Female genitaltract integrity and immunity

The insect's cuticle is a major barrier to pathogens (Neville, 1998; Siva-Jothy et al., 2005), and once it is breached the insect's constitutive effector systems work very rapidly to clear the infection (see

Figure 15.3 Phase-contrast micrographs of the genital damage caused during mating in D. melanogaster(see Kamimura, 2007). (a) Virgin female's genital tract. (b) Single-mated female's genital tract showing the melanized wounds (broken circles) caused by the male's intromittent organ. The solid black arrows indicate the oviscapt and the open black arrows indicate the analia. Figures reproduced by permission of Y. Kamimura.

Figure 15.3 Phase-contrast micrographs of the genital damage caused during mating in D. melanogaster(see Kamimura, 2007). (a) Virgin female's genital tract. (b) Single-mated female's genital tract showing the melanized wounds (broken circles) caused by the male's intromittent organ. The solid black arrows indicate the oviscapt and the open black arrows indicate the analia. Figures reproduced by permission of Y. Kamimura.

Haine et al., 2008). Although the insect cuticle is an unfavourable environment for microbes (Steinhaus, 1947; Brooks, 1963), it does not appear to be sterile (e.g. Rivault et al., 1993; Sukontason et al., 2000) and at least one study has shown that male genitalia harbour a range of microbes that are potential pathogens (Reinhardt et al, 2005) (see Figure 15.1). Any breach in the female's genital tract therefore affords surface microbes rapid access to the female's haemocoel. Not surprisingly female insects have been shown to respond to potentially damaging male genital traits by evolving thicker cuticle (Ronn et al, 2007) but it is likely that this response is constrained by the need to process and eject eggs: the genital-tract cuticle can be only so thick and tough. Females are therefore likely to have to rely on physiological defence and several studies have shown that female Drosophila express antimicrobial peptides in their genital-tract epithelium (Charlet et al., 1996; Ferrandon et al., 1998; Tzou et al., 2000). Moreover, these genital-tract peptides are regulated by a different mechanism to systemic antimicrobial peptide expression, suggesting their production in the genital tract is linked to reproduction (Ryu et al., 2004). It is possible that these antimicrobial peptides have functions other than/additional to immune defence of the genital tract; for example, they may function to protect the eggs after they have been laid (Marchini et al., 1997). Studies of genital-tract wounding have also revealed efficient melanization responses in the damaged regions (Crudgington and Siva-Jothy, 2000; Kamimura, 2007; Reinhardt et al, 2007), although these are likely to be a function of the haemolymph, rather than the genital-tract epithelium. The melanized wounds identified in these studies (see Figure 15.3) are small and localized, suggesting that the breach of the genital-tract cuticle may be sealed rapidly by haemolymph clotting mechanisms (see Theopold et al, 2002; Haine et al, 2006). It is interesting to note that in traumat-ically inseminating insects, where males always wound females during mating, the female has evolved an immune organ underlying the region where the male causes damage (Usinger, 1966; Reinhardt et al., 2003). The localization of immune-effector systems in regions subject to predictable damage may therefore be a widespread, but overlooked, phenomenon.

In summary so far, males possess a suite of traits that can cause damage to females during mate encounter. The cost of this damage to females is cuticular wound repair as well as the potential associated immune costs in dealing with opportunistic pathogens that gain entry to the haemocoel. I suggest that reproduction is a period in a female insect's life when immune insult is predictable in time (i.e. driven by temporal decisions by the female to mate) and in space (i.e. the consequence is localized wounding of the genital tract and other regions subjected to male gripping/restraint). Moreover, the fact that (a) reproductive events are usually under the temporal control of the female and (b) insects have revealed a sophisticated ability to anticipate immune insult suggests that female insects may be under selection to modulate their immunity to offset the costs of damage associated with mating. Such 'reproductive' immune anticipation remain to be demonstrated.

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