Inferring landscape resistance to gene flow when genetic drift is spatially heterogeneous.

In connectivity models, land cover types are assigned cost values characterizing their resistance to species movements. Landscape genetic methods infer these values from the relationship between genetic differentiation and cost distances. The spatial heterogeneity of population sizes, and consequently genetic drift, is rarely included in this inference although it influences genetic differentiation. Similarly, migration rates and population spatial distributions potentially influence this inference. Here, we assessed the reliability of cost value inference under several migration rates, population spatial patterns and degrees of population size heterogeneity. Additionally, we assessed whether considering intra-population variables, here using gravity models, improved the inference when drift is spatially heterogeneous. We simulated several gene flow intensities between populations with varying local sizes and spatial distributions. We then fit gravity models of genetic distances as a function of (i) the 'true' cost distances driving simulations or alternative cost distances, and (ii) intra-population variables (population sizes, patch areas). We determined the conditions making the identification of the 'true' costs possible and assessed the contribution of intra-population variables to this objective. Overall, the inference ranked cost scenarios reliably in terms of similarity with the 'true' scenario (cost distance Mantel correlations), but this 'true' scenario rarely provided the best model goodness of fit. Ranking inaccuracies and failures to identify the 'true' scenario were more pronounced when migration was very restricted (<4 dispersal events/generation), population sizes were most heterogeneous and some populations were spatially aggregated. In these situations, considering intra-population variables helps identify cost scenarios reliably, thereby improving cost value inference from genetic data.

Validating graph-based connectivity models with independent presence-absence and genetic data sets.

Habitat connectivity is a key objective of current conservation policies and is commonly modeled by landscape graphs (i.e., sets of habitat patches [nodes] connected by potential dispersal paths [links]). These graphs are often built based on expert opinion or species distribution models (SDMs) and therefore lack empirical validation from data more closely reflecting functional connectivity. Accordingly, we tested whether landscape graphs reflect how habitat connectivity influences gene flow, which is one of the main ecoevolutionary processes. To that purpose, we modeled the habitat network of a forest bird (plumbeous warbler [Setophaga plumbea]) on Guadeloupe with graphs based on expert opinion, Jacobs' specialization indices, and an SDM. We used genetic data (712 birds from 27 populations) to compute local genetic indices and pairwise genetic distances. Finally, we assessed the relationships between genetic distances or indices and cost distances or connectivity metrics with maximum-likelihood population-effects distance models and Spearman correlations between metrics. Overall, the landscape graphs reliably reflected the influence of connectivity on population genetic structure; validation R2 was up to 0.30 and correlation coefficients were up to 0.71. Yet, the relationship among graph ecological relevance, data requirements, and construction and analysis methods was not straightforward because the graph based on the most complex construction method (species distribution modeling) sometimes had less ecological relevance than the others. Cross-validation methods and sensitivity analyzes allowed us to make the advantages and limitations of each construction method spatially explicit. We confirmed the relevance of landscape graphs for conservation modeling but recommend a case-specific consideration of the cost-effectiveness of their construction methods. We hope the replication of independent validation approaches across species and landscapes will strengthen the ecological relevance of connectivity models.

La conectividad entre hábitats es un objetivo fundamental de las políticas de conservación actuales y con frecuencia se modela con grafos de paisaje (conjuntos de teselas de hábitat [nodos] conectados por vías potenciales de dispersión [enlaces]). Estos grafos se construyen a menudo con opiniones de expertos y modelos de distribución de especies (MDE), por lo que carecen de la validación empírica a partir de datos que reflejan de mejor manera la conectividad funcional. Por consiguiente, analizamos si los grafos de paisaje reflejan cómo la conectividad de hábitats influye sobre el flujo genético, que es uno de los principales procesos evolutivos. Con este propósito, modelamos la red de hábitats de un ave forestal (Setophaga plumbea) en Guadalupe con grafos basados en la opinión de un experto, en el índice de especialización de Jacobs o en un MDE. Usamos datos genéticos (712 aves de 27 poblaciones) para computar los índices genéticos locales y las distancias genéticas entre pares de poblaciones. Por último, analizamos las relaciones entre los índices o distancias genéticas y las distancias de costo o las métricas de conectividad con modelos de distancias de tipo maximum-likelihood-population-effect y correlaciones de Spearman entre las métricas e índices. En general, los grafos de paisaje reflejaron de manera confiable la influencia de la conectividad sobre la estructura genética de las poblaciones; el R2 de validación llegó hasta 0.30 y los coeficientes de correlación llegaron hasta 0.71. Aun así, la relación entre la pertinencia ecológica de los grafos, los requerimientos de datos y los métodos de construcción y análisis no fue directa porque los grafos basados en el método de construcción el más complejo (modelado a partir de la distribución de la especie) a veces tuvieron menos pertinencia ecológica que los otros. Los métodos de validación cruzada y los análisis de sensibilidad nos permitieron hacer espacialmente explícitas las ventajas y limitaciones de cada método de construcción. Así, confirmamos la pertinencia que tienen los grafos de paisaje para la conservación, aunque recomendamos se considere caso por caso el ratio entre la complejidad y la calidad de los métodos de construcción. Esperamos que la replicación de estrategias de validación independiente por varios paisajes y especies fortalezcan la pertinencia ecológica de los modelos de conectividad.

Habitat fragmentation matters more than habitat loss: The case of host-parasite interactions.

While ecologists agree that habitat loss has a substantial negative effect on biodiversity it is still very much a matter of debate whether habitat fragmentation has a lesser effect and whether this effect is positive or negative for biodiversity. Here, we assess the relative influence of tropical forest loss and fragmentation on the prevalence of vector-borne blood parasites of the genera Plasmodium and Haemoproteus in six forest bird species. We also determine whether habitat loss and fragmentation are associated with a rise or fall in prevalence. We sample more than 4000 individual birds from 58 forest sites in Guadeloupe and Martinique. Considering 34 host-parasite combinations independently and a fine characterization of the amount and spatial configuration of habitat, we use partial least square regressions to disentangle the relative effects of forest loss, forest fragmentation, landscape heterogeneity, and local weather conditions on spatial variability of parasite prevalence. Then we test for the magnitude and the sign of the effect of each environmental descriptor. Strikingly, we show that forest fragmentation explains twice as much of the variance in prevalence as habitat loss or landscape heterogeneity. In addition, habitat fragmentation leads to an overall rise in prevalence in Guadeloupe, but its effect is variable in Martinique. Both habitat loss and landscape heterogeneity exhibit taxon-specific effects. Our results suggest that habitat loss and fragmentation may have contrasting effects between tropical and temperate regions and that inter-specific interactions may not respond in the same way as more commonly used biodiversity metrics such as abundance and diversity.

Assessing the influence of the amount of reachable habitat on genetic structure using landscape and genetic graphs.

Genetic structure, i.e. intra-population genetic diversity and inter-population genetic differentiation, is influenced by the amount and spatial configuration of habitat. Measuring the amount of reachable habitat (ARH) makes it possible to describe habitat patterns by considering intra-patch and inter-patch connectivity, dispersal capacities and matrix resistance. Complementary ARH metrics computed under various resistance scenarios are expected to reflect both drift and gene flow influence on genetic structure. Using an empirical genetic dataset concerning the large marsh grasshopper (Stethophyma grossum), we tested whether ARH metrics are good predictors of genetic structure. We further investigated (i) how the components of the ARH influence genetic structure and (ii) which resistance scenario best explains these relationships. We computed local genetic diversity and genetic differentiation indices in genetic graphs, and ARH metrics in the unified and flexible framework offered by landscape graphs, and we tested the relationships between these variables. ARH metrics were relevant predictors of the two components of genetic structure, providing an advantage over commonly used habitat metrics. Although allelic richness was significantly explained by three complementary ARH metrics in the best PLS regression model, private allelic richness and MIW indices were essentially related with the ARH measured outside the focal patch. Considering several matrix resistance scenarios was also key for explaining the different genetic responses. We thus call for further use of ARH metrics in landscape genetics to explain the influence of habitat patterns on the different components of genetic structure.

Analysing landscape effects on dispersal networks and gene flow with genetic graphs.

Graph-theoretic approaches have relevant applications in landscape genetic analyses. When species form populations in discrete habitat patches, genetic graphs can be used (a) to identify direct dispersal paths followed by propagules or (b) to quantify landscape effects on multi-generational gene flow. However, the influence of their construction parameters remains to be explored. Using a simulation approach, we constructed genetic graphs using several pruning methods (geographical distance thresholds, topological constraints, statistical inference) and genetic distances to weight graph links (FST , DPS , Euclidean genetic distances). We then compared the capacity of these different graphs to (a) identify the precise topology of the dispersal network and (b) to infer landscape resistance to gene flow from the relationship between cost-distances and genetic distances. Although not always clear-cut, our results showed that methods based on geographical distance thresholds seem to better identify dispersal networks in most cases. More interestingly, our study demonstrates that a sub-selection of pairwise distances through graph pruning (thereby reducing the number of data points) can counter-intuitively lead to improved inferences of landscape effects on dispersal. Finally, we showed that genetic distances such as the DPS or Euclidean genetic distances should be preferred over the FST for landscape effect inference as they respond faster to landscape changes.

Habitat fragmentation differentially shapes neutral and immune gene variation in a tropical bird species.

Habitat fragmentation is a major cause of biodiversity loss, responsible for an alteration of intraspecific patterns of neutral genetic diversity and structure. Although neutral genetic variation can be informative for demographic inferences, it may be a poor predictor of adaptive genetic diversity and thus of the consequences of habitat fragmentation on selective evolutionary processes. In this context, we contrasted patterns of genetic diversity and structure of neutral loci (microsatellites) and immune genes (i.e., toll-like receptors) in an understorey bird species, the wedge-billed woodcreeper Glyphorynchus spirurus. The objectives were (1) to investigate forest fragmentation effects on population genetic diversity, (2) to disentangle the relative role of demography (genetic drift and migration) and selection, and (3) to assess whether immunogenetic patterns could be associated with variation of ectoparasite (i.e., ticks) pressures. Our results revealed an erosion of neutral genetic diversity and a substantial genetic differentiation among fragmented populations, resulting from a decrease in landscape connectivity and leading to the divergence of distinct genetic pools at a small spatial scale. Patterns of genetic diversity observed for TLR4 and TLR5 were concordant with neutral genetic patterns, whereas those observed for TLR3 and TLR21 were discordant. This result underlines that the dominant evolutionary force shaping immunogenetic diversity (genetic drift vs. selection) may be different depending on loci considered. Finally, tick prevalence was higher in fragmented environments. We discussed the hypothesis that pathogen selective pressures may contribute to maintain adaptive genetic diversity despite the negative demographic effect of habitat fragmentation on neutral genetic diversity.

A novel Borrelia species, intermediate between Lyme disease and relapsing fever groups, in neotropical passerine-associated ticks.

Lyme disease (LD) and relapsing fevers (RF) are vector-borne diseases caused by bacteria of the Borrelia genus. Here, we report on the widespread infection by a non-described Borrelia species in passerine-associated ticks in tropical rainforests of French Guiana, South America. This novel Borrelia species is common in two tick species, Amblyomma longirostre and A. geayi, which feed on a broad variety of neotropical mammal and bird species, including migratory species moving to North America. The novel Borrelia species is divergent from the LD and RF species, and is more closely related to the reptile- and echidna-associated Borrelia group that was recently described. Genome sequencing showed that this novel Borrelia sp. has a relatively small genome consisting of a 0.9-Mb-large chromosome and an additional 0.3 Mb dispersed on plasmids. It harbors an RF-like genomic organization but with a unique mixture of LD- and RF-specific genes, including genes used by RF Borrelia for the multiphasic antigen-switching system and a number of immune-reactive protein genes used for the diagnosis of LD. Overall, our data indicate that this novel Borrelia is an intermediate taxon between the LD and RF species that may impact a large host spectrum, including American mammals. The designation "Candidatus Borrelia mahuryensis" is proposed for this species.

Survey of ticks in French Guiana.

In this study, we examine the current pattern of tick diversity and host use in French Guiana, South America, from 97 sampling localities encompassing peri-urban, rural and natural habitats. We collected 3395 ticks, including 1485 specimens from 45 vertebrate species (humans, domestic and wild animals) and 1910 questing specimens from vegetation. Morphological examinations identified 22 species belonging to six genera: Amblyomma (16 species), Rhipicephalus (two species), Ixodes (one species), Dermacentor (one species), Haemaphysalis (one species), Ornithodoros (one species). To facilitate future identification, we produced a bank of pictures of different stages for all these species. Taxonomic identification was then confirmed by molecular characterization of two mitochondrial genes, cytochrome c oxidase CO1 and 16S rDNA. Eleven of the 22 reported species were collected on humans, six on domestic animals and 12 on wild animals. The most widespread tick species collected were A. cajennense sensu stricto and, to a lesser extent, A. oblongoguttatum; both of these species were frequently found on humans. We used these results to discuss the tick-associated risks for human and animal health in French Guiana.

Trace metals from historical mining sites and past metallurgical activity remain bioavailable to wildlife today.

Throughout history, ancient human societies exploited mineral resources all over the world, even in areas that are now protected and considered to be relatively pristine. Here, we show that past mining still has an impact on wildlife in some French protected areas. We measured cadmium, copper, lead, and zinc concentrations in topsoils and wood mouse kidneys from sites located in the Cévennes and the Morvan. The maximum levels of metals in these topsoils are one or two orders of magnitude greater than their commonly reported mean values in European topsoils. The transfer to biota was effective, as the lead concentration (and to a lesser extent, cadmium) in wood mouse kidneys increased with soil concentration, unlike copper and zinc, providing direct evidence that lead emitted in the environment several centuries ago is still bioavailable to free-ranging mammals. The negative correlation between kidney lead concentration and animal body condition suggests that historical mining activity may continue to play a role in the complex relationships between trace metal pollution and body indices. Ancient mining sites could therefore be used to assess the long-term fate of trace metals in soils and the subsequent risks to human health and the environment.

Landscape genetic analyses reveal fine-scale effects of forest fragmentation in an insular tropical bird.

Within the framework of landscape genetics, resistance surface modelling is particularly relevant to explicitly test competing hypotheses about landscape effects on gene flow. To investigate how fragmentation of tropical forest affects population connectivity in a forest specialist bird species, we optimized resistance surfaces without a priori specification, using least-cost (LCP) or resistance (IBR) distances. We implemented a two-step procedure in order (i) to objectively define the landscape thematic resolution (level of detail in classification scheme to describe landscape variables) and spatial extent (area within the landscape boundaries) and then (ii) to test the relative role of several landscape features (elevation, roads, land cover) in genetic differentiation in the Plumbeous Warbler (Setophaga plumbea). We detected a small-scale reduction of gene flow mainly driven by land cover, with a negative impact of the nonforest matrix on landscape functional connectivity. However, matrix components did not equally constrain gene flow, as their conductivity increased with increasing structural similarity with forest habitat: urban areas and meadows had the highest resistance values whereas agricultural areas had intermediate resistance values. Our results revealed a higher performance of IBR compared to LCP in explaining gene flow, reflecting suboptimal movements across this human-modified landscape, challenging the common use of LCP to design habitat corridors and advocating for a broader use of circuit theory modelling. Finally, our results emphasize the need for an objective definition of landscape scales (landscape extent and thematic resolution) and highlight potential pitfalls associated with parameterization of resistance surfaces.

Level of genetic differentiation affects relative performances of expressed sequence tag and genomic SSRs.

Microsatellites, also called simple sequence repeats (SSRs), are markers of choice to estimate relevant parameters for conservation genetics, such as migration rates, effective population size and kinship. Cross-amplification of SSRs is the simplest way to obtain sets of markers, and highly conserved SSRs have recently been developed from expressed sequence tags (EST) to improve SSR cross-species utility. As EST-SSRs are located in coding regions, the higher stability of their flanking regions reduces the frequency of null alleles and improves cross-species amplification. However, EST-SSRs have generally less allelic variability than genomic SSRs, potentially leading to differences in estimates of population genetic parameters such as genetic differentiation. To assess the potential of EST-SSRs in studies of within-species genetic diversity, we compared the relative performance of EST- and genomic SSRs following a multispecies approach on passerine birds. We tested whether patterns and levels of genetic diversity within and between populations assessed from EST- and from genomic SSRs are congruent, and we investigated how the relative efficiency of EST- and genomic SSRs is influenced by levels of differentiation. EST- and genomic SSRs ensured comparable inferences of population genetic structure in cases of strong genetic differentiation, and genomic SSRs performed slightly better than EST-SSRs when differentiation is moderate. However and interestingly, EST-SSRs had a higher power to detect weak genetic structure compared to genomic SSRs. Our study attests that EST-SSRs may be valuable molecular markers for conservation genetic studies in taxa such as birds, where the development of genomic SSRs is impeded by their low frequency.

Negative impact of urban habitat on immunity in the great tit Parus major.

Urban habitats are described as having an overall negative influence on many fitness-related traits in several bird species, but a vital function such as immunity remains poorly studied. The immune response is strongly linked to individual condition, which partly depends on resource availability and the parasitic context that often differ between urban and natural habitats. A difference between the immunity of populations dwelling in urban areas and populations from more natural habitats can, therefore, be hypothesized. We conducted a 2-year experimental study on great tits (Parus major) in urban and forest areas. We stimulated the constitutive immunity of nestlings and assessed both the inflammatory response by measuring the plasma levels of haptoglobin, an inflammatory marker, and its activation cost through the loss of body mass. In addition, we checked the nestlings for ectoparasites and assessed haemosporidian prevalence in adults. Nestlings from urban sites produced relatively less haptoglobin and lost more body mass than those from forest sites, which suggests that the activation of constitutive immunity is more costly for birds living in urban sites than for those living in the forest. We detected no ectoparasite in birds in both habitats. However, urban adults showed lower haemosporidian prevalence than forest ones, suggesting a reduced exposure to these parasites and their vectors in towns. Overall, our study provides evidence for an immune difference between urban and forest populations. Because immunity is crucial for organism fitness, it is of prime interest to identify causes and processes at the origin of this difference.

Habitat specialization predicts genetic response to fragmentation in tropical birds.

Habitat fragmentation is one of the most severe threats to biodiversity as it may lead to changes in population genetic structure, with ultimate modifications of species evolutionary potential and local extinctions. Nonetheless, fragmentation does not equally affect all species and identifying which ecological traits are related to species sensitivity to habitat fragmentation could help prioritization of conservation efforts. Despite the theoretical link between species ecology and extinction proneness, comparative studies explicitly testing the hypothesis that particular ecological traits underlies species-specific population structure are rare. Here, we used a comparative approach on eight bird species, co-occurring across the same fragmented landscape. For each species, we quantified relative levels of forest specialization and genetic differentiation among populations. To test the link between forest specialization and susceptibility to forest fragmentation, we assessed species responses to fragmentation by comparing levels of genetic differentiation between continuous and fragmented forest landscapes. Our results revealed a significant and substantial population structure at a very small spatial scale for mobile organisms such as birds. More importantly, we found that specialist species are more affected by forest fragmentation than generalist ones. Finally, our results suggest that even a simple habitat specialization index can be a satisfying predictor of genetic and demographic consequences of habitat fragmentation, providing a reliable practical and quantitative tool for conservation biology.

Contrasted patterns of genetic differentiation across eight bird species in the Lesser Antilles.

Archipelagoes are considered as "natural laboratories" for studying processes that shape the distribution of diversity. The Lesser Antilles provide a favorable geographical context for divergence to occur. However, although morphological subspecies have been described across this archipelago in numerous avian species, the potential for the Lesser Antilles in driving intra-specific genetic divergence in highly mobile organisms such as birds remains understudied. Here, we assessed level of intra-specific genetic diversity and differentiation between three islands of the Lesser Antilles (Guadeloupe, Dominica and Martinique) using a multi-species approach on eight bird species. For each species, we built a set of microsatellite markers from cross-species amplifications. Significant patterns of inter-island and/or within-island genetic differentiation were detected in all species. However, levels of intra-specific genetic differentiation among the eight bird species were not always consistent with the boundaries of subspecies previously described in the sampled islands. These results suggest different histories of colonization/expansion and/or different species-specific ecological traits affecting gene flow, advocating for multi-species studies of historical and contemporary factors shaping the distribution of diversity on islands.

Reduced inflammation in expanding populations of a neotropical bird species.

The loss of regulating agents such as parasites is among the most important changes in biotic interactions experienced by populations established in newly colonized areas. Under a relaxed parasite pressure, individuals investing less in costly immune mechanisms might experience a selective advantage and become successful colonizers as they re-allocate resources to other fitness-related traits. Accordingly, a refinement of the evolution of increased competitive ability (EICA) hypothesis proposed that immunity of invasive populations has evolved toward a reduced investment in innate immunity, the most costly component of immunity, and an increased humoral immunity that is less costly. Biogeographical approaches comparing populations between native and expansion ranges are particularly relevant in exploring this issue, but remain very scarce. We conducted a biogeographical comparison between populations of Spectacled Thrush (Turdus nudigenis) from the native area (South America) and from the expansion range (Caribbean islands). First, we compared haemosporidian prevalence and circulating haptoglobin (an acute-phase protein produced during inflammation). Second, we challenged captive birds from both ranges with Escherichia coli lipopolysaccharides (LPS) and measured postchallenge haptoglobin production and body mass change. Birds from the expansion range showed lower haemosporidian prevalence and lower levels of haptoglobin than birds from the native range. In addition, the inflammation elicited by LPS injection and its associated cost in terms of body mass loss were lower in birds from the expansion range than in birds from the native range. In accordance with the enemy release hypothesis, our results suggest that range expansion is associated with a reduced infection risk. Our study also supports the hypothesis that individuals from newly established populations have evolved mechanisms to dampen the inflammatory response and are in accordance with one prediction of the refined EICA hypothesis, proposed to understand biological invasions.

Genetic structure in insular and mainland populations of house sparrows (Passer domesticus) and their hemosporidian parasites.

Small and isolated populations usually exhibit low levels of genetic variability, and thus, they are expected to have a lower capacity to adapt to changes in environmental conditions, such as exposure to pathogens and parasites. Comparing the genetic variability of selectively neutral versus functional loci allows one to assess the evolutionary history of populations and their future evolutionary potential. The genes of the major histocompatibility complex (MHC) control immune recognition of parasites, and their unusually high diversity is genes which is likely driven by parasite-mediated balancing selection. Here, we examined diversity and differentiation of neutral microsatellite loci and functional MHC class I genes in house sparrows (Passer domesticus), living in six insular and six mainland populations, and we aimed to determine whether their diversity or differentiation correlates with the diversity and the prevalence of infection of hemosporidian parasites. We found that island bird populations tended to have lower neutral genetic variability, whereas MHC variability gene was similar between island and mainland populations. Similarly, island populations tended to show greater genetic differentiation than mainland populations, especially at microsatellite markers. The maintenance of MHC genetic diversity and its less marked structure in the island populations could be attributed to balancing-selection. The greater MHC differentiation among populations was negatively correlated with similarity in blood parasites (prevalence and diversity of parasite strains) between populations. Even at low prevalence and small geographical scale, haemosporidian parasites might contribute to structure the variability of immune genes among populations of hosts.

Females tend to prefer genetically similar mates in an island population of house sparrows.

BACKGROUND: It is often proposed that females should select genetically dissimilar mates to maximize offspring genetic diversity and avoid inbreeding. Several recent studies have provided mixed evidence, however, and in some instances females seem to prefer genetically similar males. A preference for genetically similar mates can be adaptive if outbreeding depression is more harmful than inbreeding depression or if females gain inclusive fitness benefits by mating with close kin. Here, we investigated genetic compatibility and mating patterns in an insular population of house sparrow (Passer domesticus), over a three-year period, using 12 microsatellite markers and one major histocompability complex (MHC) class I gene. Given the small population size and the distance from the mainland, we expected a reduced gene flow in this insular population and we predicted that females would show mating preferences for genetically dissimilar mates. RESULTS: Contrary to our expectation, we found that offspring were less genetically diverse (multi-locus heterozygosity) than expected under a random mating, suggesting that females tended to mate with genetically similar males. We found high levels of extra-pair paternity, and offspring sired by extra-pair males had a better fledging success than those sired by the social male. Again, unexpectedly, females tended to be more closely related to extra-pair mates than to their social mates. Our results did not depend on the type of genetic marker used, since microsatellites and MHC genes provided similar results, and we found only little evidence for MHC-dependent mating patterns. CONCLUSIONS: These results are in agreement with the idea that mating with genetically similar mates can either avoid the disruption of co-adapted genes or confer a benefit in terms of kin selection.

Epidemiology of Plasmodium relictum infection in the house sparrow.

In vertebrates, multiple host characteristics and environmental factors are known to influence infectious disease dynamics. Here, we investigated variability in prevalence and parasitemia of Plasmodium relictum in the house sparrow ( Passer domesticus ) across a large number of rural and urban populations (n = 16). We found that prevalence was not predicted by any of the host traits investigated (age, sex, body mass, or wing length). However, parasitemia was significantly higher in females when compared to males and in 1-yr-olds as compared to older individuals. Neither prevalence nor parasitemia differed according to habitat type (urban vs. rural). These results suggest that inter-population variation in parasitemia depends on host intrinsic factors whereas variation in prevalence could be due to environmental differences between populations, such as climatic variables that might affect the abundance of vectors. This large-scale study gives us a better understanding of the key factors involved in the epidemiology of avian malaria.

Social interactions modulate the virulence of avian malaria infection.

There is an increasing understanding of the context-dependent nature of parasite virulence. Variation in parasite virulence can occur when infected individuals compete with conspecifics that vary in infection status; virulence may be higher when competing with uninfected competitors. In vertebrates with social hierarchies, we propose that these competition-mediated costs of infection may also vary with social status. Dominant individuals have greater competitive ability than competing subordinates, and consequently may pay a lower prevalence-mediated cost of infection. In this study we investigated whether costs of malarial infection were affected by the occurrence of the parasite in competitors and social status in domestic canaries (Serinus canaria). We predicted that infected subordinates competing with non-infected dominants would pay higher costs than infected subordinates competing with infected dominants. We also predicted that these occurrence-mediated costs of infection would be ameliorated in infected dominant birds. We found that social status and the occurrence of parasites in competitors significantly interacted to change haematocrit in infected birds. Namely, subordinate and dominant infected birds differed in haematocrit depending on the infection status of their competitors. However, in contrast to our prediction, dominants fared better with infected subordinates, whereas subordinates fared better with uninfected dominants. Moreover, we found additional effects of parasite occurrence on mortality in canaries. Ultimately, we provide evidence for costs of parasitism mediated by social rank and the occurrence of parasites in competitors in a vertebrate species. This has important implications for our understanding of the evolutionary processes that shape parasite virulence and group living.

Predictions of avian Plasmodium expansion under climate change.

Vector-borne diseases are particularly responsive to changing environmental conditions. Diurnal temperature variation has been identified as a particularly important factor for the development of malaria parasites within vectors. Here, we conducted a survey across France, screening populations of the house sparrow (Passer domesticus) for malaria (Plasmodium relictum). We investigated whether variation in remotely-sensed environmental variables accounted for the spatial variation observed in prevalence and parasitemia. While prevalence was highly correlated to diurnal temperature range and other measures of temperature variation, environmental conditions could not predict spatial variation in parasitemia. Based on our empirical data, we mapped malaria distribution under climate change scenarios and predicted that Plasmodium occurrence will spread to regions in northern France, and that prevalence levels are likely to increase in locations where transmission already occurs. Our findings, based on remote sensing tools coupled with empirical data suggest that climatic change will significantly alter transmission of malaria parasites.