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

Hooroo mates! Phylogenomic data suggest that the closest relatives of the iconic Tasmanian cave spider Hickmania troglodytes are in Australia and New Zealand, not in South America

Siddharth Kulkarni https://orcid.org/0000-0002-7400-4704 A B and Gustavo Hormiga https://orcid.org/0000-0002-0046-1822 A
+ Author Affiliations
- Author Affiliations

A Department of Biological Sciences, The George Washington University, 2029 G Street NW, Washington, DC 20052, USA.

B Corresponding author. Email: sskspider@gwmail.gwu.edu

Invertebrate Systematics 35(8) 850-856 https://doi.org/10.1071/IS21030
Submitted: 15 April 2021  Accepted: 11 June 2021   Published: 5 November 2021

Abstract

Hickmania troglodytes is an emblematic cave spider representing a monotypic cribellate spider genus. This is the only Australian lineage of Austrochilidae while the other members of the family are found in southern South America. In addition to being the largest spider in Tasmania, Hickmania is an oddity in Austrochilidae because this is the only lineage in the family bearing posterior book lungs, tarsal spines and an embolar process on male pedipalps. Six-gene Sanger sequences and genome scale data such as ultraconserved elements (UCEs) and transcriptomes have suggested that Hickmania troglodytes is not nested with the family of current classification, Austrochilidae. We studied the phylogenetic placement of Hickmania troglodytes using an increased taxon sample by combining publicly available UCE and UCEs recovered from transcriptomic data in a parsimony and maximum likelihood framework. Based on our phylogenetic results we formally transfer Hickmania troglodytes from Austrochilidae to the family Gradungulidae. The cladistic placement of Hickmania in the family Gradungulidae fits the geographic distribution of both gradungulids (restricted to Australia and New Zealand) and austrochilids (restricted to southern South America) more appropriately.


References

Benjamini, Y., and Speed, T. P. (2012). Summarizing and correcting the GC content bias in high-throughput sequencing Nucleic Acids Research 40, e72.
Summarizing and correcting the GC content bias in high-throughput sequencingCrossref | GoogleScholarGoogle Scholar | 22323520PubMed |

Fernández, R., Kallal, R. J., Dimitrov, D., Ballesteros, J. A., Arnedo, M., Giribet, G., and Hormiga, G. (2018). Phylogenomics, diversification dynamics, and comparative transcriptomics across the spider tree of life. Current Biology 28, 1489–1497.e5.
Phylogenomics, diversification dynamics, and comparative transcriptomics across the spider tree of life.Crossref | GoogleScholarGoogle Scholar | 29706520PubMed |

Forster, R. R., Platnick, N. I., and Gray, M. R. (1987). A review of the spider superfamilies Hypochiloidea and Austrochiloidea (Araneae, Araneomorphae). Bulletin of the American Museum of Natural History 185, 1–116.

Fu, L., Niu, B., Zhu, Z., Wu, S., and Li, W. (2012). CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150–3152.
CD-HIT: accelerated for clustering the next-generation sequencing data.Crossref | GoogleScholarGoogle Scholar | 23060610PubMed |

Goloboff, P. A., Farris, J. S., Källersjö, M., Oxelman, B., Ramírez, M. J., and Szumik, C. A. (2003). Improvements to resampling measures of group support. Cladistics 19, 324–332.
Improvements to resampling measures of group support.Crossref | GoogleScholarGoogle Scholar |

Goloboff, P. A., Farris, J. S., and Nixon, K. C. (2008). TNT, a free program for phylogenetic analysis. Cladistics 24, 774–786.
TNT, a free program for phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar |

Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., Chen, Z., Mauceli, E., Hacohen, N., Gnirke, A., Rhind, N., Palma, F., Birren, B. W., Nusbaum, C., Lindblad-Toh, K., Friedman, N., and Regev, A. 2011 Full-length transcriptome assembly from RNA-Seq data without a reference genome.Nature Biotechnology29 7 64465210.1038/nbt.1883

Griswold, C. E., Ramírez, M. J., Coddington, J. A., and Platnick, N. I. (2005). Atlas of phylogenetic data for entelegyne spiders (Araneae: Araneomorphae: Entelegynae) with comments on their phylogeny. Proceedings of the California Academy of Sciences 56, 1–324.

Guindon, S., Dufayard, J., Lefort, V., Anisimova, M., Hordijk, W., and Gascuel, O. (2010). New algorithms and methods to estimate maximum- likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.
New algorithms and methods to estimate maximum- likelihood phylogenies: assessing the performance of PhyML 3.0.Crossref | GoogleScholarGoogle Scholar | 20525638PubMed |

Haas, B. J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P. D., Bowden, J., Couger, M. B., Eccles, D., Li, B., Lieber, M., MacManes, M. D., Ott, M., Orvis, J., Pochet, N., Strozzi, F., Weeks, N., Westerman, R., William, T., Dewey, C. N., Henschel, R., LeDuc, R. D., Friedman, N., and Regev, A. 2013 De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis.Nature Protocols8 8 1494151210.1038/nprot.2013.084

Hickman, V. V. (1967). ‘Some Common Spiders of Tasmania.’ (Tasmanian Museum and Art Gallery.)

Hoang, D. T., Chernomor, O., von Haeseler, A., Minh, B.-Q., and Vinh, L. S. (2018). UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35, 518–522.
UFBoot2: improving the ultrafast bootstrap approximation.Crossref | GoogleScholarGoogle Scholar | 29077904PubMed |

Kallal, R., Kulkarni, S., Dimitrov, D., Benavides, L. R., Arnedo, M., Giribet, G., and Hormiga, G. (2021). Converging on the orb: denser taxon sampling elucidates spider phylogeny and new analytical methods support repeated evolution of the orb web. Cladistics 37, 298–316.
Converging on the orb: denser taxon sampling elucidates spider phylogeny and new analytical methods support repeated evolution of the orb web.Crossref | GoogleScholarGoogle Scholar | 34478199PubMed |

Kalyaanamoorthy, S., Minh, B.-Q., Wong, T. K. F., von Haeseler, A., and Jermiin, L. S. (2017). ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods 14, 587–589.
ModelFinder: Fast model selection for accurate phylogenetic estimates.Crossref | GoogleScholarGoogle Scholar | 28481363PubMed |

Kent, W. J. (2002). BLAT—the BLAST-like alignment tool. Genome Research 12, 656–664.
BLAT—the BLAST-like alignment tool.Crossref | GoogleScholarGoogle Scholar | 11932250PubMed |

Kulkarni, S. S., Wood, H. M., Lloyd, M., and Hormiga, G. (2020). Spider-specific probe set for ultraconserved elements offers new perspectives on the evolutionary history of spiders (Arachnida, Araneae). Molecular Ecology Resources 20, 185–203.
Spider-specific probe set for ultraconserved elements offers new perspectives on the evolutionary history of spiders (Arachnida, Araneae).Crossref | GoogleScholarGoogle Scholar |

Kulkarni, S., Kallal, R. J., Wood, H., Dimitrov, D., Giribet, G., and Hormiga, G. (2021). Interrogating genomic-scale data to resolve recalcitrant nodes in the Spider Tree of Life. Molecular Biology and Evolution 38, 891–903.
Interrogating genomic-scale data to resolve recalcitrant nodes in the Spider Tree of Life.Crossref | GoogleScholarGoogle Scholar | 32986823PubMed |

Langmead, B., and Salzberg, S. (2012). Fast gapped-read alignment with Bowtie 2. Nature Methods 9, 357–359.
Fast gapped-read alignment with Bowtie 2.Crossref | GoogleScholarGoogle Scholar | 22388286PubMed |

Ledford, J., Derkarabetian, S., Ribera, C., Starrett, J., Bond, J. E., Griswold, C., and Hedin, M. (2021). Phylogenomics and biogeography of leptonetid spiders (Araneae: Leptonetidae). Invertebrate Systematics 35, 332–349.

Lehtinen, P. T. (1967). Classification of the cribellate spiders and some allied families, with notes on the evolution of the suborder Araneomorpha. Annales Zoologici Fennici 4, 199–468.

Marples, B. J. (1968). The hypochilomorph spiders. Proceedings of the Linnean Society of London 179, 11–31.
The hypochilomorph spiders.Crossref | GoogleScholarGoogle Scholar |

Michalik, P., Piacentini, L., Lipke, E., and Ramírez, M. J. (2013). The enigmatic Otway odd-clawed spider (Progradungula otwayensis Milledge, 1997, Gradungulidae, Araneae): natural history, first description of the female and micro-computed tomography of the male palpal organ. ZooKeys 335, 101–112.
The enigmatic Otway odd-clawed spider (Progradungula otwayensis Milledge, 1997, Gradungulidae, Araneae): natural history, first description of the female and micro-computed tomography of the male palpal organ.Crossref | GoogleScholarGoogle Scholar |

Murphy, J. A., and Roberts, M. J. (2015). ‘Spider Families of the World and their Spinnerets.’ (British Arachnological Society: York, UK.)

Nguyen, L. T., Schmidt, H. A., von Haeseler, A., and Minh, B. Q. (2015). IQ-TREE: a fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Molecular Biology and Evolution 32, 268–274.
IQ-TREE: a fast and effective stochastic algorithm for estimating maximum likelihood phylogenies.Crossref | GoogleScholarGoogle Scholar | 25371430PubMed |

Platnick, N. I. (1977). The Hypochiloid spiders: a cladistic analysis, with notes of the Atypoidea (Arachnida, Araneae). American Museum Novitates 2627, 1–23.

Platnick, N. I., Hormiga, G., Jäger, P., Jocqué, R., Ramírez, M. J., and Raven, R. J. (2020). Spiders of the world: a natural history. (Princeton University Press.) Available at https://press.princeton.edu/books/hardcover/9780691188850/spiders-of-the-world

Ramírez, M. J., Magalhaes, I. L. F., Derkarabetian, S., Ledford, J., Griswold, C. E., Wood, H. M., and Hedin, M. (2021). Sequence capture phylogenomics of true spiders reveals convergent evolution of respiratory systems. Systematic Biology 70, 14–20.
Sequence capture phylogenomics of true spiders reveals convergent evolution of respiratory systems.Crossref | GoogleScholarGoogle Scholar | 32497195PubMed |

Song, L., and Florea, L. (2015). Rcorrector: efficient and accurate error correction for Illumina RNA-seq reads. GigaScience 4, 48.
Rcorrector: efficient and accurate error correction for Illumina RNA-seq reads.Crossref | GoogleScholarGoogle Scholar | 26500767PubMed |

Starrett, J., Derkarabetian, S., Hedin, M., Bryson, R. W., McCormack, J. E., and Faircloth, B. C. (2017). High phylogenetic utility of an ultraconserved element probe set designed for Arachnida. Molecular Ecology Resources 17, 812–823.
High phylogenetic utility of an ultraconserved element probe set designed for Arachnida.Crossref | GoogleScholarGoogle Scholar | 27768256PubMed |

Wheeler, W. C., Coddington, J. A., Crowley, L. M., Dimitrov, D., Goloboff, P. A., Griswold, C. E., Hormiga, G., Prendini, L., Ramírez, M. J., Sierwald, P., Almeida-Silva, L. M., Álvarez-Padilla, F., Arnedo, M. A., Benavides, L. R., Benjamin, S. P., Bond, J. E., Grismado, C. J., Hasan, E., Hedin, M., Izquierdo, M. A., Labarque, F. M., Ledford, J., Lopardo, L., Maddison, W. P., Miller, J. A., Piacentini, L. N., Platnick, N. I., Polotow, D., Silva-Dávila, D., Scharff, N., Szũts, T., Ubick, D., Vink, C., Wood, H. M., and Zhang, J. X. 2017 The spider tree of life: phylogeny of Araneae based on target-gene analyses from an extensive taxon sampling.Cladistics33 57461610.1111/cla.12182

Zapfe, H. (1955). Filogenia y función en Austrochilus manni Gertsch y Zapfe (Araneae-Hypochilidae). Trabajos del Laboratorio de Zoologia de la Universidad de Chile 2, 1–53.