Ovoviviparity and genital evolution: a lesson from an earwig species with coercive traumatic mating and accidental breakage of elongated intromittent organs

Abstract

Ovoviviparity or viviparity has evolved independently in animals and involves adaptations in females to accommodate developing embryos for a prolonged duration in their bodies, a condition which has likely to have influenced the evolution of the male genitalia. We aimed to ascertain whether the elongated male genitalia of the ovoviviparous free-living earwig species Marava arachidis (Dermaptera: Spongiphoridae) delivers sperm directly to the female ovaries where fertilization occurs. Males mated coercively with females by grabbing the female antenna with their mouth parts. Although females resisted the mating attempts, pairs mated 3.3 times on average over 15 h. The elongated intromittent organ, known as a virga, was inserted into the long-tubed spermatheca during insemination. Surgical ectomy of the spermatheca confirmed that sperm migrated from here to the ovaries with a variable delay. A pair of sclerites in the male genitalia frequently inflicted wounds near the spermathecal opening, while the single, thin virga sometimes broke off during mating. However, unlike earwigs bearing a 'spare' virga, damage was restricted to the tip of the virga, without which the males could still inseminate the females. We discuss the evolution of the genitalia in this insect in the light of sexual selection and sexual conflict over mating and fertilization.

Earwigs from Brazilian caves, with notes on the taxonomic and nomenclatural problems of the Dermaptera (Insecta)

“…There is accumulating evidence that many male animals inflict wounds on the female during mating through use of their genital structures (Lange et al 2013; Tatarnic et al 2014; Reinhardt et al 2014). However, this mode of mating, termed traumatic mating, has been reported in only two species of earwigs, Echinosoma denticulatum Hincks, 1959 (Pygidicranidae: Echinosomatinae; Kamimura and Lee 2014a) and Marava arachidis (Yersin, 1860) (Spongiphoridae: Spongiphorinae; Kamimura et al 2016b). While Briceño (1997) failed to mention the occurrence of copulatory wounding in P. dorsalis , melanized patches on the membranous region at the spermathecal opening were observed in this study (n = 2; Figs 40, 41).…”

Fitness advantages of the biased use of paired laterally symmetrical penises in an insect

“…Breakage of a virga under natural conditions has also been reported in anisolabidid males ( Euborellia plebeja and Anisolabis maritima ), which have a pair of virgae longer than their bodies (Kamimura & Matsuo, ). Virgal breakage in these species is frequently accompanied by necrosis of a penis lobe, as observed in L. riparia (Kamimura & Matsuo, ; Kamimura, Tee, & Lee, ). Marava arachidis males (Spongiphoridae) possess a single but extremely elongated virga, which is inserted into the long tube‐shaped spermatheca during insemination (Kamimura et al., ).…”

“…Marava arachidis males (Spongiphoridae) possess a single but extremely elongated virga, which is inserted into the long tube‐shaped spermatheca during insemination (Kamimura et al., ). The thin virga sometimes breaks during copulation, but unlike earwigs possessing an extra virga, genital damage is restricted to the virgal tip, without which males can still inseminate females (Kamimura et al., ). These patterns of genital accidents suggest that a single penis lobe of the Forficuloidea is more robust than those of the earwigs with a spare penis.…”

Ovoviviparity in the Tropical Earwig SpeciesSpongovostox semiflavus(Dermaptera: Spongiphoridae), With Potential Convergent Elongation of Male Genitalia

“…However, nymphs of M. arachidis hatch within a few minutes after egg deposition (Herter 1943), compared with the usual oviparous species in which the maternal care of eggs generally lasts from one to several weeks (Gü nther andHerter 1974, Costa 2006). Based on previous findings (Herter 1943(Herter , 1965Patel and Habib 1978;Costa 2006;Ko c arek 2009;Kamimura et al 2016b), M. arachidis is considered ovoviviparous for the purpose of this study. Ko c arek (2009) found developed embryos in the abdomen of fixed samples of Chaetospania borneensis (Dubrony, 1879) (Spongiphoridae: Labiinae).…”

“…During a faunal and ecological study of earwigs on Penang Island, Peninsular Malaysia (Kamimura et al 2016a), we discovered that Spongovostox semiflavus (Bormans) (Spongiphorinae) is ovoviviparous. Ovoviviparity and viviparity require adaptations in females to accommodate developing embryos within their bodies for a prolonged time period, which likely influence the evolution of the male genitalia (see Kamimura et al 2016b and references therein). Our preliminary literature search revealed that all known (ovo)viviparous, free-living earwigs are characterized by elongated male genitalia (Borelli 1932, Ramamurthi 1958, Steinmann 1990, Kamimura et al 2016b).…”