Castaways: the Leeward Antilles endemic spider genus Papiamenta (Araneae: Pholcidae)
Bernhard A. Huber A * , Guanliang Meng A , Tim M. Dederichs B , Peter Michalik B , Martin Forman C and Jiří Král CA
B
C
Abstract
Ninetinae is a group of small to tiny short-legged spiders largely restricted to arid habitats. Among daddy-long-legs spiders (Pholcidae) this is by far the least diverse subfamily but this may partly be a result of inadequate collecting, poor representation in collections or scientific neglect. We build on a large recent collection of the ninetine genus Papiamenta Huber, 2000 from the Leeward Antilles and use cytochrome oxidase 1 (COI) sequences, extensive scanning electron microscopy data, transmission electron microscopy data and karyotyping to analyse this geographically isolated and poorly known island genus. COI sequences support the split between the two morphologically distinct species on Curaçao but genetic distances between these are surprisingly low (7.4–9.8%; mean 8.6%). The type species P. levii (Gertsch, 1982) may include more than one species but COI and morphology suggest conflicting clade limits. A third species, P. bonay Huber sp. nov. is newly described from Bonaire. Our data on sperm ultrastructure and karyology are puzzling as these suggest different phylogenetic affinities of Papiamenta to other genera. Males transfer sperm as individual sperm (cleistosperm), agreeing with the putative closest relatives as suggested by molecular data, the North American genera Pholcophora and Tolteca. The sex chromosome system (X1X2X3Y) of P. levii, however, is as in the South American Ninetinae genera Gertschiola and Nerudia but different from the putative closest relatives.
ZooBank: urn:lsid:zoobank.org:pub:7A6A2E84-3A61-4637-AF6F-0E31A9FA79A8
Keywords: COI barcodes, karyotype, new species, Ninetinae, sensilla, sex chromosome, sperm ultrastructure, taxonomy.
References
Aharon S, Huber BA, Gavish-Regev E (2017) Daddy-long-leg giants: revision of the spider genus Artema Walckenaer, 1837 (Araneae, Pholcidae). European Journal of Taxonomy 376, 1-57.
| Crossref | Google Scholar |
Ashfaq M, Blagoev G, Tahir HM, Khan AM, Mukhtar MK, Akhtar S, et al. (2019) Assembling a DNA barcode reference library for the spiders (Arachnida: Araneae) of Pakistan. PLoS One 14, e0217086.
| Crossref | Google Scholar | PubMed |
Astrin JJ, Huber BA, Misof B, Klütsch CFC (2006) Molecular taxonomy in pholcid spiders (Pholcidae, Araneae): evaluation of species identification methods using CO1 and 16S rRNA. Zoologica Scripta 35, 441-457.
| Crossref | Google Scholar |
Astrin JJ, Höfer H, Spelda J, Holstein J, Bayer S, Hendrich L, Huber BA, Kielhorn K-H, Krammer H-J, Lemke M, Monje JC, Morinière J, Rulik B, Petersen M, Janssen H, Muster C (2016) Towards a DNA barcode reference database for spiders and harvestmen of Germany. PLoS One 11, e0162624.
| Crossref | Google Scholar | PubMed |
Ávila Herrera IM, Král J, Pastuchová M, Forman M, Musilová J, Kořínková T, Šťáhlavský F, Zrzavá M, Nguyen P, Just P, Haddad CR, Hiřman M, Koubová M, Sadílek D, Huber BA (2021) Evolutionary pattern of karyotypes and meiosis in pholcid spiders (Araneae: Pholcidae): implications for reconstructing chromosome evolution of araneomorph spiders. BMC Ecology and Evolution 21, 75.
| Crossref | Google Scholar |
Brown BV (1993) A further chemical alternative to critical-point-drying for preparing small (or large) flies. Fly Times 11, 10.
| Google Scholar |
Castanheira P, Pérez-González A, Baptista RL (2016) Spider diversity (Arachnida: Araneae) in Atlantic Forest areas at Pedra Branca State Park, Rio de Janeiro, Brazil. Biodiversity Data Journal 4, e7055.
| Crossref | Google Scholar | PubMed |
Chrysanthus OFM (1967) Spiders from South New Guinea IX. Tijdschrift voor Entomologie 110, 89-105.
| Google Scholar |
Cock PJ, Antao T, Chang JT, Chapman BA, Cox CJ, Dalke A, Friedberg I, Hamelryck T, Kauff F, Wilczynski B, de Hoon MJ (2009) Biopython: freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics 25, 1422-1423.
| Crossref | Google Scholar | PubMed |
Dederichs TM, Huber BA, Michalik P (2022) Evolutionary morphology of sperm in pholcid spiders (Pholcidae, Synspermiata). BMC Zoology 7, 52.
| Crossref | Google Scholar | PubMed |
Eberle J, Dimitrov D, Valdez-Mondragón A, Huber BA (2018) Microhabitat change drives diversification in pholcid spiders. BMC Evolutionary Biology 18, 141.
| Crossref | Google Scholar | PubMed |
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783-791.
| Crossref | Google Scholar | PubMed |
Gertsch WJ (1982) The spider genera Pholcophora and Anopsicus (Araneae, Pholcidae) in North America, Central America and the West Indies. Texas Memorial Museum, Bulletin 28, 95-144.
| Google Scholar |
Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307-321.
| Crossref | Google Scholar | PubMed |
Hasselt AWM van (1887) Araneae exoticae quas collegit pro Museo Lugdunensi, J. R. H. Neervoort van de Poll, insulis Curaçao, Bonaire et Arubâ. Tijdschrift voor Entomologie 30, 227-244.
| Google Scholar |
Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS (2018) UFBoot2: improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35, 518-522.
| Crossref | Google Scholar | PubMed |
Huber BA (2000) New World pholcid spiders (Araneae: Pholcidae): a revision at generic level. Bulletin of the American Museum of Natural History 254, 1-348.
| Crossref | Google Scholar |
Huber BA (2001) The pholcids of Australia (Araneae; Pholcidae): taxonomy, biogeography, and relationships. Bulletin of the American Museum of Natural History 260, 1-144.
| Crossref | Google Scholar |
Huber BA (2018) Cave-dwelling pholcid spiders (Araneae, Pholcidae): a review. Subterranean Biology 26, 1-18.
| Crossref | Google Scholar |
Huber BA (2022) Revisions of Holocnemus and Crossopriza: the spotted-leg clade of Smeringopinae (Araneae, Pholcidae). European Journal of Taxonomy 795, 1-241.
| Crossref | Google Scholar |
Huber BA, Carvalho LS (2019) Filling the gaps: descriptions of unnamed species included in the latest molecular phylogeny of Pholcidae (Araneae). Zootaxa 4546, 1-96.
| Crossref | Google Scholar | PubMed |
Huber BA, Rheims CA (2011) Diversity and endemism of pholcid spiders in Brazil’s Atlantic Forest, with descriptions of four new species of the Atlantic Forest endemic genus Tupigea (Araneae: Pholcidae). Journal of Natural History 45, 275-301.
| Crossref | Google Scholar |
Huber BA, Villarreal O (2020) On Venezuelan pholcid spiders (Araneae, Pholcidae). European Journal of Taxonomy 718, 1-317.
| Crossref | Google Scholar |
Huber BA, Neumann J, Grabolle A, Hula V (2017) Aliens in Europe: updates on the distributions of Modisimus culicinus and Micropholcus fauroti (Araneae, Pholcidae). Arachnologische Mitteilungen 53, 12-18.
| Crossref | Google Scholar |
Huber BA, Eberle J, Dimitrov D (2018) The phylogeny of pholcid spiders: a critical evaluation of relationships suggested by molecular data (Araneae, Pholcidae). ZooKeys 789, 51-101.
| Crossref | Google Scholar | PubMed |
Huber BA, Meng G, Clark HL, Cazanove G (2023a) First blind daddy long-legs spiders from Australia and Réunion (Araneae, Pholcidae). Subterranean Biology 46, 1-19.
| Crossref | Google Scholar |
Huber BA, Meng G, Král J, Herrera IMA, Izquierdo MA, Carvalho LS (2023b) High and dry: integrative taxonomy of the Andean spider genus Nerudia (Araneae: Pholcidae). Zoological Journal of the Linnean Society 198, 534-591.
| Crossref | Google Scholar |
Huber BA, Meng G, Valdez-Mondragón A, Král J, Ávila Herrera I, Carvalho LS (2023c) Short-legged daddy-long-leg spiders in North America: the genera Pholcophora and Tolteca (Araneae, Pholcidae). European Journal of Taxonomy 880, 1-89.
| Crossref | Google Scholar |
Huber BA, Meng G, Král J, Ávila Herrera IM, Izquierdo MA (2023d) Revision of the South American Ninetinae genus Guaranita (Araneae, Pholcidae). European Journal of Taxonomy 900, 32-80.
| Crossref | Google Scholar |
Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14, 587-589.
| Crossref | Google Scholar | PubMed |
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772-780.
| Crossref | Google Scholar | PubMed |
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111-120.
| Crossref | Google Scholar | PubMed |
Král J (2007) Evolution of multiple sex chromosomes in the spider genus Malthonica (Araneae: Agelenidae) indicates unique structure of the spider sex chromosome systems. Chromosome Research 15, 863-879.
| Crossref | Google Scholar | PubMed |
Král J, Musilová J, Šťáhlavský F, Řezáč M, Akan Z, Edwards RL, Coyle FA, Ribera Almerje C (2006) Evolution of the karyotype and sex chromosome systems in basal clades of araneomorph spiders (Araneae: Araneomorphae). Chromosome Research 14, 859-880.
| Crossref | Google Scholar | PubMed |
Král J, Kořínková T, Forman M, Krkavcová L (2011) Insights into the meiotic behavior and evolution of multiple sex chromosome systems in spiders. Cytogenetic and Genome Research 133, 43-66.
| Crossref | Google Scholar | PubMed |
Král J, Kořínková T, Krkavcová L, Musilová J, Forman M, Ávila Herrera IM, Haddad CR, Vítková M, Henriques S, Vargas JGP, Hedin M (2013) Evolution of karyotype, sex chromosomes, and meiosis in mygalomorph spiders (Araneae: Mygalomorphae). Biological Journal of the Linnean Society 109, 377-408.
| Crossref | Google Scholar |
Král J, Forman M, Kořínková T, Reyes Lerma AC, Haddad CR, Musilová J, Řezáč M, Ávila Herrera IM, Thakur S, Dippenaar-Schoeman AS, Marec F, Horová L, Bureš P (2019) Insights into the karyotype and genome evolution of haplogyne spiders indicate a polyploid origin of lineage with holokinetic chromosomes. Scientific Reports 9, 3001.
| Crossref | Google Scholar | PubMed |
Král J, Ávila Herrera IM, Šťáhlavský F, Sadílek D, Pavelka J, Chatzaki M, Huber BA (2022) Karyotype differentiation and male meiosis in European clades of the spider genus Pholcus (Araneae, Pholcidae). Comparative Cytogenetics 16, 185-209.
| Crossref | Google Scholar | PubMed |
Kulkarni S, Wood HM, Hormiga G (2023) Advances in the reconstruction of the spider tree of life: a roadmap for spider systematics and comparative studies. Cladistics 39, 479-532.
| Crossref | Google Scholar | PubMed |
Letunic I, Bork P (2021) Interactive Tree of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Research 49, W293-W296.
| Crossref | Google Scholar | PubMed |
Levan A, Fredga K, Sandberg AA (1964) Nomenclature for centromeric position on chromosomes. Hereditas 52, 201-220.
| Crossref | Google Scholar |
Lomazi RL, Araujo D, Carvalho LS, Schneider MC (2018) Small pholcids (Araneae: Synspermiata) with big surprises: the lowest diploid number in spiders with monocentric chromosomes. The Journal of Arachnology 46, 45-49.
| Crossref | Google Scholar |
Maddison WP (1982) XXXY sex chromosomes in males of the jumping spider genus Pellenes (Araneae: Salticidae). Chromosoma 85, 23-37.
| Crossref | Google Scholar |
Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, Lanfear R (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution 37, 1530-1534.
| Crossref | Google Scholar | PubMed |
Morrone JJ (2014) Biogeographical regionalization of the Neotropical region. Zootaxa 3782, 1-110.
| Crossref | Google Scholar | PubMed |
Nolasco S, Valdez-Mondragón A (2022) To be or not to be Integrative taxonomy and species delimitation in the daddy long-legs spiders of the genus Physocyclus (Araneae, Pholcidae) using DNA barcoding and morphology. ZooKeys 1135, 93-118.
| Crossref | Google Scholar | PubMed |
Ratnasingham S, Hebert PDN (2007) BOLD: the Barcode of Life Data System (http://www.barcodinglife.org). Molecular Ecology Notes 7, 355-364.
| Crossref | Google Scholar | PubMed |
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406-425.
| Crossref | Google Scholar | PubMed |
Sember A, Pappová M, Forman M, Nguyen P, Marec F, Dalíková M, Divišová K, Doležálková-Kaštánková M, Zrzavá M, Sadílek D, Hrubá B, Král J (2020) Patterns of sex chromosome differentiation in spiders: Insights from comparative genomic hybridisation. Genes 11, 849.
| Crossref | Google Scholar | PubMed |
Suyama M, Torrents D, Bork P (2006) PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Research 34, W609-W612.
| Crossref | Google Scholar | PubMed |
Tamura K, Stecher G, Kumar S (2021) MEGA 11: molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution 38, 3022-3027.
| Crossref | Google Scholar | PubMed |
Valdez-Mondragón A (2020) COI mtDNA barcoding and morphology for species delimitation in the spider genus Ixchela Huber (Araneae: Pholcidae), with description of two new species from Mexico. Zootaxa 4747, 54-76.
| Crossref | Google Scholar | PubMed |
van Buurt G (2010) A short natural history of Curaçao. In ‘Crossing shifting boundaries, language and changing political status in Aruba, Bonaire and Curaçao’, 4–8 November 2009, Roseau, Dominica. (Eds N Faraclas, R Severing, C Weijer, E Echteld) Proceedings of the ECICC-conference, Vol. 1, pp. 229–256. (Fundashon pa Planifikashon di Idioma and University of the Netherlands Antilles: Willemstad, Curaçao)
Yang C, Zheng Y, Tan S, Meng G, et al. (2020) Efficient COI barcoding using high throughput single-end 400bp sequencing. BMC Genomics 21, 862.
| Crossref | Google Scholar | PubMed |