Phylogenetic placement of the stone-nest orb-weaving spider Nemoscolus Simon, 1895 (Araneae : Araneidae) and the description of the first species from Australia
Robert J. Kallal A B C and Gustavo Hormiga AA Department of Biological Sciences, The George Washington University, 2029 G Street NW, Washington, DC 20052, USA.
B Department of Entomology, National Museum of Natural History, 10th and Constitution Avenue NW, Washington, DC 20560, USA.
C Corresponding author. Email: kallalr@si.edu
Invertebrate Systematics 34(8) 893-905 https://doi.org/10.1071/IS20035
Submitted: 28 April 2020 Accepted: 28 June 2020 Published: 16 November 2020
Abstract
The spider genus Nemoscolus Simon, 1895 (Araneidae) has been neglected taxonomically despite the unique retreat that several species construct in their horizontal orb-webs, composed of pebbles and other detritus. The distribution of Nemoscolus is poorly known and the genus includes species from Africa and Europe. Nemoscolus is placed in Simon’s Cycloseae species group along with Cyclosa Menge, 1866, Acusilas Simon, 1895, Arachnura Vinson, 1863, Witica O. Pickard-Cambridge, 1895, among others. Here we describe a new species from Queensland, Australia, N. sandersi, sp. nov., drastically expanding the distribution range of the genus. We use nucleotide sequence data to phylogenetically place Nemoscolus using model-based inference methods within Araneidae and to explore its affinities to Simon’s Cycloseae. The data support propinquity of Nemoscolus with Acusilas and Arachnura but not with Cyclosa. Our analyses suggest that Cycloseae is not a clade, with Cyclosa, Acusilas, Witica and Nemoscolus not sharing a recent common ancestor. This use of an integrated granular retreat represents at least the second independent evolution of such a structure within Araneidae. These results improve our understanding of both phylogeny and retreat evolution in araneid spiders.
Keywords: Araneoidea, Australia, orb web, systematics, taxonomy.
References
Agnarsson, I., and Blackledge, T. A. (2009). Can a spider web be too sticky? Tensile mechanics constrains the evolution of capture spiral stickiness in orb-weaving spiders. Journal of Zoology 278, 134–140.| Can a spider web be too sticky? Tensile mechanics constrains the evolution of capture spiral stickiness in orb-weaving spiders.Crossref | GoogleScholarGoogle Scholar |
Álvarez-Padilla, F., and Hormiga, G. (2007). A protocol for digesting internal soft tissues and mounting spiders for scanning electron microscopy. The Journal of Arachnology 35, 538–542.
| A protocol for digesting internal soft tissues and mounting spiders for scanning electron microscopy.Crossref | GoogleScholarGoogle Scholar |
Álvarez-Padilla, F., Dimitrov, D., Giribet, G., and Hormiga, G. (2009). Phylogenetic relationships of the spider family Tetragnathidae (Araneae, Araneoidea) based on morphological and DNA sequence data. Cladistics 25, 109–146.
| Phylogenetic relationships of the spider family Tetragnathidae (Araneae, Araneoidea) based on morphological and DNA sequence data.Crossref | GoogleScholarGoogle Scholar |
Arnedo, M. A., Coddington, J. A., Agnarsson, I., and Gillespie, R. G. (2004). From a comb to a tree: phylogenetic relationships of the comb-footed spiders (Araneae, Theridiidae) inferred from nuclear and mitochondrial genes. Molecular Phylogenetics and Evolution 31, 225–245.
| From a comb to a tree: phylogenetic relationships of the comb-footed spiders (Araneae, Theridiidae) inferred from nuclear and mitochondrial genes.Crossref | GoogleScholarGoogle Scholar | 15019622PubMed |
Berland, L. (1920). Note sur une araignée de Madagascar (Nemoscolus waterloti nov. sp.) et sur son industrie. Bulletin du Muséum National d’Histoire Naturelle 26, 384–387.
Berland, L. (1933). Une nouvelle espèce de Nemoscolus (araignées) du Soudan français, et son industrie. Bulletin de la Société Zoologique de France 58, 247–251.
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 species. BMC Evolutionary Biology 11, 317.
| Gone with the plate: the opening of the Western Mediterranean basin drove the diversification of ground-dweller species.Crossref | GoogleScholarGoogle Scholar | 22039781PubMed |
Blackledge, T. A., Scharff, N., Coddington, J. A., Szűts, T., Wenzel, J. W., Hayashi, C. Y., and Agnarsson, I. (2009). Reconstructing web evolution and spider diversification in the molecular era. Proceedings of the National Academy of Sciences of the United States of America 106, 5229–5234.
| Reconstructing web evolution and spider diversification in the molecular era.Crossref | GoogleScholarGoogle Scholar | 19289848PubMed |
Cabra-García, J., and Hormiga, G. (2020). Exploring the impact of morphology, multiple sequence alignment and choice of optimality criteria in phylogenetic inference: a case study with the Neotropical orb-weaving spider genus Wagneriana (Araneae: Araneidae). Zoological Journal of the Linnean Society 188, 976–1151.
| Exploring the impact of morphology, multiple sequence alignment and choice of optimality criteria in phylogenetic inference: a case study with the Neotropical orb-weaving spider genus Wagneriana (Araneae: Araneidae).Crossref | GoogleScholarGoogle Scholar |
Capella-Gutiérrez, S., Silla-Martínez, J. M., and Gabaldón, T. (2009). TrimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973.
| TrimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 19505945PubMed |
Cheng, R. C., and Kuntner, M. (2014). Phylogeny suggests nondirectional and isometric evolution of sexual size dimorphism in argiopine spiders. Evolution 68, 2861–2872.
| Phylogeny suggests nondirectional and isometric evolution of sexual size dimorphism in argiopine spiders.Crossref | GoogleScholarGoogle Scholar | 25130435PubMed |
Dimitrov, D., Benavides, L. R., Arnedo, M. A., Giribet, G., Griswold, C. E., Scharff, N., and Hormiga, G. (2017). Rounding up the usual suspects: a standard target-gene approach for resolving the interfamilial phylogenetic relationships of ecribellate orb-weaving spiders with a new family-rank classification (Araneae, Araneoidea). Cladistics 33, 221–250.
| Rounding up the usual suspects: a standard target-gene approach for resolving the interfamilial phylogenetic relationships of ecribellate orb-weaving spiders with a new family-rank classification (Araneae, Araneoidea).Crossref | GoogleScholarGoogle Scholar |
Dippenaar-Schoeman, A. (2014). ‘A Field Guide to the Spiders of South Africa.’ (CTP Printers: Cape Town, South Africa.)
Fahey, B. F., and Elgar, M. A. (1997). Sexual cohabitation as mate-guarding in the leaf-curling spider Phonognatha graeffei Keyserling (Araneoidea, Araneae). Behavioral Ecology and Sociobiology 40, 127–133.
| Sexual cohabitation as mate-guarding in the leaf-curling spider Phonognatha graeffei Keyserling (Araneoidea, Araneae).Crossref | GoogleScholarGoogle Scholar |
Fernández, R., Kallal, R. J., Dimitrov, D., Ballesteros, J. A., Arnedo, M. A., Giribet, G., and Hormiga, G. (2018a). 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 |
Fernández, R., Kallal, R. J., Dimitrov, D., Ballesteros, J. A., Arnedo, M. A., Giribet, G., and Hormiga, G. (2018b). Correction: Phylogenomics, diversification dynamics, and comparative transcriptomics across the spider tree of life. Current Biology 28, 2190–2193.
| Correction: Phylogenomics, diversification dynamics, and comparative transcriptomics across the spider tree of life.Crossref | GoogleScholarGoogle Scholar | 29990448PubMed |
Foord, S. F., Dippenaar-Schoeman, A. S., Haddad, C. R., Lotz, L. N., and Lyle, R. (2011). The faunistic diversity of spiders (Arachnida: Araneae) of the Savanna Biome in South Africa. Transactions of the Royal Society of South Africa 66, 170–201.
| The faunistic diversity of spiders (Arachnida: Araneae) of the Savanna Biome in South Africa.Crossref | GoogleScholarGoogle Scholar |
Gregorič, M., Agnarsson, I., Blackledge, T. A., and Kuntner, M. (2015). Phylogenetic position and composition of Zygiellinae and Caerostris, with new insight into orb-web evolution and gigantism. Zoological Journal of the Linnean Society 175, 225–243.
| Phylogenetic position and composition of Zygiellinae and Caerostris, with new insight into orb-web evolution and gigantism.Crossref | GoogleScholarGoogle Scholar |
Guindon, S., Dufayard, J.-F., 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 |
Han, G. X., Zhu, M. S., and Levi, H. W. (2009). On two rare south-east Asian araneid genera: Deione and Talthybia (Araneae: Araneidae). Zootaxa 2297, 55–63.
| On two rare south-east Asian araneid genera: Deione and Talthybia (Araneae: Araneidae).Crossref | GoogleScholarGoogle Scholar |
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 |
Holm, A. (1979). A taxonomic study of European and East African species of the genera Pelecopsis and Trichopterna (Araneae, Linyphiidae), with descriptions of a new genus and two new species of Pelecopsis from Kenya. Zoologica Scripta 8, 255–278.
| A taxonomic study of European and East African species of the genera Pelecopsis and Trichopterna (Araneae, Linyphiidae), with descriptions of a new genus and two new species of Pelecopsis from Kenya.Crossref | GoogleScholarGoogle Scholar |
Kallal, R. J., and Hormiga, G. (2018). Systematics, phylogeny and biogeography of the Australasian leaf-curling orb-weaving spiders (Araneae: Araneidae: Zygiellinae), with a comparative analysis of retreat evolution. Zoological Journal of the Linnean Society 184, 1055–1141.
| Systematics, phylogeny and biogeography of the Australasian leaf-curling orb-weaving spiders (Araneae: Araneidae: Zygiellinae), with a comparative analysis of retreat evolution.Crossref | GoogleScholarGoogle Scholar |
Kallal, R. J., Fernández, R., Giribet, G., and Hormiga, G. (2018). A phylotranscriptomic backbone of the orb-weaving spider family Araneidae (Arachnidae, Araneae) supported by multiple methodological approaches. Molecular Phylogenetics and Evolution 126, 129–140.
| A phylotranscriptomic backbone of the orb-weaving spider family Araneidae (Arachnidae, Araneae) supported by multiple methodological approaches.Crossref | GoogleScholarGoogle Scholar | 29635025PubMed |
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 |
Katoh, K., and Standley, D. M. (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 | GoogleScholarGoogle Scholar | 23329690PubMed |
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., and Drummond, A. (2012). Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.
| Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data.Crossref | GoogleScholarGoogle Scholar | 22543367PubMed |
Kovoor, J., and Lopez, A. (1980). Variation de l’appareil séricigène dans la famille des Araneidae: Cas des genres Cyclosa Menge et Nemoscolus Simon. Comptes-Rendus de la Vème Colloque d’Arachnologie d’Expression Française IX, 119–127.
Kuntner, M., Arnedo, M. A., Trontelj, P., Lokovšek, 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 | GoogleScholarGoogle Scholar | 23811436PubMed |
Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T., and Calcott, B. (2017). PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution 34, 772–773.
| PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 28013191PubMed |
Levi, H. W. (1986). The orb-weaver genus Witica (Araneae: Araneidae). Psyche 93, 35–46.
| The orb-weaver genus Witica (Araneae: Araneidae).Crossref | GoogleScholarGoogle Scholar |
Levi, H. W. (1995). Orb-weaving spiders Actinosoma, Spilasma, Micrepeira, Pronous, and four new genera (Araneae: Araneidae). Bulletin of the Museum of Comparative Zoology 154, 153–213.
Levold, A., and Finch, O.-D. (2009). Retreats of orb web spiders (Araneae, Araneidae) as hibernation sites for terrestrial arthropods. The Journal of Arachnology 37, 122–123.
| Retreats of orb web spiders (Araneae, Araneidae) as hibernation sites for terrestrial arthropods.Crossref | GoogleScholarGoogle Scholar |
Li, C., Wang, Z.-L., Fang, W.-Y., and Xu, X.-P. (2016). The complete mitochondrial genomes of two orb-weaving spider Cyrtarachne nagasakiensis (Strand, 1918) and Hypsosinga pygmaea (Sundevall, 1831) (Araneae, Araneidae). Mitochondrial DNA – A. DNA Mapping, Sequencing, and Analysis 27, 2811–2812.
| The complete mitochondrial genomes of two orb-weaving spider Cyrtarachne nagasakiensis (Strand, 1918) and Hypsosinga pygmaea (Sundevall, 1831) (Araneae, Araneidae).Crossref | GoogleScholarGoogle Scholar |
Lopardo, L., Giribet, G., and Hormiga, G. (2011). Morphology to the rescue: molecular data and the signal of morphological characters in combined phylogenetic analyses – a case study from mysmenid spiders (Araneae, Mysmenidae), with comments on the evolution of web architecture. Cladistics 27, 278–330.
| Morphology to the rescue: molecular data and the signal of morphological characters in combined phylogenetic analyses – a case study from mysmenid spiders (Araneae, Mysmenidae), with comments on the evolution of web architecture.Crossref | GoogleScholarGoogle Scholar |
Lubin, Y. D. (1978). Seasonal abundance and diversity of web-building spiders in relation to habitat structure on Barro Colorado Island, Panama. The Journal of Arachnology 6, 31–51.
Miller, M. A., Pfeiffer, W., and Schwartz, T. (2010). Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In ‘2010 Gateway Computing Environments Workshop (GCE), 23 December 2010, New Orleans, LA, USA’. INSPEC Accession Number 11705685. (Institute of Electrical and Electronics Engineers: Piscataway, NJ, USA.)
Morano, E., and Ferrández, M. A. (1986). Especies nuevas o interes de la familia Araneidae Latreilla, 1806 (Arachnida, Araneae) de la Fauna Iberica. Miscellània Zoològica 9, 171–178.
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 |
Pyron, R. A. (2017). Novel approaches for phylogenetic inference from morphological data and total-evidence dating in squamate reptiles (lizards, snakes, and amphisbaenians). Systematic Biology 66, 38–56.
| 28173602PubMed |
Ranwez, V., Douzery, E. J. P., Cambon, C., Chantret, N., and Delsuc, F. (2018). MACSE v2: toolkit for alignment of coding sequences accounting for frameshifts and stop codons. Molecular Biology and Evolution 35, 2582–2584.
| MACSE v2: toolkit for alignment of coding sequences accounting for frameshifts and stop codons.Crossref | GoogleScholarGoogle Scholar | 30165589PubMed |
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 | GoogleScholarGoogle Scholar | 12912839PubMed |
Sanders, J. G. (2010). Program note: Cladescan, a program for automated phylogenetic sensitivity analyses. Cladistics 26, 114–116.
| Program note: Cladescan, a program for automated phylogenetic sensitivity analyses.Crossref | GoogleScholarGoogle Scholar |
Scharff, N., and Coddington, J. A. (1997). A phylogenetic analysis of the orb-weaving spider family Araneidae (Arachnida, Araneae). Zoological Journal of the Linnean Society 120, 355–434.
| A phylogenetic analysis of the orb-weaving spider family Araneidae (Arachnida, Araneae).Crossref | GoogleScholarGoogle Scholar |
Scharff, N., and Schmidt, J. B. (2008). A taxonomic revision of the orb-weaving spider genus Acusilas Simon, 1895 (Araneae, Araneidae). Insect Systematics & Evolution 39, 1–38.
| A taxonomic revision of the orb-weaving spider genus Acusilas Simon, 1895 (Araneae, Araneidae).Crossref | GoogleScholarGoogle Scholar |
Scharff, N., Coddington, J. A., Blackledge, T. A., Agnarsson, I., Framenau, V. W., Szűts, T., Hayashi, C. Y., and Dimitrov, D. (2020). Phylogeny of the orb-weaving spider family Araneidae (Araneae: Araneoidea). Cladistics 36, 1–21.
| Phylogeny of the orb-weaving spider family Araneidae (Araneae: Araneoidea).Crossref | GoogleScholarGoogle Scholar |
Simon, E. (1895). ‘Histoire Naturelle des Araignées.’ (Tip. del R. Istituto Sordo-Muti: Paris.)
Simon, E. (1903). Descriptions d’arachnides nouveaux. Annales de la Société Entomologique de Belgique 47, 21–39.
| Descriptions d’arachnides nouveaux.Crossref | GoogleScholarGoogle Scholar |
Stamatakis, A. (2014). RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.
| RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies.Crossref | GoogleScholarGoogle Scholar | 24451623PubMed |
Tan, J. (2018). Argiope hoiseni, a new species of the spider genus Argiope (Araneae, Araneidae) from Peninsular Malaysia based on morphology and molecular analyses. Zootaxa 4457, 129–142.
| Argiope hoiseni, a new species of the spider genus Argiope (Araneae, Araneidae) from Peninsular Malaysia based on morphology and molecular analyses.Crossref | GoogleScholarGoogle Scholar | 30314183PubMed |
Tan, J., Chan, Z. Y., Ong, C. A., and Yong, H. S. (2019). Phylogenetic relationships of Actinacantha Simon, Gasteracantha Sundevall, Macracantha Hasselt and Thelacantha Simon spiny orbweavers (Araneae: Araneidae) in Peninsular Malaysia. The Raffles Bulletin of Zoology 67, 32–55.
| Phylogenetic relationships of Actinacantha Simon, Gasteracantha Sundevall, Macracantha Hasselt and Thelacantha Simon spiny orbweavers (Araneae: Araneidae) in Peninsular Malaysia.Crossref | GoogleScholarGoogle Scholar |
Tanikawa, A., Shinkai, A., and Miyashita, T. (2014). Molecular phylogeny of moth-specialized spider sub-family Cyrtarachninae, which includes bolas spiders. Zoological Science 31, 716–720.
| Molecular phylogeny of moth-specialized spider sub-family Cyrtarachninae, which includes bolas spiders.Crossref | GoogleScholarGoogle Scholar | 25366153PubMed |
Wheeler, W. C., and Hayashi, C. Y. (1998). The phylogeny of the extant chelicerate orders. Cladistics 14, 173–192.
| The phylogeny of the extant chelicerate orders.Crossref | GoogleScholarGoogle Scholar |
Wheeler, W., 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., Álvarez‐Padilla, F., Arnedo, M. A., Benavides Silva, 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., Szűts, T., Ubick, D., Vink, C. J., Wood, H. M., and Zhang, J. (2017). The spider tree of life: phylogeny of Araneae based on target-gene analyses from an extensive taxon sampling. Cladistics 33, 574–616.
| The spider tree of life: phylogeny of Araneae based on target-gene analyses from an extensive taxon sampling.Crossref | GoogleScholarGoogle Scholar |
Zhang, C., Stadler, T., Klopfstein, S., Heath, T. A., and Ronquist, F. (2016). Total evidence dating under the fossilized birth–death process. Systematic Biology 65, 228–249.
| Total evidence dating under the fossilized birth–death process.Crossref | GoogleScholarGoogle Scholar | 26493827PubMed |