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7 - Coexisting Cryptic Species as a Model System in Integrative Taxonomy

Published online by Cambridge University Press:  01 September 2022

By
Cene Fišer  and
Klemen Koselj
Edited by
Alexandre K. Monro  and
Simon J. Mayo
Alexandre K. Monro
Affiliation:
Royal Botanic Gardens, Kew
Simon J. Mayo
Affiliation:
Royal Botanic Gardens, Kew
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Summary

Species are fundamental units used to describe and interpret nature. Molecular delimitation methods have shown that many species cannot be diagnosed using morphological traits. We suggest that cryptic species represent an opportunity to progress Linnean taxonomy,. We examine what can be learned from sympatric cryptic species pairs that occupy the same habitat. Their sympatry is possible under two conditions, 1) reproductive isolation, 2) the effects of interspecific competition on population growth must be neutralised. Understanding the mechanisms that maintain species differences and integrating this understanding into taxonomy will help to delineate species boundaries. We first examine the mechanisms of cryptic species origin. Then we review some well-documented cases of reproductive isolation between cryptic species, focusing on prezygotic isolation mechanisms mediated by premating recognition and communication. We follow with examples of co-occurring cryptic species, focusing on mechanisms of coexistence and ecological niche differentiation. Both mate recognition and niche differentiation are grounded in the sensory worlds that animals experience. Sensory ecology provides tools to explore hitherto hidden diversity and so identify, misunderstood and unprotected in this time of rapid anthropogenic global change. We argue that the field of sensory ecology has a potential for improving taxonomy

Keywords

sympatryreproductive isolationinterspecific competitionprezygotic isolation mechanisms sensory ecologyultraviolet lightchemistrybatsmultimodal signallingsound
Type
Chapter
Information
Cryptic Species
Morphological Stasis, Circumscription, and Hidden Diversity
 , pp. 169 - 196
Publisher: Cambridge University Press
Print publication year: 2022

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References

Adams, M., Raadik, T. A., Burridge, C. P., and Georges, A. (2014) Global biodiversity assessment and hyper-cryptic species complexes: More than one species of elephant in the room? Systematic Biology 63: 518–533. doi: 10.1093/sysbio/syu017Google Scholar
Arikawa, K. (2017) The eyes and vision of butterflies. The Journal of Physiology 16: 5457–5464. doi: 10.1113/JP273917Google Scholar
Asai, N., Fusetani, N., Matsunaga, S., and Sasaki, J. (2000) Sex pheromones of the hair crab Erimacrus isenbeckii. Part 1: Isolation and Structures of Novel Ceramides. Tetrahedron 56: 9895–9899. doi: 10.1021/np010177mGoogle Scholar
Bakus, G. J., Targett, N. M., and Schulte, B. (1986) Chemical ecology of marine organisms: An overview. Journal of Chemical Ecology 12: 951–987.CrossRefGoogle ScholarPubMed
Barbosa, D., Font, E., Desfilis, E., and Carretero, M. A. (2006) Chemically mediated species recognition in closely related Podarcis wall lizards. Journal of Chemical Ecology 32: 1587–1598. doi: 10.1007/s10886-006-9072-5Google Scholar
Barlow, K. E. and Jones, G. (1997) Function of pipistrelle social calls: Field data and a playback experiment. Animal Behaviour 53: 991–999. doi: 10.1006/anbe.1996.0398CrossRefGoogle Scholar
Barratt, E. M., Deaville, R., Burland, T. M. et al. (1997) DNA answers the call of pipistrelle bat species. Nature 387: 138-139.Google Scholar
Berry, F. C. and Breithaupt, T. (2010) To signal or not to signal? Chemical communication by urine-borne signals mirrors sexual conflict in crayfish. BMC Biology 8: 1–11. doi: 10.1186/1741-7007-8-25CrossRefGoogle ScholarPubMed
Bickford, D., Lohman, D. J., Sodhi, N. S. et al. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology & Evolution 22: 148–155. doi: 10.1016/j.tree.2006.11.004Google Scholar
Boughman, J. W. (2002) How sensory drive can promote speciation. Trends in Ecology & Evolution 17: 571–577.Google Scholar
Bradbury, J. W. and Vehrenkamp, S. L. (2011) Principals of Animal Communication. 2nd ed. Sinauer, Sunderland, MA, 697 pp.Google Scholar
Braune, P., Schmidt, S., and Zimmermann, E. (2008) Acoustic divergence in the communication of cryptic species of nocturnal primates (Microcebus ssp.). BMC Biology 6: 19. doi: 10.1186/1741-7007-6-19Google Scholar
Brunton, C. F. A. and Majerus, M. E. N. (1995) Ultraviolet colours in butterflies: Intra- or inter-specific communication? Proceedings of the Royal Society B 260: 199–204. doi: 10.1098/rspb.1995.0080Google Scholar
Butlin, R., Debelle, A., Kerth, C. et al. (2012) What do we need to know about speciation? Trends in Ecology and Evolution 27: 27–39. doi: 10.1016/j.tree.2011.09.002Google ScholarPubMed
Butlin, R. K. and Hewitt, G. M. (1986) Heritability estimates for characters under sexual selection in the grasshopper, Chorthippus brunneus. Animal Behaviour 34: 1256–1261. doi: 10.1016/S0003-3472(86)80185-3Google Scholar
Campillo, L. C., Barley, A. J., and Thomson, R. C. (2020) Model-based species delimitation: are coalescent species reproductively isolated? Systematic Biology 69: 708–721. doi: 10.1093/sysbio/syz072CrossRefGoogle Scholar
Caspers, B. A., Schroeder, F. C., Franke, S. et al. (2009) Odour-based species recognition in two sympatric species of sac-winged bats (Saccopteryx bilineata, S. leptura): Combining chemical analyses, behavioural observations and odour preference tests. Behavioral Ecology and Sociobiology 63: 741–749.Google Scholar
Catchpole, C. K. and Slater, P. J. B. (2008) Bird Song: Biological Themes and Variations. 2nd ed. Cambridge University Press, Cambridge, 335 pp.CrossRefGoogle Scholar
Chambers, A. E. and Hillis, D. M. (2019) The multispecies coalescent over-splits species in the case of geographically widespread taxa. Systematic Biology 69: 184–193. doi: 10.1093/sysbio/syz042CrossRefGoogle Scholar
Chesson, P. (2000) Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 31: 343–366. doi: 10.1146/annurev.ecolsys.31.1.343CrossRefGoogle Scholar
Claridge, M. (1985) Acoustic signals in the homoptera: Behavior, taxonomy, and evolution. Annual Review of Entomology 30: 297–317. doi: 10.1146/annurev.ento.30.1.297Google Scholar
Cocroft, R. B. and Rodríguez, R. L. (2005) The behavioral ecology of insect vibrational communication. BioScience 55: 323–334.CrossRefGoogle Scholar
Cocroft, R. B., Rodríguez, R. L., and Hunt, R. E. (2010) Host shifts and signal divergence: Mating signals covary with host use in a complex of specialized plant-feeding insects. Biological Journal of the Linnean Society 99: 60–72. doi: 10.1111/j.1095-8312.2009.01345.xGoogle Scholar
Čokl, A. and Virant-Doberlet, M. (2003) Communication with substrate-borne signals in small plant-dwelling insects. Annual Review of Entomology 48: 29–50. doi: 10.1146/annurev.ento.48.091801.1Google Scholar
Condon, M., Adams, D. C., Bann, D. et al. (2008) Uncovering tropical diversity: Six sympatric cryptic species of Blepharoneura (Diptera: Tephritidae) in flowers of Gurania spinulosa (Cucurbitaceae) in eastern Ecuador. Biological Journal of the Linnean Society 93: 779–797. doi: 10.1111/j.1095-8312.2007.00943.xGoogle Scholar
Cothran, R. D., Noyes, P., and Relyea, R. A. (2015) An empirical test of stable species coexistence in an amphipod species complex. Oecologia 178: 819–831. doi: 10.1007/s00442-015-3262-1CrossRefGoogle Scholar
Cothran, R. D., Henderson, K. A., Schmidenberg, D. et al. (2013) Phenotypically similar but ecologically distinct: Differences in competitive ability and predation risk among amphipods. Oikos 122: 1429–1440. doi: 10.1111/j.1600-0706.2013.00294.xGoogle Scholar
Deiner, K., Fronhofer, E. A., Mächler, E., Walser, J. C., and Altermatt, F. (2016) Environmental DNA reveals that rivers are conveyer belts of biodiversity information. Nature Communications 7: 12544. doi: 10.1038/ncomms12544Google Scholar
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. doi: 10.1038/s41598-017-02938-zCrossRefGoogle ScholarPubMed
De Meester, N. et al. (2011) Salinity effects on the coexistence of cryptic species: A case study on marine nematodes. Marine Biology 158: 2717–2726. doi: 10.1007/s00227-011-1769-5Google Scholar
De Queiroz, K. (2005) Different species problems and their resolution. BioEssays 27: 1263–1269. doi: 10.1002/bies.20325CrossRefGoogle ScholarPubMed
De Queiroz, K. (2007) Species concepts and species delimitation. Systematic Biology 56: 879–886. doi: 10.1080/10635150701701083CrossRefGoogle ScholarPubMed
Dieckmann, U. and Doebeli, M. (1999) On the origin of species by sympatric speciation. Nature 400: 354–357.CrossRefGoogle ScholarPubMed
Dinca, V., Lukhtanov, V. A., Talavera, G., and Vila, R. (2011) Unexpected layers of cryptic diversity in wood white. Nature Communications 2: 324. doi: 10.1038/ncomms1329CrossRefGoogle ScholarPubMed
Dinca, V., Wiklund, C., Lukhtanov, V. A. et al. (2013) Reproductive isolation and patterns of genetic differentiation in a cryptic butterfly species complex. Journal of Evolutionary Biology 26: 2095–2106. doi: 10.1111/jeb.12211CrossRefGoogle Scholar
Dionne, K., Vergilino, R., Dufresne, F., Charles, F., and Nozais, C. (2011) No evidence for temporal variation in a cryptic species community of freshwater amphipods of the Hyalella azteca species complex. Diversity 3: 390–404. doi: 10.3390/d3030390Google Scholar
Doctrow, B. (2018) QnAs with Mark Hay. Proceedings of the National Academy of Sciences of the United States of America 115: 6521–6522. doi: 10.1073/pnas.1808472115CrossRefGoogle ScholarPubMed
Doebeli, M. and Dieckmann, U. (2000) Evolutionary branching and sympatric speciation caused by different types of ecological interactions. American Naturalist 156: S77–S101.Google Scholar
van Doorn, G. S., Dieckmann, U., and Weissing, F.J. (2004) Sympatric speciation by sexual selection: A critical reevaluation. American Naturalist 163: 709–725.Google Scholar
Eisenring, M., Altermatt, F., Westram, A. M. et al. (2016) Habitat requirements and ecological niche of two cryptic amphipod species at landscape and local scales. Ecoshphere 7: e01319. doi: e01319.10.1002/ecs2.1319Google Scholar
Elbrecht, V. and Leese, F. (2015) Can DNA-based ecosystem assessments quantify species abundance? Testing primer bias and biomass–sequence relationships with an innovative metabarcoding protocol. Plos One 10: e0130324. doi: 10.1371/journal.pone.0130324Google Scholar
Eme, D., Zagmajster, M., Delić, T. et al. (2017) Do cryptic species matter in macroecology? Sequencing European groundwater crustaceans yields smaller ranges but does not challenge biodiversity determinants. Ecography 41: 1–13. doi: 10.1111/ecog.02683Google Scholar
Endler, J. A. and Basolo, A. L. (1998) Sensory ecology, receiver biases and sexual selection. Trends in Ecology and Evolution 13: 415-420.Google Scholar
Feulner, P. G. D., Kirschbaum, F., Schugardt, C. et al. (2006) Electrophysiological and molecular genetic evidence for sympatrically occurring cryptic species in African weakly electric fishes (Teleostei: Mormyridae: Campylomormyrus). Molecular Phylogenetics and Evolution 39: 198–208. doi: 10.1016/j.ympev.2005.09.008CrossRefGoogle ScholarPubMed
Finkbeiner, S. D., Fishman, D. A., Osorio, D. et al. (2017) Ultraviolet and yellow reflectance but not fluorescence is important for visual discrimination of conspecifics by Heliconius erato. Journal of Experimental Biology 220: 1267–1276. doi: 10.1242/jeb.153593Google Scholar
Fišer, C., Robinson, C. T., and Malard, F. (2018) Cryptic species as a window into the paradigm shift of the species concept. Molecular Ecology 27: 613–635. doi: 10.1111/ijlh.12426Google Scholar
Fišer, Ž., Altermatt, F., Zakšek, V., Knapič, T., and Fišer, C. (2015) 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. doi: 10.1371/journal.pone.0134384CrossRefGoogle ScholarPubMed
Flot, J.-F., Couloux, A., and Tillier, S. (2010) Haplowebs as a graphical tool for delimiting species: A revival of Doyle’s “field for recombination” approach and its application to the coral genus Pocillopora in Clipperton. BMC Evolutionary Biology 10: 372. doi: 10.1186/1471-2148-10-372Google Scholar
Fontaneto, D., Flot, J.-F., and Tang, C. Q. (2015) Guidelines for DNA taxonomy, with a focus on the meiofauna. Marine Biodiversity 45: 533–451. doi: 10.1007/s12526-015-0319-7Google Scholar
Friesen, V. L., Smith, A. L., Gómez-Díaz, E. et al. (2007) Sympatric speciation by allochrony in a seabird. Proceedings of the National Academy of Sciences of the United States of America 104: 18589–18594. doi: 10.1073/pnas.0700446104Google Scholar
Fujita, M. K., Leaché, A. D., Burbrink, F. T., McGuire, J. A., and Moritz, C. (2012) Coalescent-based species delimitation in an integrative taxonomy. Trends in Ecology & Evolution 27: 480–488. doi: 10.1016/j.tree.2012.04.012Google Scholar
Funk, C. W., Caminer, M., and Ron, S. R. (2012) High levels of cryptic species diversity uncovered in Amazonian frogs. Proceedings of the Royal Society B 279: 1806–1814. doi: 10.1098/rspb.2011.1653Google Scholar
Gabaldón, C., Montero-Pau, J., Serra, M., and Carmona, M.J. (2013) Morphological similarity and ecological overlap in two rotifer species. PLoS ONE 8: e57087. doi: 10.1371/journal.pone.0057087Google Scholar
Germain, R. M., Williams, J. L., Schluter, D., and Angert, A. L. (2018) Moving character displacement beyond characters using contemporary coexistence theory. Trends in Ecology and Evolution 33: 74-84 doi: 10.1016/j.tree.2017.11.002Google Scholar
Gilbert, L. E. (1991) Biodiversity of a Central American Heliconius community: pattern, process, and problems. In: Price, P. W., Lewinsohn, T. M., Fernandes, T. W., and Benson, W. W. (eds.) Plant-Animal Interactions: Evolutionary Ecology in Tropical and Temperate Regions. John Wiley & Sons, New York, pp. 403–427.Google Scholar
Gill, B. A., Kondratieff, B. C., Casner, K. L. et al. (2016) Cryptic species diversity reveals biogeographic support for the “mountain passes are higher in the tropics” hypothesis. Proceedings of The Royal Society B 283: 7–12. doi: 10.1098/rspb.2016.0553Google Scholar
Gillespie, R. G., Bennett, G. M., De Meester, L. et al. (2020) Comparing adaptive radiations across space, time, and taxa. Journal of Heredity 111:1–20. doi: 10.1093/jhered/esz064Google Scholar
Gogala, M. and Trilar, T. (2004) Bioacoustic investigations and taxonomic considerations on the Cicadetta montana species complex (Homoptera : Cicadoidea : Tibicinidae ). Anais de Academia Brasileira de Ciencas 76: 316–324.Google Scholar
Hardege, J. D., Jennings, A., Hayden, D. et al. (2002) Novel behavioural assay and partial purification of a female-derived sex pheromone in Carcinus maenas. Marine Ecology Progress Series 244: 179–189. doi: 10.3354/meps244179Google Scholar
Hardege, J. D. and Terschak, J. A. (2010) Identification of crustacean sex pheromones. In: Breithaupt, T. and Thiel, M. (eds.) Chemical Communication in Crustaceans. Springer, New York, pp. 373–392.Google Scholar
Häussler, U. et al. 1999. External characteristics discriminating species of European pipistrelles, Pipistrellus pipistrellus (Schreber, 1774) and P. pygmaeus (Leach, 1825). Myotis 37: 27-40.Google Scholar
Hay, M. E. (2009) Marine chemical ecology: Chemical signals and cues structure marine populations, communities, and ecosystems. Annual Review of Marine Science 1: 193–214. doi: 10.1146/annurev.marine.010908.163708Google Scholar
Hay, M. E. (2010) Crustaceans as Powerful Models in Aquatic Chemical Ecology. In: Breithaupt, T. and Thiel, M. (eds.) Chemical Communication in Crustaceans. Springer, New York, pp. 41–62. doi: 10.1007/978-0-387-77101-4Google Scholar
Hebert, P. D. N., Penton, E. H., Burns, J. M., Janzen, D. H., 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. doi: 10.1073/pnas.0406166101Google Scholar
Heethoff, M. (2018) Cryptic species – conceptual or terminological chaos? A response to Struck et al. Trends in Ecology & Evolution 33: 310. doi: 10.1016/j.tree.2018.02.006Google Scholar
Henry, C. S. (1994) Singing and cryptic speciation in insects. Trends in Ecology & Evolution 9: 388–392.Google Scholar
Henry, C. S. and Wells, M. M. (2010) Acoustic niche partitioning in two cryptic sibling species of Chrysoperla green lacewings that must duet before mating. Animal Behaviour 80: 991–1003. doi: 10.1016/j.anbehav.2010.08.021Google Scholar
Henry, C. S., Brooks, S. J., Duelli, P. et al. (2013) Obligatory duetting behaviour in the Chrysoperla carnea -group of cryptic species (Neuroptera : Chrysopidae): Its role in shaping evolutionary history. Biological Reviews 88: 787–808. doi: 10.1111/brv.12027CrossRefGoogle ScholarPubMed
Henry, C. S., Brooks, S. J., Duelli, P. (2014) A new cryptic species of the Chrysoperla carnea group (Neuroptera : Chrysopidae) from western Asia: Parallel speciation without ecological adaptation. Systematic Entomology 39: 380–393. doi: 10.1111/syen.12061Google Scholar
Herrel, A., Huyghe, K., Vanhooydonck, B. et al. (2008) Rapid large-scale evolutionary divergence in morphology and performance associated with exploitation of a different dietary resource. Proceedings of the National Academy of Sciences of the United States of America 105: 4792–4795. doi: 10.1073/pnas.0711998105Google Scholar
Hertach, T., Puissant, S., Gogala, M. et al. (2016) Complex within a complex : Integrative taxonomy reveals hidden diversity in Cicadetta brevipennis ( Hemiptera : Cicadidae ) and unexpected relationships with a song divergent relative. PLoS ONE 11: e0165562. doi: 10.1371/journal.pone.0165562Google Scholar
Hey, J. (2006) On the failure of modern species concepts. Trends in Ecology and Evolution 21: 447–450. doi: 10.1016/j.tree.2006.05.011CrossRefGoogle ScholarPubMed
Hobel, G. and Gerhardt, C. H. (2003) Reproductive character displacement in the acoustic communication system of green tree frogs (Hyla cinerea). Evolution 57: 894–904.Google Scholar
Holt, R. D. (2006) Emergent neutrality. Trends in Ecology and Evolution 21: 531–533. doi: 10.1016/j.tree.2006.08.003CrossRefGoogle ScholarPubMed
Hoyal Cuthill, J. W., Guttenberg, N., Ledger, S., Crowther, R., and Huertas, B. (2019) Deep learning on butterfly phenotypes tests evolution’s oldest mathematical model. Science Advances 5: eaaw4967. doi: 10.1126/sciadv.aaw4967Google Scholar
Imafuku, M. (2008) Variation in UV light reflected from the wings of Favonius and Quercusia butterflies. Entomological Science 11: 75–80. doi: 10.1111/j.1479-8298.2007.00247.xCrossRefGoogle Scholar
Izzo, A. S. and Gray, D. A. (2004) Cricket song in sympatry: Species specificity of song without reproductive character displacement in Gryllus rubens. Annals of the Entomological Society of America 97: 831–837. doi: 10.1603/0013-8746(2004)097Google Scholar
Jones, G. (1997) Acoustic signals and speciation: The roles of natural and sexual selection in the evolution of cryptic species. Advances in the Study of Behavior 26: 317–354.Google Scholar
Jones, G. and van Parijs, S. M. (1993) Bimodal echolocation in pipistrelle bats: Are cryptic species present? Proceedings of the Royal Society B 251: 119–125. doi: 10.1098/rspb.1993.0017Google Scholar
Jones, G. and Siemers, B. M. (2011) The communicative potential of bat echolocation pulses. Journal of Comparative Physiology A 197: 447–457. doi: 10.1007/s00359-010-0565-xCrossRefGoogle ScholarPubMed
Jones, J. (2001) Habitat selection studies in avian ecology: A critical review. The Auk 118: 557–562.Google Scholar
Jugovic, J., Jalžić, B., Prevorčnik, S., and Sket, B. (2012) Cave shrimps Troglocaris s. str. (Dormitzer, 1853), taxonomic revision and description of new taxa after phylogenetic and morphometric studies. Zootaxa 3421: 1–31.Google Scholar
Kaliszewska, Z. A., Seger, J., Rowntree, V. J. et al. (2005) Population histories of right whales (Cetacea: Eubalaena) inferred from mitochondrial sequence diversities and divergences of their whale lice (Amphipoda: Cyamus). Molecular Ecology 14: 3439–3456. doi: 10.1111/j.1365-294X.2005.02664Google Scholar
Kalko, E. K. and Schnitzler, H. U. (1993) Plasticity in echolocation signals of European pipistrelle bats in search flight: Implications for habitat use and prey detection. Behavioral Ecology and Sociobiology 33(6): 415–428. https://link.springer.com/article/10.1007/BF00170257Google Scholar
Kapli, P., Lutteropp, S., Zhang, J. et al. (2017) Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics 33: 1630–1638. doi: 10.1093/bioinformatics/btx025Google Scholar
Karanovic, T., Djurakic, M., and Eberhard, S. M. (2016) Cryptic species or inadequate taxonomy? Implementation of 2D geometric morphometrics based on integumental organs as landmarks for delimitation and description of copepod taxa. Systematic Biology 65: 304–327. doi: 10.1093/sysbio/syv088Google Scholar
Kemp, D. J. (2007) Female butterflies prefer males bearing bright iridescent ornamentation. Proceedings of the Royal Society B 274: 1043–1047. doi: 10.1098/rspb.2006.0043Google Scholar
Kemp, D. J. and Rutowski, R. L. (2011) The role of coloration in mate choice and sexual interactions in butterflies. In: Brockmann, J. H. and Roper, T. (eds.) Advances in the Study of Behavior, Volume 43. Elsevier Inc., New York, pp. 55–92. doi: 10.1016/B978-0-12-380896-7.00002-2Google Scholar
Kirschel, A. N. G., Blumstein, D. T., and Smith, T. B. (2009) Character displacement of song and morphology in African tinkerbirds. Proceedings of the National Academy of Sciences 106: 8256–8261.Google Scholar
Knowlton, N. (1993) Sibling species in the sea. Annual Review of Ecology and Systematics 24: 189–216.Google Scholar
Knuttel, H. and Fiedler, K. (2000) On the use of ultraviolet photography and ultraviolet wing patterns in butterfly morphology and taxonomy. Journal of the Lepidopterists’ Society 54: 137–144.Google Scholar
Koselj, K., Schnitzler, H.-U., and Siemers, B. M. (2011) Horseshoe bats make adaptive prey-selection decisions, informed by echo cues. Proceedings of the Royal Society B 278, 3034–3041.Google Scholar
Kubisch, A., Holt, R. D., Poethke, H.-J., and Fronhofer, E.A. (2014) Where am I and why? Synthesizing range biology and the eco-evolutionary dynamics of dispersal. Oikos 123: 5–22. doi: 10.1111/j.1600-0706.2013.00706.xCrossRefGoogle Scholar
Lagrue, C., Wattier, R., Galipaud, M. et al. (2014) Confrontation of cryptic diversity and mate discrimination within Gammarus pulex and Gammarus fossarum species complexes. Freshwater Biology 59: 2555–2570. doi: 10.1111/fwb.12453Google Scholar
Lajus, D., Sukhikh, N., and Alekseev, V. (2015) Cryptic or pseudocryptic: Can morphological methods inform copepod taxonomy? An analysis of publications and a case study of the Eurytemora affinis species complex. Ecology and Evolution 5: 2374–2385. doi: 10.1002/ece3.1521Google Scholar
Lassance, J.-M., Svensson, G. P., Kozlov, M. V., Francke, W., and Löfstedt, C. (2019) Pheromones and barcoding delimit boundaries between cryptic species in the primitive moth genus Eriocrania (Lepidoptera: Eriocraniidae). Journal of Chemical Ecology 45: 429—439. doi: 10.1007/s10886-019-01076-2CrossRefGoogle ScholarPubMed
Leache, A. D., Fujita, M. K., Minin, V. N., and Bouckaert, R. R. (2014) Species delimitation using genome-wide SNP Data. Systematic Biology 63: 534–542. doi: 10.1093/sysbio/syu018Google Scholar
Leese, F., Altermatt, F., Bouchez, A. et al. (2016) DNAqua-Net: Developing new genetic tools for bioassessment and monitoring of aquatic ecosystems in Europe. Research Ideas and Outcomes 2: e11321. doi: 10.3897/rio.2.e11321Google Scholar
Leibold, M. A. and McPeek, M. A. (2006) Coexistence of the niche and neutral perspectives in community ecology. Ecology 87: 1399–410. doi: 10.1890/0012-9658(2006)87[1399:cotnan]2.0.co;2Google Scholar
Leibold, M. A., Urban, M. C., De Meester, L., Klausmeier, C. A., and Vanoverbeke, J. (2018) Regional neutrality evolves through local adaptive niche evolution. Proceedings of the National Academy of Sciences 116: 2612–2617. doi: 10.1073/pnas.1808615116Google Scholar
Li, L. and Chesson, P. (2016) The effects of dynamical rates on species coexistence in a variable environment: The Paradox of the Plankton revisited. The American Naturalist 188: E46–E58. doi: 10.1086/687111Google Scholar
Lim, M. L. M., Land, M. F., and Li, D. (2007) Sex-specific UV and fluorescence signals in jumping spiders. Science 315: 481. doi: 10.1126/science.1134254Google Scholar
Lindquist, N. (2002) Chemical defense of early life stages of benthic marine invertebrates. Journal of Chemical Ecology 28: 1987–2000. doi: 10.1023/A:1020745810968Google Scholar
Lukhtanov, V. A. (2010) Dobzhansky’s rule and reinforcement of pre-zygotic reproductive isolation in zones of secondary contact. Zhurnal Obshchei Biologii 71: 372–385. doi: 10.1134/s2079086411010051Google ScholarPubMed
Lukhtanov, V. A., Kandul, N. P., Plotkin, J. B. et al. (2005) Reinforcement of pre-zygotic isolation and karyotype evolution in Agrodiaetus butterflies. Nature 436: 385–389. doi: 10.1038/nature03704Google Scholar
Lukić, M., Delić, T., Pavlek, M., Deharveng, L., and Zagmajster, M. (2019) Distribution pattern and radiation of the European subterranean genus Verhoeffiella (Collembola , Entomobryidae). Zoologica Scripta: 1–15. doi: 10.1111/zsc.12392Google Scholar
Luo, A., Ling, C., Ho, S. Y., and Zhu, C. (2018) Comparison of methods for molecular species delimitation across a range of speciation scenarios. Systematic Biology 67: 830–846. doi: 10.1093/sysbio/syy011/4866060Google Scholar
Maan, M. E., Hofker, K. D., van Alphen, J. J. M., and Seehausen, O. (2006) Sensory drive in cichlid speciation. American Naturalist 167: 947–954.Google Scholar
Macher, J. N., Weiss, M., Beermann, A. J., and Leese, F. (2016) Cryptic diversity and population structure at small scales: the freshwater snail Ancylus (Planorbidae, Pulmonata) in the Montseny mountain range. Annales de Limnologie (International Journal of Limnology) 52: 387–399. doi: 10.1051/limn/2016026Google Scholar
Mallet, J. and Gilbert, L. E. (1995) Why are there so many mimicry rings? Correlations between habitat, behaviour and mimicry in Heliconius butterflies. Biological Journal of the Linnean Society 55: 159–180.Google Scholar
Marsteller, S., Adams, D. C., Collyer, M. L., and Condon, M. (2009) Six cryptic species on a single species of host plant: Morphometric evidence for possible reproductive character displacement. Ecological Entomology 34: 66–73. doi: 10.1111/j.1365-2311.2008.01047.xGoogle Scholar
Mayden, R. L. (1997) A hierarchy of species concepts: The denouement in the saga of the species problem. In: Claridge, M.F., Dawah, H. A., and Wilson, M. R. (eds.) Species: The Units of Biodiversity. Chapman and Hall, London, pp. 381–423.Google Scholar
Mayer, F. and Von Helversen, O. (2001) Sympatric distribution of two cryptic bat species across Europe. Biological Journal of the Linnean Society 74: 365–374. doi: 10.1006/bijl.200l.0586Google Scholar
Mayer, F., Dietz, C., and Kiefer, A. (2007) Molecular species identification boosts bat diversity. Frontiers in Zoology 4: 4. doi: 10.1186/1742-9994-4-4Google Scholar
Mayr, E. (1942) Systematics and the Origin of Species from the Viewpoint of Zoologist. Harvard University Press, Cambridge, MA, 337 pp.Google Scholar
Meyer-Rochow, V. B. (1991) Differences in ultraviolet wing patterns in the New Zealand lycaenid butterflies Lycaena salustius, L. rauparaha, and L. feredayi as a likely isolating mechanism. Journal of the Royal Society of New Zealand 21: 169–177. doi: 10.1080/03036758.1991.10431405Google Scholar
Mielewczik, M., Leibisch, F., Walter, A., and Greven, H. (2012) Near-Infrared (NIR) reflectance in insects: Phenetic studies of 181 species. Entomologie Heute 24: 183–215.Google Scholar
Molbo, D., Machado, C. A., Sevenster, J. G., Keller, L., and Herre, E. A. (2003). Cryptic species of fig-pollinating wasps: Implications for the evolution of the fig-wasp mutualism, sex allocation, and precision of adaptation. Proceedings of the National Academy of Sciences of the United States of America 100: 5867–5872.Google Scholar
Montero-Pau, J. and Serra, M. (2011) Life-cycle switching and coexistence of species with no niche differentiation. PloS ONE 6: e20314. doi: 10.1371/journal.pone.0020314Google Scholar
Montero-Pau, J., Ramos-Rodríguez, E., Serra, M., and Gómez, A. (2011) Long-term coexistence of rotifer cryptic species. PloS ONE 6: e21530. doi: 10.1371/journal.pone.0021530Google Scholar
Morinière, J., Hendrich, L., Balke, M. et al. (2017) A DNA barcode library for Germany′s mayflies, stoneflies and caddisflies (Ephemeroptera, Plecoptera and Trichoptera). Molecular Ecology Resources 17: 1293–1307. doi: 10.1111/1755-0998.12683Google Scholar
Morris, D. W. (2003) Toward an ecological synthesis: A case for habitat selection. Oecologia 136: 1–13. doi: 10.1007/s00442-003-1241-4Google Scholar
Moskalik, B. and Uetz, G. W. (2011) Experience with chemotactile cues indicating female feeding history impacts male courtship investment in the wolf spider Schizocosa ocreata. Behavioral Ecology and Sociobiology 65: 2175–2181. doi: 10.1007/s00265-011-1225-zGoogle Scholar
Naisbit, R. E., Jiggins, C. D., and Mallet, J. (2001) Disruptive sexual selection against hybrids contributes to speciation between Heliconius cydno and Heliconius melpomene. Proceedings of the Royal Society B 268: 1849–1854. doi: 10.1098/rspb.2001.1753Google Scholar
Nosil, P. (2012) Ecological Speciation. Oxford Series in Ecology and Evolution, Oxford, 300pp.Google Scholar
Obara, Y., Watanabe, K., and Satoh, T. (2010) UV reflectance of inter-subspecific hybrid females obtained by crossing cabbage butterflies from Japan (Pieris rapae crucivora) with those from New Zealand (P . rapae rapae). Entomological Science 13: 156–158. doi: 10.1111/j.1479-8298.2010.00364.xGoogle Scholar
Olds, B. P., Jerde, C. L., Renshaw, M. A. et al. (2016) Estimating species richness using environmental DNA. Ecology and Evolution 6: 1–13. doi: 10.1002/ece3.2186Google Scholar
Onda-Sumi, E. (2005) Difference in calling song of three field crickets of the genus Teleogryllus: The role in premating isolation. Animal Behaviour 69: 881–889. doi: 10.1016/j.anbehav.2004.05.015CrossRefGoogle Scholar
Padial, J. M., Miralles, A., De la Riva, I., and Vences, M. (2010) The integrative future of taxonomy. Frontiers in Zoology 7: 16. doi: 10.1186/1742-9994-7-16Google Scholar
Pante, E., Schoelinck, C., and Puillandre, N. (2015) From integrative taxonomy to species description: One step beyond. Systematic Biology 64: 152–160. doi: 10.1093/sysbio/syu083Google Scholar
Park, K. J., Altringham, J. D., and Jones, G. (1996) Assortative roosting in the two phonic types of Pipistrellus pipistrellus during the mating season. Proceedings of the Royal Society B 263: 1495–1499. doi: 10.1098/rspb.1996.0218Google Scholar
Pecháček, P., Stella, D., and Kleisner, K. (2019) A morphometric analysis of environmental dependences between ultraviolet patches and wing venation patterns in Gonepteryx butterflies (Lepidoptera, Pieridae). Evolutionary Ecology 33: 89–110. doi: 10.1007/s10682-019-09969-0Google Scholar
Pérez-Ponce de León, G. and Poulin, R. (2016) Taxonomic distribution of cryptic diversity among metazoans: Not so homogeneous after all. Biology Letters 12: 20160371. doi: 10.1098/rsbl.2016.0371Google Scholar
Pfenninger, M. and Schwenk, K. (2007) Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evolutionary Biology 7: 121. doi: 10.1186/1471-2148-7-121Google Scholar
Pons, J., Barraclough, T., Gomez-Zurita, J. et al. (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55: 595–609. doi: 10.1080/10635150600852011Google Scholar
Powell, T. H. Q., Cha, D. H., Linn, C. E., and Feder, J. L. (2012) On the scent of standing variation for speciation: Behavioral evidence for native sympatric host races of Rhagoletis pomonella (Diptera: Tephritidae) in the southern United States. Evolution 66: 2739–2756. doi: 10.1111/j.1558-5646.2012.01625.xGoogle Scholar
Raxworthy, C., Ingram, C., Rabibisoa, N., and Pearson, R. (2007) Applications of ecological niche modeling for species delimitation: A review and empirical evaluation using day geckos (Phelsuma) from Madagascar. Systematic Biology 56: 907–923. doi: 10.1080/10635150701775111Google Scholar
Renner, S. S. (2016) A return to Linnaeus’s focus on diagnosis, not description: The use of DNA characters in the formal naming of species. Systematic Biology 65: 1086–1095. doi: 10.1093/sysbio/syw032Google Scholar
Roberts, R. E. W. and Uetz, G. W. (2005) Information content of female chemical signals in the wolf spider, Schizocosa ocreata: Male discrimination of reproductive state and receptivity. Animal Behaviour 70: 217–223. doi: 10.1016/j.anbehav.2004.09.026Google Scholar
Rodríguez, R. L., Ramaswamy, K., and Cocroft, R. B. (2006) Evidence that female preferences have shaped male signal evolution in a clade of specialized plant-feeding insects. Proceedings of the Royal Society B 273: 2585–2593. doi: 10.1098/rspb.2006.3635CrossRefGoogle Scholar
Rodríguez, R. L., Sullivan, L. E., and Cocroft, R. B. (2004) Vibrational communication and reproductive isolation in the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae). Evolution 58: 571–578. doi: 10.1111/j.0014-3820.2004.tb01679.xGoogle Scholar
Russo, D. and Jones, G. (2000) The two cryptic species of Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) occur in Italy: Evidence from echolocation and social calls. Mammalia 64: 187–197. doi: 10.1515/mamm.2000.64.2.187Google Scholar
Rutowski, R. L. and Rajyaguru, P. K. (2013) Male-specific iridescent coloration in the pipevine swallowtail (Battus philenor) is used in mate choice by females but not sexual discrimination by males. Journal of Insect Behavior 26: 200–211. doi: 10.1007/s10905-012-9348-2Google Scholar
Scheffer, M. and van Nes, E. H. (2006) Self-organized similarity, the evolutionary emergence of groups of similar species. Proceedings of the National Academy of Sciences of the United States of America 103: 6230–6235. doi: 10.1073/pnas.0508024103Google Scholar
Schuchmann, M. and Siemers, B. M. (2010) Behavioral evidence for community-wide species discrimination from echolocation calls in bats. American Naturalist 176: 72–82. doi: 10.1086/652993Google Scholar
Schluter, D. (2009) Evidence for ecological speciation and its alternative. Science 323: 737–741. doi: 10.1126/science.1160006Google Scholar
Scriven, J. J., Whitehorn, P. R., Goulson, D., and Tinsley, M. C. (2016) Niche partitioning in a sympatric cryptic species complex. Ecology and Evolution 6: 1328–1339. doi: 10.1002/ece3.1965Google Scholar
Seehausen, O., Terai, Y., Magalhaes, I. S. et al. (2008) Speciation through sensory drive in cichlid fish. Nature 455: 620–626. doi: 10.1038/nature07285Google Scholar
Servedio, M. R. and Boughman, J. W. (2017) The role of sexual selection in local adaptation and speciation. Annual Review of Ecology and Systematics 48: 85–109. doi: 10.1146/annurev-ecolsys-110316-022905Google Scholar
Shinen, J. L. and Navarrete, S. A. (2014) Lottery coexistence on rocky shores: Weak niche differentiation or equal competitors engaged in neutral dynamics? The American Naturalist 183: 342–362. doi: 10.1086/674898Google Scholar
Siemers, B. M. and Schnitzler, H.-U. (2004) Echolocation signals reflect niche differentiation in five sympatric congeneric bat species. Nature 429: 657–661.Google Scholar
Siepielski, A. M. and McPeek, M. A. (2010) On the evidence for species coexistence: A critique of the coexistence program. Ecology 91: 3153–3164. doi: 10.1890/10-0154.1Google Scholar
Silberglied, R. and Taylor, O. (1973) Ultraviolet differences between the sulphur butterflies, Colia eurytheme and C. philodice, and a possible isolating mechanism. Nature 241: 406–408. doi: 10.1038/246421a0Google Scholar
Sites, J. W. and Marshall, J. C. (2003) Delimiting species: A Renaissance issue in systematic biology. Trends in Ecology and Evolution 18: 462–470. doi: 10.1016/S0169-5347(03)00184-8Google Scholar
Sites, J. W. and Marshall, J. C. (2004) Operational criteria for delimiting species. Annual Review of Ecology, Evolution, and Systematics 35: 199–227. doi: 10.1146/annurev.ecolsys.35.112202.130128Google Scholar
Smadja, C. and Butlin, R. K. (2009) On the scent of speciation: The chemosensory system and its role in premating isolation. Heredity 102: 77–97. doi: 10.1038/hdy.2008.55Google Scholar
Smotherman, M., Knörnschild, M., Smarsh, G., and Bohn, K. (2016) The origins and diversity of bat songs. Journal of Comparative Physiology A 202: 535–554. doi: 10.1007/s00359-016-1105-0Google Scholar
Soares, D. and Niemiller, M. L. (2013) Sensory adaptations of fishes to subterranean environments. BioScience 63: 274–283. doi: 10.1525/bio.2013.63.4.7Google Scholar
Stella, D., Pecháček, P., Meyer-Rochow, V. B., and Kleisner, K. (2018) UV reflectance is associated with environmental conditions in Palaearctic Pieris napi (Lepidoptera: Pieridae). Insect Science 25: 508–518. doi: 10.1111/1744-7917.12429Google Scholar
Stella, D., Rindoš, M., Kleisner, K., and Pechá, P. (2018) Distribution of ultraviolet ornaments in Colias butterflies (lepidoptera : pieridae). Environmetal Entomology 47: 1344–1354. doi: 10.1093/ee/nvy111Google Scholar
Stevens, M. (2013) Sensory Ecology, Behavior, and Evolution. Oxford University Press, Glasgow, 260 pp.Google Scholar
Struck, T. H., Feder, J. L., Bendiksby, M. et al. (2018) Finding evolutionary processes hidden in cryptic species. Trends in Ecology and Evolution 33: 153–163. doi: 10.1016/j.tree.2017.11.007Google Scholar
Tang, C. Q., Humphreys, A., Fontaneto, D., and Barraclough, T. G. (2014) Effects of phylogenetic reconstruction method on the robustness of species delimitation using single locus data. Methods in Ecology and Evolution 5: 1086–1094. doi: 10.1111/2041-210X.12246Google Scholar
Tovée, M. J. (1995) Ultra-violet photoreceptors in the animal kingdom: Their distribution and function. Trends in Ecology and Evolution 10: 455–460. doi: 10.1016/S0169-5347(00)89179-XGoogle Scholar
Uetz, G. W. and Roberts, J. A. (2002) Multisensory cues and multimodal communication in spiders: Insights from video/audio playback studies. Brain, Behavior and Evolution 59: 222–230.Google Scholar
Uetz, G. W. Roberts, J. A., Clark, D. L., Gibson, J. S., and Gordon, S. D. (2013) Multimodal signals increase active space of communication by wolf spiders in a complex litter environment. Behavioral Ecology and Sociobiology 67: 1471–1482. doi: 10.1007/s00265-013-1557-yGoogle Scholar
von Uexküll, J. J. (1956) Streifzüge durch die Umwelten von Tieren und Menschen/Bedeutungslehre. Reprint. Rowohlt, Hamburg, 182 pp.Google Scholar
Veech, J. A. (2013) A probabilistic model for analysing species co-occurrence. Global Ecology and Biogeography 22: 252–260. doi: 10.1111/j.1466-8238.2012.00789.xGoogle Scholar
Veech, J. A. (2014) The pairwise approach to analysing species co-occurrence. Journal of Biogeography 41: 1029–1035. doi: 10.1111/jbi.12318Google Scholar
Vickers, N. J. (2002) Defining a synthetic pheromone blend attractive to male Heliothis subflexa under wind tunnel conditions. Journal of Chemical Ecology 28: 1255–1267.Google Scholar
Voda, R., Dapporto, L., Dinca, V., and Vila, R. (2015a) Why do cryptic species tend not to co-occur? A case study on two cryptic pairs of butterflies. PLoS ONE 10: e0117802. doi: 10.1371/journal.pone.0117802Google Scholar
Voda, R., Dapporto, L., Dinca, V., and Vila, R. (2015b) Cryptic matters: Overlooked species generate most butterfly beta-diversity. Ecography 38: 405–409. doi: 10.1111/ecog.00762Google Scholar
Warren, D. L., Cardillo, M., Rosauer, D. F., and Bolnick, D. I. (2014) Mistaking geography for biology: Inferring processes from species distributions. Trends in Ecology and Evolution 29: 572–580. doi: 10.1016/j.tree.2014.08.003Google Scholar
Wellborn, G. A. and Cothran, R. D. (2004) Phenotypic similarity and differentiation among sympatric cryptic species in a freshwater amphipod species complex. Freshwater Biology 49: 1–13.Google Scholar
Wellborn, G. A. and Cothran, R. D. (2007) Niche diversity in crustacean cryptic species: Complementarity in spatial distribution and predation risk. Oecologia 154: 175–183. doi: 10.1007/s00442-007-0816-xGoogle Scholar
Wilkins, M. R., Seddon, N., and Safran, R. J. (2013) Evolutionary divergence in acoustic signals: Causes and consequences. Trends in Ecology & Evolution 28: 156–166. doi: 10.1016/j.tree.2012.10.002Google Scholar
Yeates, D. K., Seago, A., Nelson, L. et al. (2011) Integrative taxonomy, or iterative taxonomy? Systematic Entomology 36: 209–217. doi: 10.1111/j.1365-3113.2010.00558.xGoogle Scholar
Yen, J. and Lasley, R. (2010) Chemical communication between copepods: Finding the mate in a fluid environment. In: Breithaupt, T. and Thiel, M. (eds.) Chemical Communication in Crustaceans. Springer, New York, pp. 177–198. doi: 10.1007/978-0-387-77101-4Google Scholar
Zettler, M. L., Proffitt, C. E., Darr, A. et al. (2013) On the myths of indicator species: Issues and further consideration in the use of static concepts for ecological applications. PLoS ONE 8: e78219. doi: 10.1371/journal.pone.0078219Google Scholar
Zhang, D. Y., Lin, K., and Hanski, I. (2004) Coexistence of cryptic species. Ecology Letters 7: 165–169. doi: 10.1111/j.1461-0248.2004.00569.xGoogle Scholar
Zhang, J., Kapli, P., Pavlidis, P., and Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29: 2869–2876. doi: 10.1093/bioinformatics/btt499Google Scholar

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