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

1. 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.This work was financed by Spanish Ministerio de Ciencia e Innovaci on, European funds (FEDER) (CGL2010-19233-C03-01, CGL2013-48193-C3-1-P). MRR and DMG received a postdoc from the program “JAE-Doc”, GT from the “Juan de la Cierva”, and CRC had a predoctoral fellowship, all from the Spanish Government.Peer reviewe

Context dependent effects of an experimental increase of hunger level in house sparrow nestlings

Exploring the links between parental supply and nestling demands and between nestling demand and food supply is of central importance for understanding the evolution of parent-offspring communication. It has been suggested that optimal food supply by parents and begging effort of nestlings are context dependent, and we here test some predictions of this hypothesis. House sparrow (Passer domesticus) nestlings were experimentally fed with a pharmacological appetitive stimulant (cyproheptadine) that increases nestling demands, and explore its effect on nestling growth (i.e. body mass and tarsus length), which can be considered as the net payoff of inflated and costly offspring demand. As assumed by the experimental protocol, nestlings with an exaggerated demand were preferentially fed by parents. In accordance with the hypothesis, net benefits in terms of growth were mainly detected in first breeding attempt of parents that successfully reared three broods. Because costs associated with parental feeding should be lower for first breeding attempts and for parents of higher phenotypic quality (those able to successfully rear three clutches), our results provide to our knowledge, the first experimental evidence supporting a dynamic role of costs of food supply affecting net payoff of offspring demands, which may help to understand the mechanisms allowing the evolutionary equilibrium between intensities of offspring begging and parental provisioning.This work was financed by Spanish Ministerio de Ciencia e Innovación, Ministerio de Economía y Competitividad, European funds (FEDER) (CGL2013-48193-C3-1-P to JJS and CGL2007-61940/BOS To MS). DM-G received a postdoc from the programme “JAE-Doc” of the CSIC, and CR-C had a pre-doctoral grant from the Spanish Government.Peer reviewe

Functional explanation of extreme hatching asynchrony: Male Manipulation Hypothesis

Hatching asynchrony in birds is considered an adaptation to facilitate brood reduction because under conditions of food scarcity, the smallest nestling usually dies soon after hatching, thereby minimizing parental effort. However, in species with extreme hatching asynchrony, the last hatchlings paradoxically experience a very low probability of survival and death can take so long that it can hardly be considered an adaptation. Here, we propose and experimentally tested a new adaptive hypothesis explaining the brood reduction paradox, namely the “Male Manipulation Hypothesis”. Our hypothesis suggests that by inducing asynchronous hatching, females increase the feeding requirements of the brood, which will induce males to increase provisioning effort. In addition, females may extend the period of male manipulation by feeding the smallest nestling just enough to sustain life. Our study showed that male common blackbirds (Turdus merula) increased their effort (i.e., number of food items per hour) in experimental asynchronous broods compared to synchronous broods, while females reduced their contribution, as predicted by the hypothesis

Nest Material Shapes Eggs Bacterial Environment

Selective pressures imposed by pathogenic microorganisms to embryos have selected in hosts for a battery of antimicrobial lines of defenses that includes physical and chemical barriers. Due to the antimicrobial properties of volatile compounds of green plants and of chemicals of feather degrading bacteria, the use of aromatic plants and feathers for nest building has been suggested as one of these barriers. However, experimental evidence suggesting such effects is scarce in the literature. During two consecutive years, we explored experimentally the effects of these nest materials on loads of different groups of bacteria (mesophilic bacteria, Enterobacteriaceae, Staphylococcus and Enterococcus) of eggshells in nests of spotless starlings (Sturnus unicolor) at the beginning and at the end of the incubation period. This was also explored in artificial nests without incubation activity. We also experimentally increased bacterial density of eggs in natural and artificial nests and explored the effects of nest lining treatments on eggshell bacterial load. Support for the hypothetical antimicrobial function of nest materials was mainly detected for the year and location with larger average values of eggshell bacterial density. The beneficial effects of feathers and plants were more easily detected in artificial nests with no incubation activity, suggesting an active role of incubation against bacterial colonization of eggshells. Pigmented and unpigmented feathers reduced eggshell bacterial load in starling nests and artificial nest boxes. Results from artificial nests allowed us to discuss and discard alternative scenarios explaining the detected association, particularly those related to the possible sexual role of feathers and aromatic plants in starling nests. All these results considered together confirm the antimicrobial functionality mainly of feathers but also of plants used as nest materials, and highlight the importance of temporally and geographically environmental variation associated with risk of bacterial proliferation determining the strength of such effects. Because of costs associated to nest building, birds should adjust nest building effort to expected bacterial environments during incubation, a prediction that should be further explored.This work was financed by Spanish Ministerio de Ciencia e Innovación, European funds (FEDER) (CGL2010-19233-C03-01, CGL2010-19233-C03-03, CGL2013-48193-C3-1-P, CGL2013-48193-C3-3-P). MRR and DMG received a postdoc from the programmes “JAE-Doc” and CRC had a predoctoral grant from the Spanish Government. GT was supported by Juan de la Cierva programme (Spain) and by Secretaría de Educación Superior, Ciencia, Tecnología e Innovación del Ecuador (SENESCYT) through a Prometeo research grant.Peer reviewe

Intraspecific avian brood parasites avoid host nests infested by ectoparasites

Intraspecific brood parasitism is widespread among birds and provides clues for elucidating the evolutionary origin of interspecific brood parasitism. Studies suggest that brood parasitism does not occur at random, but that parasitic females select nests with advantages such as higher physical stability, reduced predation risk, or lower ectoparasite infestations. However, this evidence is sparse and mainly correlative. By experimentally increasing the abundance of Carnus hemapterus (a common, generalist and widespread ectoparasitic nest fly of a multitude of bird species) in half of the nests, we show that parasitic Spotless Starlings (Sturnus unicolor) avoid conspecific nests infested by ectoparasites. Since Carnus ectoparasites impinge costs on their avian nestling hosts, this avoidance response would be adaptive for parasitic Starlings. Further, we suggest a mechanism by which parasitic females may assess the level of ectoparasite infestation to select host nests accordingly: by using parasite cues such as faeces and blood remains. Additionally, these cues may be used by parasitic females for synchronization with the reproductive cycle of host females because ectoparasite cues also indicate that incubation has already commenced. Whatever the functionality, the mechanism suggested here may be employed by intra- and interspecific brood parasites, so it might represent a widespread strategy in nature.Financial support was provided by the Spanish Ministerio de Economía y Competitividad and FEDER (CGL2013- 48193-C3-1-P), the JAE programme to D. M. G. and M. R. R., and the Ramo´n y Cajal programme (Spain) and the Secretarı´a de Educacio ´n Superior, Ciencia, Tecnologı´a e Innovacio´n del Ecuador (SENESCYT) through a Prometeo research grant to G. TPeer reviewe

Fecal sacs attract insects to the nest and provoke an activation of the immune system of nestlings

Background: Nest sanitation is a widespread but rarely studied behavior in birds. The most common form of nest sanitation behavior, the removal of nestling feces, has focused the discussion about which selective pressures determine this behavior. The parasitism hypothesis, which states that nestling fecal sacs attract parasites that negatively affect breeding birds, was proposed 40 years ago and is frequently cited as a demonstrated fact. But, to our knowledge, there is no previous experimental test of this hypothesis. Results: We carried out three different experiments to investigate the parasitism hypothesis. First, we used commercial McPhail traps to test for the potential attraction effect of nestling feces alone on flying insects. We found that traps with fecal sacs attracted significantly more flies (Order Diptera), but not ectoparasites, than the two control situations. Second, we used artificial blackbird (Turdus merula) nests to investigate the combined attraction effect of feces and nest materials on arthropods (not only flying insects). Flies, again, were the only group of arthropods significantly attracted by fecal sacs. We did not detect an effect on ectoparasites. Third, we used active blackbird nests to investigate the potential effect of nestling feces in ecto- and endoparasite loads in real nestlings. The presence of fecal sacs near blackbird nestlings did not increase the number of louse flies or chewing lice, and unexpectedly reduced the number of nests infested with mites. The endoparasite prevalence was also not affected. In contrast, feces provoked an activation of the immune system as the H/L ratio of nestlings living near excrements was significantly higher than those kept under the two control treatments. Conclusions: Surprisingly, our findings do not support the parasitism hypothesis, which suggests that parasites are not the main reason for fecal sac removal. In contrast, the attraction of flies to nestling feces, the elevation of the immune response of chicks, and the recently described antimicrobial function of the mucous covering of fecal sacs suggest that microorganisms could be responsible of this important form of parental care behavior (microbial hypothesisPeer reviewe

Egg-recognition abilities in non-incubating males:Implications for the evolution of anti-parasitic host defenses

In the field of brood parasitism, it has been traditionally assumed that only the incubating sex rejects parasitic eggs, but this assumption has been rarely explored despite its important implications for the evolutionary relationship between brood parasites and hosts. Here, we used information on previous egg-rejection experiments to explore the recognition abilities of both males and females of Eurasian blackbirds Turdus merula towards experimental eggs with a variable degree of mimicry. We found that both sexes recognized non-mimetic eggs, supporting the idea that visits to the nest can favor the evolution of rejection abilities. In contrast, only females recognized mimetic eggs, indicating that although recognition abilities can evolve in both sexes, they are subsequently refined in females probably due to their more frequent interaction with parasitic eggs. Clutch size affected nest attendance since females, but not males, spent more time at the nest and visited it more frequently in larger clutches. Finally, our recordings showed that blackbird males are able not only to recognize, but also to eject parasitic eggs. Our results provide new insights into the main anti-parasitic defense in birds, egg rejection, and highlight the need of considering the role of the non-incubating sex in egg-rejection studies.Significance statementGiven the high costs associated to avian brood parasitism, both sexes are expected to evolve anti-parasitic defenses. However, in those species in which only females incubate, females have traditionally been assumed to be the responsible for egg rejection. Here, using the Eurasian blackbird (Turdus merula), we investigated the existence of egg-rejection abilities in non-incubating males and compared them to those exhibited by females. We found that males can recognize non-mimetic eggs, although their recognition abilities were less fine-tuned compared to females, who also recognized mimetic eggs. Even though females were the responsible for most documented egg-ejection events, recordings confirmed that males could also be involved in egg ejection, which could have important implication for the evolution of anti-parasitic defenses in host populations