Evolutionary ecology, taxonomy, and systematics of avian malaria and related parasites

Aim: Macroecological analyses provide valuable insights into factors that influence how parasites are distributed across space and among hosts. Amid large uncertainties that arise when generalizing from local and regional findings, hierarchical approaches applied to global datasets are required to determine whether drivers of parasite infection patterns vary across scales. We assessed global patterns of haemosporidian infections across a broad diversity of avian host clades and zoogeographical realms to depict hotspots of prevalence and to identify possible underlying drivers. Location: Global. Time period: 1994–2019. Major taxa studied: Avian haemosporidian parasites (genera Plasmodium, Haemoproteus, Leucocytozoon and Parahaemoproteus). Methods: We amalgamated infection data from 53,669 individual birds representing 2,445 species world-wide. Spatio-phylogenetic hierarchical Bayesian models were built to disentangle potential landscape, climatic and biotic drivers of infection probability while accounting for spatial context and avian host phylogenetic relationships. Results: Idiosyncratic responses of the three most common haemosporidian genera to climate, habitat, host relatedness and host ecological traits indicated marked variation in host infection rates from local to global scales. Notably, host ecological drivers, such as migration distance for Plasmodium and Parahaemoproteus, exhibited predominantly varying or even opposite effects on infection rates across regions, whereas climatic effects on infection rates were more consistent across realms. Moreover, infections in some low-prevalence realms were disproportionately concentrated in a few local hotspots, suggesting that regional-scale variation in habitat and microclimate might influence transmission, in addition to global drivers. Main conclusions: Our hierarchical global analysis supports regional-scale findings showing the synergistic effects of landscape, climate and host ecological traits on parasite transmission for a cosmopolitan and diverse group of avian parasites. Our results underscore the need to account for such interactions, in addition to possible variation in drivers across regions, to produce the robust inference required to predict changes in infection risk under future scenarios.

Global drivers of avian haemosporidian infections vary across zoogeographical regions

Zika virus is an emerging arbovirus of humans in the western hemisphere. With its potential spread into new geographical areas, it is important to define the vector competence of native mosquito species. We tested the vector competency of Aedes vexans (Meigen) from the Lake Agassiz Plain of northwestern Minnesota and northeastern North Dakota. Aedes aegypti (L.) was used as a positive control for comparison. Mosquitoes were fed blood containing Zika virus and 2 wk later were tested for viral infection and dissemination. Aedes vexans (n = 60) were susceptible to midgut infection (28% infection rate) but displayed a fairly restrictive midgut escape barrier (3% dissemination rate). Cofed Ae. aegypti (n = 22) displayed significantly higher rates of midgut infection (61%) and dissemination (22%). To test virus transmission, mosquitoes were inoculated with virus and 16-17 d later, tested for their ability to transmit virus into fluid-filled capillary tubes. Unexpectedly, the transmission rate was significantly higher for Ae. vexans (34%, n = 47) than for Ae. aegypti (5%, n = 22). The overall transmission potential for Ae. vexans to transmit Zika virus was 1%. Because of its wide geographic distribution, often extreme abundance, and aggressive human biting activity, Ae. vexans could serve as a potential vector for Zika virus in northern latitudes where the conventional vectors, Ae. aegypti and Ae. albopictus Skuse, cannot survive. However, Zika virus is a primate virus and humans are the only amplifying host species in northern latitudes. To serve as a vector of Zika virus, Ae. vexans must feed repeatedly on humans. Defining the propensity of Ae. vexans to feed repeatedly on humans will be key to understanding its role as a potential vector of Zika virus.

https://par.nsf.gov/servlets/purl/10026151

Potential of a Northern Population of Aedes vexans (Diptera: Culicidae) to Transmit Zika Virus.

To understand local transmission of vector-borne diseases, it is important to identify potential vectors, characterize their host feeding patterns, and determine if vector-borne pathogens are circulating within the region. This study simultaneously investigated these aspects of disease transmission by collecting engorged mosquitoes within two rural study sites in the central Red River Valley of North Dakota. Mosquitoes were identified, midguts were excised, and the blood was expelled from the midguts. DNA was extracted from blood meals and subjected to PCR and direct sequencing to identify the vertebrate origin of the blood. Using different primer sets, PCR was used to screen for two types of vector-borne pathogens, filarioid nematodes and hemosporidian parasites. White-tailed deer were the primary source of blood meals for the eight aedine mosquito species collected. None of the 288 deer-derived blood meals contained filarioid or hemosporidian DNA. In contrast, 18 of 32 Culex tarsalis and three of three Cx. pipiens blood meals contained avian blood, representing eight different species of birds. Of 24 avian-derived blood meals examined, 12 contained Plasmodium DNA, three of which also contained Leucocytozoon DNA (i.e., dual infection). Potential confounding effects resulting from parasite acquisition and development from previous blood meals (e.g., oocysts) were eliminated because host blood had been removed from the midguts prior to DNA extraction. Thus, specific parasite lineages/species could be unequivocally linked to specific vertebrate species. By combining mosquito identification with molecular techniques for identifying blood meal source and pathogens, a relatively small sample of engorged mosquitoes yielded important new information about mosquito feeding patterns and hemosporidia infections in birds. Thorough analyses of wild-caught engorged mosquitoes and other arthropods represent a powerful tool in understanding the local transmission of vector-borne and zoonotic diseases.

/pdf/molecular-identification-of-vertebrate-and-hemoparasite-dna-oi31crjm6i.pdf

Molecular Identification of Vertebrate and Hemoparasite DNA Within Mosquito Blood Meals From Eastern North Dakota

Migration has an important impact on the transmission of pathogens. Migratory birds disperse parasites through their routes and may consequently introduce them to new areas and hosts. Hence, haemosporidian parasites, which are among the most prevalent, diverse and important bird pathogens, are potentially dispersed when infecting migrant hosts. Further, migrant hosts could enhance local parasite prevalence and richness by transporting new parasite strains to new areas. Here, we hypothesize and aim to evaluate if 1) migratory birds spread parasite lineages along their routes, and 2) localities crossed by more migratory birds have greater prevalence and richness of haemosporidians. For the first hypothesis, we tested whether parasite lineages found 1) in both migrants and residents, and 2) only in residents, differ in their frequencies of occurrence among localities. For the second hypothesis, we tested for a relationship among localities between the overall local haemosporidian parasite richness and prevalence, and the proportion of migratory bird individuals present in a locality. We combined a dataset on 13 200 bird samples with additional data from the MalAvi database (total: ~2800 sequenced parasites comprising 675 distinct lineages, from 506 host species and 156 localities) from South America, and used Bayesian multi‐level models to test our hypotheses. We demonstrate that parasites shared between resident and migratory species are the most spatially widespread, highlighting the potential of migrants to carry and transmit haemosporidians. Further, the presence of migrants in a locality was negatively related to local parasite richness, but not associated with local prevalence. Here, we confirm that migrants can contribute to parasite dispersal and visiting migrants are present in regions with lower Plasmodium prevalence. Also, we observed their presence might raise Haemoproteus community prevalence. Therefore, we demonstrate migrants enhance pathogens spread and their presence may influence parasite community transmission.

Migrant birds disperse haemosporidian parasites and affect their transmission in avian communities

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.

An inverse latitudinal gradient in infection probability and phylogenetic diversity for Leucocytozoon blood parasites in New World birds.

Vertebrate reservoirs of arboviruses are often infected with microfilariae (MF). Laboratory studies have shown that MF can enhance the infectivity of arboviruses to mosquitoes. Soon after being ingested, MF penetrate the mosquito midgut. If the host blood also contains virus (i.e., vertebrate is dually infected), penetrating MF may introduce virus into the hemocoel. This can transform otherwise virus-incompetent mosquito species into virus-competent species and simultaneously accelerate viral development, allowing mosquitoes to transmit virus sooner than normal. This phenomenon is termed microfilarial enhancement of arboviral transmission. The prevalence of MF is very high in many passerine populations in North America. Therefore, we investigated if microfilarial enhancement could have facilitated the establishment and rapid spread of West Nile virus (WNV) across the mid-western United States. Our investigations revealed that mosquitoes, WNV, and passerine MF do interact in nature because; 1) 17% of 54 common grackles (Quiscalus quiscula L.), 8% of 26 American robins (Turdus migratorius L.), and 33% of three eastern kingbirds (Tyrannus tyrannus L.) were concurrently microfilaremic and seropositive to WNV; 2) feeding activities of mosquitoes overlapped temporally with the appearance of MF in the blood of common grackles; 3) mosquitoes fed on common grackles and American robins in nature; and 4) mosquito ingestion of two taxonomically distant species of passerine MF (i.e., Chandlerella quiscali and Eufilaria spp.) resulted in penetration of mosquito midguts. To estimate the theoretical effect that MF enhancement could have on WNV transmission in areas of high MF prevalence, vectorial capacity values were calculated for Culex mosquitoes feeding on common grackles, whereby MF enhancement was either invoked or ignored. For Cx. pipiens, vectorial capacity increased over three-fold when potential effects of MF were included in the calculations. For Cx. tarsalis, the effect was less (i.e., 1.4-fold increase). Closer attention should be paid to the potential of MF to enhance mosquito transmission of arboviruses.

https://bioone.org/journals/journal-of-medical-entomology/volume-49/issue-6/ME12103/Theoretical-Potential-of-Passerine-Filariasis-to-Enhance-the-Enzootic-Transmission/10.1603/ME12103.pdf

Theoretical potential of passerine filariasis to enhance the enzootic transmission of West Nile virus.

Prevalence, Statistical Trends and Phylogenetics of Blood Parasites (Haemosporidia: Haemoproteus, Plasmodium and Leucocytozoon) in Songbird Passerines from Grasslands of northwest Minnesota

Danielle Kay Kvasager

Papers

An inverse latitudinal gradient in infection probability and phylogenetic diversity for Leucocytozoon blood parasites in New World birds.

Theoretical potential of passerine filariasis to enhance the enzootic transmission of West Nile virus.

Prevalence, Statistical Trends and Phylogenetics of Blood Parasites (Haemosporidia: Haemoproteus, Plasmodium and Leucocytozoon) in Songbird Passerines from Grasslands of northwest Minnesota