Sexual ornamentation reflects antibacterial activity of ejaculates in mallards

Abstract

Bacteria present in ejaculates can impair sperm function and reduce male reproductive success. Thus, selection should favour the evolution of antimicrobial defences to limit the detrimental effects of sperm-associated bacteria. Additionally, current hypotheses suggest that ornamental traits may signal information about the infection status of an individual or the ability of an individual to resist bacterial-induced sperm damage. However, despite the evolutionary implications of ejaculate antimicrobials, and the putative importance of pathogens for the evolution of male ornamentation, tests of these hypotheses are lacking. We examined the antibacterial activity of semen from mallard ducks (Anas platyrhynchos) and tested whether the bactericidal capacity of semen was associated with bill coloration, a sexually selected trait. We show that mallard semen exhibits significant antibacterial activity, as measured by the in vitro capacity to kill Escherichia coli and Staphylococcus aureus. Furthermore, we demonstrate that males with more colourful bills have semen with superior bacterial-killing ability. These results suggest that females could use male phenotypic traits to avoid sexually transmitted pathogens and acquire partners whose sperm suffer less bacteria-induced damage.

The Seminal fluid proteome of the polyandrous Red junglefowl offers insights into the molecular basis of fertility, reproductive ageing and domestication

“…Immunity proteins are widespread in both male and female reproductive systems38 and some SFPs are known to target microbes that pose a threat to sperm viability and clear pathogens introduced during copulation, thus protecting the egg from potential infections4849505152. Evidence suggests that avian semen can harbour bacteria5354 and that the SF of some birds may have antibacterial properties61852. Our results confirm that antimicrobial proteins gallinacin 9 and 10, of the defensin protein family, are amongst the most abundant proteins in the RJF SF proteome, a finding consistent with SF analysis in domestic chickens24 and of particular relevance for promiscuous populations of RJF, where ejaculates host diverse bacterial communities (R. Eccleston & T. Pizzari, unpublished).…”

“…In particular, little is known about SFPs and their functional significance in wild birds (but see ref. 16), despite the fact that birds have long served as a paragon of sexual selection and more recent evidence that supports the influence of SF on reproductive fitness1718. Avian SFP biology also has the potential to be unique because birds lack accessory tissues dedicated to the production of SFPs, such as the seminal vesicle in mammals and accessory gland present in some insects.…”

In vitro antimicrobial sperm protection by an ejaculate‐like substance

“…For example, in mallards, there is a correlation between the bill coloration and constitutive antimicrobial activity (Rowe et al . ). On the other hand, variation exists in local microbial communities that sperm are potentially exposed to (Marius‐Jestin et al .…”

“…; Rowe et al . ) suggests that natural selection for antimicrobial protection of sperm may be important. Although the antimicrobial function of seminal fluid has been discussed in the human and livestock literature (e.g.…”

Lysozyme-associated bactericidal activity in the ejaculate of a wild passerine

“…Moreover, a number of potentially pathogenic bacterial species have been isolated from the cloaca of both male and female Malurus cyaneus (Poiani & Gwozdz, ). Finally, a recent study of captive mallards ( Anas platyrhynchos ) reported a correlation between male carotenoid‐based bill coloration and total antibacterial activity of ejaculates, suggesting that sexual ornamentation may reveal information about a male's ability to resist ejaculate microbial attack (Rowe et al ., ). Consequently, we tested for an association between male coloration and the lysozyme‐associated antibacterial activity of male ejaculates in order to examine the generality of this relationship across taxa and ornament types (e.g.…”