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Systematics, phylogeny and biogeography
RESEARCH ARTICLE

A multi-layered approach uncovers overlooked taxonomic and physiological diversity in Alpine subterranean spiders (Araneae: Linyphiidae: Troglohyphantes)

Marco Isaia https://orcid.org/0000-0001-5434-2127 A * , Miquel A. Arnedo https://orcid.org/0000-0003-1402-4727 B and Stefano Mammola https://orcid.org/0000-0002-4471-9055 C D
+ Author Affiliations
- Author Affiliations

A Department of Life Science and Systems Biology, University of Turin, Turin, Italy.

B Department of Evolutionary Biology, Ecology and Environmental Sciences, and Biodiversity Research Institute (IRBio), Universitat de Barcelona, Barcelona, Spain.

C Laboratory for Integrative Biodiversity Research (LIBRe), Finnish Museum of Natural History (LUOMUS), University of Helsinki, Helsinki, Finland.

D Molecular Ecology Group (MEG), IRSA Water Research Institute, National Research Council, Verbania Pallanza, Italy.

* Correspondence to: marco.isaia@unito.it

Handling Editor: Prashant Sharma

Invertebrate Systematics 36(4) 354-371 https://doi.org/10.1071/IS21054
Submitted: 23 July 2021  Accepted: 18 November 2021   Published: 5 May 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing.

Abstract

The integration of multiple lines of evidence in the delimitation of taxa is becoming the gold standard in modern taxonomy and systematics. However, multi-layered taxonomy is still incipient when it comes to species description within a mega-diverse group of organisms (e.g. arthropods), especially those inhabiting secluded environments such as caves. This may represent a significant shortcoming, because species in subterranean habitats generally show deep convergence in their somatic traits, perplexing our ability to delimit species by traditional approaches. The genus Troglohyphantes Joseph, 1882 (Araneae: Linyphiidae) is presently known to include 129 species and 5 subspecies, all of which are primarily distributed in subterranean habitats of the European mountain ranges. Recent studies on Italian alpine species covered taxonomy and faunistic, biogeography and ecology. However, our knowledge about the actual species diversity of Troglohyphantes spiders is far from complete, and it is expected that significant levels of overlooked diversity might exist within the genus. In this work, we combined morphological data with target gene molecular data, functional trait analysis and thermal physiology to explore overlooked diversity in Troglohyphantes vignai auct., a species of subterranean spider in the Western Italian Alps with an apparently broader distribution than its congeners. Our approach proved effective in uncovering overlooked diversity and further supporting the split of T. vignai auct. into three distinct species whose distribution ranges how striking resemblances with that of other subterranean spiders. We here describe the new species and discuss their origins in light of their geographical vicariance, niche convergence, thermal ecology and divergence time.

Keywords: cave dwelling spiders, cryptic diversity, endemic species, functional traits, geographical vicariance, morphology, niche convergence, phylogeny, speciation, thermal ecology.


References

Arnò C, Lana E (2005) ‘Ragni cavernicoli del Piemonte e della Valle d’Aosta.’ (Associazione Gruppi Speleologici Piemontesi, Ed. “La Grafica Nuova”: Torino, Italy)

Badino, G (2010). Underground meteorology. What’s the weather underground? Acta Carsologica 39, 427–448.
Underground meteorology. What’s the weather underground?Crossref | GoogleScholarGoogle Scholar |

Bickford, D, Lohman, DJ, Sodhi, NS, Ng, PK, Meier, R, Winker, K, Ingram, KK, and Das, I (2007). Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution 22, 148–155.
Cryptic species as a window on diversity and conservation.Crossref | GoogleScholarGoogle Scholar |

Bidegaray-Batista, L, and Arnedo, MA (2011). Gone with the plate: the opening of the Western Mediterranean basin drove the diversification of ground-dweller spiders. BMC Evolutionary Biology 11, 317.
Gone with the plate: the opening of the Western Mediterranean basin drove the diversification of ground-dweller spiders.Crossref | GoogleScholarGoogle Scholar | 22039781PubMed |

Blair, C, and Bryson, RW Jr (2017). Cryptic diversity and discordance in single-locus species delimitation methods within horned lizards (Phrynosomatidae: Phrynosoma). Molecolus Ecology Resources 17, 1168–1182.
Cryptic diversity and discordance in single-locus species delimitation methods within horned lizards (Phrynosomatidae: Phrynosoma).Crossref | GoogleScholarGoogle Scholar |

Blonder, B, Lamanna, C, Violle, C, and Enquist, BJ (2014). The n-dimensional hypervolume. Global Ecology and Biogeography 23, 595–609.
The n-dimensional hypervolume.Crossref | GoogleScholarGoogle Scholar |

Blonder, B, Morrow, CB, Maitner, B, Harris, DJ, Lamanna, C, Violle, C, Enquist, BJ, and Kerkhoff, AJ (2018). New approaches for delineating n-dimensional hypervolumes. Methods in Ecology and Evolution 9, 305–319.
New approaches for delineating n-dimensional hypervolumes.Crossref | GoogleScholarGoogle Scholar |

Bologna MA, Vigna Taglianti A (1982) Il popolamento cavernicolo delle Alpi Occidentali. In ‘Biogeografia delle caverne italiane – Atti del XXII Congresso nazionale della Società Italiana di Biospeleologia.’ pp. 515–544. (Società Italiana di Biogeografia)

Bologna, MA, and Vigna Taglianti, A (1985). Fauna cavernicola delle Alpi Liguri. Annali del Museo Civico di Storia Naturale Giacomo Doria 84, 1–389.

Brignoli, PM (1971). Note sui ragni cavernicoli italiani. Fragmenta Entomologica 7, 121–229.

Brignoli, PM (1972). Catalogo dei ragni cavernicoli italiani. Quaderni di Speleologia del Circolo Speleologico Romano 1, 5–212.

Brignoli, PM (1975). Ragni d’Italia XXV. Su alcuni ragni cavernicoli d’Italia settentrionale. Notiziario del Circolo Speleologico Romano 20, 1–35.

Brignoli, PM (1979). Sur quelques araignées cavernicoles des Alpes Maritimes françaises et italiennes (Araneae). Bulletin de la Société d’Histoire Naturelle de Toulouse 115, 316–322.

Casale, A (1971). Note biologiche. I ragni delle grotte piemontesi. Grotte, Bollettino del Gruppo Speleologico Piemontese GSP CAI-UGET 46, 14–16.

Casale, A (1986). Ricerche biospeleologiche 1986. Grotte, Bollettino del Gruppo Speleologico Piemontese, GSP CAI-UGET 92, 52–55.

Casale, A, and Longhetto, A (1970). Note biologiche. Grotte, Bollettino del Gruppo Speleologico Piemontese. GSP CAI-UGET 42, 14–16.

Casale, A, Giachino, PM, and Lana, E (2000). Attività biospeleologica 1999. Grotte, Bollettino del Gruppo Speleologico Piemontese, GSP CAI-UGET 132, 38–44.

Christiansen KA (2012) Morphological adaptations. In ‘Encyclopedia of Caves’. (Eds WB White, DC Culver) (Elsevier: New York, NY, USA)

Clement, M, Posada, DCKA, and Crandall, KA (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.
TCS: a computer program to estimate gene genealogies.Crossref | GoogleScholarGoogle Scholar | 11050560PubMed |

Colado, R, Pallares, S, Fresneda, J, Mammola, S, Rizzo, V, and Sánchez-Fernandez, D (2022). Climatic stability, not average habitat temperature, determines thermal tolerance of subterranean beetles. Ecology 103, 1–11.
Climatic stability, not average habitat temperature, determines thermal tolerance of subterranean beetles.Crossref | GoogleScholarGoogle Scholar |

Dayrat, B (2005). Towards integrative taxonomy. Biological Journal of the Linnean Society. Linnean Society of London 85, 407–415.
Towards integrative taxonomy.Crossref | GoogleScholarGoogle Scholar |

de Queiroz, K (2005). A unified concept of species and its consequences for the future of taxonomy. Proceedings of the California Academy of Sciences 56, 196–215.

Deeleman-Reinhold, CL (1978). Revision of the cave-dwelling and related spiders of the genus Troglohyphantes Joseph (Linyphiidae), with special reference to the Yugoslav species. Opera Academia Scientiarum et Artium Slovenica 23, 1–221.

Delić, T, Trontelj, P, Rendoš, M, and Fišer, C (2017). The importance of naming cryptic species and the conservation of endemic subterranean amphipods. Scientific Reports 7, 3391.
The importance of naming cryptic species and the conservation of endemic subterranean amphipods.Crossref | GoogleScholarGoogle Scholar | 28611400PubMed |

Denis, J (1949). Notes sur les érigonides. XVI. Essai sur la détermination des femelles d’érigonides. Bulletin de la Société d’Histoire Naturelle de Toulouse 83, 129–158.

Drummond, AJ, Suchard, MA, 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 | GoogleScholarGoogle Scholar | 22367748PubMed |

Eme, D, Zagmajster, M, Delić, T, Fišer, C, Flot, JF, Konecny‐Dupré, L, Pálsson, S, Stoch, F, Zakšek, V, Douady, CJ, and Malard, F (2018). Do cryptic species matter in macroecology? Sequencing European groundwater crustaceans yields smaller ranges but does not challenge biodiversity determinants. Ecography 41, 424–436.
Do cryptic species matter in macroecology? Sequencing European groundwater crustaceans yields smaller ranges but does not challenge biodiversity determinants.Crossref | GoogleScholarGoogle Scholar |

Esposito, LA, Bloom, T, Caicedo-Quiroga, L, Alicea-Serrano, AM, Sánchez-Ruíz, JA, May-Collado, LJ, Binford, GJ, and Agnarsson, I (2015). Islands within islands: diversification of tailless whip spiders (Amblypygi, Phrynus) in Caribbean caves. Molecular Phylogenetics and Evolution 93, 107–117.
Islands within islands: diversification of tailless whip spiders (Amblypygi, Phrynus) in Caribbean caves.Crossref | GoogleScholarGoogle Scholar | 26220837PubMed |

Fišer, C, Robinson, CT, and Malard, F (2018). Cryptic species as a window into the paradigm shift of the species concept. Molecular Ecology 27, 613–635.
Cryptic species as a window into the paradigm shift of the species concept.Crossref | GoogleScholarGoogle Scholar | 29334414PubMed |

Fujisawa, T, and Barraclough, TG (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, 707–724.
Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets.Crossref | GoogleScholarGoogle Scholar | 23681854PubMed |

Gruppo Speleologico Alpi Marittime (1987). ‘Grotte, Barme ed Abissi.’ (C.A.I. Cuneo, G.S.A.M., Cuneo, Ed. Manzone)

Harvey, MS (2002). Short-range endemism amongst the Australian fauna: some examples from non-marine environments. Invertebrate Systematics 16, 555–570.
Short-range endemism amongst the Australian fauna: some examples from non-marine environments.Crossref | GoogleScholarGoogle Scholar |

Hebert, PD, Cywinska, A, Ball, SL, and deWaard, JR (2003). Biological identifications through DNA barcodes. Proceedings. Biological Sciences 270, 313–321.
Biological identifications through DNA barcodes.Crossref | GoogleScholarGoogle Scholar | 12614582PubMed |

Hebert, PD, Penton, EH, Burns, JM, Janzen, DH, and 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, 14812–14817.
Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator.Crossref | GoogleScholarGoogle Scholar | 15465915PubMed |

Hedin, M (2015). High-stakes species delimitation in eyeless cave spiders (Cicurina, Dictynidae, Araneae) from central Texas. Molecular Ecology 24, 346–361.
High-stakes species delimitation in eyeless cave spiders (Cicurina, Dictynidae, Araneae) from central Texas.Crossref | GoogleScholarGoogle Scholar | 25492722PubMed |

Isaia, M, and Pantini, P (2007). A new species of Troglohyphantes (Araneae, Linyphiidae) from the western Italian Alps. The Journal of Arachnology 35, 427–431.
A new species of Troglohyphantes (Araneae, Linyphiidae) from the western Italian Alps.Crossref | GoogleScholarGoogle Scholar |

Isaia, M, and Pantini, P (2010). New data on the spider genus Troglohyphantes (Araneae, Linyphiidae) in the Italian Alps, with the description of a new species and a new synonymy. Zootaxa 2690, 1–18.
New data on the spider genus Troglohyphantes (Araneae, Linyphiidae) in the Italian Alps, with the description of a new species and a new synonymy.Crossref | GoogleScholarGoogle Scholar |

Isaia, M, Pantini, P, Beikes, S, and Badino, G (2007). Catalogo ragionato dei ragni (Arachnida, Araneae) del Piemonte e della Lombardia. Memorie dell’Associazione Naturalistica Piemontese 9, 1–161.

Isaia M, Lana E, Pantini P (2010) Ecology and distribution of the genus Troglohyphantes Joseph, 1882 in the Western Italian Alps. In ‘European Arachnology 2008’. (Eds W Nentwig, M Schmidt-Entling, C Kropf) pp. 89–97. (Natural History Museum Bern: Bern, Switzerland)

Isaia M, Paschetta M, Lana E, Pantini P, Schönhofer AL, Christian E, Badino G (2011a) ‘Subterranean Arachnids of the Western Italian Alps (Arachnida: Araneae, Opiliones, Palpigradi, Pseudoscorpiones).’ Monografie XLVII. (Museo Regionale di Scienze Naturali: Torino, Italy)

Isaia, M, Giachino, PM, Sapino, E, Casale, A, and Badino, G (2011b). Conservation value of artificial subterranean systems: a case study in an abandoned mine in Italy. Journal for Nature Conservation 19, 24–33.
Conservation value of artificial subterranean systems: a case study in an abandoned mine in Italy.Crossref | GoogleScholarGoogle Scholar |

Isaia, M, Mammola, S, Mazzuca, P, Arnedo, MA, and Pantini, P (2017). Advances in the systematics of the spider genus Troglohyphantes (Araneae, Linyphiidae). Systematics and Biodiversity 15, 307–326.
Advances in the systematics of the spider genus Troglohyphantes (Araneae, Linyphiidae).Crossref | GoogleScholarGoogle Scholar |

Janzen, DH, Burns, JM, Cong, Q, Hallwachs, W, Dapkey, T, Manjunath, R, Hajibabaei, M, Hebert, PDN, and Grishin, NV (2017). Nuclear genomes distinguish cryptic species suggested by their DNA barcodes and ecology. Proceedings of the National Academy of Sciences of the United States of America 114, 8313–8318.
Nuclear genomes distinguish cryptic species suggested by their DNA barcodes and ecology.Crossref | GoogleScholarGoogle Scholar | 28716927PubMed |

Jones, KK, Humphreys, WF, Saccò, M, Bertozzi, T, Austin, AD, and Cooper, SJ (2021). The critical thermal maximum of diving beetles (Coleoptera: Dytiscidae): a comparison of subterranean and surface-dwelling species. Current Research in Insect Science 1, 100019.
The critical thermal maximum of diving beetles (Coleoptera: Dytiscidae): a comparison of subterranean and surface-dwelling species.Crossref | GoogleScholarGoogle Scholar |

Kalyaanamoorthy, S, Minh, BQ, Wong, TKF, von Haeseler, A, and Jermiin, LS (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 |

Kapli, P, Lutteropp, S, Zhang, J, Kobert, K, Pavlidis, P, Stamatakis, A, and Flouri, T (2017). Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics 33, 1630–1638.
Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo.Crossref | GoogleScholarGoogle Scholar | 28108445PubMed |

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 |

Kumar , S, Stecher , G, Li , M, Knyaz , C, and Tamura , K (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547–1549.
MEGA X: molecular evolutionary genetics analysis across computing platforms.Crossref | GoogleScholarGoogle Scholar | 29722887PubMed |

Lana E (2001) ‘Biospeleologia del Piemonte. Atlante fotografico sistematico.’ (A.G.S.P., Regione Piemonte, Ed. La grafica nuova: Torino, Italy)

Lana, E, Casale, A, and Giachino, PM (2002). Attività biospeleologica 2001. Grotte, Bollettino del Gruppo Speleologico Piemontese, GSP CAI-UGET 137, 35–39.

Lanfear, R, Frandsen, PB, Wright, AM, 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.
| 28013191PubMed |

Leaché, AD, Davis, HR, Singhal, S, Fujita, MK, Lahti, ME, and Zamudio, KR (2021). Phylogenomic assessment of biodiversity using a reference-based taxonomy: an example with horned lizards (Phrynosoma). Frontiers in Ecology and Evolution 9, 678110.
Phylogenomic assessment of biodiversity using a reference-based taxonomy: an example with horned lizards (Phrynosoma).Crossref | GoogleScholarGoogle Scholar |

Löytynoja, A, and Goldman, N (2010). webPRANK: a phylogeny-aware multiple sequence aligner with interactive alignment browser. BMC Bioinformatics 11, 579.
webPRANK: a phylogeny-aware multiple sequence aligner with interactive alignment browser.Crossref | GoogleScholarGoogle Scholar | 21110866PubMed |

Mammola, S (2019). Assessing similarity of n-dimensional hypervolumes: which metric to use? Journal of Biogeography 46, 2012–2023.
Assessing similarity of n-dimensional hypervolumes: which metric to use?Crossref | GoogleScholarGoogle Scholar |

Mammola, S, and Isaia, M (2016). The ecological niche of a specialized subterranean spider. Invertebrate Biology 135, 20–30.
The ecological niche of a specialized subterranean spider.Crossref | GoogleScholarGoogle Scholar |

Mammola, S, and Isaia, M (2017). Spiders in caves. Proceedings of the Royal Society of London – B. Biological Sciences 284, 20170193.
Spiders in caves.Crossref | GoogleScholarGoogle Scholar |

Mammola, S, and Cardoso, P (2020). Functional diversity metrics using kernel density n-dimensional hypervolumes. Methods in Ecology and Evolution 11, 986–995.
Functional diversity metrics using kernel density n-dimensional hypervolumes.Crossref | GoogleScholarGoogle Scholar |

Mammola, S, Isaia, M, and Arnedo, MA (2015). Alpine endemic spiders shed light on the origin and evolution of subterranean species. PeerJ 3, e1384.
Alpine endemic spiders shed light on the origin and evolution of subterranean species.Crossref | GoogleScholarGoogle Scholar | 26734503PubMed |

Mammola, S, Hormiga, G, Arnedo, MA, and Isaia, M (2016). Unexpected diversity in the relictual European spiders of the genus Pimoa (Araneae: Pimoidae). Invertebrate Systematics 30, 566–587.
Unexpected diversity in the relictual European spiders of the genus Pimoa (Araneae: Pimoidae).Crossref | GoogleScholarGoogle Scholar |

Mammola, S, Hormiga, G, and Isaia, M (2017). Species conservation profile of the stenoendemic cave spider Pimoa delphinica (Araneae, Pimoidae) from the Varaita valley (NW-Italy). Biodiversity Data Journal 5, e11509.
Species conservation profile of the stenoendemic cave spider Pimoa delphinica (Araneae, Pimoidae) from the Varaita valley (NW-Italy).Crossref | GoogleScholarGoogle Scholar |

Mammola, S, Goodacre, SL, and Isaia, M (2018a). Climate change may drive cave spiders to extinction. Ecography 41, 233–243.
Climate change may drive cave spiders to extinction.Crossref | GoogleScholarGoogle Scholar |

Mammola, S, Arnedo, MA, Pantini, P, Piano, E, Chiappetta, N, and Isaia, M (2018b). Ecological speciation in darkness? Spatial niche partitioning in sibling subterranean spiders (Araneae: Linyphiidae: Troglohyphantes). Invertebrate Systematics 32, 1069–1082.
Ecological speciation in darkness? Spatial niche partitioning in sibling subterranean spiders (Araneae: Linyphiidae: Troglohyphantes).Crossref | GoogleScholarGoogle Scholar |

Mammola, S, Piano, E, Malard, F, Vernon, P, and Isaia, M (2019). Extending Janzen’s hypothesis to temperate regions: a test using subterranean ecosystems. Functional Ecology 33, 1638–1650.
Extending Janzen’s hypothesis to temperate regions: a test using subterranean ecosystems.Crossref | GoogleScholarGoogle Scholar |

Mammola, S, Arnedo, MA, Fišer, C, Cardoso, P, Dejanaz, AJ, and Isaia, M (2020). Environmental filtering and convergent evolution determine the ecological specialization of subterranean spiders. Functional Ecology 34, 1064–1077.
Environmental filtering and convergent evolution determine the ecological specialization of subterranean spiders.Crossref | GoogleScholarGoogle Scholar |

Marazzi S (2005) ‘Atlante orografico delle Alpi. SOIUSA. Suddivisione orografica internazionale unificata del Sistema Alpino.’ (Priuli and Verlucca: Scarmagno, Italy)

Monaghan, MT, Wild, R, Elliot, M, Fujisawa, T, Balke, M, Inward, DJG, Lees, DC, Ranaivosolo, R, Eggleton, P, Barraclough, TG, and Vogler, AP (2009). Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Systematic Biology 58, 298–311.
Accelerated species inventory on Madagascar using coalescent-based models of species delineation.Crossref | GoogleScholarGoogle Scholar | 20525585PubMed |

Morisi, A (1971). Nuovi animali cavernicoli recentemente descritti. Mondo Ipogeo 7, 48–51.

Nguyen, LT, Schmidt, HA, von Haeseler, A, and Minh, BQ (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 |

Niemiller, ML, Near, TJ, and Fitzpatrick, BM (2012). Delimiting species using multilocus data: diagnosing cryptic diversity in the southern cavefish, Typhlichthys subterraneus (Teleostei: Amblyopsidae). Evolution 66, 846–866.
Delimiting species using multilocus data: diagnosing cryptic diversity in the southern cavefish, Typhlichthys subterraneus (Teleostei: Amblyopsidae).Crossref | GoogleScholarGoogle Scholar | 22380444PubMed |

Pallarés, S, Colado, R, Pérez‐Fernández, T, Wesener, T, Ribera, I, and Sánchez‐Fernández, D (2019). Heat tolerance and acclimation capacity in subterranean arthropods living under common and stable thermal conditions. Ecology and Evolution 9, 13731.
Heat tolerance and acclimation capacity in subterranean arthropods living under common and stable thermal conditions.Crossref | GoogleScholarGoogle Scholar | 31938477PubMed |

Pallarés, S, Sanchez-Hernandez, JC, Colado, R, Balart-García, P, Comas, J, and Sánchez-Fernández, D (2020). Beyond survival experiments: using biomarkers of oxidative stress and neurotoxicity to assess vulnerability of subterranean fauna to climate change. Conservation Physiology 8, coaa067.
Beyond survival experiments: using biomarkers of oxidative stress and neurotoxicity to assess vulnerability of subterranean fauna to climate change.Crossref | GoogleScholarGoogle Scholar | 34504711PubMed |

Pallarés, S, Colado, R, Botella‐Cruz, M, Montes, A, Balart‐García, P, Bilton, DT, Millan, A, Ribera, I, and Sánchez‐Fernández, D (2021). Loss of heat acclimation capacity could leave subterranean specialists highly sensitive to climate change. Animal Conservation 24, 482–490.
Loss of heat acclimation capacity could leave subterranean specialists highly sensitive to climate change.Crossref | GoogleScholarGoogle Scholar |

Pekár, S, Wolff, JO, Černecká, Ľ, Birkhofer, K, Mammola, S, Lowe, EC, Fukushima, CS, Herberstein, ME, Kučera, A, Buzatto, BA, Djoudi, EA, Domenech, M, Enciso, AV, Piñanez Espejo, YMG, Febles, S, García, LF, Gonçalves-Souza, T, Isaia, M, Lafage, D, Líznarová, E, Macías-Hernández, N, Magalhães, I, Malumbres-Olarte, J, Michálek, O, Michalik, P, Michalko, R, Milano, F, Munévar, A, Nentwig, W, Nicolosi, G, Painting, CJ, Pétillon, J, Piano, E, Privet, K, Ramírez, MJ, Ramos, C, Řezáč, M, Ridel, A, Růžička, V, Santos, I, Sentenská, L, Walker, L, Wierucka, K, Zurita, GA, and Cardoso, P (2021). The World Spider Trait database (WST): a centralised global open repository for curated data on spider traits. Database (Oxford) 2021, baab064.
The World Spider Trait database (WST): a centralised global open repository for curated data on spider traits.Crossref | GoogleScholarGoogle Scholar | 34651181PubMed |

Pesarini, C (1988). Osservazioni su alcuni Troglohyphantes della fauna Italiana, con descrizione di due nuove specie (Araneae Linyphiidae). Atti della Società Italiana di Scienze Naturali e del Museo Civico di Storia Naturale di Milano 129, 237–247.

Pesarini, C (2001). Note sui Troglophyphantes italiani, con descrizione di quattro nuove specie (Araneae Linyphiidae). Atti della Società Italiana di Scienze Naturali e del Museo Civico di Storia Naturale di Milano 142, 109–133.

Rambaut, A, Drummond, AJ, Xie, D, Baele, G, and Suchard, MA (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67, 901–904.
Posterior summarization in Bayesian phylogenetics using Tracer 1.7.Crossref | GoogleScholarGoogle Scholar | 29718447PubMed |

Raschmanová, N, Šustr, V, Kováč, Ľ, Parimuchová, A, and Devetter, M (2018). Testing the climatic variability hypothesis in edaphic and subterranean Collembola (Hexapoda). Journal of Thermal Biology 78, 391–400.
Testing the climatic variability hypothesis in edaphic and subterranean Collembola (Hexapoda).Crossref | GoogleScholarGoogle Scholar | 30509663PubMed |

Rubel, F, Brugger, K, Haslinger, K, and Auer, I (2017). The climate of the European Alps: shift of very high resolution Köppen–Geiger climate zones 1800–2100. Meteorologische Zeitschrift 26, 115–125.
The climate of the European Alps: shift of very high resolution Köppen–Geiger climate zones 1800–2100.Crossref | GoogleScholarGoogle Scholar |

Ryder, OA (1986). Species conservation and systematics: the dilemma of subspecies. Trends in Ecology & Evolution 1, 9–10.
Species conservation and systematics: the dilemma of subspecies.Crossref | GoogleScholarGoogle Scholar |

Sánchez-Fernández, D, Rizzo, V, Bourdeau, C, Cieslak, A, Comas, J, Faille, A, Fresneda, J, Lleopart, E, Millán, A, Montes, A, Pallares, S, and Ribera, I (2018). The deep subterranean environment as a potential model system in ecological, biogeographical and evolutionary research. Subterranean Biology 25, 1–7.
The deep subterranean environment as a potential model system in ecological, biogeographical and evolutionary research.Crossref | GoogleScholarGoogle Scholar |

Schlick-Steiner, BC, Steiner, FM, Seifert, B, Stauffer, C, Christian, E, and Crozier, RH (2010). Integrative taxonomy: a multisource approach to exploring biodiversity. Annual Review of Entomology 55, 421–438.
Integrative taxonomy: a multisource approach to exploring biodiversity.Crossref | GoogleScholarGoogle Scholar | 19737081PubMed |

Simmons, MP, and Ochoterena, H (2000). Gaps as characters in sequence-based phylogenetic analyses. Systematic Biology 49, 369–381.
Gaps as characters in sequence-based phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar | 12118412PubMed |

Templeton, AR, Crandall, KA, and Sing, CF (1992). A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132, 619–633.
A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation.Crossref | GoogleScholarGoogle Scholar | 1385266PubMed |

Vigna Taglianti, A, and Follis, G (1968). Due nuove grotte del cuneese e la loro fauna. Notiziario del Circolo Speleologico Romano 17, 13–21.