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Divergent mating patterns and a unique mode of external sperm transfer in Zoraptera: an enigmatic group of pterygote insects

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Abstract

A remarkable external sperm transfer is described for the first time in a species of a group of winged insects (Pterygota), the enigmatic Zoraptera. Mating and sperm transfer of two species of the order were examined in detail, documented, and compared with each other and with patterns described for other species belonging to the order. The behavior differs strikingly in Zorotypus impolitus and Zorotypus magnicaudelli. A copula is performed by males and females of the latter, as it is also the case in other zorapteran species and generally in pterygote insects. In striking contrast to this, males of Z. impolitus do not copulate but deposit small (100 μm in diameter) spermatophores externally on the abdomen of the female. Each spermatophore contains only one giant spermatozoon (3 mm long and 3 μm wide), a unique feature in the entire Hexapoda. External sperm transfer in Pterygota is a highly unusual case of evolutionary reversal. The very small relict group Zoraptera displays a uniform general morphology but exhibits very different reproductive structures and patterns of mating behavior. This may be an extreme form of a more general situation in insects, with a specific form of selection resulting in an accelerated rate of evolution in the reproductive system.

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Acknowledgments

For financial support of this project we want to thank the MIUR (PRIN 2008/FL2237 to RD), the VolkswagenStiftung (to RGB), and the Japan Society for the Promotion of Science (Grant-in-Aid Scientific Research C, 21570089 to RM).

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Correspondence to R. Dallai.

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Communicated by: Sven Thatje

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ESM 1

Schematic sequences of Zorotypus impolitus mating behavior (DOC 24 kb)

ESM 2

Schematic sequences of Zorotypus magnicaudelli mating behavior (DOC 24 kb)

ESM 3

Video showing the mating behavior of Zorotypus impolitus (MPG 8460 kb)

ESM 3

Video showing the mating behavior of Zorotypus magnicaudelli (MPG 3706 kb)

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Dallai, R., Gottardo, M., Mercati, D. et al. Divergent mating patterns and a unique mode of external sperm transfer in Zoraptera: an enigmatic group of pterygote insects. Naturwissenschaften 100, 581–594 (2013). https://doi.org/10.1007/s00114-013-1055-0

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