Two intromittent organs inZorotypus caudelli(Insecta, Zoraptera): the paradoxical coexistence of an extremely long tube and a large spermatophore

Abstract

Very unusual genitalia of the species Zorotypus caudelli are described. It contains the unique configuration of two different intromittent organs, one of them strongly elongated. Hyper elongated genitalia are known in different groups of insects. Males have to accommodate these unwieldy structures in the limited spaces of the abdomen and manipulate them acutely during copulation. A crucial question is how do species with elongated genitalia cope with these requirements? To investigate this, we studied key features enabling storage, insertion, and withdrawal of the elongated genitalia. The co-existence of an elongated narrow tube and a bulky spermatophore is a highly unusual and apparently paradoxical condition. However, we demonstrate that the tube is not involved in sperm transmission, whereas the large spermatophore is transferred to females by a membranous fold of the genitalia. The movement of the spermatophore is caused by haemolymph pressure, which likely also promotes the insertion of both intromittent organs. A comparison with the genital anatomy and reproductive mode in related groups suggests that the elongated tube and its accommodating pouch is a de novo structure, and that the ancestral sperm transport via spermatophore is a preadaptive condition for the acquisition of this unusual structure

Experimental reduction of intromittent organ length reduces male reproductive success in a bug

“…Such an extremely long male intromittent organ is common in the Heteroptera [26 -28], and is also found in several other insect groups including the Coleoptera [15,16,29,30], Dermaptera [31,32] and Zoraptera [22]. A previous correlational study in L. simulans found stabilizing post-copulatory selection on processus length: males with an average processus length were most likely to inseminate a female [33].…”

“…The technique allows taxonomists to carry out non-destructive 'virtual dissections' of taxonomically important characters, such as genitalia [21]. Thus far, few studies have used micro-CT to study the functional morphology of genitalia (although see [22,23]). …”

The evolution of Zoraptera

“…However, considering the very specific and complex anatomy of the male genital apparatus of Z. caudelli (IM, c2b), studied in detail by Matsumura et al . (), it appears unlikely that the type with a complex, spiral‐shaped element has evolved several times independently. The entire apparatus is exceptionally complicated, with structures of unclear homology [e.g.…”

“…From a morphological point of view, this is also supported by obvious differences between the straight elongated intromittent organ of Z. barberi (NT, c3) (Gurney, 1938) and the spiral-shaped elongated one found in many species of Zoraptera (Table S3). However, considering the very specific and complex anatomy of the male genital apparatus of Z. caudelli (IM, c2b), studied in detail by Matsumura et al (2014), it appears unlikely that the type with a complex, spiral-shaped element has evolved several times independently. The entire apparatus is exceptionally complicated, with structures of unclear homology [e.g.…”

“…In the present study we treated asymmetric genitalia as one category, even though structural differences were reported between Z. hubbardi (NA, c1) and Z. shannoni (NT, c1) (illustrated in Gurney, 1938). Detailed morphological data on male genitalia, including musculature and related membranes, are available for only two species, Z. hubbardi and Z. caudelli (Hünefeld, 2007;Matsumura et al, 2014). Although zorapterans are rather small, technical problems caused by size reduction play a minor role in state-of-the-art insect anatomy, if at all .…”