Bacteria and the evolution of honest signals. The case of ornamental throat feathers in spotless starlings

Abstract

Summary1. Mechanisms guaranteeing reliability of messages are essential in understanding the underlying information and evolution of signals. Micro-organisms may degrade signalling traits and therefore influence the transmitted information and evolution of these characters. The role of micro-organisms in animal signalling has, however, rarely been investigated. 2. Here, we explore a possible role for feather-degrading bacteria driving the design of ornamental throat feathers in male spotless starlings (Sturnus unicolor). We estimated length, bacterial load, degradation status and susceptibility to degradation by keratinolytic bacteria in those feathers, compared with non-ornamental adjacent feathers in males, as well as to throat feathers in females. In addition, the volume of the uropygial gland and its secretion was measured and the secretion extracted. We also experimentally evaluated the capacity of each secretion to inhibit growth of a keratinolytic bacterium. 3. The apical part of male ornamental throat feathers harboured more bacteria and degraded more quickly than the basal part; these patterns were not detected in female throat feathers or in non-ornamental male feathers. Moreover, degradation status of male and female throat feathers did not differ, but was positively associated with feather bacterial density. Finally, the size of the uropygial gland in both males and females predicted volume and the inhibitory capacity of secretion against feather-degrading bacteria. Only in males was uropygial gland size negatively associated with the level of feather degradation. 4. All results indicate differential susceptibility of different parts of throat feathers to keratinolytic bacterial attack, which supports the possibility that throat feathers in starlings reflect individual ability to combat feather-degrading bacteria honestly. This is further supported by the relationship detected between antimicrobial properties of uropygial secretion and the level of feather degradation. 5. Our results suggest that selection pressures exerted by feather-degrading bacteria on hosts may promote evolution of particular morphologies of secondary sexual traits with different susceptibility to bacterial degradation that reliably inform of their bacterial load. Those results will help to understand the evolution of ornamental signals.

Defenses against keratinolytic bacteria in birds living in radioactively contaminated areas

“…Previous studies of other birds found a positive relationship between uropygial gland size and amount of secretion produced (Martín-Vivaldi et al 2009;Ruiz-Rodríguez et al 2015). We also found a positive association between gland height and volume of secretion, but only for swallows captured in contaminated areas in Ukraine, which might be related to the relatively higher selection pressures at these locations (see above).…”

“…Although the antimicrobial activity of uropygial secretions is an ongoing topic of discussion in the literature, several studies have found antimicrobial components in uropygial secretion (Martín-Platero et al 2006;Martín-Vivaldi et al 2010;Ruiz-Rodríguez et al 2013) and direct evidence of inhibition of bacterial growth (Shawkey et al 2003;Ruiz-Rodríguez et al 2015), including feather-degrading bacteria (Møller et al 2009). However, other studies have failed to detect antimicrobial properties of secretion (Giraudau et al 2013;Reneerkens et al 2008).…”

“…Thus, since bacterial communities in contaminated areas changed, we could expect investment in defenses to be adjusted to the new microbial environment. The intensity of selection exerted by bacteria differs between sexes for feathers subject to sexual selection (Ruiz- de-Castañeda et al 2012;Ruiz-Rodríguez et al 2015). Hence, defenses against bacterial degradation of ornaments may also differ between males and females.…”

A small badge of longevity: opposing survival selection on the size of white and black wing markings

“…We suggest that a possible link here would involve physiological pathways that increase resistance of wing feathers to abrasion. For instance, resistance to feather‐degrading bacteria and ectoparasites is likely to be mediated by uropygial gland functioning (reviewed by Ruiz‐Rodríguez et al ). This gland produces waxes, sterols and hydrocarbons that are important to maintain the plumage supple, rigid and to protect it against abrasion (Jacob and Ziswiler , Shawkey et al ).…”

Ectoparasite Activity During Incubation Increases Microbial Growth on Avian Eggs

“…Nevertheless, it has recently started to be subject of in-depth research from an ecological and evolutionary framework (e.g., [17,18]). Regarding interactions between bacteria and birds, it has been shown that different types of bacteria interact with nestling growth [19,20], may increase adult predation rates [21], and may be involved for instance in the evolution of uropygial glands [22], plumage colouration or maintenance [23][24][25], nest material composition [26,27], incubation behaviours [28,29], or even cognitive skills of birds [30]. Because of the important and diverse roles that bacteria may play in the ecology and evolution of life histories and behaviour in higher organisms (reviewed in [31][32][33][34]), detecting a causal link between ectoparasitism and bacterial infections would contribute to the understanding of parasite-host interactions.…”