Southeast Brazil is a neotropical region composed of a mosaic of different tropical habitats and mountain chains, which allowed for the formation of bird-rich communities with distinct ecological niches. Although this region has the potential to harbor a remarkable variety of avian parasites, there is a lack of information about the diversity of malarial parasites. We used molecular approaches to characterize the lineage diversity of Plasmodium and Haemoproteus in bird communities from three different habitats in southeast Brazil based on the prevalence, richness and composition of lineages. We observed an overall prevalence of 35.3%, with a local prevalence ranging from 17.2% to 54.8%. Moreover, no significant association between prevalence and habitat type could be verified (p>0.05). We identified 89 Plasmodium and 22 Haemoproteus lineages, with 86% of them described for the first time here, including an unusual infection of a non-columbiform host by a Haemoproteus (Haemoproteus) parasite. The composition analyses of the parasite communities showed that the lineage composition from Brazilian savannah and tropical dry forest was similar, but it was different from the lineage composition of Atlantic rainforest, reflecting the greater likeness of the former habitats with respect to seasonality and forest density. No significant effects of habitat type on lineage richness were observed based on GLM analyses. We also found that sites whose samples had a greater diversity of bird species showed a greater diversity of parasite lineages, providing evidence that areas with high bird richness also have high parasite richness. Our findings point to the importance of the neotropical region (southeast Brazil) as a major reservoir of new haemosporidian lineages.
Identifying the ecological factors that shape parasite distributions remains a central goal in disease ecology. These factors include dispersal capability, environmental filters and geographic distance. Using 520 haemosporidian parasite genetic lineages recovered from 7,534 birds sampled across tropical and temperate South America, we tested (a) the latitudinal diversity gradient hypothesis and (b) the distance–decay relationship (decreasing proportion of shared species between communities with increasing geographic distance) for this host–parasite system. We then inferred the biogeographic processes influencing the diversity and distributions of this cosmopolitan group of parasites across South America. We found support for a latitudinal gradient in diversity for avian haemosporidian parasites, potentially mediated through higher avian host diversity towards the equator. Parasite similarity was correlated with climate similarity, geographic distance and host composition. Local diversification in Amazonian lineages followed by dispersal was the most frequent biogeographic events reconstructed for haemosporidian parasites. Combining macroecological patterns and biogeographic processes, our study reveals that haemosporidian parasites are capable of circumventing geographic barriers and dispersing across biomes, although constrained by environmental filtering. The contemporary diversity and distributions of haemosporidian parasites are mainly driven by historical (speciation) and ecological (dispersal) processes, whereas the parasite community assembly is largely governed by host composition and to a lesser extent by environmental conditions.
How are ecological systems assembled? Here, we aim to contribute to answering this question by harnessing the framework of a novel integrative hypothesis. We shed light on the assembly rules of a multilayer network formed by frugivory and nectarivory interactions between bats and plants in the Neotropics. Our results suggest that, at a large scale, phylogenetic trade-offs separate species into different layers and modules. At an intermediate scale, the modules are also shaped by geographic trade-offs. And at a small scale, the network shifts to a nested structure within its modules, probably as a consequence of resource breadth processes. Finally, once the topology of the network is shaped, morphological traits related to consuming fruits or nectar determine which species are central or peripheral. Our results help understand how different processes contribute to the assemblage of ecological systems at different scales, resulting in a compound topology.
Identifying the mechanisms driving the distribution and diversity of parasitic organisms and characterizing the structure of parasite assemblages are critical to understanding host–parasite evolution, community dynamics, and disease transmission risk. Haemosporidian parasites of the genera Plasmodium and Haemoproteus are a diverse and cosmopolitan group of bird pathogens. Despite their global distribution, the ecological and historical factors shaping the diversity and distribution of these protozoan parasites across avian communities and geographic regions remain unclear. Here we used a region of the mitochondrial cytochrome b gene to characterize the diversity, biogeographical patterns, and phylogenetic relationships of Plasmodium and Haemoproteus infecting Amazonian birds. Specifically, we asked whether, and how, host community similarity and geography (latitude and area of endemism) structure parasite assemblages across 15 avian communities in the Amazon Basin. We identified 265 lineages of haemosporidians recovered from 2661 sampled birds from 330 species. Infection prevalence varied widely among host species, avian communities, areas of endemism, and latitude. Composition analysis demonstrated that both malarial parasites and host communities differed across areas of endemism and as a function of latitude. Thus, areas with similar avian community composition were similar in their parasite communities. Our analyses, within a regional biogeographic context, imply that host switching is the main event promoting diversification in malarial parasites. Although dispersal of haemosporidian parasites was constrained across six areas of endemism, these pathogens are not dispersal‐limited among communities within the same area of endemism. Our findings indicate that the distribution of malarial parasites in Amazonian birds is largely dependent on local ecological conditions and host evolutionary relationships.
One of the unresolved issues in the ecology of parasites is the relationship between host specificity and performance. Previous studies tested this relationship in different systems and obtained all possible outcomes. This led to the proposal of two hypotheses to explain conflicting results: the trade-off and resource breadth hypotheses, which are treated as mutually exclusive in the literature and were corroborated by different studies. In the present study, we used an extensive database on avian malaria from Brazil and combined analyses based on specificity indices and network theory, in order to test which of those hypotheses might best explain our model system. Contrary to our expectations, there was no correlation between specificity and prevalence, which contradicts both hypotheses. In addition, we detected a strong modular structure in our host-parasite network and found that its modules were not composed of geographically close, but of phylogenetically close, host species. Based on our results, we reached the conclusion that trade-off and resource breadth hypotheses are not really mutually exclusive. As a conceptual solution we propose "The Integrative Hypothesis of Parasite Specialization", a novel theoretical model that explains the contradictory results found in our study and reported to date in the literature.
13The architecture of interaction networks has been extensively studied in the past 14 decades, and different topologies have been observed in natural systems. Despite 15 several phenomenological explanations proposed, we still understand little of the 16 mechanisms that generate those topologies. Here we present a mechanistic model based 17on the integrative hypothesis of specialization, which aims at explaining the emergence 18 of topology and specialization in consumer-resource networks. By following three first-19 principles and adjusting five parameters, our model was able to generate synthetic 20 weighted networks that show the main patterns of topology and specialization observed 21 in nature. Our results prove that topology emergence is possible without network-level 22 selection. In our simulations, the intensity of trade-offs in the performance of each 23 consumer species on different resource species is the main factor driving network 24 topology. We predict that interaction networks with low species diversity and low 25 dissimilarity between resources should have a nested topology, although more diverse 26 networks with large dissimilarity should have a compound topology. Additionally, our 27 results highlight scale as a key factor. Our model generates predictions consistent with 28 ecological and evolutionary theories and real-world observations. Therefore, it supports 29 the IHS as a useful conceptual framework to study the architecture of interaction 30 networks. 31
Nestedness and modularity have been recurrently observed in species interaction networks. Some studies argue that those topologies result from selection against unstable networks, and others propose that they likely emerge from processes driving the interactions between pairs of species. Here we present a model that simulates the evolution of consumer species using resource species following simple rules derived from the integrative hypothesis of specialization (IHS). Without any selection on stability, our model reproduced all commonly observed network topologies. Our simulations demonstrate that resource heterogeneity drives network topology. On the one hand, systems containing only homogeneous resources form generalized nested networks, in which generalist consumers have higher performance on each resource than specialists. On the other hand, heterogeneous systems tend to have a compound topology: modular with internally nested modules, in which generalists that divide their interactions between modules have low performance. Our results demonstrate that all real‐world topologies likely emerge through processes driving interactions between pairs of species. Additionally, our simulations suggest that networks containing similar species differ from heterogeneous networks and that modules may not present the topology of entire networks.
What is the prevalent topology among interaction networks? How do consumers balance between generalism and performance when exploiting different resources? These two long-standing, still open questions have been unified under a common framework by the integrative hypothesis of specialization (IHS). According to the IHS, ecological specialization is structured by different processes at small and large network hierarchical levels, from an entire network to its modules and nodes. From those hierarchical processes, two patterns are expected. First, a modular network with internally nested modules, i.e. a compound topology. Second, different relationships between consumer performance and generalism on different network hierarchical levels. We confirmed those predictions using an extensive data set of host-parasite interactions, compiled from several studies, and spanning decades of fieldwork in the Palearctic Region. We used a set of topological analyses combined in a novel protocol based on the IHS to disentangle the complexity of this data set at different geographic scales, from local to regional. As predicted, the studied network indeed has a compound topology at both local and regional geographic scales. In addition, the relationship between parasite generalism and performance changes from negative in an entire network to positive within its modules. But, as expected, this shift in the signal of the generalism versus performance relationship happens only in local networks with a compound structure. Our results shed light on two central debates about topology and performance and provide insight into their solution.
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