The reproductive and mating strategies of the twisted-winged parasites (Insecta: Strepsiptera): novel insights in the reproductive biology of an enigmatic insect order
Systematics and Morphology (Zoology)
Final Report Abstract
Traumatic mating is an unusual and bizarre form of copulation because it involves injury to a sexual partner. It is rare but occurs in different forms in few groups of insects. It is a form of sexual conflict and can be the result of intense intraspecific male competition. The two best known examples of this mode of reproduction are the bed bugs (Heteroptera: Cimicoidea) and the twisted-winged parasites (Strepsiptera). Both groups are textbook examples of insects that reproduce exclusively by traumatic insemination, a form of traumatic mating that results in sperm injection. However, it has been unclear whether traumatic insemination is the general mode of copulation in Strepsiptera. Due to lacking observations and experiments, this and other aspects of the reproductive biology of Strepsiptera remained poorly understood, especially whether females are inseminated by one or more males, or whether females have evolved traits to resist or tolerate traumatic insemination. We addressed these questions with an interdisciplinary approach. Using multiple imaging techniques, we visualized the physical piercing of the female's integument by the penis, thereby establishing how and where this process occurs, and also that Strepsiptera indeed perform traumatic insemination rather than another form of traumatic mating. We found compelling evidence that traumatic mating is phylogenetically widespread in Strepsiptera and likely represents the ancestral mode of copulation (groundplan). Using μCT-based 3D reconstructions and confocal laser scanning microscopy, we found that the integument of Strepsiptera females is rich in the elastomeric protein resilin and locally thickened at sites of male penetration. Micro-indentation experiments showed that this thickening of the integument requires higher forces to penetrate the cuticle. However, as the thickening of the integument does not prevent male mating, we interpret the female morphological features as tolerance rather than resistance: they may reduce penetration damage and hemolymph loss and improve wound sealing. Using paternity tests, we found that the offspring of a single female can have multiple fathers, in some cases up to four, establishing that Strepsiptera are not generally monandrous. Finally, attraction and interspecific mating experiments combined with a geometric-morphometric analysis of penis shapes suggest that the paragenital organ (structure where penetration takes place) described in Stylops, and which we consider as an autapomorphy of Stylopidae, may represent a prezygotic mating barrier that prevents heterospecific mating. We have documented our findings in four manuscripts, three of which have now been published in internationally peer-reviewed journals.
Publications
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Have female twisted-wing parasites (Insecta: Strepsiptera) evolved tolerance traits as response to traumatic penetration?. PeerJ, 10, e13655.
Jandausch, Kenny; Michels, Jan; Kovalev, Alexander; Gorb, Stanislav N.; van de Kamp, Thomas; Beutel, Rolf Georg; Niehuis, Oliver & Pohl, Hans
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‘Stab, chase me, mate with me, seduce me’: how widespread is traumatic insemination in Strepsiptera?. Biological Journal of the Linnean Society, 140(2), 206-223.
Jandausch, Kenny; van de Kamp, Thomas; Beutel, Rolf G.; Niehuis, Oliver & Pohl, Hans
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Polyandry and sperm competition in two traumatically inseminating species of Strepsiptera (Insecta). Scientific Reports, 14(1).
Jandausch, Kenny; Wanjura, Nico; Escalona, Hermes; Sann, Manuela; Beutel, Rolf G.; Pohl, Hans & Niehuis, Oliver
