Description of a new species of Loxosceles Heineken & Lowe (Araneae, Sicariidae) recluse spiders from Hidalgo, Mexico, under integrative taxonomy: morphological and DNA barcoding data (CO1 + ITS2)

  • Claudia Isabel Navarro-Rodríguez Laboratory of Arachnology (LATLAX), Laboratorio Regional de Biodiversidad y Cultivo de Tejidos Vegetales (LBCTV), Instituto de Biología, Universidad Nacional Autónoma de Mexico (UNAM), sede Tlaxcala, Ex-Fábrica San Manuel, San Miguel Contla, 90640 Santa Cruz Tlaxcala, Tlaxcala
  • Alejandro Valdez-Mondragón CONACYT Research Fellow. Laboratory of Arachnology (LATLAX), Laboratorio Regional de Biodiversidad y Cultivo de Tejidos Vegetales (LBCTV), Instituto de Biología, Universidad Nacional Autónoma de Mexico (UNAM), sede Tlaxcala, Ex-Fábrica San Manuel, San Miguel Contla, 90640 Santa Cruz Tlaxcala, Tlaxcala
Keywords: integrative taxonomy, molecular markers, Synspermiata, species delimitation, Hidalgo

Abstract

Based on an integrative taxonomic approach, a new species of the genus Loxosceles Heineken & Lowe, 1832, is described from the state of Hidalgo, Mexico. Loxosceles tolantongo sp. nov. is described based on DNA barcoding using cytochrome c oxidase subunit 1 (CO1) and internal transcribed spacer 2 (ITS2), and morphology. For species delimitation, four molecular methods were implemented: 1) corrected p-distances under neighbor joining (NJ); 2) automatic barcode gap discovery (ABGD); 3) general mixed yule coalescent model (GMYC) and 4) Bayesian Poisson tree processes (bPTP). The new species morphologically resembles L. jaca, another species from Hidalgo, but there are morphological differences mainly in the tibiae of the male palp, the seminal receptacles of the females and also the high genetic p-distances. CO1 was more informative than ITS2 for the genetic separation; however, both concatenated genes (CO1 + ITS2) present robust evidence for species delimitation. Loxosceles tolantongo sp. nov. is considered a unique species for four reasons: 1) it can be diagnosed and distinguished by morphological characters (of the male palps mainly, but also of the seminal receptacles of the females); 2) the genetic p-distances with CO1 were high (>10%); 3) the molecular species delimitation methods were congruent under CO1 and CO1 + ITS2; and 4) under CO1 and CO1 + ITS2, the new species is a putative sister group of L. jaca + L. tenango.

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 (2): 377–382. https://doi.org/10.1636/B10-01.1

Astrin J.J. & Stüben P.E. 2008. Phylogeny in cryptic weevils: molecules, morphology and new genera of western Palaearctic Cryptorhynchinae (Coleoptera: Curculionidae). Invertebrate Systematics 22 (5): 503–522. https://doi.org/10.1071/IS07057

Bickford D., Lohman D.J., Sodhi N.S., Ng P.K., Meier R., Winker K., Ingram K.K. & Das I. 2007. Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22 (3): 148–155. https://doi.org/10.1016/j.tree.2006.11.004

Binford G.J., Callahan M.S., Bodner M.R., Rynerson M.R., Berea-Núñez P., Ellison C.E & Duncan R.P. 2008. Phylogenetic relationships of Loxosceles and Sicarius spiders are consistent with Western Gondwanan vicariance. Molecular Phylogenetics and Evolution 49 (2): 538–553. https://doi.org/10.1016/j.ympev.2008.08.003

Brignoli P. 1968. Note sugli Scytodidae d’Italia e Malta (Araneae). Fragmenta Entomologica 6: 121–166.

Cao X., Liu J., Chen J., Zheng G., Kuntner M. & Agnarsson I. 2016. Rapid dissemination of taxonomic discoveries based on DNA barcoding and morphology. Scientific Reports 6: 37066. https://doi.org/10.1038/srep37066

Carstens B.C., Pelletier T.A., Reid N.M. & Satler J.D. 2013. How to fail at species delimitation. Molecular Ecology 22: 4369–4383. https://doi.org/10.1111/mec.12413

Clement M., Posada D. & Crandall K.A. 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9 (10): 1657–1659. https://doi.org/10.1046/j.1365-294x.2000.01020.x

DeSalle R., Egan M.G. & Siddall M. 2005. The unholy trinity: taxonomy, species delimitation and DNA barcoding. Philosophical Transactions of the Royal Society of London, B, Biological Sciences 360 (1462): 1905–1916. https://doi.org/10.1098/rstb.2005.1722

Duncan R.P., Rynerson M.R., Ribera C. & Binford G.J. 2010. Diversity of Loxosceles spiders in Northwestern Africa and molecular support for cryptic species in the Loxosceles rufescens lineage. Molecular Phylogenetics and Evolution 55 (1): 234–248. https://doi.org/10.1016/j.ympev.2009.11.026

Drummond A.J., Suchard M.A., Xie D. & Rambaut A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29 (8): 1969–1973. https://doi.org/10.1093/molbev/mss075

Foelix R.F. 2011. Biology of Spiders. Harvard University Press, Cambridge, Massachusetts.

Folmer M., Black W., Lutz R. & Vrijenhoek R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.

Fujisawa T. & Barraclough T.G. 2013. Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Systematic Biology 62 (5): 707–724. https://doi.org/10.1093/sysbio/syt033

Fukushima C.S., Gonçalves de Andrade R.M. & Bertani R. 2017. Two new Brazilian species of Loxosceles Heinecken & Lowe, 1832 with remarks on amazonica and rufescens groups (Araneae, Sicariidae). ZooKeys 667: 67–94. https://doi.org/10.3897/zookeys.667.11369

Gertsch W.J. 1967. The spider genus Loxosceles in South America (Araneae, Scytodidae). Bulletin of the American Museum of Natural History 136: 117–174.

Gertsch W.J. 1958. The spider genus Loxosceles in North America, Central America, and the West Indies. American Museum Novitates 1907: 1–46.

Gertsch W.J. 1973. A report on cave spiders from Mexico and Central America. Association for Mexican Cave Studies Bulletin 5: 141–163.

Gertsch W.J. & Ennik F. 1983. The spider genus Loxosceles in North America, Central America, and the West Indies (Araneae, Loxoscelidae). Bulletin of the American Museum of Natural History 175: 264–360.

Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.

Hamilton C.A., Formanowicz D.R. & Bond J.E. 2011. Species delimitation and phylogeography of Aphonopelma hentzi (Araneae, Mygalomorphae, Theraphosidae): cryptic diversity in North American tarantulas. PLoS ONE 6 (10): e26207. https://doi.org/10.1371/journal.pone.0026207

Hamilton C.A., Hendrixson B.E., Brewer M.S. & Bond J.E. 2014. An evaluation of sampling effects on multiple DNA barcoding methods leads to an integrative approach for delimiting species: A case study of the North American tarantula genus Aphonopelma (Araneae, Mygalomorphae, Theraphosidae). Molecular Phylogenetics and Evolution 71: 79–93. https://doi.org/10.1016/j.ympev.2013.11.007

Hamilton C.A., Hendrixson B.E. & Bond J.E. 2016. Taxonomic revision of the tarantula genus Aphonopelma Pocock, 1901 (Araneae, Mygalomorphae, Theraphosidae) within the United States. ZooKeys 560: 1–340. https://doi.org/10.3897/zookeys.560.6264

Hebert P.D.N., Cywinska A., Ball S.L. & Dewaard J.R. 2003. Biological identifications through DNA barcodes. Proceedings of the Royal Society, B, Biological Sciences 270 (1512): 313–321. https://doi.org/10.1098/rspb.2002.2218

Hebert P.D.N., Penton E.H., Burns J.M., Janzen D.H. & Hallwachs W. 2004. Ten species in one: DNA barcoding reveals cryptic species in the Neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America 101 (41): 14812–14817. https://doi.org/10.1073/pnas.0406166101

Huber B.A. 2003. Rapid evolution and species-specificity of arthropod genitalia: fact or artifact? Organisms Diversity & Evolution 3 (1): 63–71. https://doi.org/10.1078/1439-6092-00059

Huber B.A., Rheims C.A. & Brescovit A.D. 2005. Speciation without changes in genital shape: a case study on Brazilian pholcid spiders (Araneae: Pholcidae). Zoologischer Anzeiger 243 (4): 273–279. https://doi.org/10.1016/j.jcz.2004.12.001

Huber B.A. & Dimitrov D. 2014. Slow genital and genetic but rapid non-genital and ecological differentiation in a pair of spider species (Araneae, Pholcidae). Zoologischer Anzeiger 253 (5): 394–403. https://doi.org/10.1016/j.jcz.2014.04.001

Jarman S.N. & Elliott N.G. 2000. DNA evidence for morphological and cryptic Cenozoic speciations in the Anaspididae ‘living fossils’ from the Triassic. Journal of Evolutionary Biology 13 (4): 624–633. https://doi.org/10.1046/j.1420-9101.2000.00207.x

Ji Y.-J., Zhang D.-X., He L.-J. 2003. Evolutionary conservation and versatility of a new set of primers for amplifying the ribosomal internal transcribed spacer regions in insects and other invertebrates. Molecular Ecology Notes 3 (4): 581–585. https://doi.org/10.1046/j.1471-8286.2003.00519.x

Kapli P., Lutteropp S., Zhang J., Kobert K., Pavlidis P., Stamatakis A. & Flouri T. 2017. Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics 33 (11): 1630–1638. https://doi.org/10.1093/bioinformatics/btx025

Katoh K. & Toh H. 2008. Recent developments in the MAFFT multiple sequence alignment program. Briefings in Bioinformatics 4 (9): 286–298. https://doi.org/10.1093/bib/bbn013

Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., Buxton S., Cooper A., Markowitz S., Duran C., Thierer T., Ashton B., Meintjes P. & Drummond A. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28 (12): 1647–1649. https://doi.org/10.1093/bioinformatics/bts199

Leigh J.W. & Bryant D. 2015. PopArt: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6 (9): 1110–1116. https://doi.org/10.1111/2041-210X.12410

Monaghan M.T., Wild R., Elliot M., Fujisawa T., Balke M., Inward D.J. & Vogler A.P. 2009. Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Systematic Biology 58 (3): 298–311. https://doi.org/10.1093/sysbio/syp027

Ortiz D. & Francke O.F. 2016. Two DNA barcodes and morphology for multi-method species delimitation in Bonnetina tarantulas (Araneae: Theraphosidae). Molecular Phylogenetics and Evolution 101: 176–193. https://doi.org/10.1016/j.ympev.2016.05.003

Planas E. & Ribera C. 2014. Uncovering overlooked island diversity: colonization and diversification of the medically important spider genus Loxosceles (Arachnida: Sicariidae) on the Canary Islands. Journal of Biogeography 41 (7): 1255–1266. https://doi.org/10.1111/jbi.12321

Planas E. & Ribera C. 2015. Description of six new species of Loxosceles (Araneae: Sicariidae) endemic to the Canary Islands and the utility of DNA barcoding for their fast and accurate identification. Zoological Journal of the Linnean Society 174 (1): 47–73. https://doi.org/10.1111/zoj.12226

Pons J., Barraclough T.G. & Gomez-Zurita J. 2006. Sequence based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55 (4): 595–609. https://doi.org/10.1080/10635150600852011

Posada D., 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 (5): 793–808. https://doi.org/10.1080/10635150490522304

Proudlove G. & Wood P.J. 2003. The blind leading the blind: cryptic subterranean species and DNA taxonomy. Trends in Ecology and Evolution 18 (6): 272–273. https://doi.org/10.1016/S0169-5347(03)00095-8

Puillandre N., Lambert A., Brouillet S. & Achaz G. 2012. ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21 (8): 1864–1877. https://doi.org/10.1111/j.1365-294X.2011.05239.x

Rambaut A. & Drummond A.J. 2014. TRACER, MCMC Trace Analysis Tool Version 1.6. University of Edinburgh / University of Auckland, Edinburgh / Auckland.

Ronquist F. & Huelsenbeck J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 (12): 1572–1574. https://doi.org/10.1093/bioinformatics/btg180

Sandidge J.S. & Hopwood J.L. 2005. Brown recluse spiders: a review of biology, life history and pest management. Transactions of the Kansas Academy of Science 108 (3): 99–108. https://doi.org/10.1660/0022-8443(2005)108[0099:BRSARO]2.0.CO;2

Tahami M.S., Zamani A., Sadeghil S. & Ribera C. 2017. A new species of Loxosceles Heineken & Lowe, 1832 (Araneae: Sicariidae) from Iranian caves. Zootaxa 4318(2): 377–387. https://doi.org/10.11646/zootaxa.4318.2.10

Valdez-Mondragón A. & Francke O.F. 2015. Phylogeny of the spider genus Ixchela Huber, 2000 (Araneae: Pholcidae) based on morphological and molecular evidence (CO1 and 16S), with a hypothesized diversification in the Pleistocene. Zoological Journal of the Linnean Society 175: 20–58. https://doi.org/10.1111/zoj.12265

Valdez-Mondragón A., Cortez-Roldán M.R., Juárez-Sánchez A.R., Solís-Catalán K.P. & Navarro-Rodríguez C.I. 2018a. Arañas de Importancia Medica: Arañas violinistas del género Loxosceles en México: ¿que sabemos acerca de su distribución y biología hasta ahora? Boletín de la Asociación Mexicana de Sistemática de Artrópodos (AMXSA) 2 (1): 14–24.

Valdez-Mondragón A., Cortez-Roldán M.R., Juárez-Sánchez A.R. & Solís-Catalán K.P. 2018b. A new species of Loxosceles Heineken & Lowe (Araneae, Sicariidae), with updated distribution records and biogeographical comments for the species from Mexico, including a new record of Loxosceles rufescens (Dufour). ZooKeys 802: 39–66. https://doi.org/10.3897/zookeys.802.28445

Valdez-Mondragón A., Navarro-Rodríguez C.I., Solís-Catalán K.P., Cortez-Roldán M.R. & Juárez-Sánchez A.R. 2019. Under an integrative taxonomic approach: the description of a new species of the genus Loxosceles (Araneae, Sicariidae) from Mexico City. ZooKeys 892: 93–133. https://doi.org/10.3897/zookeys.892.39558

Vetter R.S. 2008. Spiders of the genus Loxosceles (Araneae, Sicariidae): a review of biological, medical and psychological aspects regarding envenomations. Journal of Arachnology 36 (1): 150–163. https://doi.org/10.1636/RSt08-06.1

Vetter R.S. 2015. The Brown Recluse Spider. Cornell University Press / Comstock Publishing Associates, Ithaca / London.

Witt J.D.S. & Hebert P.D.N. 2000. Cryptic species diversity and evolution in the amphipod genus Hyalella within central glaciated North America: a molecular phylogenetic approach. Canadian Journal of Fisheries and Aquatic Sciences 57 (4): 687–698. https://doi.org/10.1139/f99-285

World Spider Catalog. 2020. World Spider Catalog. Version 20.0. Natural History Museum Bern. Available from http://wsc.nmbe.ch [accessed 20 Jan. 2020]. https://doi.org/10.24436/2

Zhang J., Kapli P., Pavlidis P. & Stamatakis A. 2013. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29 (22): 2869–2876. https://doi.org/10.1093/bioinformatics/btt499

Published
2020-08-19
How to Cite
Navarro-Rodríguez, C. I., & Valdez-Mondragón, A. (2020). Description of a new species of Loxosceles Heineken & Lowe (Araneae, Sicariidae) recluse spiders from Hidalgo, Mexico, under integrative taxonomy: morphological and DNA barcoding data (CO1 + ITS2). European Journal of Taxonomy, (704). https://doi.org/10.5852/ejt.2020.704
Section
Zoology