Staffan Jacob

Habitat matching and spatial heterogeneity of phenotypes: implications for metapopulation and metacommunity functioning

Abstract Spatial heterogeneity in the distribution of phenotypes among populations is of major importance for species evolution and ecosystem functioning. Dispersal has long been assumed to homogenise populations in structured landscapes by generating maladapted gene flows, making spatial heterogeneity of phenotypes traditionally considered resulting from local adaptation or plasticity. However, there is accumulating evidence that individuals, instead of dispersing randomly in the landscapes, adjust their dispersal decisions according to their phenotype and the environmental conditions. Specifically, individuals might move in the landscape to find and settle in the environmental conditions that best match their phenotype, therefore maximizing their fitness, a hypothesis named habitat matching. Although habitat matching and associated non-random gene flows can produce spatial phenotypic heterogeneity, their potential consequences for metapopulation and metacommunity functioning are still poorly understood. Here, we discuss evidence for intra and interspecific drivers of habitat matching, and highlight the potential consequences of this process for metapopulation and metacommunity functioning. We conclude that habitat matching might deeply affect the eco-evolutionary dynamics of meta-systems, pointing out the need for further empirical and theoretical research on its incidence and implications for species and communities evolution under environmental changes.

Variation in clutch size in relation to nest size in birds

Nests are structures built to support and protect eggs and/or offspring from predators, parasites, and adverse weather conditions. Nests are mainly constructed prior to egg laying, meaning that parent birds must make decisions about nest site choice and nest building behavior before the start of egg-laying. Parent birds should be selected to choose nest sites and to build optimally sized nests, yet our current understanding of clutch size-nest size relationships is limited to small-scale studies performed over short time periods. Here, we quantified the relationship between clutch size and nest size, using an exhaustive database of 116 slope estimates based on 17,472 nests of 21 species of hole and non-hole-nesting birds. There was a significant, positive relationship between clutch size and the base area of the nest box or the nest, and this relationship did not differ significantly between open nesting and hole-nesting species. The slope of the relationship showed significant intraspecific and interspecific heterogeneity among four species of secondary hole-nesting species, but also among all 116 slope estimates. The estimated relationship between clutch size and nest box base area in study sites with more than a single size of nest box was not significantly different from the relationship using studies with only a single size of nest box. The slope of the relationship between clutch size and nest base area in different species of birds was significantly negatively related to minimum base area, and less so to maximum base area in a given study. These findings are consistent with the hypothesis that bird species have a general reaction norm reflecting the relationship between nest size and clutch size. Further, they suggest that scientists may influence the clutch size decisions of hole-nesting birds through the provisioning of nest boxes of varying sizes.

Uropygial gland size and composition varies according to experimentally modified microbiome in Great tits

BackgroundParasites exert important selective pressures on host life history traits. In birds, feathers are inhabited by numerous microorganisms, some of them being able to degrade feathers or lead to infections. Preening feathers with secretions of the uropygial gland has been found to act as an antimicrobial defence mechanism, expected to regulate feather microbial communities and thus limit feather abrasion and infections. Here, we used an experimental approach to test whether Great tits (Parus major) modify their investment in the uropygial gland in response to differences in environmental microorganisms.ResultsWe found that males, but not females, modified the size of their gland when exposed to higher bacterial densities on feathers. We also identified 16 wax esters in the uropygial gland secretions. The relative abundance of some of these esters changed in males and females, while the relative abundance of others changed only in females when exposed to greater bacterial loads on feathers.ConclusionBirds live in a bacterial world composed of commensal and pathogenic microorganisms. This study provides the first experimental evidence for modifications of investment in the defensive trait that is the uropygial gland in response to environmental microorganisms in a wild bird.

Clutch-size variation in Western Palaearctic secondary hole-nesting passerine birds in relation to nest box design

Secondary hole-nesting birds that do not construct nest holes themselves and hence regularly breed in nest boxes constitute important model systems for field studies in many biological disciplines with hundreds of scientists and amateurs involved. Those research groups are spread over wide geographic areas that experience considerable variation in environmental conditions, and researchers provide nest boxes of varying designs that may inadvertently introduce spatial and temporal variation in reproductive parameters. We quantified the relationship between mean clutch size and nest box size and material after controlling for a range of environmental variables in four of the most widely used model species in the Western Palaearctic: great tit Parus major, blue tit Cyanistes caeruleus, pied flycatcher Ficedula hypoleuca and collared flycatcher F.albicollis from 365 populations and 79610 clutches. Nest floor area and nest box material varied non-randomly across latitudes and longitudes, showing that scientists did not adopt a random box design. Clutch size increased with nest floor area in great tits, but not in blue tits and flycatchers. Clutch size of blue tits was larger in wooden than in concrete nest boxes. These findings demonstrate that the size of nest boxes and material used to construct nest boxes can differentially affect clutch size in different species. The findings also suggest that the nest box design may affect not only focal species, but also indirectly other species through the effects of nest box design on productivity and therefore potentially population density and hence interspecific competition.

Interspecific variation in the relationship between clutch size, laying date and intensity of urbanization in four species of hole-nesting birds

Abstract The increase in size of human populations in urban and agricultural areas has resulted in considerable habitat conversion globally. Such anthropogenic areas have specific environmental characteristics, which influence the physiology, life history, and population dynamics of plants and animals. For example, the date of bud burst is advanced in urban compared to nearby natural areas. In some birds, breeding success is determined by synchrony between timing of breeding and peak food abundance. Pertinently, caterpillars are an important food source for the nestlings of many bird species, and their abundance is influenced by environmental factors such as temperature and date of bud burst. Higher temperatures and advanced date of bud burst in urban areas could advance peak caterpillar abundance and thus affect breeding phenology of birds. In order to test whether laying date advance and clutch sizes decrease with the intensity of urbanization, we analyzed the timing of breeding and clutch size in relation to intensity of urbanization as a measure of human impact in 199 nest box plots across Europe, North Africa, and the Middle East (i.e., the Western Palearctic) for four species of hole‐nesters: blue tits (Cyanistes caeruleus), great tits (Parus major), collared flycatchers (Ficedula albicollis), and pied flycatchers (Ficedula hypoleuca). Meanwhile, we estimated the intensity of urbanization as the density of buildings surrounding study plots measured on orthophotographs. For the four study species, the intensity of urbanization was not correlated with laying date. Clutch size in blue and great tits does not seem affected by the intensity of urbanization, while in collared and pied flycatchers it decreased with increasing intensity of urbanization. This is the first large‐scale study showing a species‐specific major correlation between intensity of urbanization and the ecology of breeding. The underlying mechanisms for the relationships between life history and urbanization remain to be determined. We propose that effects of food abundance or quality, temperature, noise, pollution, or disturbance by humans may on their own or in combination affect laying date and/or clutch size.

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.

Social odours covary with bacterial community in the anal secretions of wild meerkats

The fermentation hypothesis for animal signalling posits that bacteria dwelling in an animal’s scent glands metabolize the glands’ primary products into odorous compounds used by the host to communicate with conspecifics. There is, however, little evidence of the predicted covariation between an animal’s olfactory cues and its glandular bacterial communities. Using gas chromatography-mass spectrometry, we first identified the volatile compounds present in ‘pure’ versus ‘mixed’ anal-gland secretions (‘paste’) of adult meerkats (Suricata suricatta) living in the wild. Low-molecular-weight chemicals that likely derive from bacterial metabolism were more prominent in mixed than pure secretions. Focusing thereafter on mixed secretions, we showed that chemical composition varied by sex and was more similar between members of the same group than between members of different groups. Subsequently, using next-generation sequencing, we identified the bacterial assemblages present in meerkat paste and documented relationships between these assemblages and the host’s sex, social status and group membership. Lastly, we found significant covariation between the volatile compounds and bacterial assemblages in meerkat paste, particularly in males. Together, these results are consistent with a role for bacteria in the production of sex- and group-specific scents, and with the evolution of mutualism between meerkats and their glandular microbiota.

Social information from immigrants: multiple immigrant‐based sources of information for dispersal decisions in a ciliate

1. Dispersal is increasingly recognized as being an informed process, based on information organisms obtain about the landscape. While local conditions are often found to drive dispersal decisions, local context is not always a reliable predictor of conditions in neighbouring patches, making the use of local information potentially useless or even maladaptive. In this case, using social information gathered by immigrants might allow adjusting dispersal decisions without paying the costs of prospecting. However, this hypothesis has been largely neglected despite its major importance for ecological and evolutionary processes. 2. We investigated three fundamental questions about immigrant-informed dispersal: Do immigrants convey information that influences dispersal, do organisms use multiple cues from immigrants, and is immigrant-informed dispersal genotype dependent? 33. Using Tetrahymena thermophila ciliates in microcosms, we manipulated the number of immigrants arriving, the density of congeners, the resource quality in neighbouring patches, matrix characteristics and the level of cooperation of individuals in the neighbouring populations. 4. We provide the first experimental evidence that immigrants convey a number of different cues about neighbouring patches and matrix (patch quality, matrix characteristics and cooperation in neighbouring populations) in this relatively simple organism. Furthermore, we demonstrate genotype-dependent immigrant-informed dispersal decisions about patch quality and matrix characteristics. 5. Multiple cues from immigrants and genotype-dependent use of cues have major implications for theoretical metapopulation dynamics and the potential for local adaptation.

Climate warming reduces gut microbiota diversity in a vertebrate ectotherm

Climate change is now considered to be the greatest threat to biodiversity and ecological networks, but its impacts on the bacterial communities associated with plants and animals remain largely unknown. Here, we studied the consequences of climate warming on the gut bacterial communities of an ectotherm, the common lizard (Zootoca vivipara), using a semi-natural experimental approach. We found that 2–3 °C warmer climates cause a 34% loss of populations’ microbiota diversity, with possible negative consequences for host survival.

Cooperation-mediated plasticity in dispersal and colonization

Kin selection theory predicts that costly cooperative behaviors evolve most readily when directed toward kin. Dispersal plays a controversial role in the evolution of cooperation: dispersal decreases local population relatedness and thus opposes the evolution of cooperation, but limited dispersal increases kin competition and can negate the benefits of cooperation. Theoretical work has suggested that plasticity of dispersal, where individuals can adjust their dispersal decisions according to the social context, might help resolve this paradox and promote the evolution of cooperation. Here, we experimentally tested the hypothesis that conditional dispersal decisions are mediated by a cooperative strategy: we quantified the density‐dependent dispersal decisions and subsequent colonization efficiency from single cells or groups of cells among six genetic strains of the unicellular Tetrahymena thermophila that differ in their aggregation level (high, medium, and low), a behavior associated with cooperation strategy. We found that the plastic reaction norms of dispersal rate relative to density differed according to aggregation level: highly aggregative genotypes showed negative density‐dependent dispersal, whereas low‐aggregation genotypes showed maximum dispersal rates at intermediate density, and medium‐aggregation genotypes showed density‐independent dispersal with intermediate dispersal rate. Dispersers from highly aggregative genotypes had specialized long‐distance dispersal phenotypes, contrary to low‐aggregation genotypes; medium‐aggregation genotypes showing intermediate dispersal phenotype. Moreover, highly aggregation genotypes showed evidence for beneficial kin‐cooperation during dispersal. Our experimental results should help to resolve the evolutionary conflict between cooperation and dispersal: cooperative individuals are expected to avoid kin‐competition by dispersing long distances, but maintain the benefits of cooperation by dispersing in small groups.