Have female twisted-wing parasites (Insecta: Strepsiptera) evolved tolerance traits as response to traumatic penetration?

Abstract

Traumatic insemination describes an unusual form of mating during which a male penetrates the body wall of its female partner to inject sperm. Females unable to prevent traumatic insemination have been predicted to develop either traits of tolerance or of resistance, both reducing the fitness costs associated with the male-inflicted injury. The evolution of tolerance traits has previously been suggested for the bed bug. Here we present data suggesting that tolerance traits also evolved in females of the twisted-wing parasite species Stylops ovinae and Xenos vesparum. Using micro-indentation experiments and confocal laser scanning microscopy, we found that females of both investigated species possess a uniform resilin-rich integument that is notably thicker at penetration sites than at control sites. As the thickened cuticle does not seem to hamper penetration by males, we hypothesise that thickening of the cuticle resulted in reduced penetration damage and loss of haemolymph and in improved wound sealing. To evaluate the evolutionary relevance of the Stylops-specific paragenital organ and penis shape variation in the context of inter- and intraspecific competition, we conducted attraction and interspecific mating experiments, as well as a geometric-morphometric analysis of S. ovinae and X. vesparum penises. We found that S. ovinae females indeed attract sympatrically distributed congeneric males. However, only conspecific males were able to mate. In contrast, we did not observe any heterospecific male attraction by Xenos females. We therefore hypothesise that the paragenital organ in the genus Stylops represents a prezygotic mating barrier that prevents heterospecific matings.

Phylogenomic species delimitation of the twisted‐winged parasite genus Stylops (Strepsiptera)

“…Ironically, it is also one with the most controversial nomenclature, detailed in Straka, Alqarni, et al (2015). Currently, two names are in use for the Stylops parasitizing A. vaga Panzer, 1799: S. ater Reichert, 1914 (e.g., Smit et al, 2020; Straka et al, 2015) and S. ovinae Noskiewicz & Poluszynski, 1928 (e.g., Fraulob et al, 2015; Jandausch et al, 2022; Löwe et al, 2016). Furthermore, Cook (2019) reinstated two more species associated with A. vaga : S. muelleri Borchert, 1971, and S. krygeri Perkins, 1918.…”

“…S. ater Reichert, 1914(e.g., Smit et al, 2020 and Poluszynski, 1928(e.g., Fraulob et al, 2015Jandausch et al, 2022;Löwe et al, 2016). Furthermore, Cook (2019) reinstated two more species associated with A. vaga: S. muelleri Borchert, 1971, andS.…”

“…Based on these findings, Straka et al (2015) constructed a preliminary world checklist for the genus, where 30 species names in Europe were reinstated, largely based on hosts and DNA barcode distances (mitochondrial COI). Additional support came from a recent interspecific mating experiment study that included three species from the WP region (Jandausch et al, 2022). This study found that interspecific variation in female paragenital organs was correlated with male penis shape, allowing only conspecific matings to succeed.…”

The puncture mechanics: an example from the bed bug Cimex lectularius showing traumatic insemination using the paramere

“…In other insect groups displaying traumatic insemination, such as mirid plant bugs and twisted-winged insects, distinctly higher diversity in the puncture organ has been reported [2,6], although the diversity level differs between groups in twisted-winged insects [7]. These facts may indicate that multiple solutions exist to overcome mechanical limitations.…”

“…Traumatic insemination, or hypodermic insemination, is an infrequently observed yet widespread phenomenon in sexual animals [1]. It is particularly well-known in Hexapoda, namely Hemiptera [2,3], Diptera [4] and Strepsiptera [5][6][7]. Since this remarkable phenomenon and relevant structures were first discovered in Cimex lectularius Linnaeus, 1758 (Hemiptera: Cimicidae) [8,9], cimicomorph bugs became the most studied model species in terms of evolutionary trajectory and mechanism (e.g.…”