Philipp Heeb

The geographic scale of diversification on islands: genetic and morphological divergence at a very small spatial scale in the Mascarene grey white-eye (Aves: Zosterops borbonicus)

BackgroundOceanic islands provide unique scenarios for studying the roles of geography and ecology in driving population divergence and speciation. Assessing the relative importance of selective and neutral factors in driving population divergence is central to understanding how such divergence may lead to speciation in small oceanic islands, where opportunities for gene flow and population mixing are potentially high. Here we report a case of genetic and morphological structure in the Mascarene grey white-eye (Zosterops borbonicus) a species that shows a striking, geographically structured plumage polymorphism on the topographically and ecologically complex island of Réunion, yet is monotypic on the relatively uniform neighbouring island of Mauritius.ResultsAnalysis of 276 AFLP loci in 197 individuals revealed prolonged independent evolution of Réunion and Mauritius populations, which is congruent with previous mtDNA assessments. Furthermore, populations on Réunion showed significant differentiation into three main genetic groups separating lowland from highland areas despite the small geographic distances involved. Genetic differentiation along the altitudinal gradient is consistent with morphometric analysis of fitness-related traits. Birds in the highlands were larger, yet had relatively smaller beaks than in the lowlands, suggesting the role of selection in shaping morphology and restricting gene flow along the gradient. No genetic differentiation between plumage morphs was detected in neutral markers, suggesting that plumage differences are of recent origin.ConclusionsOur results suggest a dual role of vicariance and natural selection in differentiating populations of a passerine bird in an oceanic island at very small spatial scales. We propose a combination of past microallopatry driven by volcanic activity and selection-constrained dispersal along steep ecological gradients to explain the striking levels of population structure found within the island, although the possibility that genetic differences evolved in situ along the gradient cannot be ruled out at present. The lack of congruence between genetic groups and plumage morphs suggests that the latter are of recent origin and likely due to social or sexual selection acting on few loci. The presence of sharp and stable contact zones between plumage morphs suggests that they could be on independent evolutionary trajectories, yet whether or not they represent incipient species will require further research to directly assess the degree of reproductive isolation among them.

Preen gland removal increases plumage bacterial load but not that of feather-degrading bacteria

The preen gland is a holocrine sebaceous gland of the avian integument which produces an oily secretion that is spread on the plumage during preening. It has been suggested that birds may defend themselves against feather-degrading bacteria (FDB) and other potential pathogens using preen gland secretions. However, besides some in vitro studies, the in vivo bacterial inhibitory effects of the preen oil on the abundance of feather-associated bacterial species has not yet been studied in passerines. Here we tested the effect of gland removal on the abundance of FDB and other-cultivable bacterial loads (OCB) of male house sparrows (Passer domesticus). Our results did not support earlier results on in vitro antibacterial activity of preen oil against FDB since the absence of the preen gland did not significantly affect their loads related to the control birds. In contrast, we found that preen gland removal led to higher loads of OCB. This result suggests that the antimicrobial spectrum of the preen oil is broader than previously thought and that, by reducing the overall feather bacterial loads, the preen gland could help birds to protect themselves against a variety of potentially harmful bacteria.

Extremely reduced dispersal and gene flow in an island bird

The Réunion grey white-eye, Zosterops borbonicus, a passerine bird endemic to Réunion Island in the Mascarene archipelago, represents an extreme case of microgeographical plumage colour variation in birds, with four distinct colour forms occupying different parts of this small island (2512 km2). To understand whether such population differentiation may reflect low levels of dispersal and gene flow at a very small spatial scale, we examined population structure and gene flow by analysing variation at 11 microsatellite loci among four geographically close localities (<26 km apart) sampled within the distribution range of one of the colour forms, the brown-headed brown form. Our results revealed levels of genetic differentiation that are exceptionally high for birds at such a small spatial scale. This strong population structure appears to reflect low levels of historical and contemporary gene flow among populations, unless very close geographically (<10 km). Thus, we suggest that the Réunion grey white-eye shows an extremely reduced propensity to disperse, which is likely to be related to behavioural processes.

Effect of preen oil on plumage bacteria: An experimental test with the mallard

Feathers are essential for avian thermoregulation, communication or flight and a reduction of plumage condition may alter these functions and reduce individual fitness. Recently, descriptive studies provided evidence that birds carry feather-degrading bacteria on their plumage that have the ability to degrade feathers rapidly under laboratory conditions. If such bacteria reduce avian fitness, natural selection should favour the evolution of anti-bacterial defences to limit the effects of these detrimental microorganisms. Preening behaviour and associated preen gland secretions have been proposed as the main factor used by birds to limit feather-degrading bacterial growth and some recent in vitro studies provided evidence that uropygial oil inhibited the growth of some keratinolytic strains in passerines. However, preen oil antimicrobial properties remained to be experimentally tested in vivo. We conducted an experiment with mallards (Anas platyrhynchos) onto which we fixed a removable mechanism that blocked access to the uropygial gland in a first group of mallards, whilst birds in a second group had the same removable mechanism but access to their gland and a third group of birds had normal access to their gland. We found no significant effect of our treatment on total and feather-degrading bacterial loads. Three hypotheses may explain the discrepancy between our results and previous in vitro studies. First, in vitro studies may have over-estimated the bactericidal properties of the preen oil. Second, preen gland deprivation may have affected only a small portion of the feather-degrading bacterial community. Third, ducks and passerine oils might have different bactericidal properties.

The role of immigration and in-situ radiation in explaining blood parasite assemblages in an island bird clade.

Parasite communities on islands are assembled through multiple immigrations and/or in‐situ diversification. In this study, we used a phylogenetic approach to investigate the role of such processes in shaping current patterns of diversity in Leucocytozoon, a group of haemosporidian blood parasites infecting whites eyes (Zosterops) endemic to the Mascarene archipelago (south‐western Indian Ocean). We found that this parasite community arose through a combination of multiple immigrations and in‐situ diversification, highlighting the importance of both processes in explaining island diversity. Specifically, two highly diverse parasite clades appear to have been present in the Mascarenes for most of their evolutionary history and have diversified within the archipelago, while another lineage apparently immigrated more recently, probably with human‐introduced birds. Interestingly, the evolutionary histories of one clade of parasites and Indian Ocean Zosterops seem tightly associated with a significant signal for phylogenetic congruence, suggesting that host–parasite co‐divergence may have occurred in this system.

Effect of Restricted Preen-Gland Access on Maternal Self Maintenance and Reproductive Investment in Mallards

Background As egg production and offspring care are costly, females should invest resources adaptively into their eggs to optimize current offspring quality and their own lifetime reproductive success. Parasite infections can influence maternal investment decisions due to their multiple negative physiological effects. The act of preening – applying oils with anti-microbial properties to feathers – is thought to be a means by which birds combat pathogens and parasites, but little is known of how preening during the reproductive period (and its expected disease-protecting effects) influences maternal investment decisions at the level of the egg. Methodology/Principal Findings Here, we experimentally prevented female mallards (Anas platyrhynchos) from accessing their preen gland during breeding and monitored female immunoresponsiveness (e.g., plasma lysozyme concentration) as well as some egg traits linked to offspring quality (e.g., egg mass, yolk carotenoid content, and albumen lysozyme levels). Females with no access to their preen gland showed an increase in plasma lysozyme level compared to control, normally preening females. In addition, preen-gland-restricted females laid significantly lighter eggs and deposited higher carotenoid concentrations in the yolk compared to control females. Albumen lysozyme activity did not differ significantly between eggs laid by females with or without preen gland access. Conclusion/Significance Our results establish a new link between an important avian self-maintenance behaviour and aspects of maternal health and reproduction. We suggest that higher yolk carotenoid levels in eggs laid by preen-gland-restricted females may serve to boost health of offspring that would hatch in a comparatively microbe-rich environment.

Microbiome affects egg carotenoid investment, nestling development and adult oxidative costs of reproduction in Great tits

Summary 1. Parasites influence allocation trade-offs between reproduction and self-maintenance and consequently shape host life-history traits. The host microbiome includes pathogenic and commensal micro-organisms that are remarkable in their diversity and ubiquity. However, experimental studies investigating whether the microbiome shapes host reproduction are still lacking. 2. In this study, we tested whether the microbiome affects three important components of bird reproduction, namely (i) the maternal transfer of anti-microbial compounds to the eggs, (ii) the development of nestlings and (iii) the trade-off between reproduction and self-maintenance, here measured by the oxidative costs of reproduction. 3. We experimentally modified the microbiome of wild breeding Great tits (Parus major )b y spraying nests with liquid solution that either favoured or inhibited bacterial growth compared to a control. These treatments modified the bacterial communities in the nests and on adult feathers. 4. We found that females from the treatment that decreased bacterial densities in the nests laid eggs with less carotenoids than females from the control, while we found no significant effect of increasing bacterial densities and modifying community composition compared to the control. Nestlings exposed to decreased bacterial densities grew faster and had longer tarsus length at fledging. Moreover, our analyses revealed that the relationship between investment in reproduction and oxidative damage was affected by the treatments. Adults raising larger clutches suffered higher oxidative damage in control nests, whereas this oxidative cost of reproduction was not detected when we modified bird microbiome. 5. Our study provides experimental evidence for an effect of the microbiome on egg carotenoid investment, nestling development and oxidative cost of reproduction and thus highlights the major effect that the microbiome may have on the evolution of host life-history strategies.

Timing and number of colonizations but not diversification rates affect diversity patterns in hemosporidian lineages on a remote oceanic archipelago.

Parasite diversity on remote oceanic archipelagos is determined by the number and timing of colonizations and by in situ diversification rate. In this study, we compare intra-archipelago diversity of two hemosporidian parasite genera, Plasmodium and Leucocytozoon, infecting birds of the Mascarene archipelago. Despite the generally higher vagility of Plasmodium parasites, we report a diversity of Plasmodium cytochrome b haplotypes in the archipelago much lower than that of Leucocytozoon. Using phylogenetic data, we find that this difference in diversity is consistent with differences in the timing and number of colonizations, while rates of diversification do not vary significantly between the two genera. The prominence of immigration history in explaining current diversity patterns highlights the importance of historical contingencies in driving disparate biogeographic patterns in potentially harmful blood parasites infecting island birds.

Do feather-degrading bacteria actually degrade feather colour? No significant effects of plumage microbiome modifications on feather colouration in wild great tits

Parasites are known to exert selective pressures on host life history traits since the energy and nutrients needed to mount an immune response are no longer available to invest in other functions. Bird feathers harbour numerous microorganisms, some of which are able to degrade feather keratin (keratinolytic microorganisms) and affect feather integrity and colouration in vitro. Although named “feather-degrading” microorganisms, experimental evidence for their effects on feathers of free-living birds is still lacking. Here, we tested whether (i) keratinolytic microorganisms can degrade feathers in vivo and thus modify the colour of feathers during the nesting period and (ii) whether feather microorganisms have a long-term effect on the investment in colouration of newly moulted feathers. We designed treatments to either favour or inhibit bacterial growth, thus experimentally modifying plumage bacterial communities, in a wild breeding population of great tits (Parus major). Our analyses revealed no significant effects of the treatments on feather colours. Moreover, we found that differences in bacterial exposure during nesting did not significantly affect the colouration of newly moulted feathers. Our results suggest that significant feather degradation obtained during in vitro studies could have led to an overestimation of the potential of keratinolytic microorganisms to shape feather colouration in free-living birds.

Isolation and characterization of twelve polymorphic microsatellite loci for investigating an extreme case of microgeographical variation in an island bird (Zosterops borbonicus)

Twelve polymorphic microsatellite loci were characterized in order to investigate an extreme case of microgeographical variation in an island-dwelling passerine (Zosterops borbonicus). Variation was examined in two distinct natural populations of 27 individuals each. The loci displayed 5–20 alleles, with observed heterozygosities ranging between 0.33 and 0.93. All but one loci (Z16) conformed to Hardy–Weinberg equilibrium. None of the pairwise comparisons among loci showed significant linkage disequilibrium after sequential Bonferonni correction. Successful cross-species amplification in additional Zosterops species and other passerines suggests their broad applicability.