleoptera, Chrysomelidae). Mol Ecol 9:557–570

    Article  PubMed  Google Scholar 

  • Gutiérrez Larena B, Fuertes Aguilar J, Nieto Feliner G (2002) Glacial-induced altitudinal migrations in Armeria (Plumbaginaceae) inferred from patterns of chloroplast DNA haplotype sharing. Mol Ecol 11:1965–1974

    Article  PubMed  Google Scholar 

  • Hafernik JEJ (1992) Threats to invertebrate biodiversity: implications for conservation strategies. In: Fiedler PL, Jain SK (eds) Conservation biology: the theory and practice of nature conservation, preservation, and management. Chapman and Hall, New York and London, pp 171–195

    Google Scholar 

  • Harpending HC, Batzer MA, Gurven M, Jorde LB, Rogers AR, Sherry ST (1998) Genetic traces of ancient demography. Proc Natl Acad Sci USA 95:1961–1967

    Article  PubMed  CAS  Google Scholar 

  • Harris DJ, Batista V, Carretero MA (2004) Assessment of genetic diversity within Acanthodactylus erythrurus (Reptilia: Lacertidae) in Morocco and the Iberian Peninsula using mitochondrial DNA sequence data. Amphibia–Reptilia 25:227–232

    Google Scholar 

  • Hedin M, Bond JE (2006) Molecular phylogenetics of the spider infraorder Mygalomorphae using nuclear rRNA genes (18S and 28S): conflict and agreement with the current system of classification. Mol Phylogenet Evol 41:454–471

    Article  PubMed  CAS  Google Scholar 

  • Hedin MC (1997) Molecular phylogenetics at the population/species interface in cave spiders of the Southern Appalachians (Araneae: Nesticidae: Nesticus). Mol Biol Evol 14:309–324

    PubMed  CAS  Google Scholar 

  • Hendrixson BE, Bond JE (2005) Testing species boundaries in the Antrodiaetus unicolor complex (Araneae: Mygalomorphae: Antrodiaetidae): “paraphyly” and cryptic diversity. Mol Phylogenet Evol 36:405–416

    Article  PubMed  Google Scholar 

  • Hewitt G (1999) Post-glacial recolonization of European biota. Biol J Linn Soc 68:87–112

    Article  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913

    Article  PubMed  CAS  Google Scholar 

  • Hewitt G (2001) Speciation, hybrid zones and phylogeography—or seeing genes in space and time. Mol Ecol 10:537–549

    Article  PubMed  CAS  Google Scholar 

  • Hung S-W, Wang T-L (2004) Arachnid envenomation in Taiwan. Ann Disast Med 3:S12–S17

    Google Scholar 

  • Irwin DE (2002) Phylogeographic breaks without geographic barriers to gene flow. Evol Int J Org Evol 56:2383–2394

    Google Scholar 

  • Kass RE, Raftery AE (1995) Bayes factors. J Am Stat Assoc 90:773–795

    Article  Google Scholar 

  • Krijgsman W, Hilgen FJ, Raffi I, Sierro FJ, Wilson DS (1999) Chronology, causes and progression of the Messinian salinity crisis. Nature 400:652–655

    Article  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Kuo C, Avise J (2005) Phylogeographic breaks in low-dispersal species: the emergence of concordance across gene trees. Genetica 124:179–186

    Article  PubMed  Google Scholar 

  • Lin CP, Danforth BN (2004) How do insect nuclear and mitochondrial gene substitution patterns differ? Insights from Bayesian analyses of combined datasets. Mol Phylogenet Evol 30:686–702

    Article  PubMed  CAS  Google Scholar 

  • Lucas H (1839) Arachnides, myriapodes et thysanoures. In: Barker-Webb, Berthelod S (eds) Histoire naturelle des îles Canaries, II, 2e partie: Zoologie. Paris, pp 19–52

  • Martínez-Solano I, Goncalves HA, Arntzen JW, Garcia-Paris M (2004) Phylogenetic relationships and biogeography of midwife toads (Discoglossidae: Alytes). J Biogeogr 31:603–618

    Google Scholar 

  • Medail F, Quezel P (1997) Hot-spots analysis for conservation of plant biodiversity in the Mediterranean Basin. Ann MO Bot Gard 84:112–127

    Article  Google Scholar 

  • Medail F, Quezel P (1999) Biodiversity hotspots in the Mediterranean basin: setting global conservation priorities. Conserv Biol 13:1510–1513

    Article  Google Scholar 

  • Mickevich MF, Farris JS (1981) The implications of incongruence in Menidia. Syst Zool 30:351–370

    Article  Google Scholar 

  • Moore WS (1995) Inferring phylogenies from mtDNA variation: Mitochondrial-gene trees versus nuclear-gene trees. Evolution 49:718–726

    Article  Google Scholar 

  • Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol Evol 9:373–375

    Article  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CC, da Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Google Scholar 

  • Nylander JAA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey JL (2004) Bayesian phylogenetic analysis of combined data. Syst Biol 53:47–67

    Article  PubMed  Google Scholar 

  • Palmer M, Cambefort Y (2000) Evidence for reticulate palaeogeography: beetle diversity linked to connection–disjunction cycles of the Gibraltar strait. J Biogeogr 27:403–416

    Article  Google Scholar 

  • Perry L (2002) Captive breeding of funnelweb spider Macrothele calpeiana (Walckenaer, 1805). J Br Tarantula Soc 17:113–121

    Google Scholar 

  • Platnick NI (2005) The world spider catalog. American Museum of Natural History, online at http://www.research.amnh.org/entomology/spiders/catalog81–87/INTRO1.html, New York

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Prager EM, Wilson AC (1988) Ancient origin of lactalbumin from lysozyme: analysis of DNA and amino acid sequences. J Mol Evol 27:326–335

    Article  PubMed  CAS  Google Scholar 

  • Rambaut A, Drummond AJ (2003) TRACER. Available from http://www.evolve.zoo.ox.ac.uk/tracer/

  • Rapoport EH (1982) Areography: geographical strategies of species. Pergamon Press, Oxford

    Google Scholar 

  • Raven RJ (1980) The evolution and biogeography of the mygalomorph spider family Hexathelidae (Araneae, Chelicerata). J Arachnol 8:251–266

    Google Scholar 

  • Ribera I (2000) Biogeography and conservation of Iberian water beetles. Biol Conserv 92:131–150

    Article  Google Scholar 

  • Roest WR, Srivastava SP (1991) Kinematics of the plate boundaries between Eurasia, Iberia, and Africa in the North Atlantic from the Late Cretaceous to the present. Geology 19:613–616

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP, van der Mark P (2005) MyBayes 3.1 manual. online at http://www.mrbayes.csit.fsu.edu/wiki/index.php/Manual

  • Ryder O (1986) Species conservation and systematics: the dilemma of subspecies. Trends Ecol Evol 1:9–10

    Article  Google Scholar 

  • Sanger F, Nicklen S, Coulsen AR (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5468

    Article  PubMed  CAS  Google Scholar 

  • Sanz de Galdeano CM (1996) Tertiary tectonic framework of the Iberian peninsula. In: Friend PF, Dabrio CJ (eds) Tertiary basins of Spain. Cambridge University Press, Cambridge, pp 9–14

    Google Scholar 

  • Scheller J, Guhrs K-H, Grosse F, Conrad U (2001) Production of spider silk proteins in tobacco and potato. Nat Biotechnol 19:573–577

    Article  PubMed  CAS  Google Scholar 

  • Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089

    PubMed  CAS  Google Scholar 

  • Selden PA, Shear WA, Bonamo PM (1991) A spider and other arachnids from the Devonian of New York, and reinterpretations of Devonian Araneae. Palaeontology 34:241–281

    Google Scholar 

  • Shear WA, Palmer JM, Coddington JA, Bonamo PM (1989) A Devonian spinneret: early evidence of spiders and silk use. Science 246:479–481

    Article  Google Scholar 

  • Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116

    CAS  Google Scholar 

  • Simmons MP, Ochoterena H (2000) Gaps as characters in sequence-based phylogenetic analyses. Syst Biol 49:369–381

    Article  PubMed  CAS  Google Scholar 

  • Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–701

    CAS  Google Scholar 

  • Snazell RG (1986) The spider genus Macrothele Ausserer in Spain (Araneae, Dipluridae). Bull Br Arachnol Soc 17:80–83

    Google Scholar 

  • Snazell RG, Allison R (1989) The genus Macrothele Ausserer (Araneae; Hexathelidae) in Europe. Bull Br Arachnol Soc 8:65–72

    Google Scholar 

  • Sollod B, Wilson D, Zhaxybayeva O, Gogarten J, Drinkwater R, King G (2005) Were arachnids the first to use combinatorial peptide libraries. Peptides 26:131–139

    Article  PubMed  CAS  Google Scholar 

  • Swofford DL (2001) PAUP*: Phylogenetic analysis using parsimony (and other methods). Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Templeton AR (1983) Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the humans and apes. Evolution 37:221–244

    Article  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  • Valdés B (1991) Andalucía and the Rif. Floristic links and a common Flora. Bot Chron 10:117–124

    Google Scholar 

  • Van Helsdingen PJ (1993) Can Macrothele calpeiana (Walckenaer) (Araneae, Hexathelidae) be used as a bio-indicator? Bull Soc Neuch Sci Nat 116:253–258

    Google Scholar 

  • Van Helsdingen PJ, Decae A (1992) Ecolgy, distribution and vulnerability of Macrothele calpeiana (Walckenaer) (Araneae, Hexathelidae). Tijdschr Entomol 135:169–178

    Google Scholar 

  • Vargas JM, Real R, Guerrero JC (1998) Biogeograpahical regions of the Iberian peninsula based on freshwater fish and amphibian distributions. Ecography 21:371–382

    Article  Google Scholar 

  • Verdú JR, Galante E (2005) Libro Rojo de los Invertebrados de España. Dirección General para la Biodiversidad, Ministerio de Medio Ambiente, Madrid

  • Wiens JJ, Penkrot TA (2002) Delimiting species using DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus). Syst Biol 51:69–91

    Article  PubMed  Google Scholar 

  • Wise DH (1993) Spiders in ecological webs. Cambridge University Press, Cambridge, New York

    Google Scholar 

  • Young ND, Healy J (2002) GapCoder. http://www.trinity.edu/nyoung/GapCoder/Download.html

  • Zeng X, Xiao Q, Liang S (2003) Purification and characterization of raventoxin-I and raventoxin-III, two neurotoxic peptides from the venom of the spider Macrothele raveni. Toxicon 41:651–656

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The Dirección General de la Conservación de la Naturaleza of the Spanish Ministry of the Environment provided funding for fieldwork that has greatly improved our knowledge of the distribution of M. calpeiana and that provided most of the samples used in the present study. Leticia Bidegaray provided insightful comments on the draft versions of the paper, which also greatly benefited from the suggestions of three anonymous reviewers. Jesús Miñano assisted with the preparation of the map. Some of the sequences were obtained by M.A. during a period of postdoctoral study in the laboratory of Dr. Alfried Vogler at the Natural History Museum in London. MA was supported by the Program Ramon y Cajal funded by the Spanish Ministry of Education and Science and EU FEDER program. This project was partially funded by the Spanish Ministry of Education and Science grant BOS2003-05876 (MA) and additional financial support was provided by project 2005SGR00045 from the Catalan Autonomous Government.

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  1. Departament de Biologia Animal, Universitat de Barcelona, Av. Diagonal 645, 08028, Barcelona, Spain

    Miquel A. Arnedo

  2. Sociedad para el Estudio y la Conservación de las Arañas, c/ Villafranca 24, 1_C, 28028, Madrid, Spain

    Miguel-Angel Ferrández

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Arnedo, M.A., Ferrández, MA. Mitochondrial markers reveal deep population subdivision in the European protected spider Macrothele calpeiana (Walckenaer, 1805) (Araneae, Hexathelidae). Conserv Genet 8, 1147–1162 (2007). https://doi.org/10.1007/s10592-006-9270-2

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