Ecological speciation in darkness? Spatial niche partitioning in sibling subterranean spiders (Araneae : Linyphiidae : Troglohyphantes)
Stefano Mammola A , Miquel A. Arnedo B , Paolo Pantini C , Elena Piano A , Nicolò Chiappetta A and Marco Isaia A DA Department of Life Sciences and Systems Biology, University of Turin, Turin, Italy.
B Department of Evolutionary Biology, Ecology and Environmental Sciences & Biodiversity Research Institute, University of Barcelona, Barcelona, Spain.
C Museo civico di Scienze Naturali ‘E. Caffi’, Bergamo, Italy.
D Corresponding author. Email: marco.isaia@unito.it
Invertebrate Systematics 32(5) 1069-1082 https://doi.org/10.1071/IS17090
Submitted: 30 November 2017 Accepted: 14 March 2018 Published: 4 October 2018
Abstract
Speciation in subterranean habitats is commonly explained as the result of divergent selection in geographically isolated populations; conversely, the contribution of niche partitioning in driving subterranean species diversification has been rarely quantified. The present study integrated molecular and morphological data with a hypervolume analysis based on functional traits to investigate a potential case of parapatric speciation by means of niche differentiation in two sibling spiders inhabiting contiguous subterranean habitats within a small alpine hypogean site. Troglohyphantes giachinoi, sp. nov. and T. bornensis are diagnosed by small details of the genitalia, which are likely to be involved in a reproductive barrier. Molecular analysis recovered the two species as sister, and revealed a deep genetic divergence that may trace back to the Messinian (~6 million years ago). The hypervolume analysis highlighted a marginal overlap in their ecological niches, coupled with morphological character displacement. Specifically, T. giachinoi, sp. nov. exhibits morphological traits suitable for thriving in the smaller pores of the superficial network of underground fissures (Milieu Souterrain Superficiel, MSS), whereas T. bornensis shows a greater adaptation to the deep subterranean habitat. Our results suggest that different selective regimes within the subterranean environment, i.e. deep caves v. MSS, may either drive local speciation or facilitate contiguous distributions of independently subterranean adapted species.
References
Amarasekare, P. (2003). Competitive coexistence in spatially structured environments: a synthesis. Ecology Letters 6, 1109–1122.| Competitive coexistence in spatially structured environments: a synthesis.Crossref | GoogleScholarGoogle Scholar |
Arcangeli, A. (1940). Il genere Alpioniscus Racov (Triconiscidi, Isopodi terrestri). Bollettino del Museo di Zoologia e Anatomia Comparata di Torino 48, 17–30.
Arnedo, M. A., Oromi, P., Múrria, C., Macías-Hernández, N., and Ribera, C. (2007). The dark side of an island radiation: systematics and evolution of troglobitic spiders of the genus Dysdera Latreille (Araneae: Dysderidae) in the Canary Islands. Invertebrate Systematics 21, 623–660.
| The dark side of an island radiation: systematics and evolution of troglobitic spiders of the genus Dysdera Latreille (Araneae: Dysderidae) in the Canary Islands.Crossref | GoogleScholarGoogle Scholar |
Arnedo, M. A., Hormiga, G., and Scharff, N. (2009). Higher-level phylogenetics of linyphiid spiders (Araneae, Linyphiidae) based on morphological and molecular evidence. Cladistics 25, 231–262.
| Higher-level phylogenetics of linyphiid spiders (Araneae, Linyphiidae) based on morphological and molecular evidence.Crossref | GoogleScholarGoogle Scholar |
Arnò, C., and Lana, E. (2005). ‘Ragni cavernicoli del Piemonte e della Valle d’Aosta.’ (La Grafica Nuova: Turin, Italy.)
Barluenga, M., Stölting, K. N., Salzburger, W., Muschick, M., and Meyer, A. (2006). Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439, 719–723.
| Sympatric speciation in Nicaraguan crater lake cichlid fish.Crossref | GoogleScholarGoogle Scholar |
Barr, T. C., and Holsinger, J. R. (1985). Speciation in cave faunas. Annual Review of Ecology and Systematics 16, 313–337.
| Speciation in cave faunas.Crossref | GoogleScholarGoogle Scholar |
Benjamin, S. P., and Zschokke, S. (2004). Homology, behaviour and spider webs: web construction behaviour of Linyphia hortensis and Linyphia triangularis (Araneae: Linyphiidae) and its evolutionary significance. Journal of Evolutionary Biology 17, 120–130.
| Homology, behaviour and spider webs: web construction behaviour of Linyphia hortensis and Linyphia triangularis (Araneae: Linyphiidae) and its evolutionary significance.Crossref | GoogleScholarGoogle Scholar |
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 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 |
Blonder, B. (2015). ‘Hypervolume: High-dimensional Kernel Density Estimation and Geometry Operations. R package version 1.2.2.’ Available at http://CRAN.R-project.org/ package1/4hypervolume.
Blonder B. 2017
Blonder, B., Lamanna, C., Violle, C., and Enquist, B. J. (2014). The n-dimensional hyper-volume. Global Ecology and Biogeography 23, 595–609.
| The n-dimensional hyper-volume.Crossref | GoogleScholarGoogle Scholar |
Bolnick, D. I., and Fitzpatrick, B. M. (2007). Sympatric speciation: models and empirical evidence. Annual Review of Ecology Evolution and Systematics 38, 459–487.
| Sympatric speciation: models and empirical evidence.Crossref | GoogleScholarGoogle Scholar |
Caccone, A. (1985). Gene flow in cave arthropods: a qualitative and quantitative approach. Evolution 39, 1223–1235.
| Gene flow in cave arthropods: a qualitative and quantitative approach.Crossref | GoogleScholarGoogle Scholar |
Capra, F. (1924). Sulla fauna della Grotta del Pugnetto in Val di Lanzo. Atti della Reale Accademia della Scienze di Torino 59, 153–161.
Capra, F., and Conci, C. (1951). Nota sulle grotte del Pugnetto in val di Lanzo e sulla loro fauna (Piemonte). Rassegna Speleologica Italiana 3, 73–76.
Cardoso, P. (2012). Diversity and community assembly patterns of epigean vs. troglobiont spiders in the Iberian Peninsula. International Journal of Speleology 41, 83–94.
| Diversity and community assembly patterns of epigean vs. troglobiont spiders in the Iberian Peninsula.Crossref | GoogleScholarGoogle Scholar |
Casale, A. (1980). Trechini e Bathysciinae nuovi o poco noti delle Alpi Occidentali, e note sinonimiche (Coleoptera, Carabidae e Catopidae). Fragmenta Entomologica 15, 305–306.
Casale, A., Giachino, P. M., and Lana, E. (1997). Attività biospeleologica 1996. Grotte Bollettino del Gruppo Speleologico Piemontese 123, 48–50.
Christiansen, K. A. (2012). Morphological adaptations. In ‘Encyclopedia of Caves’. (Eds W. B. White and D. C. Culver.) (Elsevier: New York.)
Christman, M. C., Culver, D. C., Madden, M. K., and White, D. (2005). Patterns of endemism of the eastern North American cave fauna. Journal of Biogeography 32, 1441–1452.
| Patterns of endemism of the eastern North American cave fauna.Crossref | GoogleScholarGoogle Scholar |
Cokendolpher, J. C. (2004). Cicurina spiders from caves in Bexar County, Texas (Araneae: Dictynidae). Texas Memorial Museum Speleological Monographs 6, 13–58.
Cooper, S. J. B., Hinze, S., Leys, R., Watts, C. H. S., and Humphreys, W. F. (2002). Islands under the desert: molecular systematics and evolutionary origins of stygobitic water beetles (Coleoptera: Dytiscidae) from central Western Australia. Invertebrate Systematics 16, 589–598.
| Islands under the desert: molecular systematics and evolutionary origins of stygobitic water beetles (Coleoptera: Dytiscidae) from central Western Australia.Crossref | GoogleScholarGoogle Scholar |
Coyne, J. A., and Orr, H. A. (2004). ‘Speciation.’ (Sinauer: Sunderland, MA.)
Culver, D. C. (1970a). Analysis of simple cave communities I: caves as islands. Evolution 24, 463–474.
| Analysis of simple cave communities I: caves as islands.Crossref | GoogleScholarGoogle Scholar |
Culver, D. C. (1970b). Analysis of simple cave communities: niche separation and species packing. Ecology 51, 949–958.
| Analysis of simple cave communities: niche separation and species packing.Crossref | GoogleScholarGoogle Scholar |
Culver, D. C. (1971). Caves as archipelagoes. National Speleological Society 33, 97–100.
Culver, D. C., and Pipan, T. (2014). ‘Shallow Subterranean Habitats. Ecology, Evolution and Conservation.’ (Oxford University Press: Oxford, MS.)
Culver, D. C., and Pipan, T. (2016). Shifting paradigms of the evolution of cave life. Acta Carsologica 44, 415–425.
| Shifting paradigms of the evolution of cave life.Crossref | GoogleScholarGoogle Scholar |
Deeleman-Reinhold, C. L. (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.
Drummond, A. J., Suchard, M. A., 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 |
Esposito, L. A., Bloom, T., Caicedo-Quiroga, L., Alicea-Serrano, A. M., Sánchez-Ruíz, J. A., May-Collado, L. J., Binford, G. J., 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 |
Fattorini, S., Borges, P. A., Fiasca, B., and Galassi, D. M. (2016). Trapped in the web of water: groundwater-fed springs are island-like ecosystems for the meiofauna. Ecology and Evolution 6, 8389–8401.
| Trapped in the web of water: groundwater-fed springs are island-like ecosystems for the meiofauna.Crossref | GoogleScholarGoogle Scholar |
Filchak, K. E., Roethele, J. B., and Feder, J. L. (2000). Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella. Nature 407, 739–742.
| Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella.Crossref | GoogleScholarGoogle Scholar |
Fišer, C., Blejec, A., and Trontelj, P. (2012). Niche-based mechanisms operating within extreme habitats: a case study of subterranean amphipod communities. Biology Letters 8, 578–581.
| Niche-based mechanisms operating within extreme habitats: a case study of subterranean amphipod communities.Crossref | GoogleScholarGoogle Scholar |
Fišer, C., Luštrik, R., Sarbu, S., Flot, J. F., and Trontelj, P. (2015a). Morphological evolution of coexisting amphipod species pairs from sulfidic caves suggests competitive interactions and character displacement, but no environmental filtering and convergence. PLoS One 10, e0123535.
| Morphological evolution of coexisting amphipod species pairs from sulfidic caves suggests competitive interactions and character displacement, but no environmental filtering and convergence.Crossref | GoogleScholarGoogle Scholar |
Fišer, Ž., Altermatt, F., Zakšek, V., Knapič, T., and Fišer, C. (2015b). Morphologically cryptic amphipod species are “ecological clones” at regional but not at local scale: a case study of four Niphargus species. PLoS One 10, e0134384.
| Morphologically cryptic amphipod species are “ecological clones” at regional but not at local scale: a case study of four Niphargus species.Crossref | GoogleScholarGoogle Scholar |
Fujisawa, T., and 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, 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 |
Futuyma, D. J., and Mayer, G. C. (1980). Non-allopatric speciation in animals. Systematic Biology 29, 254–271.
| Non-allopatric speciation in animals.Crossref | GoogleScholarGoogle Scholar |
Gavrilets, S. (2003). Models of speciation: what have we learned in 40 years? Evolution 57, 2197–2215.
| Models of speciation: what have we learned in 40 years?Crossref | GoogleScholarGoogle Scholar |
Gavrilets, S., Vose, A., Barluenga, M., Salzburger, W., and Meyer, A. (2007). Case studies and mathematical models of ecological speciation. 1. Cichlids in a crater lake. Molecular Ecology 16, 2893–2909.
| Case studies and mathematical models of ecological speciation. 1. Cichlids in a crater lake.Crossref | GoogleScholarGoogle Scholar |
Gers, C. (1998). Diversity of energy fluxes and interactions between arthropod communities: from soil to cave. Acta Oecologica 19, 205–213.
| Diversity of energy fluxes and interactions between arthropod communities: from soil to cave.Crossref | GoogleScholarGoogle Scholar |
Gertsch, W. J. (1992). Distribution patterns and speciation in North American cave spiders with a list of the troglobites and revision of the cicurinas of the subgenus Cicurella. Texas Memorial Museum Speleological Monographs 3, 75–122.
Giachino, P. M., and Vailati, D. (2010). ‘The Subterranean Environment. Hypogean Life, Concepts and Collecting Techniques.’ (WBA Handbooks: Verona, Italy.)
Gillespie, R. G., and Croom, H. B. (1995). Comparison of speciation mechanisms in web-building and non-web-building groups within a lineage of spiders. In ‘Hawaiian Biogeography: Evolution on a Hot Spot Archipelago’. (Eds W. L. Wagner and V. A. Funk.) (Smithsonian Institution: Washington, DC.)
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 |
Gonzalez, B. C., Worsaae, K., Fontaneto, D., and Martínez, A. (2018). Anophthalmia and elongation of body appendages in cave scale worms (Annelida: Aphroditiformia). Zoologica Scripta 47, 106–121.
| Anophthalmia and elongation of body appendages in cave scale worms (Annelida: Aphroditiformia).Crossref | GoogleScholarGoogle Scholar |
Heuts, M. J. (1953). Regressive evolution in cave animals. Symposia of the Society for Experimental Biology 7, 290–309.
Isaia, M., and Pantini, P. (2008). 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.
Isaia, M., Lana, E., and Pantini, P. (2010). Ecology and distribution of the genus Troglohyphantes Joseph, 1881 in the Western Italian Alps. In ‘European Arachnology 2008’. (Eds W. Nentwig, M. Schmidt-Entling and C. Kropf.) pp. 89–97. (Natural History Museum: Bern, Switzerland.)
Isaia, M., Paschetta, M., Lana, E., Pantini, P., Schönhofer, A. L., Christian, E., and Badino, G. (2011). ‘Subterranean Arachnids of the Western Italian Alps’. (Museo Regionale Scienze Naturali Monografie: Torino, Italy.)
Isaia, M., Mammola, S., Mazzuca, P., Arnedo, M. A., 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 |
Jeffery, W. R. (2009). Regressive evolution in Astyanax cavefish. Annual Review of Genetics 43, 25–47.
| Regressive evolution in Astyanax cavefish.Crossref | GoogleScholarGoogle Scholar |
Jiggins, C. D. (2006). Sympatric speciation: why the controversy? Current Biology 16, 333–334.
| Sympatric speciation: why the controversy?Crossref | GoogleScholarGoogle Scholar |
Jiménez-Moreno, G., Fauquette, S., and Suc, J. P. (2010). Miocene to Pliocene vegetation reconstruction and climate estimates in the Iberian Peninsula from pollen data. Review of Palaeobotany and Palynology 162, 403–415.
| Miocene to Pliocene vegetation reconstruction and climate estimates in the Iberian Peninsula from pollen data.Crossref | GoogleScholarGoogle Scholar |
Jones, R., Culver, D. C., and Kane, T. C. (1992). Are parallel morphologies of cave organisms the result of similar selection pressures? Evolution 46, 353–365.
| Are parallel morphologies of cave organisms the result of similar selection pressures?Crossref | GoogleScholarGoogle Scholar |
Juan, C., Guzik, M. T., Jaume, D., and Cooper, S. J. (2010). Evolution in caves: Darwin’s ‘wrecks of ancient life’ in the molecular era. Molecular Ecology 19, 3865–3880.
| Evolution in caves: Darwin’s ‘wrecks of ancient life’ in the molecular era.Crossref | GoogleScholarGoogle Scholar |
Juberthie, C., Delay, D., and Bouillon, M. (1980). Extension du milieu souterrain en zone non calcaire: description d’un nouveau milieu et de son peuplement par les Coléoptères troglobies. Memoires de Biospeologie 7, 19–52.
Juberthie, C., Delay, B., and Bouillon, M. (1981). Sur l’existence du milieu souterrain superficiel en zone calcaire. In Les entrees d’energie dans le karst et communications libres. Memoires de Biospeologie 8, 77–93.
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 |
Kirkpatrick, M., and Ravigné, V. (2002). Speciation by natural and sexual selection: models and experiments. American Naturalist 159, 22–35.
| Speciation by natural and sexual selection: models and experiments.Crossref | GoogleScholarGoogle Scholar |
Klaus, S., Mendoza, J. C., Liew, J. H., Plath, M., Meier, R., and Yeo, D. C. (2013). Rapid evolution of troglomorphic characters suggests selection rather than neutral mutation as a driver of eye reduction in cave crabs. Biology Letters 9, 20121098.
| Rapid evolution of troglomorphic characters suggests selection rather than neutral mutation as a driver of eye reduction in cave crabs.Crossref | GoogleScholarGoogle Scholar |
Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.
| MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets.Crossref | GoogleScholarGoogle Scholar |
Lanfear, R., Calcott, B., Ho, S. Y., and Guindon, S. (2012). Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution 29, 1695–1701.
| Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses.Crossref | GoogleScholarGoogle Scholar |
Leys, R., and Watts, C. H. S. (2008). Systematics and evolution of the Australian subterranean hydroporine diving beetles (Dytiscidae), with notes on Carabhydrus. Invertebrate Systematics 22, 217–225.
| Systematics and evolution of the Australian subterranean hydroporine diving beetles (Dytiscidae), with notes on Carabhydrus.Crossref | GoogleScholarGoogle Scholar |
Leys, R., Watts, C., Cooper, S. J. B., and Humphreys, W. F. (2003). Evolution of subterranean diving beetles (Coleoptera: Dytiscidae: Hydroporini, Bidessini) in the arid zone of Australia. Evolution 57, 2819–2834.
López, H., and Oromí, P. (2010). A pitfall trap for sampling the mesovoid shallow substratum (MSS) fauna. Speleobiology Notes 2, 7–11.
Mammola, S., and Isaia, M. (2014). Niche differentiation in Meta bourneti and M. menardi (Araneae, Tetragnathidae) with notes on the life history. International Journal of Speleology 43, 343–353.
| Niche differentiation in Meta bourneti and M. menardi (Araneae, Tetragnathidae) with notes on the life history.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. (2017a). Spiders in caves. Proceedings. Biological Sciences 284, 20170193.
| Spiders in caves.Crossref | GoogleScholarGoogle Scholar |
Mammola, S., and Isaia, M. (2017b). Rapid poleward distributional shifts in the European cave‐dwelling Meta spiders under the influence of competition dynamics. Journal of Biogeography 44, 2789–2797.
| Rapid poleward distributional shifts in the European cave‐dwelling Meta spiders under the influence of competition dynamics.Crossref | GoogleScholarGoogle Scholar |
Mammola, S., Piano, E., Giachino, P. M., and Isaia, M. (2015a). Seasonal dynamics and microclimatic preference of two Alpine endemic hypogean beetles. International Journal of Speleology 44, 239–249.
| Seasonal dynamics and microclimatic preference of two Alpine endemic hypogean beetles.Crossref | GoogleScholarGoogle Scholar |
Mammola, S., Isaia, M., and Arnedo, M. A. (2015b). 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 |
Mammola, S., Hormiga, G., Arnedo, M. A., and Isaia, M. (2016a). Unexpected diversity in the relictual European spiders of the genus Pimoa (Araneae : Pimoidae). Invertebrate Systematics 30, 566–587.
Mammola, S., Giachino, P. M., Piano, E., Jones, A., Barberis, M., Badino, G., and Isaia, M. (2016b). Ecology and sampling techniques of an understudied subterranean habitat: the Milieu Souterrain Superficiel (MSS). The Science of Nature 103, 88.
Mammola, S., Piano, E., Giachino, P. M., and Isaia, M. (2017). An ecological survey on invertebrate communities at the epigean/hypogean interface. Subterranean Biology 24, 27–52.
Marazzi, S. (2005). ‘Atlante orografico delle Alpi. SOIUSA. Suddivisione orografica internazionale unificata del Sistema Alpino.’ (Priuli & Verlucca: Scarmagno, Italy.)
Masters, B. C., Fan, V., and Ross, H. A. (2011). Species delimitation - a geneious plugin for the exploration of species boundaries. Molecular Ecology Resources 11, 154–157.
| Species delimitation - a geneious plugin for the exploration of species boundaries.Crossref | GoogleScholarGoogle Scholar |
Mayr, E. (1942). ‘Systematics and the Origin of Species.’ (Columbia University Press: New York, USA.)
Mayr, E. (1947). Ecological factors in speciation. Evolution 1, 263–288.
| Ecological factors in speciation.Crossref | GoogleScholarGoogle Scholar |
Miller, J. A. (2005). Cave adaptation in the spider genus Anthrobia (Araneae, Linyphiidae, Erigoninae). Zoologica Scripta 34, 565–592.
| Cave adaptation in the spider genus Anthrobia (Araneae, Linyphiidae, Erigoninae).Crossref | GoogleScholarGoogle Scholar |
Niemiller, M. L., and Zigler, K. S. (2013). Patterns of cave biodiversity and endemism in the Appalachians and Interior Plateau of Tennessee, USA. PLoS One 8, e64177.
| Patterns of cave biodiversity and endemism in the Appalachians and Interior Plateau of Tennessee, USA.Crossref | GoogleScholarGoogle Scholar |
Niemiller, M. L., Fitzpatrick, B. M., and Miller, B. T. (2008). Recent divergence with gene flow in Tennessee cave salamanders (Plethodontidae: Gyrinophilus) inferred from gene genealogies. Molecular Ecology 17, 2258–2275.
| Recent divergence with gene flow in Tennessee cave salamanders (Plethodontidae: Gyrinophilus) inferred from gene genealogies.Crossref | GoogleScholarGoogle Scholar |
Nitzu, E., Nae, A., Băncilă, R., Popa, I., Giurginca, A., and Plăiaşu, R. (2014). Scree habitats: ecological function, species conservation and spatialtemporal variation in the arthropod community. Systematics and Biodiversity 12, 65–75.
| Scree habitats: ecological function, species conservation and spatialtemporal variation in the arthropod community.Crossref | GoogleScholarGoogle Scholar |
Nosil, P. (2008). Speciation with gene flow could be common. Molecular Ecology 17, 2103–2106.
| Speciation with gene flow could be common.Crossref | GoogleScholarGoogle Scholar |
Novak, T., Tkvac, T., Kuntner, M., Arnett, E. A., Delakorda, S. L., Perc, M., and Janžekovič, F. (2010). Niche partitioning in orbweaving spiders Meta menardi and Metellina merianae (Tetragnathidae). Acta Oecologica 36, 522–529.
| Niche partitioning in orbweaving spiders Meta menardi and Metellina merianae (Tetragnathidae).Crossref | GoogleScholarGoogle Scholar |
Panhuis, T. M., Butlin, R., Zuk, M., and Tregenza, T. (2001). Sexual selection and speciation. Trends in Ecology & Evolution 16, 364–371.
| Sexual selection and speciation.Crossref | GoogleScholarGoogle Scholar |
Pesarini, C. (2001). Note sui Troglohyphantes 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.
Pipan, T., and Culver, D. C. (2017). The unity and diversity of the subterranean realm with respect to invertebrate body size. Journal of Caves and Karst Studies 79, 1–9.
| The unity and diversity of the subterranean realm with respect to invertebrate body size.Crossref | GoogleScholarGoogle Scholar |
Porter, M. L., and Crandall, K. A. (2003). Lost along the way: the significance of evolution in reverse. Trends in Ecology & Evolution 18, 541–547.
| Lost along the way: the significance of evolution in reverse.Crossref | GoogleScholarGoogle Scholar |
Poulson, T. L. (1977). A tale of two spiders. Cave Research Foundation Annual Report, pp. 245–248. Cave Research Foundation, Laurel, MD.
Protas, M., and Jeffery, W. R. (2012). Evolution and development in cave animals: from fish to crustaceans. Wiley Interdisciplinary Reviews. Developmental Biology 1, 823–845.
| Evolution and development in cave animals: from fish to crustaceans.Crossref | GoogleScholarGoogle Scholar |
Rambaut, A., and Drummond, A. (2013). ‘Tracer 1.6.’ (University of Edinburgh: Edinburgh, UK.)
Rendoš, M., Mock, A., and Jászay, T. (2012). Spatial and temporal dynamics of invertebrates dwelling karstic mesovoid shallow substratum of Sivec National Nature Reserve (Slovakia), with emphasis on Coleoptera. Biologia 67, 1143–1151.
| Spatial and temporal dynamics of invertebrates dwelling karstic mesovoid shallow substratum of Sivec National Nature Reserve (Slovakia), with emphasis on Coleoptera.Crossref | GoogleScholarGoogle Scholar |
Rétaux, S. R., and Casane, D. (2013). Evolution of eye development in the darkness of caves: adaptation, drift, or both? EvoDevo 4, 26.
| Evolution of eye development in the darkness of caves: adaptation, drift, or both?Crossref | GoogleScholarGoogle Scholar |
Rundle, H. D., and Nosil, P. (2005). Ecological speciation. Ecology Letters 8, 336–352.
| Ecological speciation.Crossref | GoogleScholarGoogle Scholar |
Savolainen, V., Anstett, M. C., Lexer, C., Hutton, I., Clarkson, J. J., Norup, M. V., Powel, M. P., Springate, D., Salamin, N., and Baker, W. J. (2006). Sympatric speciation in palms on an oceanic island. Nature 441, 210–213.
| Sympatric speciation in palms on an oceanic island.Crossref | GoogleScholarGoogle Scholar |
Schluter, D. (2000). ‘The Ecology of Adaptive Radiation.’ (Oxford University Press: Oxford, UK.)
Schluter, D. (2001). Ecology and the origin of species. Trends in Ecology & Evolution 16, 372–380.
| Ecology and the origin of species.Crossref | GoogleScholarGoogle Scholar |
Schluter, D., and Conte, G. L. (2009). Genetics and ecological speciation. Proceedings of the National Academy of Sciences of the United States of America 106, 9955–9962.
| Genetics and ecological speciation.Crossref | GoogleScholarGoogle Scholar |
Sharratt, N. J., Picker, M. D., and Samways, M. J. (2000). The invertebrate fauna of the sandstone caves of the Cape Peninsula (South Africa): patterns of endemism and conservation priorities. Biodiversity and Conservation 9, 107–143.
| The invertebrate fauna of the sandstone caves of the Cape Peninsula (South Africa): patterns of endemism and conservation priorities.Crossref | GoogleScholarGoogle Scholar |
Shevenell, A. E., Kennett, J. P., and Lea, D. W. (2004). Middle Miocene southern ocean cooling and Antarctic cryosphere expansion. Science 305, 1766–1770.
| Middle Miocene southern ocean cooling and Antarctic cryosphere expansion.Crossref | GoogleScholarGoogle Scholar |
Silvestro, D., and Michalak, I. (2012). raxmlGUI: a graphical front-end for RAxML. Organisms, Diversity & Evolution 12, 335–337.
| raxmlGUI: a graphical front-end for RAxML.Crossref | GoogleScholarGoogle Scholar |
Snowman, C. V., Zigler, K. S., and Hedin, M. (2010). Caves as islands: mitochondrial phylogeography of the cave-obligate spider species Nesticus barri (Araneae: Nesticidae). The Journal of Arachnology 38, 49–56.
| Caves as islands: mitochondrial phylogeography of the cave-obligate spider species Nesticus barri (Araneae: Nesticidae).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 |
Strecker, U., Hausdorf, B., and Wilkens, H. (2012). Parallel speciation in Astyanax cave fish (Teleostei) in Northern Mexico. Molecular Phylogenetics and Evolution 62, 62–70.
| Parallel speciation in Astyanax cave fish (Teleostei) in Northern Mexico.Crossref | GoogleScholarGoogle Scholar |
Sturani, M. (1942). ‘Caccia grossa tra le erbe.’ (Giulio Einaudi Editore: Torino, Italy.)
Suc, J. P. (1984). Origin and evolution of the Mediterranean vegetation and climate in Europe. Nature 307, 429–432.
| Origin and evolution of the Mediterranean vegetation and climate in Europe.Crossref | GoogleScholarGoogle Scholar |
Tregenza, T., and Butlin, R. K. (1999). Speciation without isolation. Nature 400, 311–312.
| Speciation without isolation.Crossref | GoogleScholarGoogle Scholar |
Uéno, S. I. (1987). The derivation of terrestrial cave animals. Zoological Science 4, 593–606.
Vailati, D. (1988). ‘Studi sui Bathysciinae delle prealpi centro-occidentali. Revisione sistematica, ecologia, biogeografia della serie filetica di Boldoria (Coleoptera Catopidae).’ (Monografie del Museo Civico di Scienze Naturali di Brescia: Brescia, Italy.)
Wang, F., Ballesteros, J. A., Hormiga, G., Chesters, D., Zhan, Y., Sun, N., Zhu, C., Chen, W., and Tu, L. (2015). Resolving the phylogeny of a speciose spider group, the family Linyphiidae (Araneae). Molecular Phylogenetics and Evolution 91, 135–149.
| Resolving the phylogeny of a speciose spider group, the family Linyphiidae (Araneae).Crossref | GoogleScholarGoogle Scholar |
Weckstein, J. D., Johnson, K. P., Murdoch, J. D., Krejca, J. K., Takiya, D. M., Veni, G., Reddel, J. R., and Taylor, S. J. (2016). Comparative phylogeography of two codistributed subgenera of cave crickets (Orthoptera: Rhaphidophoridae: Ceuthophilus spp.). Journal of Biogeography 43, 1450–1463.
| Comparative phylogeography of two codistributed subgenera of cave crickets (Orthoptera: Rhaphidophoridae: Ceuthophilus spp.).Crossref | GoogleScholarGoogle Scholar |
Wiens, J. J., Chippindale, P. T., and Hillis, D. M. (2003). When are phylogenetic analyses misled by convergence? A case study in Texas cave salamanders. Systematic Biology 52, 501–514.
| When are phylogenetic analyses misled by convergence? A case study in Texas cave salamanders.Crossref | GoogleScholarGoogle Scholar |
Wilcox, T. P., de León, F. G., Hendrickson, D. A., and Hillis, D. M. (2004). Convergence among cave catfishes: long-branch attraction and a Bayesian relative rates test. Molecular Phylogenetics and Evolution 31, 1101–1113.
| Convergence among cave catfishes: long-branch attraction and a Bayesian relative rates test.Crossref | GoogleScholarGoogle Scholar |
Wilkens, H., and Hüppop, K. (1986). Sympatric speciation in cave fishes? Journal of Zoological Systematics and Evolutionary Research 24, 223–230.
| Sympatric speciation in cave fishes?Crossref | GoogleScholarGoogle Scholar |
World Spider Catalog (2018). World Spider Catalog. Natural History Museum Bern. Available at http://wsc.nmbe.ch, version 18.5,
Wynne, J. J., Bernard, E. C., Howarth, F. G., Sommer, S., Soto-Adames, F. N., Taiti, S., Mockford, E. L., Lázaro, M. H., and Pakarati-Hotus, V. (2014). Disturbance relicts in a rapidly changing world: the Rapa Nui (Easter Island) factor. Bioscience 64, 711–718.
| Disturbance relicts in a rapidly changing world: the Rapa Nui (Easter Island) factor.Crossref | GoogleScholarGoogle Scholar |
Zuur, A. F., Ieno, E. N., and Elphick, C. S. (2010). A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1, 3–14.
| A protocol for data exploration to avoid common statistical problems.Crossref | GoogleScholarGoogle Scholar |