Abstract
Current knowledge of “micronetine” female genitalia is almost exclusively based on transmitted light microscopy data. As such, our understanding of the epigynal anatomy is incomplete and somewhat misleading, to the extent that it hinders comparative studies of linyphiid diversity. We used scanning electronic microscopy (SEM) to study the complex epigynal morphology of “micronetine” spiders. Enzymatic digestion of soft tissues allowed us to examine the internal chitinized structures in detail using SEM. A taxonomic sample of nine species was selected to represent the morphological genitalic diversity of female “micronetines” (including one member of the Erigoninae clade). Results reveal that the epigynum consists of a pair of grooves formed by integument folds (copulatory and fertilization grooves). The protruding epigynal region is divided into a ventral and a dorsal plate by the grooves; both plates can be modified to form an epigynal cavity and/or a scape. Our observations confirm the widespread occurrence of epigynal grooves, rather than ducts, in “micronetines”. Epigynal grooves seem to be common in linyphioids and other spider groups.
Similar content being viewed by others
References
Agnarsson I (2004) Morphological phylogeny of cobweb spiders and their relatives (Araneae, Araneoidea, Theridiidae). Zool J Linn Soc 141:447–626. doi:10.1111/j.1096-3642.2004.00120.x
Álvarez-Padilla F (2007) Systematics of the spider genus Metabus O. P.-Cambridge, 1899 (Araneoidea: Tetragnathidae) with additions to the tetragnathid fauna of Chile and comments on the phylogeny of Tetragnathidae. Zool J Linn Soc 151:285–335. doi:10.1111/j.1096-3642.2007.00304.x
Álvarez-Padilla F, Hormiga G (2008) A protocol for digesting internal soft tissues and mounting spiders for scanning electron microscopy. J Arachnol 35:538–542. doi:10.1636/Sh06-55.1
Arnedo M, Hormiga G, Scharff N (2009) Higher level phylogenetics of linyphiid spiders (Araneae, Linyphiidae) based on morphological and molecular evidence. Cladistics. doi:10.1111/j.1096-0031.2009.00249.x
Berendonck B, Greven H (2000) Morphology of female and male genitalia of Latrodectus revivensis Shulov, 1948 (Araneae, Theridiidae) with regard to sperm priority patterns. Eur Arachnol 15:7–167
Berendonck B, Greven H (2005) Genital structures in the entelegyne widow spider Latrodectus revivensis (Arachnida; Araneae; Theridiidae) indicate a low ability for cryptic female choice by sperm manipulation. J Morphol 263:118–132. doi:10.1002/jmor.10296
Blauvelt HH (1936) The comparative morphology of the secondary sexual organs of Linyphia and some related genera, including a revision of the group. Festschr Strand 2:81–171
Coddington JA (1983) A temporary slide mount allowing precise manipulation of small structures. In: Kraus O (ed) Taxonomy, biology, and ecology of Araneae and Myriapoda. Verh naturwiss Ver Hamburg 26:291–292
Coddington JA (1986) The genera of the spider family Theridiosomatidae. Smithson Contrib Zool 422:1–96
Coddington JA (1990) Ontogeny and homology in the male palpus of orb weaving spiders and their relatives, with comments on phylogeny (Araneoclada: Araneoidea, Deinopoidea). Smithson Contrib Zool 496:1–52
Coddington JA (2005) Phylogeny and Classification of Spiders. In: Ubick D, Paquin P, Cushing PE, Roth V (eds) Spiders of North America: an identification manual. Chap. 2, pp 18–24
Coddington JA, Levi HW (1991) Systematics and evolution of spiders (Araneae). Annu Rev Ecol Syst 22:565–592. doi:10.1146/annurev.es.22.110191.003025
Eberhard WG (1985) Sexual selection and animal genitalia. Harvard University Press, Cambridge
Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton
Eberhard WG (2004a) Why study spider sex: special traits of spiders facilitate studies of sperm competition and cryptic female choice. J Arachnol 32:545–556. doi:10.1636/0161-8202(2004)032[0545:WSSSST]2.0.CO;2
Eberhard WG (2004b) Rapid divergent evolution of sexual morphology: comparative tests of antagonistic coevolution and traditional female choice. Evolution Int J Org Evolution 58(9):1947–1970
Engelhardt V (1910) Beiträge zur Kenntnis der weiblichen Copulationsorgane einiger. Spinnen Z Wiss Zool 96:32–117
Foelix RF (1996) Biology of spiders, 2nd edn. Oxford University Press, New York
Forster RR (1980) Evolution of the tarsal organ, the respiratory system and the female genitalia in spiders. Verh int arachnol Kong 8:269–284 (Wien, 1980)
Grandjean F (1949) Observation et conservation des très petits arthropodes. Bull Mus Nat Hist Nat Paris 21:363–370
Griswold CE (1990) A revision and phylogenetic analysis of the spider subfamily Phyxelidinae (Araneae, Amaurobiidae). Bull Am Mus Nat Hist 196:1–206
Griswold CE (1997) The spider family Cyatholipidae in Madagascar (Araneae, Araneoidea). J Arachnol 25:53–83
Griswold CE, Ubick D (2001) Zoropsidae: a spider family newly introduced to the USA (Araneae, Entelegynae, Lycosoidea). J Arachnol 29:111–113. doi:10.1636/0161-8202(2001)029[0111:ZASFNI]2.0.CO;2
Griswold CE, Coddington JA, Hormiga G, Scharff N (1998) Phylogeny of the orb web building spiders (Araneomorphae, Orbiculariae: Deinopoidea, Araneoidea). Zool J Linn Soc 123:1–99. doi:10.1111/j.1096-3642.1998.tb01290.x
Griswold CE, Ramírez MJ, Coddington JA, Platnick NI (2005) Atlas of phylogenetic data for entelegyne spiders (Araneae: Araneomorphae: Entelegynae) with comments on their phylogeny. Proc Calif Acad Sci 56(Suppl II):1–324
Holm Å (1979) A taxonomic study of European and East African species of the genera Pelecopsis and Trichopterna (Araneae, Linyphiidae), with descriptions of a new genus and two new species of Pelecopsis from Kenya. Zool Scr 8:255–278. doi:10.1111/j.1463-6409.1979.tb00638.x
Hormiga G (1994) Cladistics and the comparative morphology of linyphiid spiders and their relatives (Araneae, Araneoidea, Linyphiidae). Zool J Linn Soc 111:1–71. doi:10.1111/j.1096-3642.1994.tb01491.x
Hormiga G (2000) Higher level phylogenetics of erigonine spiders (Araneae, Linyphiidae, Erigoninae). Smithson Contrib Zool 609:1–160
Hormiga G (2002) Orsonwelles, a new genus of giant linyphiid spiders (Araneae) from the Hawaiian Islands. Invertebr Syst 16:369–448. doi:10.1071/IT01026
Hormiga G, Scharff N (2005) Monophyly and phylogenetic placement of the spider genus Labulla Simon, 1884 (Araneae, Linyphiidae) and description of the new genus Pecado. Zool J Linn Soc 143:359–404. doi:10.1111/j.1096-3642.2005.00147.x
Hormiga G, Tu L (2008) On Putaoa, a new genus of the spider family Pimoidae (Araneae) from China, with a cladistic test of its monophyly and phylogenetic placement. Zootaxa 1792:1–21
Huber BA (1993) Genital mechanics and sexual selection in the spider Nesticus cellulanus (Araneae: Nesticidae). Can J Zool 71:2437–2447. doi:10.1139/z93-340
Huber BA (2004) Evolutionary transformation from muscular to hydraulic movements in spider (Arachnida, Araneae) genitalia: a study based on histological serial sections. J Morphol 26:364–376. doi:10.1002/jmor.10255
Huber BA (2005a) Sexual selection research on spiders: progress and biases. Biol Rev Camb Philos Soc 80:363–385. doi:10.1017/S1464793104006700
Huber BA (2005b) High species diversity, male–female coevolution, and metaphyly in Southeast Asian pholcid spiders: the case of Belisana Thorell 1898 (Araneae, Pholcidae). Zool 155:1–126
Huber BA (2006) Cryptic female exaggeration: the asymmetric female internal genitalia of Kaliana yuruani (Araneae: Pholcidae). J Morphol 267:705–712. doi:10.1002/jmor.10431
Kuntner M, Hormiga G (2002) The African spider genus Singafrotypa (Araneae, Araneidae). J Arachnol 30:129–139. doi:10.1636/0161-8202(2002)030[0129:TASGSA]2.0.CO;2
Kuntner M, Coddington JA, Hormiga G (2008) Phylogeny of extant nephilid orb-weaving spiders (Araneae, Nephilidae): testing morphological and ethological homologies. Cladistics 24:147–217. doi:10.1111/j.1096-0031.2007.00176.x
Kuntner M, Coddington JA, Schneider JM (2009) Intersexual arms race? Genital coevolution in nephilid spiders (Araneae, Nephilidae). Evolution Int J Org Evolution. doi:10.1111/j.1558-5646.2009.00634.x
Lopardo L, Hormiga G (2007) On the Synaphrid Spider Cepheia longiseta (Simon 1881) (Araneae, Synaphridae). Am Mus Novit 3575:1–18. doi:10.1206/0003-0082(2007)3575[1:OTSSCL]2.0.CO;2
Miller JA (2007) Review of Erigonine Spider genera in the Neotropics (Araneae: Linyphiidae, Erigoninae). Zool J Linn Soc 149(Suppl. 1):1–263. doi:10.1111/j.1096-3642.2007.00233.x
Miller JA, Hormiga G (2004) Clade stability and the addition of data-a case study from Erigonine Spiders (Araneae: Linyphiidae, Erigoninae). Cladistics 20:385–442. doi:10.1111/j.1096-0031.2004.00033.x
Millidge AF (1984) The taxonomy of the Linyphiidae, based chiefly on the epigynal and tracheal characters (Araneae: Linyphiidae). Bull Br Arachnol Soc 6:229–267
Millidge AF (1993) Further remarks on the taxonomy and relationships of the Linyphiidae, based on the epigynal duct conformation and other characters. Bull Br Arachnol Soc 9:145–156
Opell BD (1983) The female genitalia of Hyptiotes cavatus (Araneae: Uloboridae). Trans Am Microsc Soc 102:97–104. doi:10.2307/3225878
Platnick NI (2009) The world spider catalog (version 9.5). American Museum of Natural History. online at http://research.amnh.org/entomology/spiders/catalog/INTRO1.html
Ramos M, Coddington JA, Christenson TE, Irschick DJ (2005) Have male and female genitalia coevolved? A phylogenetic analysis of genitalic morphology and sexual size dimorphism in web-building spiders (Araneae: Araneoidea). Evolution Int J Org Evolution 59:1989–1999
Ruiz GRS, Brescovit AD (2008) Revision of Helvetia (Araneae: Salticidae: Heliophaninae). Rev Brasilera Zool 25:139–147
Saaristo MI (1971) Revision of the genus Maro O. P.-Cambridge (Araneae, Linyphiidae). Ann Zool Fenn 8:463–482
Saaristo MI (1972) Redelimitation of the genus Oreonetides Strand, 1901 (Araneae, Linyphiidae) based on an analysis of the genital organs. Ann Zool Fenn 9:69–74
Saaristo MI (1975) On the evolution of the secondary genital organs of Lepthyphantinae (Araneae, Linyphiidae). In: Proceedings of 6th international arachnological Congress, pp 21–25
Saaristo MI (1977) Secondary genital organs in the taxonomy of Lepthyphantinae (Araneae, Linyphiidae). Rep Dept Zool Univ Turku 5:1–16
Saaristo MI, Tanasevitch AV (1996) Redelimitation of the subfamily Micronetinae Hull, 1920 and the genus Lepthyphantes Menge, 1866 with descriptions of some new genera. Ber naturwiss-med Ver Innsb 83:163–186
Scharff N, Coddington JA (1997) A phylogenetic analysis of the orb weaving spider family Araneidae (Arachnida, Araneae). Zool J Linn Soc 120:355–434. doi:10.1111/j.1096-3642.1997.tb01281.x
Sierwald P (1989) Morphology and ontogeny of female copulatory organs in American Pisauridae, with special reference to homologous features (Arachnida: Araneae). Smithson Contrib Zool 484:1–24
Uhl G (2000) Female genital morphology and sperm priority patterns in spiders (Araneae). In: Toft S, Scharff N (eds) European Arachnology 2000. Aarhus University Press, Aarhus, pp 145–156
Uhl G, Gunnarsson B (2001) Female genitalia in Pityohyphantes phrygianus, a spider with a skewed sex ratio. J Zool (Lond) 255:367–376. doi:10.1017/S0952836901001467
van Helsdingen PJ (1965) Sexual behaviour of Lepthyphantes leprosus (Ohlert) (Araneida, Linyphiidae), with notes on the function of the genital organs. Zool Meded Leiden 41:15–42
van Helsdingen PJ (1969) A reclassification of the species of Linyphia Latreille, based on the functioning of the genitalia (Araneida, Linyphiidae) I. Zool Verh Leiden 105:1–303
Wang X (2002) A generic-level revision of the spider subfamily Coelotinae (Araneae, Amaurobiidae). Bull Am Mus Nat Hist 269:1–150. doi:10.1206/0003-0090(2002)269<0001:AGLROT>2.0.CO;2
Wanless FR (1972) The female genitalia of the spider genus Lepthyphantes (Linyphiidae) I. Bull Br Arachnol Soc 2:20–28
Wanless FR (1973) The female genitalia of British spiders of the genus Lepthyphantes (Linyphiidae) II. Bull Br Arachnol Soc 2:127–142
Acknowledgments
We would like to thank Jinzhong Fu for his help in the development of the ideas expressed in this study and Martín J. Ramírez, Dimitar Dimitrov, Jeremy Miller and two anonymous reviewers for their comments on an earlier version of this paper. We also want to thank Lara Lopardo and Fernando Álvarez-Padilla for their help with the preparation of specimens for SEM. The following individuals and institutions kindly loaned specimens for this study: Shuqiang Li (Institute of Zoology, Chinese Academy of Sciences in Beijing, China, IZCAS), Norman Platnick and Louis Sorkin (American Museum of Natural History, New York, AMNH). We would like to thank the late Michael Saaristo for help and for many fruitful discussions on linyphiid genitalia. Funding for this research has been provided by National Natural Sciences Foundation, China (NSFC-30670244), the Scientific Research Common Program of Beijing Municipal Commission of Education, China (KM200610028008), and a Collection Study Grant from the American Museum of Natural History to L. Tu, by a U.S. National Science Foundation grant (DEB-0328644) to G. Hormiga and G. Giribet, by Research Enhancement Fund and Selective Excellence grants from The George Washington University to G. Hormiga, and by an ATOL grant from the U.S. National Science Foundation (EAR-0228699) to W. Wheeler, J. Coddington, G. Hormiga, L. Prendini and P. Sierwald.
Author information
Authors and Affiliations
Corresponding author
Appendix
Appendix
Specimen data of the species examined. Museum abbreviations: CNU—Capital Normal University, Beijing; IZCAS—Institute of Zoology, Chinese Academy of Sciences, Beijing; AMNH—American Museum of Natural History, New York.
-
Lepthyphantes minutus (Blackwall, 1833)—1 m and 1 fm, Finland, Sundholm, Houtskari, Aug. 24-Oct. 24, 1968, Lehtinen coll. (IZCAS)
-
Arcuphantes arcuatus (Roewer, 1942)—1 fm, USA, Oregon, Sixes (1 mile north), W124.30:N42.51, Sept. 30, 1959, Vincent Roth coll. (AMNH)
-
Bifurcia ramosa (Li and Zhu, 1987)—2 m and 3 fm, China, Prov. Sichuan, Count Tianquan, Erlangshan National Forest Park, July 8, 2004, Tu and Li coll. (IZCAS)
-
Drapetisca alteranda Chamberlin, 1909—4 m and 4 fm, USA, Ontario, Island 1024, Lake Temagami, W80.03, N46.59, Aug. 15–25, 1946, Gertsch coll. (AMNH)
-
Drapetisca socialis (Sundevall, 1833)—2 m and 2 fm, Finland, Mustfinnö, Parainen, Sept. 1968, Saaristo coll. (IZCAS)
-
Erigone atra (Blackwall, 1833)—2 m and 4 fm, China, Xinjiang Uygur Autonomous Region, Burgin County, Kirzlesu River, Alt. 469 m, E86.50, N47.41, Sept. 20 2007, Tu and Chen coll. (CNU)
-
Mansuphantes fragilis (Thorell, 1875)—1 m and 1 fm, France, Bishop coll. (no detailed locality and collecting data) (AMNH)
-
Meioneta rurestris (C. L. Koch, 1836)—2 m and 2 fm, Germany, Torfstgebiet, Haidgauer, Wurzacher Ried, MTB 8025, July 22, 1992, WJ coll. (IZCAS)
-
Helophora insignis (Blackwall, 1841)—2 m and 2 fm, Canada, Alberta, 10 miles N·W. of Whitecourt, W115.47, N54.15, Aug. 4, 1965, Ivie coll. (AMNH)
Rights and permissions
About this article
Cite this article
Tu, L., Hormiga, G. The female genitalic morphology of “micronetine” spiders (Araneae, Linyphiidae). Genetica 138, 59–73 (2010). https://doi.org/10.1007/s10709-009-9368-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10709-009-9368-9