Maria Svensson-Coelho

Species formation by host shifting in avian malaria parasites

Significance Emerging infectious diseases pose threats to humans and livestock, but little is known about the general propensity of parasitic organisms to shift between hosts or the role of host shifting in the diversification of parasite lineages. The malaria parasites of contemporary vertebrate species descended from a common ancestor, likely after the diversification of their major host taxa, requiring rapid speciation and shifting between hosts across large host–taxonomic distances. Examination of sister lineages of avian malaria parasites in the New World suggests that such host shifting is common and often leads to the origin of new evolutionary lineages of parasites. The malaria parasites (Apicomplexa: Haemosporida) of birds are believed to have diversified across the avian host phylogeny well after the origin of most major host lineages. Although many symbionts with direct transmission codiversify with their hosts, mechanisms of species formation in vector-borne parasites, including the role of host shifting, are poorly understood. Here, we examine the hosts of sister lineages in a phylogeny of 181 putative species of malaria parasites of New World terrestrial birds to determine the role of shifts between host taxa in the formation of new parasite species. We find that host shifting, often across host genera and families, is the rule. Sympatric speciation by host shifting would require local reproductive isolation as a prerequisite to divergent selection, but this mechanism is not supported by the generalized host-biting behavior of most vectors of avian malaria parasites. Instead, the geographic distribution of individual parasite lineages in diverse hosts suggests that species formation is predominantly allopatric and involves host expansion followed by local host–pathogen coevolution and secondary sympatry, resulting in local shifting of parasite lineages across hosts.

Structure and organization of an avian haemosporidian assemblage in a Neotropical savanna in Brazil.

Studies on avian haemosporidia are on the rise, but we still lack a basic understanding of how ecological and evolutionary factors mold the distributions of haemosporidia among species in the same bird community. We studied the structure and organization of a local avian haemosporidian assemblage (genera Plasmodium and Haemoproteus) in the Cerrado biome of Central Brazil for 5 years. We obtained 790 blood samples from 54 bird species of which 166 (21%) were infected with haemosporidians based on molecular diagnostics. Partial sequences of the parasite cytochrome b gene revealed 18 differentiated avian haemosporidian lineages. We also analysed the relationship of life-history traits (i.e., nesting height, migration status, nest type, sociality, body mass, and embryo development period) of the 14 most abundant bird species with the prevalence of avian haemosporidia. It was found that host species that bred socially presented a higher prevalence of Haemoproteus (Parahaemoproteus) than bird species that bred in pairs. Thus, aspects of host behaviour could be responsible for differential exposure to vectors. The assemblage of avian haemosporidia studied here also confirms a pattern that is emerging in recent studies using molecular markers to identify avian haemosporidians, namely that many lineages are host generalists.

Host phylogeography and beta diversity in avian haemosporidian (Plasmodiidae) assemblages of the Lesser Antilles

1. We estimated the correlation between host phylogeographical structure and beta diversity of avian haemosporidian assemblages of passerine birds to determine the degree to which parasite communities change with host evolution, expressed as genetic divergence between island populations, and we investigated whether differences among islands in the haemosporidia of a particular host species reflect beta diversity in the entire parasite assemblage, beta diversity in vectors, turnover of bird species and/or geographical distance. 2. We used Mantel tests to assess the significance of partial correlations between host nucleotide difference (based on cytochrome b) and haemosporidian (Haemoproteus spp. and Plasmodium spp.) mitochondrial lineage beta diversity within a given host species and between Plasmodium mitochondrial lineage beta diversity and mosquito and bird species beta diversity (or turnover). Three abundant and widespread host species (Tiaris bicolor, Coereba flaveola and Loxigilla noctis/barbadensis) were included in the study. Haemosporidian lineage beta diversity among nine islands was assessed using the Chao-Jaccard, Chao-Sørensen and Morisita-Horn indices of community similarity. Beta diversity indices of mosquito species and turnover of bird species were calculated from data in published records and field guides. 3. In Loxigilla spp., we found a positive correlation with geographical distance and an unexpected negative correlation between haemosporidian beta diversity and host genetic distance. Tiaris bicolor exhibited a significant positive correlation between haemosporidian beta diversity and beta diversity within the entire parasite assemblage. We did not find significant correlations between parasite beta diversity and mosquito beta diversity or bird species turnover. 4. Host phylogeographical structure does not appear to drive within-host beta diversity of haemosporidian lineages. Instead, the array of parasites on one host can reflect the haemosporidian assemblage on other hosts.

Reciprocal Specialization in Multihost Malaria Parasite Communities of Birds: A Temperate-Tropical Comparison

How specialization of consumers with respect to resources varies with respect to latitude is poorly understood. Coexistence of many species in the tropics might be possible only if specialization also increases. Alternatively, lower average abundance of more diverse biotic resources in the tropics might force consumers to become more generalized foragers. We examine levels of reciprocal specialization in an antagonistic system—avian malaria—to determine whether the number of host species used and/or parasite lineages harbored differ between a temperate and a tropical assemblage. We evaluate the results of network analysis, which can incorporate both bird and parasite perspectives on specialization in one quantitative index, in comparison to null models. Specialization was significantly greater in both sample sites than predicted from null models. We found evidence for lower per-host species parasite diversity in temperate compared to tropical birds. However, specialization did not differ between the tropical and temperate sites from the parasite perspective. We supplemented the network analysis with estimates of specialization that incorporate phylogenetic relationships of associates and found no differences between sites. Thus, our analyses indicate that specialization within an antagonistic host-parasite (resource-consumer) system varies little between tropical and temperate localities.

Lower Detection Probability of Avian Plasmodium in Blood Compared to Other Tissues.

Abstract We tested whether the probability of detecting avian haemosporidia (Plasmodium and Haemoproteus) using molecular techniques differs among blood, liver, heart, and pectoral muscle tissues. We used a paired design, sampling the 4 tissue types in 55 individuals of a wild South American suboscine antbird, the white-shouldered fire-eye (Pyriglena leucoptera). We also identified parasites to cytochrome b lineage. Detection probability was significantly lower in blood compared to the other 3 tissue types combined. Eight of 22 infections were not detected in blood samples; 4–7 infections were not detected in the other individual tissues. The same parasite lineage was recovered from different tissues.

The “Atlantis Forest hypothesis” does not explain Atlantic Forest phylogeography

Leite et al. (1) conclude that isolation according to the forest refuge hypothesis (FRH) may have had a minor, if any, role on Atlantic Forest (AF) biotic evolution based on genetic data from five mammal species. Their evidence comes from signatures of population expansion during both glacial and interglacial periods, and fragmentation of reconstructed distributions during interglacial periods. Despite its novelty (i.e., the influence of sea-level changes in AF phylogeography), Leite et al.’s study presents many issues that need a critical appraisal. First, analyses based on a single locus are prone to stochastic error and often lack sufficient variation for detecting historical processes, such as bottlenecks and shallow population structure, which are key in contrasting refugium vs. nonrefugium hypotheses. Leite et al.’s (1 … [↵][1]1To whom correspondence should be addressed. Email: fabioraposo{at}gmail.com. [1]: #xref-corresp-1-1

Resource predictability and specialization in avian malaria parasites

We tested the hypothesis that avian haemosporidian (malaria) parasites specialize on hosts that can be characterized as predictable resources at a site in Amazonian Ecuador. We incorporated host phylogenetic relationship and relative abundance in assessing parasite specialization, and we examined associations between parasite specialization and three host characteristics – abundance, mass and longevity – using quantile regression, phylogenetic logistic regression and t‐tests. Hosts of specialist malaria parasite lineages were on average more abundant than hosts of generalist parasite lineages, but the relationship between host abundance and parasite specialization was not consistent across analyses. We also found support for a positive association between parasite specialization and host longevity, but this also was not consistent across analyses. Nonetheless, our findings suggest that the predictability of a host resource may play a role in the evolution of specialization. However, we also discuss two alternative explanations to the resource predictability hypothesis for specialization: (i) that interspecific interactions among the parasites themselves might constrain some parasites to a specialist strategy, and (ii) that frequent encounters with multiple host species, mediated by blood‐sucking insects, might promote generalization within this system.

Host associations and turnover of haemosporidian parasites in manakins (Aves: Pipridae)

Parasites of the genera Plasmodium and Haemoproteus (Apicomplexa: Haemosporida) are a diverse group of pathogens that infect birds nearly worldwide. Despite their ubiquity, the ecological and evolutionary factors that shape the diversity and distribution of these protozoan parasites among avian communities and geographic regions are poorly understood. Based on a survey throughout the Neotropics of the haemosporidian parasites infecting manakins (Pipridae), a family of Passerine birds endemic to this region, we asked whether host relatedness, ecological similarity and geographic proximity structure parasite turnover between manakin species and local manakin assemblages. We used molecular methods to screen 1343 individuals of 30 manakin species for the presence of parasites. We found no significant correlations between manakin parasite lineage turnover and both manakin species turnover and geographic distance. Climate differences, species turnover in the larger bird community and parasite lineage turnover in non-manakin hosts did not correlate with manakin parasite lineage turnover. We also found no evidence that manakin parasite lineage turnover among host species correlates with range overlap and genetic divergence among hosts. Our analyses indicate that host switching (turnover among host species) and dispersal (turnover among locations) of haemosporidian parasites in manakins are not constrained at this scale.

Duration of embryo development and the prevalence of haematozoan blood parasites in birds

ABSTRACT We used the prevalence of avian haemosporidian blood parasites (Plasmodium and Haemoproteus), quantified by PCR screening and DNA sequencing, to reevaluate a previously described negative relationship, based on microscopic examination of blood smears, between the prevalence of parasites in an avian host population and the length of the embryo development period of the host species. Analyses were restricted to small land birds in continental areas of the Americas. Prevalence determined by DNA methods averaged 22.5% and did not differ between tropical and temperate latitudes. Compared across taxonomic families or subfamilies, parasitism levels obtained by microscopic examination of blood smears and by DNA methods were strongly correlated and decreased, similarly in tropical and temperate latitudes, with increasing length of the embryo development period. Understanding the association of reduced haemosporidian infection with prolonged embryo development remains a fundamental challenge that emphasizes a potential role for defense against pathogens in the evolution of avian life histories.