Copulatory Wounding and Traumatic Insemination

Abstract

Copulatory wounding (CW) is widespread in the animal kingdom, but likely underreported because of its cryptic nature. We use four case studies (Drosophila flies, Siphopteron slugs, Cimex bugs, and Callosobruchus beetles) to show that CW entails physiological and lifehistory costs, but can evolve into a routine mating strategy that, in some species, involves insemination through the wound. Although interspecific variation in CW is documented, few data exist on intraspecific and none on individual differences. Although defensive mechanisms evolve in the wound recipient, our review also indicates that mating costs in species with CW are slightly higher than in other species. Whether such costs are dose-or frequencydependent, and whether defense occurs as resistance or tolerance, decisively affects the evolutionary outcome. In addition to sexual conflict, CW may also become a model system for reproductive isolation. In this context, we put forward a number of predictions, including (1) occasional CW is more costly than routine CW, (2) CW is more costly in between-than within-population matings, and (3) in the presence of CW, selection may favor the transmission of sexually transmitted diseases if they induce resource allocation. Finally, we outline, and briefly discuss, several medical implications of CW in humans.

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

“…The horn-like structure functioned as a guiding sheath for the virga, potentially to facilitate insertion into the female spermatheca. 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).…”

Sexual Conflict in Hermaphrodites

“…Wounding during insemination, and the subsequent need to process/remove ejaculate components transferred in this manner, likely results in significant costs of traumatic insemination to the sperm recipient (e.g., Smolensky et al 2009; see also Reinhardt et al 2014). The taxonomic distribution of traumatic insemination suggests that the evolution of this fertilization route is common in simultaneous hermaphrodites (Lange et al 2013a), but it is currently unclear whether simultaneous hermaphroditism is itself a cause of this bias, as might be expected from theoretical predictions of a greater propensity toward escalated mate harm in hermaphrodites (Michiels and Koene 2006; see also Preece et al 2009), or whether the pattern arises as a consequence of other common features of simultaneous hermaphrodites such as their tendency to be soft-bodied (Lange et al 2013a) and/or to possess a high capacity for regeneration.…”

Genitalia‐associated microbes in insects

“…Although copulatory wounds are not necessary for the evolution of a specific microbe community on or within genitalia, they open an opportunity for an easy transmission route as the host itself breaches the mechanical barriers of transmission. Copulatory wounding is widespread throughout the animal kingdom spanning from wounding through anchorage when ensuring connection to female while copulating to traumatic insemination of sperm and seminal fluid (Lange et al ., ; Reinhardt et al ., ). All categories of copulatory wounding can potentially transmit microbes.…”

“…All categories of copulatory wounding can potentially transmit microbes. The most extreme case of wounding, that is, traumatic insemination, is assumed to have evolved in males to circumvent the female genital tract and its potentially hostile environment for sperm (Reinhardt et al ., ). By piercing holes into the wall of the genital tract males of several species inseminate directly into the female body cavity and thereby avoid the processes or mechanisms by which females manipulate the fertilization of their ova in their own interest (Lange et al ., ).…”

“…Intuitively, one would assume this to be a rare case in many insect species. However, in insects that have alternative copulation tactics, such as traumatic insemination, or inflict copulatory wounds (Reinhardt et al ., ), such microbe transmission will likely be more regular during mating. Therefore, microbes on the female integument will potentially enter the female body or transmit to male reproductive organs.…”