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The factors that influence whether a parasite is likely to cause death in a given host species are not well known. Generalist parasites with high local abundances, broad distributions and the ability to infect a wide phylogenetic diversity of hosts are often considered especially dangerous for host populations, though comparatively little research has been done on the potential for specialist parasites to cause host mortality. Here, using a novel database of avian mortality records, we tested whether phylogenetic host specialist or host generalist haemosporidian blood parasites were associated with avian host deaths based on infection records from over 81 000 examined hosts. In support of the hypothesis that host specialist parasites can be highly virulent in novel hosts, we found that the parasites that were associated with avian host mortality predominantly infected more closely related host species than expected under a null model. Hosts that died tended to be distantly related to the host species that a parasite lineage typically infects, illustrating that specialist parasites can cause death outside of their limited host range. Overall, this study highlights the overlooked potential for host specialist parasites to cause host mortality despite their constrained ecological niches.

Turnover in species composition between sites, or beta diversity, is a critical component of species diversity that is typically influenced by geography, environment, and biotic interactions. Quantifying turnover is particularly challenging, however, in multi-host, multi-parasite assemblages where undersampling is unavoidable, resulting in inflated estimates of turnover and uncertainty about its spatial scale. We developed and implemented a framework using null models to test for community turnover in avian haemosporidian communities of three sky islands in the southwestern United States. We screened 776 birds for haemosporidian parasites from three genera (Parahaemoproteus, Plasmodium, and Leucocytozoon) by amplifying and sequencing a mitochondrial DNA barcode. We detected infections in 280 birds (36.1%), sequenced 357 infections, and found a total of 99 parasite haplotypes. When compared to communities simulated from a regional pool, we observed more unique, single-mountain haplotypes and fewer haplotypes shared among three mountain ranges than expected, indicating that haemosporidian communities differ to some degree among adjacent mountain ranges. These results were robust even after pruning datasets to include only identical sets of host species, and they were consistent for two of the three haemosporidian genera. The two more distant mountain ranges were more similar to each other than the one located centrally, suggesting that the differences we detected were due to stochastic colonization-extirpation dynamics. These results demonstrate that avian haemosporidian communities of temperate-zone forests differ on relatively fine spatial scales between adjacent sky islands. Null models are essential tools for testing the spatial scale of turnover in complex, undersampled, and poorly known systems.

Geographic variation in environmental conditions as well as host traits that promote parasite transmission may impact infection rates and community assembly of vector-transmitted parasites. Identifying the ecological, environmental and historical determinants of parasite distributions and diversity is therefore necessary to understand disease outbreaks under changing environments. Here, we identified the predictors and contributions of infection probability and phylogenetic diversity of Leucocytozoon (an avian blood parasite) at site and species levels across the New World. To explore spatial patterns in infection probability and lineage diversity for Leucocytozoon parasites, we surveyed 69 bird communities from Alaska to Patagonia. Using phylogenetic Bayesian hierarchical models and high-resolution satellite remote-sensing data, we determined the relative influence of climate, landscape, geography and host phylogeny on regional parasite community assembly. Infection rates and parasite diversity exhibited considerable variation across regions in the Americas. In opposition to the latitudinal gradient hypothesis, both the diversity and prevalence of Leucocytozoon parasites decreased towards the equator. Host relatedness and traits known to promote vector exposure neither predicted infection probability nor parasite diversity. Instead, the probability of a bird being infected with Leucocytozoon increased with increasing vegetation cover (NDVI) and moisture levels (NDWI), whereas the diversity of parasite lineages decreased with increasing NDVI. Infection rates and parasite diversity also tended to be higher in cooler regions and higher latitudes. Whereas temperature partially constrains Leucocytozoon diversity and infection rates, landscape features, such as vegetation cover and water body availability, play a significant role in modulating the probability of a bird being infected. This suggests that, for Leucocytozoon, the barriers to host shifting and parasite host range expansion are jointly determined by environmental filtering and landscape, but not by host phylogeny. Our results show that integrating host traits, host ancestry, bioclimatic data and microhabitat characteristics that are important for vector reproduction are imperative to understand and predict infection prevalence and diversity of vector-transmitted parasites. Unlike other vector-transmitted diseases, our results show that Leucocytozoon diversity and prevalence will likely decrease with warming temperatures., (© 2019 The Authors. Journal of Animal Ecology © 2019 British Ecological Society.)

Metatranscriptomics is a powerful method for studying the composition and function of complex microbial communities. The application of metatranscriptomics to multispecies parasite infections is of particular interest, as research on parasite evolution and diversification has been hampered by technical challenges to genome-scale DNA sequencing. In particular, blood parasites of vertebrates are abundant and diverse although they often occur at low infection intensities and exist as multispecies infections, rendering the isolation of genomic sequence data challenging. Here, we use birds and their diverse haemosporidian parasites to illustrate the potential for metatranscriptome sequencing to generate large quantities of genome-wide sequence data from multiple blood parasite species simultaneously. We used RNA-sequencing of 24 blood samples from songbirds in North America to show that metatranscriptomes can yield large proportions of haemosporidian protein-coding gene repertoires even when infections are of low intensity (<0.1% red blood cells infected) and consist of multiple parasite taxa. By bioinformatically separating host and parasite transcripts and assigning them to the haemosporidian genus of origin, we found that transcriptomes detected ~23% more total parasite infections across all samples than were identified using microscopy and DNA barcoding. For single-species infections, we obtained data for >1,300 loci from samples with as low as 0.03% parasitaemia, with the number of loci increasing with infection intensity. In total, we provide data for 1,502 single-copy orthologous loci from a phylogenetically diverse set of 33 haemosporidian mitochondrial lineages. The metatranscriptomic approach described here has the potential to accelerate ecological and evolutionary research on haemosporidians and other diverse parasites., (© 2019 John Wiley & Sons Ltd.)

Haemosporidian parasites of birds are ubiquitous in terrestrial ecosystems, but their coevolutionary dynamics remain poorly understood. If species turnover in parasites occurs at a finer scale than turnover in hosts, widespread hosts would encounter diverse parasites, potentially diversifying as a result. Previous studies have shown that some wide-ranging hosts encounter varied haemosporidian communities throughout their range, and vice-versa. More surveys are needed to elucidate mechanisms that underpin spatial patterns of diversity in this complex multi-host multi-parasite system. We sought to understand how and why a community of avian haemosporidian parasites varies in abundance and composition across elevational transects in eight sky islands in southwestern North America. We tested whether bird community composition, environment, or geographic distance explain haemosporidian parasite species turnover in a widespread host that harbors a diverse haemosporidian community, the Audubon's Warbler (Setophaga auduboni). We tested predictors of infection using generalized linear models, and predictors of bird and parasite community dissimilarity using generalized dissimilarity modeling. Predictors of infection differed by parasite genus: Parahaemoproteus was predicted by elevation and climate, Leucocytozoon varied idiosyncratically among mountains, and Plasmodium was unpredictable, but rare. Parasite turnover was nearly three-fold higher than bird turnover and was predicted by elevation, climate, and bird community composition, but not geographic distance. Haemosporidian communities vary strikingly at fine spatial scales (hundreds of kilometers), across which the bird community varies only subtly. The finer scale of turnover among parasites implies that their ranges may be smaller than those of their hosts. Avian host species should encounter different parasite species in different parts of their ranges, resulting in spatially varying selection on host immune systems. The fact that parasite turnover was predicted by bird turnover, even when considering environmental characteristics, implies that host species or their phylogenetic history plays a role in determining which parasite species will be present in a community., (Copyright © 2019 Australian Society for Parasitology. Published by Elsevier Ltd. All rights reserved.)