Microbial infection risk predicts antimicrobial potential of avian symbionts

Funding EM-R was financed by a predoctoral contract (PRE2018-085378) while the whole research group received funds from the projects CGL2017-83103-P, PID2020-117429GB-C21, and PID2020-117429GB-C22, funded by the Ministerio de Ciencia e Innovación/Agencia Estatal de Investigación/10.13039/501100011033 and by “Fondo Europeo de Desarrollo Regional, a way of making Europe.” The research group also benefits from facilities, including accommodation, provided by the City Hall of Guadix, where a small lab to quickly process the samples was installed.Data availability statement Data used in this paper can be found in CSIC Institutional Repository: https://doi.org/10.20350/digitalCSIC/14748.Symbiotic bacteria on animal hosts can prevent pathogenic bacterial infections by several mechanisms. Among them, symbiotic bacteria can indirectly enhance host’s immune responses or, directly, produce antimicrobial substances against pathogens. Due to differences in life-style, different host species are under different risks of microbial infections. Consequently, if symbiotic bacteria are somewhat selected by genetically determined host characteristics, we would expect the antimicrobial properties of bacterial symbionts to vary among host species and to be distributed according to risk of infection. Here we have tested this hypothesis by measuring the antimicrobial ability of the bacterial strains isolated from the uropygial-gland skin of 19 bird species differing in nesting habits, and, therefore, in risk of microbial infection. In accordance with our predictions, intensity and range of antimicrobial effects against the indicator strains assayed varied among bird species, with hole-and open-nesters showing the highest and the lowest values, respectively. Since it is broadly accepted that hole-nesters have higher risks of microbial infection than open nesters, our results suggest that the risk of infection is a strong driver of natural selection to enhance immunocompetence of animals through selecting for antibiotic-producing symbionts. Future research should focus on characterizing symbiotic bacterial communities and detecting coevolutionary processes with particular antibiotic-producing bacteria within-host species.Ministerio de Ciencia e Innovación projects CGL2017-83103-P, PID2020-117429GB-C21, and PID2020-117429GB-C22European Regional Development FundAgencia Estatal de Investigación 10.13039/50110001103

Spatial heterogeneity in distribution and ecology of Western Palearctic birds

Copyright by the Ecological Society of AmericaSpecies vary in abundance and heterogeneity of spatial distribution, and the ecological and evolutionary consequences of such variability are poorly known. Evolutionary adaptation to heterogeneously distributed resources may arise from local adaptation with individuals of such locally adapted populations rarely dispersing long distances and hence having small populations and small overall ranges. We quantified mean population density and spatial heterogeneity in population density of 197 bird species across 12 similarly sized regions in the Western Palearctic. Variance in population density among regions differed significantly from a Poisson distribution, suggesting that random processes cannot explain the observed patterns. National estimates of means and variances in population density were positively correlated with continental estimates, suggesting that means and variances were maintained across spatial scales. We used Morisita's index of population abundance as an estimate of heterogeneity in distribution among regions to test a number of predictions. Heterogeneously distributed passerine bird species as reflected by Morisita's index had small populations, low population densities, and small breeding ranges. Their breeding populations had been consistently maintained at low levels for considerable periods of time, because the degree of genetic variation in a subsample of non-passerines and passerines was significantly negatively related to heterogeneity in distribution. Heterogeneously distributed passerine species were not more often habitat specialists than homogeneously distributed species. Furthermore, heterogeneously distributed passerine species had high annual adult survival rates but did not differ in annual fecundity from homogeneously distributed species. Heterogeneously distributed passerine species rarely colonized urban habitats. Finally, homogeneously distributed bird species were hosts to a greater diversity of blood parasite species than heterogeneously distributed species. In conclusion, small breeding ranges, population sizes, and population densities of heterogeneously distributed passerine bird species, combined with their low degree of genetic variability, and their inability to colonize urban areas may render such species particularly susceptible to human-influenced global climatic changes.The study received financial support from project CGL2007-61251/BOS-FEDER (to J. J. Soler and A. P. Møller) and Junta de Andalucía grants to research groups RNM 340 (to J. J. Soler) and RNM 341 (to M. M. Vivaldi).Peer reviewe

Avian sibling cannibalism: Hoopoe mothers regularly use their last hatched nestlings to feed older siblings

DATA AVAILABILITY Data used in this paper can be found at https://figshare.com/s/55775bd4f5e31a464fd2ACKNOWLEDGMENTS We thank Carmen Zamora, Manuel Soler Cruz, Juan Moreno Klemming, Anders Pape Møller, and Graham Tebb for discussion and comments on a preliminary version of the manuscript. Alberto Ruiz Moreno and Enrique Cortés Sánchez helped with the recording equipment. Natalia Juárez García Pelayo and Lola Barón helped with fieldwork. The Spanish research group was supported by the Spanish Ministerio de Ciencia, Innovación y Universidades and European (FEDER) funds (CGL2017-83 103-P), and from facilities, including an apartment, provided by the city authorities of Guadix, where a small lab to process samples quickly was installed. Finally, we would like to thank Renate Hengsberger for revising earlier drafts.Sibling cannibalism is relatively common in nature, but its evolution in birds and certain other vertebrates with extended parental care had been discarded. Here, however, we demonstrate its regular occurrence in two European populations of the Eurasian hoopoe (Upupa epops) and explore possible adaptive and non-adaptive explanations. Results showed that sibling cannibalism was more frequently detected in Spain (51.7%) than in Austria (5.9%). In these two populations, the hoopoes laid similar clutch sizes, resulting in similar fledging production, but hatching failures were more frequent in the northern population. Consequently, having more nestlings condemned to die in the southern population may explain the higher incidence of sibling cannibalism. In accordance with this interpretation, hatching span and failure, but not breeding date, explained the probability of sibling cannibalism in the Spanish hoopoes, while all three variables predicted brood reduction intensity. Furthermore, experimental food supply reduced the probability of sibling cannibalism, but not the intensity of brood reduction. Finally, females allocated fewer resources to the smallest nestlings when they were going to starve, but not necessarily when they were going to be used as food for their siblings. These results suggest that hoopoes produce extra eggs that, in the case of reduced hatching failure and food scarcity, produce nestlings that are used to feed older siblings. These findings provide the first evidence that sibling cannibalism occurs regularly in a bird species, thus expanding our evolutionary understanding of clutch size, hatching asynchrony, parent-offspring conflict, infanticide, and sibling cannibalism in the animal kingdom.Spanish Ministerio de Ciencia, Innovación y Universidades and European (FEDER) Funds (CGL2017-83103-P

Geographic distribution of suitable hosts explains the evolution of specialized gentes in the European cuckoo Cuculus canorus

Background Several types of selective forces can act to promote parasite specialization. Parasites might specialize on some suitable hosts at the cost of decreasing effectiveness when exploiting other species of hosts, and specialization can be more easily selected for in hosts that the parasites will easily find. Thus demographic characteristics of suitable hosts such as population density and its spatial consistency could be key factors predicting probability of parasite specialization and speciation. Here, we explore this hypothesis by studying the relationship between occurence of specialized races of the European cuckoo (Cuculus canorus) (i.e. gentes) and mean and coefficient of variation in population density estimated for 12 different European regions. Results The results were in accordance with the hypothesis because specialized cuckoo egg morphs were more common in suitable hosts with high population density and low variation in population density at the level of host species or genera. Conclusion We have presented evidence suggesting that population density and homogeneity of geographic distribution of hosts explain, at least partly, the evolution of specialized egg-morphs of the European cuckoo. These results are consistent with the hypothesis that resource (i.e., host) predictability explains the evolution of host races and species of parasites.The study received financial support from project CGL2007-61251/BOS – FEDER to JJS and APM and Junta de Andalucía grants to research groups RNM 340 (JJS) and RNM 341 (MMV)

Fledgling discrimination in the hoopoe, a potential host species of the great spotted cuckoo

Obligate brood parasites lay their eggs in nests of other species, with host parents bearing the cost of raising their offspring. These costs imposed on hosts select for the evolution of host defenses against parasitism at all stages of the reproductive cycle. The most effective defense is egg rejection at early stages of the breeding cycle, with later-stage defenses (nestling and fledgling discrimination) being less common. In this study, we tested whether the hoopoe (Upupa epops), a potential host of the great spotted cuckoo (Clamator glandarius) without egg rejection ability, presents defenses after the egg stage. We experimentally parasitized hoopoe nests with great spotted cuckoo nestlings creating mixed broods (with hoopoe and cuckoo nestlings) and broods with only cuckoo nestlings and measured parental feeding behavior and survival of nestlings and fledglings of both species. Cuckoo fledglings were fed fewer often than hoopoe fledglings in mixed broods, and adults approached more often to feed hoopoe fledglings than cuckoo fledglings. Consequently, the survival of cuckoo fledglings in both mixed and only-cuckoo-broods, was significantly lower than that of hoopoe fledglings. These results suggest that hoopoes would discriminate great spotted cuckoo fledglings, with or without direct comparison with their own fledglings. However, the survival of some cuckoos suggests that hoopoes have not reached highly efficient defenses so, other life history traits hindering parasitism by cuckoos may explain low parasitism rates and low levels of defenses in this speciesUniversidad de Granada/ CBUASpanish Ministry of Science and Innovation, European funds (FEDER) (CGL2007-61940/BOS, CGL2010-19233-C03-03)Junta de Andalucía (P09-RNM- 4557, P18-FR-2215)Spanish Ministry of Science and Innovation (Subprogram PTA-MICINN) (Ref. PTA2010-4298-I

Gut Microbiota of Great Spotted Cuckoo Nestlings is a Mixture of Those of Their Foster Magpie Siblings and of Cuckoo Adults

Diet and host genetic or evolutionary history are considered the two main factors determining gut microbiota of animals, although studies are scarce in natural populations. The system of great spotted cuckoos (Clamator glandarius) parasitizing magpies (Pica pica) is ideal to study both effects since magpie adults feed cuckoo and magpie nestlings with the same diet and, consequently, differences in gut microbiota of nestlings of these two species will mainly reflect the importance of genetic components. Moreover, the diet of adults and of nestling cuckoos drastically differ from each other and, thus, differences and similarities in their microbiotas would respectively reflect the effect of environmental and genetic factors. We used next-generation sequencing technologies to analyze the gut microbiota of cuckoo adults and nestlings and of magpie nestlings. The highest -diversity estimates appeared in nestling cuckoos and the lowest in nestling magpies. Moreover, despite the greatest differences in the microbiome composition of magpies and cuckoos of both ages, cuckoo nestlings harbored a mixture of the Operational Taxonomic Units (OTUs) present in adult cuckoos and nestling magpies. We identified the bacterial taxa responsible for such results. These results suggest important phylogenetic components determining gut microbiome of nestlings, and that diet might be responsible for similarities between gut microbiome of cuckoo and magpie nestlings that allow cuckoos to digest food provided by magpie adults.This work was supported by the Ministerio de Ciencia, Innovacion y Universidades and European (FEDER) funds (CGL2017-83103-P)

Special structures of hoopoe eggshells enhance the adhesion of symbionts-carrying uropygial secretion to prevent embryo infection

This is the pre-peer-reviewed version of the following article: Martín-Vivaldi, M.; et al. Special structures of hoopoe eggshells enhance the adhesion of symbionts-carrying uropygial secretion to prevent embryo infection. Journal of Animal Ecology, (2014). which has been published in final form at: http://onlinelibrary.wiley.com/doi/10.1111/1365-2656.12243/abstract1. Animals live in a bacterial world, and detecting and exploring adaptations favouring mutualistic relationships with antibiotic-producing bacteria as a strategy to fight pathogens are of prime importance for evolutionary ecologists. 2. Uropygial secretion of European hoopoes (Upupa epops, Linnaeus) contains antimicrobials from mutualistic bacteria that may be used to prevent embryo infection. Here, we investigated the microscopic structure of hoopoe eggshells looking for special features favouring the adhesion of antimicrobial uropygial secretions. 3. We impeded female access to the uropygial gland and compared microscopic characteristics of eggshells, bacterial loads of eggs and of uropygial secretion, and hatching success of experimental and control females. Then, we explored the link between microbiological characteristics of uropygial secretion and these of eggs of hoopoes, as well as possible fitness benefits. 4. The microscopic study revealed special structures in hoopoes' eggshells (crypts). The experimental prevention of females' gland access demonstrated that crypts are filled with uropygial secretion and that symbiotic enterococci bacteria on the eggshells come, at least partially, from those in the female's uropygial gland. Moreover, the experiment resulted in a higher permeability of eggshells by several groups of bacteria and in elimination of the positive relationships detected for control nests between hatching success and density of symbiotic bacteria, either in the uropygial secretion of females or on the eggshell. 5. The findings of specialized crypts on the eggshells of hoopoes, and of video-recorded females smearing secretion containing symbiotic bacteria at a high density onto the eggshells strongly support a link between secretion and bacteria on eggs. Moreover, the detected associations between bacteria and hatching success suggest that crypts enhancing the adhesion of symbiont-carrying uropygial secretion likely protect embryos against infections.Support by funding was provided by Spanish Ministerio de Ciencia e Innovación, European funds (FEDER) (CGL2009-14006, CGL2010-19233-C03-01 and CGL2010-19233-C03-03) and Junta de Andalucía (P09-RNM-4557)

Estudio comparativo de los mecanismos de crecimiento de cristales de yeso en geles de TMS, Sílice y Agar

Depto. de Mineralogía y PetrologíaFac. de Ciencias GeológicasTRUEpu

Seasonal and Sexual Differences in the Microbiota of the Hoopoe Uropygial Secretion

The uropygial gland of hoopoe nestlings and nesting females hosts bacterial symbionts that cause changes in the characteristics of its secretion, including an increase of its antimicrobial activity. These changes occur only in nesting individuals during the breeding season, possibly associated with the high infection risk experienced during the stay in the hole-nests. However, the knowledge on hoopoes uropygial gland microbial community dynamics is quite limited and based so far on culture-dependent and molecular fingerprinting studies. In this work, we sampled wild and captive hoopoes of different sex, age, and reproductive status, and studied their microbiota using quantitative polymerase chain reaction (qPCR), fluorescence in situ hybridization (FISH) and pyrosequencing. Surprisingly, we found a complex bacterial community in all individuals (including non-nesting ones) during the breeding season. Nevertheless, dark secretions from nesting hoopoes harbored significantly higher bacterial density than white secretions from breeding males and both sexes in winter. We hypothesize that bacterial proliferation may be host-regulated in phases of high infection risk (i.e., nesting). We also highlight the importance of specific antimicrobial-producing bacteria present only in dark secretions that may be key in this defensive symbiosis. Finally, we discuss the possible role of environmental conditions in shaping the uropygial microbiota, based on differences found between wild and captive hoopoes.This work was supported by the Spanish Ministry of Economy and Competitiveness and European (FEDER) funds (CGL2013-48193-C3-1-P/BOS, CGL2013-48193-C3-2-P/BOS, CGL2017-83103-P), and the Junta de Andalucía (RNM 339, RNM 340). S. M. Rodríguez-Ruano received a grant from the Spanish Ministry of Science and Innovation (FPI program)

The Hoopoe's Uropygial Gland Hosts a Bacterial Community Influenced by the Living Conditions of the Bird

Molecular methods have revealed that symbiotic systems involving bacteria are mostly based on whole bacterial communities. Bacterial diversity in hoopoe uropygial gland secretion is known to be mainly composed of certain strains of enterococci, but this conclusion is based solely on culture-dependent techniques. This study, by using culture-independent techniques (based on the 16S rDNA and the ribosomal intergenic spacer region) shows that the bacterial community in the uropygial gland secretion is more complex than previously thought and its composition is affected by the living conditions of the bird. Besides the known enterococci, the uropygial gland hosts other facultative anaerobic species and several obligated anaerobic species (mostly clostridia). The bacterial assemblage of this community was largely invariable among study individuals, although differences were detected between captive and wild female hoopoes, with some strains showing significantly higher prevalence in wild birds. These results alter previous views on the hoopoe-bacteria symbiosis and open a new window to further explore this system, delving into the possible sources of symbiotic bacteria (e.g. nest environments, digestive tract, winter quarters) or the possible functions of different bacterial groups in different contexts of parasitism or predation of their hoopoe host.This work was supported by the Ministerio de Ciencia y Tecnología (projects CGL2005-06975/BOSFEDER; CGL2007-61251/BOSFEDER), the Ministerio de Ciencia e Innovación (projects CGL2009-14006/BOSFEDER; CGL2010-19233-C03-01/BOSFEDER; CGL2010-19233-C03-03/BOSFEDER), the Ministerio de Economía y Competitividad (projects CGL2013-48193-C3-1-P/BOSFEDER; CGL2013-48193-C3-2-P/BOSFEDER), and the Junta de Andalucía (RNM 345, P09-RNM-4557). SMRR received a grant from the Ministerio de Ciencia e Innovación (FPI program, BES-2011-047677)