Invertebrate Systematics Invertebrate Systematics Society
Systematics, phylogeny and biogeography
RESEARCH ARTICLE

Molecular phylogenetics of Caribbean Micrathena (Araneae : Araneidae) suggests multiple colonisation events and single island endemism

Anne McHugh A C , Carol Yablonsky A , Greta Binford B and Ingi Agnarsson A

A University of Vermont, Department of Biology, 109 Carrigan Drive, Burlington, VT 05405, USA.

B Lewis & Clark College, Department of Biology, 0615 SW Palatine Hill Rd, Portland, OR 97219, USA.

C Corresponding author. Email: akmchugh@gmail.com

Invertebrate Systematics 28(4) 337-349 http://dx.doi.org/10.1071/IS13051
Submitted: 18 October 2013  Accepted: 3 February 2014   Published: 12 September 2014

Abstract

The terrestrial biota of the Caribbean islands includes many lineages, some whose presence on the islands dates back some 35–40 million years ago, when land bridges are thought to have linked islands to continents, and others that have colonised more recently via dispersal. The New World spiny orb-weavers (Micrathena Sundevall, 1833) are a diverse group of mostly Neotropical spiders. Eight species have been described on the Greater Antilles islands: three widespread and five single island endemics. Here, using three molecular markers (16S rRNA, ITS-2 and COI) we provide a preliminary phylogenetic test of the taxonomy and biogeography of Caribbean Micrathena through the first molecular phylogeny of the genus. Our analyses support monophyly of the genus, but not that of Caribbean Micrathena with at least 3–4 colonisations from South America. We sampled six of the eight nominal Caribbean species (M. banksi, M. cubana, M. similis, M. forcipata, M. horrida, M. militaris), but demark eight divergent genetic lineages that all are single island endemics, and morphologically distinct. Thus a revision of the taxonomy of Caribbean Micrathena is needed. Our results function foremost to guide more thorough taxon sampling of Micrathena that enable more rigorous assessments of its diversity and biogeography in the Caribbean.

Additional keywords: biogeography, Cenozoic dispersal, phylogeography, spiny orb-weavers, vicariance.


References

Agnarsson, I. (2010). The utility of ITS2 in spider phylogenetics: notes on prior work and an example from Anelosimus. The Journal of Arachnology 38, 377–382.
The utility of ITS2 in spider phylogenetics: notes on prior work and an example from Anelosimus.CrossRef | open url image1

Agnarsson, I., and Kuntner, M. (2012). The generation of a biodiversity hotspot: biogeography and phylogeography of the western Indian Ocean islands. In ‘Current Topics in Phylogenetics and Phylogeography of Terrestrial and Aquatic Systems’. (Ed. K. Anamthawat-Jonsson.) pp. 33–82. (InTech Publishers: Rijeka, Croatia.)

Agnarsson, I., Maddison, W. P., and Aviles, L. (2007). The phylogeny of the social Anelosimus spiders (Araneae: Theridiidae) inferred from six molecular loci and morphology. Molecular Phylogenetics and Evolution 43, 833–851.
The phylogeny of the social Anelosimus spiders (Araneae: Theridiidae) inferred from six molecular loci and morphology.CrossRef | 1:CAS:528:DC%2BD2sXlvVOrurk%3D&md5=6e762f9f10b630e730a71b095b976637CAS | 17081775PubMed | open url image1

Altekar, G., Dwarkadas, S., Huelsenbeck, J. P., and Ronquist, F. (2004). Parallel Metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics 20, 407–415.
Parallel Metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference.CrossRef | 1:CAS:528:DC%2BD2cXht1Kks7g%3D&md5=636559846154381fc6923a596b038cdaCAS | 14960467PubMed | open url image1

Bell, J. R., Bohan, D. A., Shaw, E. M., and Weyman, G. S. (2005). Ballooning dispersal using silk: world fauna, phylogenies, genetics and models. Bulletin of Entomological Research 95, 69–114.
| 1:STN:280:DC%2BD2M3ktlGhsA%3D%3D&md5=d5ee6b433be4b3c41ab96e282e33e2ecCAS | 15877859PubMed | open url image1

Bidegaray-Batista, L., and Arnedo, M. A. (2011). Gone with the plate: the opening of the Western Mediterranean basin drove the diversification of ground-dweller spiders. BMC Evolutionary Biology 11, 317.
| 22039781PubMed | open url image1

Binford, G. J., Callahan, M. S., Bodner, M. R., Rynerson, M. R., Nunez, P. B., Ellison, C. E., and Duncan, R. P. (2008). Phylogenetic relationships of Loxosceles and Sicarius spiders are consistent with Western Gondwanan vicariance. Molecular Phylogenetics and Evolution 49, 538–553.
Phylogenetic relationships of Loxosceles and Sicarius spiders are consistent with Western Gondwanan vicariance.CrossRef | 1:CAS:528:DC%2BD1cXhtlCrtb7I&md5=e376b53dc1e53002351cfcd2c7ee30f1CAS | 18755282PubMed | open url image1

Cloudsley-Thompson, J. L. (1995). A review of the anti-predator devices of spiders. Bulletin of the British Arachnological Society 10, 81–96. open url image1

Crews, S., and Gillespie, R. (2010). Molecular systematics of Selenops spiders (Araneae:Selenopidae) from North and Central America: implications for Caribbean biogeography. Biological Journal of the Linnean Society. Linnean Society of London 101, 288–322.
Molecular systematics of Selenops spiders (Araneae:Selenopidae) from North and Central America: implications for Caribbean biogeography.CrossRef | open url image1

Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
jModelTest 2: more models, new heuristics and parallel computing.CrossRef | 1:CAS:528:DC%2BC38XhtFWmsbfP&md5=3cacc445e0743c5953b436bc2cf6a350CAS | 22847109PubMed | open url image1

Dávalos, L. M. (2004). Phylogeny and biogeography of Caribbean mammals. Biological Journal of the Linnean Society 81, 373–394. open url image1

Decae, A. E. (1987). Dispersal: ballooning and other mechanisms. In ‘Ecophysiology of Spiders’. (Ed. W. Nentwig.) pp. 348–356. (Springer Verlag: Berlin, Germany.)

Drummond, A. J., Suchard, M. A., Xie, D., and Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.
Bayesian phylogenetics with BEAUti and the BEAST 1.7.CrossRef | 1:CAS:528:DC%2BC38XhtFagu7fO&md5=beec25ccf0d2a98903aa512fd45babe5CAS | 22367748PubMed | open url image1

Eberhard, W. G. (1987). How spiders initiate airborne lines. The Journal of Arachnology 15, 1–9. open url image1

Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 1:CAS:528:DyaK2MXjt12gtLs%3D&md5=41891c10f444b637826cbf6001a4954cCAS | 7881515PubMed | open url image1

Green, P. (2009). ‘Phrap 1.090518.’ Available at http://www.phrap.org [Verified May 2014]

Green, P., and Ewing, B. (2002). ‘Phred 0.020425c.’ Available at http://www.phrap.org [Verified May 2014]

Hedin, M. C., and Maddison, W. P. (2001). A combined molecular approach to phylogeny of the jumping spider subfamily Dendryphantinae (Araneae: Salticidae). Molecular Phylogenetics and Evolution 18, 386–403.
A combined molecular approach to phylogeny of the jumping spider subfamily Dendryphantinae (Araneae: Salticidae).CrossRef | 1:CAS:528:DC%2BD3MXit1ansbg%3D&md5=cedf4973ea9822c87cf2bcd4c96f698aCAS | 11277632PubMed | open url image1

Huelsenbeck, J. P., Ronquist, F., Nielsen, R., and Bollback, J. P. (2001). Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294, 2310–2314.
Bayesian inference of phylogeny and its impact on evolutionary biology.CrossRef | 1:CAS:528:DC%2BD3MXptFGkt7k%3D&md5=ecf42cc9ac8235c31da3d20783494aedCAS | 11743192PubMed | open url image1

Iturralde-Vinent, M. A. (2006). Meso-Cenozoic Caribbean paleogeography: implications for the historical biogeography of the region. International Geology Review 48, 791–827.
Meso-Cenozoic Caribbean paleogeography: implications for the historical biogeography of the region.CrossRef | open url image1

Iturralde-Vinent, M., and MacPhee, R. D. E. (1999). Paleogeography of the Caribbean region: implications for Cenozoic biogeography. Bulletin of the American Museum of Natural History 238, 1–95. open url image1

Katoh, S. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.
MAFFT multiple sequence alignment software version 7: improvements in performance and usability.CrossRef | 1:CAS:528:DC%2BC3sXksFWisLc%3D&md5=14a6e5bc04e61af99a92f9a397a54c77CAS | open url image1

Kuntner, M., and Agnarsson, I. (2011). Biogeography and diversification of hermit spiders on Indian Ocean islands (Nephilidae: Nephilengys). Molecular Phylogenetics and Evolution 59, 477–488.
Biogeography and diversification of hermit spiders on Indian Ocean islands (Nephilidae: Nephilengys).CrossRef | 21316478PubMed | open url image1

Kuntner, M., Arnedo, M. A., Trontelj, P., Lokovsek, T., and Agnarsson, I. (2013). A molecular phylogeny of nephilid spiders: evolutionary history of a model lineage. Molecular Phylogenetics and Evolution 69, 961–979.
A molecular phylogeny of nephilid spiders: evolutionary history of a model lineage.CrossRef | 1:CAS:528:DC%2BC3sXhtFSmt77K&md5=f12200ce3dd52d6424ee263921a38694CAS | 23811436PubMed | open url image1

Levi, H. W. (1985). The spiny orb-weaver genera Micrathena and Chaetacis (Araneae:Araneidae). Bulletin of the Museum of Comparitive Zoology 150, 429–618. open url image1

Losos, J. B., and Schluter, D. (2000). Analysis of an evolutionary species–area relationship. Nature 408, 847–850.
Analysis of an evolutionary species–area relationship.CrossRef | 1:CAS:528:DC%2BD3MXhtlaisw%3D%3D&md5=29a49eda1f3e996c0dae53addbf19f3bCAS | 11130721PubMed | open url image1

Losos, J. B., Glor, R. E., Kolbe, J. J., and Nicholson, K. (2006). Adaption, speciation and convergence: a hierarchical analysis of adaptive radiation in Caribbean Anolis lizards. Annals of the Missouri Botanical Garden 93, 24–33.
Adaption, speciation and convergence: a hierarchical analysis of adaptive radiation in Caribbean Anolis lizards.CrossRef | open url image1

Maddison, D. R., and Maddison, W. P. (2011a). Chromaseq 1.0: a Mesquite package for analyzing sequence chromatograms. Available at http://www.mesquiteproject.org/packages/chromaseq [Verified May 2014]

Maddison, W. P., and Maddison, D. R. (2011b). Mesquite 2.75: a modular system for evolutionary analysis. Available at http://www.mesquiteproject.org [Verified May 2014]

Magalhães, I. L. F., and Santos, A. J. (2012). Phylogenetic analysis of Micrathena and Chaetacis spiders (Araneae: Araneidae) reveals multiple origins of extreme sexual size dimorphism and long abdominal spines. Zoological Journal of the Linnean Society 166, 14–53. open url image1

Miller, M. A., Pfeiffer, W., and Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘Proceedings of the Gateway Computing Environments Workshop (GCE)’. pp. 1–8. (New Orleans, LA.)

Myers, N., Mittermeier, R. A., Mittermeier, C. G., Fonseca, G. A. B., and Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature 403, 853–858.
Biodiversity hotspots for conservation priorities.CrossRef | 1:CAS:528:DC%2BD3cXhs1Olsr4%3D&md5=1cc99c5a896239eddf235fea5787c687CAS | 10706275PubMed | open url image1

Platnick, N. L. (2013). ‘The World Spider Catalog, Version 14.0.’ (American Museum of Natural History: Washington, DC.)

Posada, D., and Buckley, T. R. (2004). Model selection and model averaging in phylogenetics: advantages of Akaike Information Criterion and Bayesian Approaches over Likelihood Ratio Tests. Systematic Biology 53, 793–808.
| 15545256PubMed | open url image1

Rambaut, A., and Drummond, A. J. (2007). ‘Tracer 1.4.’ Available at http://beast.bio.ed.ac.uk/Tracer [Verified May 2014]

Ree, R. H., and Smith, S. A. (2008). Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis. Systematic Biology 57, 4–14.
Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis.CrossRef | 18253896PubMed | open url image1

Říčan, O., Piálek, L., Zardoya, R., Doadrio, I., Zrzavý, J., and Crame, A. (2013). Biogeography of the Mesoamerican Cichlidae (Teleostei: Heroini): colonization through the GAARlandia land bridge and early diversification. Journal of Biogeography 40, 579–593.
Biogeography of the Mesoamerican Cichlidae (Teleostei: Heroini): colonization through the GAARlandia land bridge and early diversification.CrossRef | open url image1

Ricklefs, R., and Bermingham, E. (2008). The West Indies as a laboratory of biogeography and evolution. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 363, 2393–2413.
The West Indies as a laboratory of biogeography and evolution.CrossRef | 17446164PubMed | open url image1

Ronquist, F., and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.
MrBayes 3: Bayesian phylogenetic inference under mixed models.CrossRef | 1:CAS:528:DC%2BD3sXntlKms7k%3D&md5=d5b84f5cc16cfb75b367ced57a76cb2cCAS | 12912839PubMed | open url image1

Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H., and Flook, P. (1994). Evolution, weighting and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651–701.
| 1:CAS:528:DyaK2MXis1Wiu7g%3D&md5=d5c73c20640b01d4cb1718c8d993d994CAS | open url image1

White, T. J., Bruns, T., Lee, S., and Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In ‘PCR Protocols: a Guide to Methods and Applications’. (Ed. M. A. Innis, J. J. Sninsky and T. J. White.) pp. 315–322. (Academic Press: New York, NY.)

Zhang, J., and Maddison, W. P. (2013). Molecular phylogeny, divergence times and biogeography of spiders of the subfamily Euophryinae (Araneae: Salticidae) Molecular Phylogenetics and Evolution 68, 81–92.
Molecular phylogeny, divergence times and biogeography of spiders of the subfamily Euophryinae (Araneae: Salticidae)CrossRef | 23542001PubMed | open url image1

Zwickl, D. J. (2006). Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. PhD Thesis, The University of Texas, Austin, USA.



Export Citation