Abstract
Mayflies (order Ephemeroptera) are primitive winged insects with a life cycle of aquatic nymphal development until emergence as adults that briefly fly seeking mates. Mayflies have reproductive morphology and strategies promoting efficient copulation and oviposition during the ephemeral terrestrial phase. The anatomy of the reproductive tract in males and females of Thraulodes latinus (Leptophlebiidae) is described in relation to the reproductive behavior of Ephemeroptera. Males have a pair of testes that are degenerate in the preadult life stage (subimago) and a pair of deferent ducts that open directly into the gonopores, without ejaculatory duct and accessory glands that are common in other insects. Adult females have a pair of pectinate ovaries with many mature oocytes, a pair of lateral oviducts, and a common oviduct, but lack spermatheca for storage of sperm and associated glands as in most insects. During mating, the paired deferent ducts of males inject sperm directly into females’ lateral oviducts, where mass fertilization occurs. Contraction of the intrinsic muscles of the male’s deferent ducts directs and rapidly propels the flow of spermatozoa. Reproductive strategies, such as facultative parthenogenesis in mayflies and associated selective pressures involved in the morphology and reproductive behavior of these insects, are discussed.
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All data are presented in the “Results” section.
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References
Bauernfeind E, Moog O (2000) Mayflies (Insecta: Ephemeroptera) and the assessment of ecological integrity: a methodological approach. Hydrobiologia 422:71–83. https://doi.org/10.1023/A:1017090504518
Brito P, Salles FF, Dolder H (2011) Characteristics of the male reproductive system and spermatozoa of Leptophlebiidae (Ephemeroptera). Neotrop Entomol 40:103–107. https://doi.org/10.1590/S1519-566X2011000100015
Brito P, Salles FF, Dolder H (2012) Morphology of male reproductive systems in Ephemeroptera: intrinsic musculature. Neotrop Entomol 41:306–310. https://doi.org/10.1007/s13744-012-0039-7
Brittain JE (1982) Biology of mayflies. Annu Rev Entomol 27:119–147. https://doi.org/10.1146/annurev.en.27.010182.001003
Edmunds GF, McCafferty WP (1988) The mayfly submimago. Annu Rev Entomol 33:509–527. https://doi.org/10.1146/annurev.en.33.010188.002453
Encalada AC, Peckarsky BL (2007) A comparative study of the costs of alternative mayfly oviposition behaviors. Behav Ecol Sociobiol 61:1437–1448. https://doi.org/10.1007/s00265-007-0376-4
Funk DH, Sweeney BW, Jackson JK (2010) Why stream mayflies can reproduce without males but remain bisexual: a case of lost genetic variation. J North Am Benthol Soc 29:1258–1266. https://doi.org/10.1899/10-015.1
Gaino E, Mazzini M (1991) Spermatozoon of mayflies (Ephemeroptera): an ultrastructural approach. In: Alba T, Sanchez O (eds) Overview and strategies of Ephemeroptera and Plecoptera. The Sandhill Crane Press, Gainesville, pp 27–38
Grimm VR (1985) Vergleichend-anatomischeuntersuchong der abdominalenmuskulatur und der GonoductemanlicherEphemeroptera-Imagines (Insecta). Stuttgarter Beitr Naturk 384:59
Jackson JK, Fisher SG (1986) Secondary production, emergence, and export of aquatic insects of a Sonoran desert stream. Ecology 67:629–638. https://doi.org/10.2307/1937686
Jamieson BGM, Dallai R, Afzelius BA (1999) Insects: their spermatozoa and phylogeny. Science Publisher, Enfield
King M, Eubel H, Millar H, Baer B (2011) Proteins within the seminal fluid are crucial to keep sperm viable in the honeybee Apis mellifera. J Insect Physiol 57:409–414. https://doi.org/10.1016/j.jinsphys.2010.12.011
Liegeois M, Sartori M, Schwander T (2019) Extremely widespread parthenogenesis and a trade-off between alternative forms of reproduction in mayflies (Ephemeroptera). BioRxiv. https://doi.org/10.1101/841122
Lozano-Fernandez JCR, Tanner AR, Blaxter M, Vinther J, Olesen J, Giribet G, Edgecombe GD, Pisani D (2016) A molecular palaeobiological exploration of arthropod terrestrialization. Phil Trans R Soc B. https://doi.org/10.1098/rstb.2015.0133
Munhoz ILA, Serrão JE, Dias G, Lino-Neto J, Melo AL, Araújo VA (2020) Anatomy and histology of the male reproductive tract in giant water bugs of the genus BelostomaLatreille, 1807 (Heteroptera, Belostomatidae). Int J Trop Insect Sci 40:1608–1614. https://doi.org/10.1007/s42690-020-00207-7
Peckarsky BL, McIntosh AR, Caudill CC, Dahl J (2002) Swarming and mating behavior of a mayfly Baetisbicaudatus suggest stabilizing selection for male body size. Behav Ecol Sociobiol 51:530–537. https://doi.org/10.1007/s00265-002-0471-5
Sartori M, Brittain JE (2015) Order Ephemeroptera. In: Thorp JH, Rogers DC (eds) Ecology and general biology: Thorp and Covich’s freshwater invertebrates. Elsevier Academic Press, Boston, pp 873–891
Simon S, Blanke A, Meusemann K (2018) Reanalyzing the Palaeoptera problem the origin of insect flight remains obscure. Arthropod Struct Dev 47:328–338. https://doi.org/10.1016/j.asd.2018.05.002
Soldán T (1979a) The structure and development of the male internal reproductive organs in six European species of Ephemeroptera. Acta Entomol Boh 76:22–33
Soldán T (1979b) A comparative study of spermatozoa of some central European Ephemeroptera. Acta Entomol Boh 76:223–230
Schwander T, Vuilleumier S, Dubman J, Crespi BJ (2010) Positive feedback in the transition from sexual reproduction to parthenogenesis. Proc R Soc B Biol Sci 277(1435):1442. https://doi.org/10.1098/rspb.2009.2113
Sweeney BW, Vannote RL (1982) Population synchrony in mayflies: a predator satiation hypothesis. Evolution 36:810–821. https://doi.org/10.2307/2407894
Werner M, Simmons LW (2008) Insect sperm motility. Biol Rev 83:191–208. https://doi.org/10.1111/j.1469-185X.2008.00039.x
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All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Vinícius A. Araújo, Lucimar G. Dias, and José Eduado Serrão. The first draft of the manuscript was written by Vinícius A. Araújo, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
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Collection of specimens received official authorization (Resolution No. 00854) of the Colombian Ministry of Environment and Sustainable Development, granted to researcher Dr. Lucimar Gomes Dias. All applicable institutional and/or national guidelines for the care and use of animals were followed.
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Araújo, V.A., Dias, L.G. & Serrão, J.E. Rapid and efficient mating in mayflies (Ephemeroptera): morphological and reproductive strategies in primitive winged insects. Sci Nat 108, 10 (2021). https://doi.org/10.1007/s00114-021-01721-5
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DOI: https://doi.org/10.1007/s00114-021-01721-5