Abstract
Crickets of the genus Endecous (Orthoptera: Grylloidea: Phalangopsidae) are frequently found in caves, in some cases presenting strictly subterranean lifestyle. In addition to the morphological diagnostic characters of the group, bioacoustic and karyotype, also help on delimiting species. Here, we describe two new sympatric species of this genus, which occur in the largest cave of Minas Gerais state, Brazil, using the morphology of phallic complex, the courtship song and karyotype. Moreover, we discuss the criteria used, the troglomorphisms for this genus, as well as hypothesis on the speciation process involving these species.
References
Acosta, R.C., Timm, V.F., Szinwelski, N., Costa, M.K.M. & Zefa, E. (2020) Mating behavior and acoustic communication of the long-legged cricket Endecous (Notendecous) onthophagus (Berg, 1891) from Southern Brazil (Orthoptera: Grylloidea: Phalangopsidae). Zootaxa, 4743 (3), 427–437.
https://doi.org/10.11646/zootaxa.4743.3.10
Alexander, R.D. (1962) Evolutionary change in cricket acoustical communication. Evolution, 16 (4), 443–467.
https://doi.org/10.2307/2406178
Alexander, R.D. & Otte, D. (1967) The evolution of genitalia and mating behavior in crickets (Gryllidae) and other Orthoptera. Miscellaneous Publications, 133, 1–62.
Alkmim F.F. & Martins-Neto M.A. (2001) A Bacia Intracratônica do São Francisco: Arcabouço estrutural e cenários evolutivos. In: Pinto, C.P. & Martins-Neto, M.A (Eds.), Bacia do São Francisco: Geologia e Recursos Naturais, Belo Horizonte, SBG-MG, 1, pp. 9–30.
Alvares, C.A., Stape, J.L., Sentelhas, P.C., Moraes, G., Leonardo, J. & Sparovek, G. (2013) Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift, 22 (6), 711–728.
https://doi.org/10.1127/0941-2948/2013/0507
Auler, A (2019) Histórico, ocorrência e potencial de cavernas no Brasil. In: Auler, A.S., Rubbioli, E., Menin, D. & Brandi, R. (Eds.), Cavernas, Atlas do Brasil Subterrâneo. Editora IABS, Brasília, pp. 14–51.
Benedix Jr., J.H. & Howard, D.J. (1991) Calling song displacement in a zone of overlap and hybridization. Evolution, 45, 1751–1759.
https://doi.org/10.2307/2409829
Bennet-Clark, H.C. (2003) Wing resonances in the Australian field cricket Teleogryllus oceanicus. Journal of Experimental Biology, 206 (9), 1479–1496.
https://doi.org/10.1242/jeb.00281
Bhattacharya, M., Isvaran, K. & Balakrishnan, R. (2017) A statistical approach to understanding reproductive isolation in two sympatric species of tree crickets. Journal of Experimental Biology, 220 (7), 1222–1232.
https://doi.org/10.1242/jeb.146852
Blankers, T., Hennig, R.M. & Gray, D.A. (2015) Conservation of multivariate female preference functions and preference mechanisms in three species of trilling field crickets. Journal of Evolutionary Biology, 28 (3), 630–641.
https://doi.org/10.1111/jeb.12599
Bolfarini, M.P. & Bichuette, M.E. (2015) Endecous peruassuensis n. sp. (Orthoptera: Grylloidea: Phalangopsidae) from caves of Eastern Brazil: evidence of isolation in the subterranean realm and discussion about troglomorphisms. Zootaxa, 4032 (3), 297–308.
https://doi.org/10.11646/zootaxa.4032.3.5
Bolnick, D.I. & Fitzpatrick, B.M. (2007) Sympatric speciation: models and empirical evidence. Annual Review of Ecology, Evolution, and Systematics, 38, 459–487.
https://doi.org/10.1146/annurev.ecolsys.38.091206.095804
Castro-Souza, R.A., Zefa, E. & Ferreira, R.L. (2017) Two new species of cave crickets Endecous (Notoendecous) Gorochov, 2014 (Orthoptera: Grylloidea: Phalangopsidae) from northeastern Brazil. Zootaxa, 4318 (3), 474–498.
https://doi.org/10.11646/zootaxa.4318.3.3
Christiansen, K., Culver, D.C., Howarth, F.G. & Wilkens, H. (1986) Speciation and adaptation to cave life: Gradual vs. rectangular evolution. Bollettino di Zoologia, 53 (Supplement 1), 11–14.
https://doi.org/10.1080/11250008609355535
Christiansen K. (1962) Proposition pour la classification des animaux cavernicoles. Spelunca, 2, 75–78.
Cigliano, M.M., Braun, H., Eades, D.C. & Otte, D. (2020) Orthoptera Species File. Version 5.0/5.0. Available from: http://Orthoptera.SpeciesFile.org (accessed 26 April 2020)
Deharveng L. & Bedos A. (2018) Diversity of Terrestrial Invertebrates in Subterranean Habitats. In: Moldovan, O. T., Kováč, Ľ. & Halse, S. (Ed.), Cave Ecology. Vol. 235. Springer, Cham, pp. 107–172.
https://doi.org/10.1007/978-3-319-98852-8_7
Desutter, L. (1987) Structure et évolution du complexe phallique des Gryllidea (Orthoptera) et classification des genres Nétropicaux de Grylloidea, Première Partie. Annales de la Sociét Entomolologique de France, 23 (3), 213–239.
Desutter, L. (1988) Structure et évolution du complexe phallique des Gryllidea (Orthoptèra) et classification des genres Nétropicaux de Grylloidea. Annales de la Sociét Entomolologique de France, 24, 343–373.
Desutter, L. (1990) Etude phylogénétique, biogéographique et écologique dês Gryllidea Neotropicaux (Insectes, Orthoptères). Doctoral Thesis, Université de Paris-Sud Centre d’Orsay, Paris, 347 pp.
Desutter-Grandcolas, L. (1993) The cricket fauna of Chiapanecan caves (Mexico): systematics, phylogeny and the evolution of troglobitic life (Orthoptera, Grylloidea, Phalangopsidae, Luzarinae). International Journal of Speleology, 22 (1), 1–82.
https://doi.org/10.5038/1827-806X.22.1.1
Desutter-Grandcolas, L. (1995) Nouveaux grillons cavernicoles de la région néotropicale (Orthoptera, Grylloidea, Phalangopsidae). Annales de la Société entomologique de France, 17, 97–106.
Desutter-Grandcolas, L. (1997) Studies in cave life evolution: a rationale for future theoretical developments using phylogenetic inference. Journal of Zoological Systematics and Evolutionary Research, 35, 23–31.
https://doi.org/10.1111/j.1439-0469.1997.tb00400.x
Desutter-Grandcolas, L. (1998) II—faune souterraine II. 4—Insecta, 56—Ortóptera, B—Grylloidea. In: Juberthie, C. & Decu, V. (Eds.), Encyclopaedia Biospeologica. v. Tome II. Société de Biospéologie, Moulis, pp. 989–1001.
Desutter-Grandcolas, L. (2003) Phylogeny and the evolution of acoustic communication in extant Ensifera (Insecta, Orthoptera). Zoologica Scripta, 32, 525–561
https://doi.org/10.1046/j.1463-6409.2003.00142.x
Di Russo & Sbordoni, V. (1998) II—Faune Souterraine II. 4—Insecta, 56—Ortóptera, A—Gryllacridoidea. In: Juberthie, C. & Decu, V. (Eds.), Encyclopaedia Biospeologica, v. Tome II. Société de Biospéologie, Moulis, pp. 979–987.
Diwakar, S. & Balakrishnan, R. (2007) Vertical stratification in an acoustically communicating ensiferan assemblage of a tropical evergreen forest in southern India. Journal of Tropical Ecology, 23 (4), 479–486.
https://doi.org/10.1017/s0266467407004208
Drosopoulos, S. & Claridge, M.F. (2005) Insect sounds and communication: physiology, behaviour, ecology, and evolution. CRC press, Boca Raton, Florida, 552 pp.
https://doi.org/10.1201/9781420039337
Ferreira, R.L., Martins, V.M., Paixão, E.A. & Silva, M.S. (2015) Spatial and temporal fluctuations of the abundance of Neotropical cave-dwelling moth Hypena sp. (Noctuidae, Lepidoptera) influenced by temperature and humidity. Subterranean Biology, 16, 47–60.
https://doi.org/10.3897/subtbiol.16.5137
Fianco, M., Souza-Dias, P.G.B., Farias-Martins, F., Magro, S., Prasniewski, V.M., Ricci, J., Zefa, E. & Szinwelski, N. (2018) Ethology of the cricket Endecous (Endecous) chape Souza-Dias & de Mello, 2017 (Orthoptera: Grylloidea: Phalangopsidae) I: Agonistic and reproductive behavior. Journal of Orthoptera Research, 27 (2), 193–201.
https://doi.org/10.3897/jor.27.29687
Ganem, R.S. (2009) As cavidades naturais subterrâneas e o Decreto nº 6.640/2008. Available from: http://bd.camara.gov.br/bd/handle/bdcamara/2522 (accessed 28 April 2019)
Glaubrecht, M. (2010) Evolution in action: Case studies in adaptive radiation, speciation and the origin of biodiversity. Springer, Berlin, Heidelberg, 586 pp.
https://doi.org/10.1007/978-3-642-12425-9
Gorochov, A.V. (2014) Classification of the Phalangopsinae subfamily group, and new taxa from the subfamilies Phalangopsinae and Phaloriinae (Orthoptera: Gryllidae). Zoosystematica Rossica, 23 (1), 7–88.
https://doi.org/10.31610/zsr/2014.23.1.7
Heads, S.W. (2010) The first fossil spider cricket (Orthoptera: Gryllidae: Phalangopsinae): 20 million years of troglobiomorphosis or exaptation in the dark?. Zoological Journal of the Linnean Society, 158 (1), 56–65.
https://doi.org/10.1111/j.1096-3642.2009.00587.x
Heller, K.G. (2006) Song evolution and speciation in bushcrickets. In: Drosopoulos, S. & Claridge, M.F. (Eds.), Insect sounds and communication. CRC Press, Boca Raton, Florida, pp. 137–151.
https://doi.org/10.1201/9781420039337.ch9
Hill, K.G., Loftus-Hills, J.J. & Gartside, D.F. (1972) Pre-mating isolation between the Australian field crickets Teleogryllus commodus and T. oceanicus (Orthoptera: Gryllidae). Australian Journal of Zoology, 20 (2), 153–163.
https://doi.org/10.1071/ZO9720153
Hödl, W. (1977) Call differences and calling site segregation in anuran species from Central Amazonian floating meadows. Oecologia, 28 (4), 351–363.
https://doi.org/10.1007/bf00345990
Honda-Sumi, E. (2005) Difference in calling song of three field crickets of the genus Teleogryllus: the role in premating isolation. Animal Behaviour, 69 (4), 881–889.
https://doi.org/10.1016/j.anbehav.2004.05.015
Levan, A., Fredga, K. & Sandberg, A.A. (1964) Nomenclature for centromeric position on chromosomes. Hereditas, 52, 201–220.
https://doi.org/10.1111/j.1601-5223.1964.tb01953.x
Lavoie, K.H., Helf, K.L. & Poulson, T.L. (2007) The biology and ecology of North American cave crickets. Journal of Cave and Karst Studies, 69 (1), 114–134. [https://caves.org/pub/journal/PDF/v69/cave-69-01-114.pdf]
Leroy, Y. (1965) Exemple d’ espèces cryptiques distinguéed par leurs émissions acoustiques (Teleogryllus commodus Walk., Teleogryllus oceanicus Lê Guillou, Gryllinae, Orthoptères Ensifères). Comptes Rendus Hebdomadaires Des Seances De L’Academie Des Sciences, 260, 5343–5346.
Mammola, S., Arnedo, M.A., Pantini, P., Piano, E., Chiappetta, N. & Isaia, M. (2018) Ecological speciation in darkness? Spatial niche partitioning in sibling subterranean spiders (Araneae: Linyphiidae: Troglohyphantes). Invertebrate Systematics, 32 (5), 1069–1082.
https://doi.org/10.1071/IS17090
Mello, F.A.G. & Pellegatti-Franco, F. (1998) A new cave cricket of the genus Endecous from southeastern Brazil and characterization of male and female genitália of E. itatibensis Rehn, 1918 (Orthoptera: Grylloidea: Phalangopsinae: Luzarinae). Journal of Orthoptera Research, 7, 185–188.
https://doi.org/10.2307/3503517
Mews, C.M. & Sperber, C.F. (2008) A new species of Endecous Saussure, 1878 and redescription of Endecous cavernicolus CostaLima, 1940 (Orthoptera: Grylloidea: Phalangopsidae). Studies on Neotropical Fauna and Environment, 43 (2), 159–167.
https://doi.org/10.1080/01650520701492389
Mousseau, T.A. & Howard, D.J. (1998) Genetic variation in cricket calling song across a hybrid zone between two sibling species. Evolution, 52 (4), 1104–1110.
https://doi.org/10.2307/2411240
Nosil, P. (2012) Ecological Speciation. Oxford University Press, Oxford, 280 pp.
https://doi.org/10.1093/acprof:osobl/9780199587100.001.0001
Otte, D. (1989) Speciation in Hawaiian crickets. In: Otte, D. & Endler, J. (Eds.), Speciation and Its Consequences. Sinauer, Sunderland, Massachusetts, pp. 482–526.
Otte, D. (1992) Evolution of cricket songs. Journal of Orthoptera Research, (1), 25–49.
https://doi.org/10.2307/3503559
Riesch, R., Plath, M. & Schlupp, I. (2011) Speciation in caves: experimental evidence that permanent darkness promotes reproductive isolation. Biology Letters, 7 (6), 909–912.
https://doi.org/10.1098/rsbl.2011.0237
Rundle, H.D. & Nosil, P. (2005) Ecological speciation. Ecology Letters, Series 8, 8, 336–352.
https://doi.org/10.1111/j.1461-0248.2004.00715.x
Saussure, H. (1877–1878) Mélanges Orthoptérologiques. Mémoires de la Société de Physique et D’ Histoire Naturelle de Geneve, VI Fascicule, Tome XXV, Seconde Partie, 1–705.
Smith, J.M. (1966) Sympatric speciation. The American Naturalist, 100 (916), 637–950.
https://doi.org/10.1086/282457
Souza-Dias, P.G.B., Bolfarini, M.P., Nihei, S.S. & de Mello, F.A.G. (2014) Endecous apterus: a new species of cave cricket from northeast Brazil, with comments on the use of subterranean habitats by Luzarinae crickets (Orthoptera: Grylloidea: Phalangopsidae: Luzarinae). Zootaxa, 3784 (2), 120–130.
https://doi.org/10.11646/zootaxa.3784.2.2
Souza-Dias, P.G.B. (2015) Análise cladística e morfologia do complexo fálico de Phalangopsidae, com ênfase em Luzarinae (Orthoptera, Ensifera, Grylloidea). Doctoral thesis, Instituto de Biociências da Universidade de São Paulo, São Paulo, 183 pp.
Souza-Dias, P.G.B., Szinwelski, N., Fianco M., De Oliveira, E.C., Mello, F.A.G. & Zefa, E. (2017) New species of Endecous (Grylloidea, Phalangopsidae, Luzarinae) from the Iguaçu National Park (Brazil), including bioacoustics, cytogenetic and distribution data. Zootaxa, 4237 (3), 454–470.
https://doi.org/10.11646/zootaxa.4237.3.2
Strecker, U., Hausdorf, B. & Wilkens, H. (2012) Parallel speciation in Astyanax cave fish (Teleostei) in Northern Mexico. Molecular Phylogenetics and Evolution, 62 (1), 62–70.
https://doi.org/10.1016/j.ympev.2011.09.005
Sueur, J. (2002) Cicada acoustic communication: potential sound partitioning in a multispecies community from Mexico. Biological Journal of the Linnean Society, 75 (3), 379–394.
https://doi.org/10.1111/j.1095-8312.2002.tb02079.x
Sueur, J. (2005) Insect Species and Their Songs. In: Drosopoulos, S. & Claridge, M.F. (Eds.), Insect sounds and communication. CRC Press, Boca Raton, Florida, pp. 207–217.
https://doi.org/10.1201/9781420039337.ch15
Taylor, E.B. & Donald-McPhail, J. (2000) Historical contingency and ecological determinism interact to prime speciation in sticklebacks, Gasterosteus. Proceedings of the Royal Society of London, 267 (1460), 2375–2384.
https://doi.org/10.1098/rspb.2000.1294
Tobler, M. (2009) Does a predatory insect contribute to the divergence between cave-and surface-adapted fish populations?. Biology Letters, 5 (4), 506–509.
https://doi.org/10.1098/rsbl.2009.0272
Walker T.J. (1980) Reproductive behavior and mating success of male short-tailed crickets: differences within and between demes. In: Hecht, M.K., Steere, W.C. & Wallace B. (Eds), Evolutionary Biology. Springer, Boston, pp. 219–260.
https://doi.org/10.1007/978-1-4615-6962-6_6
Walker, T.J. & Cooper, T.M. (2020) Singing Insects of North America (SINA). Available from: http://entnemdept.ifas.ufl.edu/walker/Buzz/ (accessed 27 May 2020)
Zefa, E. (2006) Comparison of calling songs in three allopatric populations of Endecous itatibensis (Orthoptera, Phalangopsinae). Iheringia Série Zoológica, 96 (1), 13–16.
https://doi.org/10.1590/s0073-47212006000100002
Zefa, E., Mesa, A. & Martins, L.D.P. (2010a) New Brazilian species of Endecous Saussure, 1878: Phallic sclerites, calling song and tegmen morphometry (Orthoptera: Grylloidea: Phalangopsinae). Entomological science, 13 (1), 150–155.
https://doi.org/10.1111/j.1479-8298.2010.00371.x
Zefa, E., Fontanetti, C.S. & Martins, L.D.P. (2010b) Cytotaxonomy of the crickets Endecous Saussure, 1878 with an overview of the chromosomes of Phalangopsinae Group (Orthoptera: Phalangopsinae). Zootaxa, 2498 (1), 53–58.
https://doi.org/10.11646/zootaxa.2498.1.4
Zefa, E., Redu, D.R., Costa, M.K.M., Gottschalk, M.S., Padilha, G.B., Silva, A.F. & Martins, L.P. (2014) A new species of Endecous Saussure, 1878 (Orthoptera, Gryllidae) from northeast Brazil with the first X1X20 chromosomal sex system in Gryllidae. Zootaxa, 3847 (1), 125–132.
https://doi.org/10.11646/zootaxa.3847.1.7
Zuk, M. & Simmons, L.W. (1997) Reproductive strategies of the crickets (Orthoptera: Gryllidae). In: Choe, J.C., & Crespi, B.J. (Eds.), The Evolution of Mating Systems in Insects and Arachnids. Cambridge University Press, Cambridge, pp. 89–109.
https://doi.org/10.1017/CBO9780511721946.006