Continental-scale patterns of pathogen prevalence: a case study on the corncrake

Pathogen infections can represent a substantial threat to wild populations, especially those already limited in size. To determine how much variation in the pathogens observed among fragmented populations is caused by ecological factors, one needs to examine systems where host genetic diversity is consistent among the populations, thus controlling for any potentially confounding genetic effects. Here, we report geographic variation in haemosporidian infection among European populations of corncrake. This species now occurs in fragmented populations, but there is little genetic structure and equally high levels of genetic diversity among these populations. We observed a longitudinal gradient of prevalence from western to Eastern Europe negatively correlated with national agricultural yield, but positively correlated with corncrake census population sizes when only the most widespread lineage is considered. This likely reveals a possible impact of local agriculture intensity, which reduced host population densities in Western Europe and, potentially, insect vector abundance, thus reducing the transmission of pathogens. We conclude that in the corncrake system, where metapopulation dynamics resulted in variations in local census population sizes, but not in the genetic impoverishment of these populations, anthropogenic activity has led to a reduction in host populations and pathogen prevalence

RELATIONSHIPS OF HAEMOSPORIDIAN PARASITES TO POPULATIONS OF THEIR AVIAN HOSTS IN EASTERN NORTH AMERICA

Avian Haemosporida are common, vector-transmitted blood parasites of birds throughout the world. During my dissertation research, I explored how multiple host species respond immunologically to natural infections in the wild (Chapter 1) and to experimental infections in the laboratory (Chapter 2). Despite their tractability as a model host-parasite system and a burgeoning literature on avian Haemosporida, little is known about how their populations interact across large areas (hereafter “regions”). I present data from parasite surveys of birds across eastern North America suggesting that continental parasite populations track host populations across the region, but also that the host breadth of a parasite can be variable across space and time (Chapter 3). Parasite lineages replace each other spatially within a host population, likely due to interspecific parasite competition mediated by host immune systems (Chapter 3). Parasite prevalence is positively related to host abundance within local assemblages (Chapter 4), but within host species across their ranges, prevalence does not vary with abundance (Chapters 3 and 4). Finally, a 12 year survey of parasites and their hosts in the Missouri Ozarks demonstrates that parasite populations vary through time, and that this variability is related to host breadth—specialist parasites (i.e., parasites infecting primarily one host) were more variable than generalist parasites (i.e., parasites infecting multiple hosts; Chapter 5). Overall my dissertation work contributes to the natural history and ecology of avian Haemosporidian parasites and their avian hosts, and to host-parasite ecological and evolutionary theory

Co- and mixed-infections of avian haemosporidian parasites in great tits and blue tits of the French Pyrenees

Avian haemosporidia have played a significant role in advancing our understanding of vectored disease epidemiology, and continue to do so. These diverse blood parasites (inclusive of those responsible for avian malaria) are globally distributed, adopt both host-generalist and host-specialist infection strategies, and can be highly pathogenic. Due the diversity of haemosporidia, many avian populations play host to species rich communities of blood parasites. Interactions between parasites coinfecting a single host can lead to increased pathological costs, between-parasite competition may additionally influence spatial and/or temporal parasite distributions. However, many questions remain regarding the implications of these parasite-parasite interactions and their relevance in nature. In this thesis, I study three genera of avian haemosporidia (Haemoproteus, Leucocytozoon, and Plasmodium) which form a community infecting two geographically overlapping host species, blue tits (Cyanistes caeruleus) and great tits (Parus major). In chapter one, I apply a novel-PCR detection method, which improves the sensitivity of such techniques, to survey the complete local haemosporidian community infecting these birds. Leucocytozoon is the most prevalent genus, infecting >90% of individuals. I identify a significant negative association between Leucocytozoon and Haemoproteus spp., which exists despite similar spatial distributions. An interaction is also identified between two clades of Leucocytozoon, Clade A and Clade D, as mixed-infections are lower than predicted. In chapter two, I further explore this Leucocytozoon clade interaction. Clade A is more prevalent in great tits, while Clade D more prevalent in blue tits, neither impact reproductive measures in their typical host. Clade A has lower prevalence in blue tits, but does carry reproductive costs. Blue tits which have Clade D infections are less likely to be infected by Clade A, which implies a conferred resistance against this great tit-typical parasite. Collectively, these studies reveal complex interactions occurring within a multi-host, multi-parasite community which have important implications for haemosporidia epidemiology and parasite-host co-evolution

Avian Haemosporidians: Detection, Host, and Climate Association Across Contrasting Regions of Africa

Avian haemosporidians make up one of the most widely distributed and diverse vector borne parasite systems, found nearly worldwide. While there has been growth in the use of avian haemosporidians as a model system for vector borne parasites, there remain unanswered questions in this system. Little remains known of the variation in results when assessing various source materials and how these recoveries bias our results. Further, a majority of avian haemosporidian diversity likely remains undiscovered particularly across sub-Saharan Africa. Each new recovery helps to further elucidate distributional patterns of diversification. Few studies have addressed the importance of source material selection when assessing these relationships. We show that source material, here blood and pectoral muscle, do not yield equivalent results when assessing prevalence and genetic diversity of haemosporidian genera. We find higher prevalence and genetic diversity is recovered from blood versus pectoral muscle for Haemoproteus. Contrastingly, we find that a higher prevalence of Plasmodium is detected from pectoral muscle, while higher genetic diversity is recovered from blood. Results indicate that source material may bias parasite detection and be an important factor in study design. We conducted the first sampling of avian haemosporidians, Haemoproteus, Leucocytozoon, and Plasmodium from Benin located in tropical West Africa and the Democratic Republic of the Congo. We sampled 222 and 421 birds, respectively, across distinct ecoregions with varied habitats. We detected haemosporidians in 113 of 222 individuals, resulting in a 50.9% infection rate in Benin. We detected haemosporidians in 187 of 421 individuals, resulting in a 42.4% infection rate in the Democratic Republic of the Congo. We molecularly recovered a high number of novel lineages, 52.9% and 71.4%, respectively. We characterized the multivariate variables which influence the distributions of haemosporidians genetic lineages, including host associations and bioclimatic variables for sampling from Benin. We introduce a novel visualization method to better capture the multivariate environment of haemosporidians, and this approach resulted in the recovery of intra-generic distribution patterns of diversity. We assessed host life history traits as a proxy for vector encounter rate and examined the variation in expressed traits across families with high sampling

Factors affecting the distribution of haemosporidian parasites within an oceanic island

Understanding how different ecological and evolutionary processes influence the distribution of pathogens within the environment is important from many perspectives including wildlife epidemiology, evolutionary ecology and conservation. The simultaneous use of ecological and evolutionary frameworks can enhance our conceptual understanding of host-parasite interactions, however such studies are rare in the wild. Using samples from 12 bird species caught across all habitats existing on an oceanic island, we evaluated how environmental variables, parasite host specificity and parasite phylogenetic relationships determine the distribution and prevalence of haemosporidians (Haemoproteus, Plasmodium and Leucocytozoon) in the wild living avifauna. Differences were found in the prevalence of Plasmodium, but not Leucocytozoon, strains between habitats. The warmest temperature best predicted Plasmodium prevalence in the low altitude habitats, which had the highest incidence of Plasmodium. The prevalence of Leucocytozoon lineages was associated with natural factors, i.e. rainfall, temperature and habitat, but the two most important predictors (from model averaging) for models of Leucocytozoon were anthropogenic: poultry farms and distance to a water reservoir. We found no relationship between local (Tenerife, Canary Islands) versus global host range indices (which assess the diversity of hosts that a parasite is observed to infect), thus global generalist lineages do not behave in the same way on Tenerife (i.e. they infected less avian hosts than was expected). Phylogenetic analysis revealed that the most abundant haemosporidians on Tenerife grouped with lineages found in African host species. Our data indicate that climatic and anthropogenic factors, plus proximity to the African mainland, are the main factors influencing the presence and distribution of avian haemosporidians on Tenerife. Future climate projections for the archipelago foresee significant temperature increases which would, given our results, increase rates of Plasmodium infection in bird species in all habitats. Such patterns could be of concern if those increase mortality rates in the unique avifauna of these islands

Avian haemosporidian diversity on Sardinia: a first general assessment for the Insular Mediterranean

The Western Palearctic is one of the most investigated regions for avian haemosporidian parasites (Haemoproteus, Plasmodium and Leucocytozoon), yet geographic gaps in our regional knowledge remain. Here, we report the first haemosporidian screening of the breeding birds from Sardinia (the second-largest Mediterranean Island and a biodiversity hotspot), and the first for the insular Mediterranean in general. We examined the occurrence of haemosporidians by amplifying their mtDNA cytb gene in 217 breeding birds, belonging to 32 species. The total prevalence of infected birds was 55.3%, and of the 116 haplotypes recovered, 84 were novel. Despite the high number of novel lineages, phylogenetic analysis did not highlight Sardinia-specific clades; instead, some Sardinian lineages were more closely related to lineages previously recovered from continental Europe. Host-parasite network analysis indicated a specialized host-parasite community. Binomial generalized linear models (GLMs), performed at the community level, suggested an elevational effect on haemosporidian occurrence probability (negative for Haemoproteus; positive for Leucocytozoon) likely due to differences in the abundance of insect vectors at different elevations. Furthermore, a GLM revealed that sedentary birds showed a higher probability of being infected by novel haplotypes and long-distance migrants showed a lower probability of novel haplotype infection. We hypothesize that the high diversity of haemosporidians is linked to the isolation of breeding bird populations on Sardinia. This study adds to the growing knowledge on haemosporidians lineage diversity and distribution in insular environments and presents new insights on potential host-parasite associations

Revealing the drivers of parasite community assembly: using avian haemosporidians to model global dynamics of parasite species turnover

Why do some regions share more or fewer species than others? Community assembly relies on the ability of individuals to disperse, colonize and thrive in new regions. Therefore, many distinct factors, such as geographic distance and environmental features, can determine the odds of a species colonizing a new environment. For parasites, host community composition (i.e. resources) also plays a key role in their ability to colonize a new environment as they rely on their hosts to complete their life cycle. Thus, variation in host community composition and environmental conditions should determine parasite turnover among regions. Here, we explored the global drivers of parasite turnover using avian malaria and malaria-like (haemosporidian) parasites. We compiled global databases on avian haemosporidian lineages distributions, environmental conditions, avian species distributions and functional traits, and ran generalized dissimilarity models to uncover the main drivers of parasite turnover. We demonstrated that haemosporidian parasite turnover is mainly driven by geographic distance followed by host functional traits, environmental conditions and host distributions. The main host functional traits associated with high parasite turnover were the predominance of resident (i.e. non-migratory) species and strong territoriality, while the most important climatic drivers of haemosporidian turnover were mean temperature and temperature seasonality. Overall, we established the importance of geographic distance as a key predictor of ecological dissimilarity and showed that host resources influence parasite turnover more strongly than environmental conditions. We also evidenced that parasite turnover is most pronounced among tropical and less interconnected regions (i.e. regions with mostly territorial and non-migratory hosts). Our findings provide a robust foundation for the prediction of avian pathogen spread and the emergence of infectious diseases.Fil: de Angeli Dutra, Daniela. University of Otago; Nueva ZelandaFil: Barros Pereira Pinheiro, Rafael. Universidade Estadual de Campinas; BrasilFil: Fecchio, Alan. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte. Centro de Investigación Esquel de Montaña y Estepa Patagónica. Universidad Nacional de la Patagonia "San Juan Bosco". Centro de Investigación Esquel de Montaña y Estepa Patagónica; ArgentinaFil: Poulin, Robert. University of Otago; Nueva Zeland

Biogeografía de los parásitos sanguíneos en un hospedador aviar modelo con diversas estrategias migratorias: la curruca capirotada "Sylvia atricapilla"

Tesis inédita de la Universidad Complutense de Madrid, Facultad de Ciencias Biológicas, Departamento de Zoología y Antropología Física, leída el 17/09/2013The negative effects that parasites have on their hosts’ fitness make of parasitism one of the main evolutive agents. The knowledge of which are the factors that determine the spatiotemporal distribution of parasites impacts is hence critical if we are to anticipate the threat posed by emergent diseases in a context of global change. This PhD Thesis used the blackcap Sylvia atricapilla (Aves: Sylviidae) and its haemosporidian parasites (genera Plasmodium, Haemoproteus y Leucocytozoon; Apicomplexa) as a model system to test how several sources of environmental variation determine the differences on parasite impacts. First we identified which variables in an Iberian context were the main determinants of parasite diversity, finding out that although climatic variables (mainly temperature) were the most relevant ones, including orographic variables into the analyses increased their significance. Then we used this information to predict the current and future distribution of the areas under a strong parasitic pressure in the Iberian Peninsula, forecasting a future reshuffling of the current host-parasite relationships mosaic. We also performed a reconstruction of how different strategies of seasonal transmission (summer transmission, extended summer transmission and year-round transmission) have evolved through the evolutionary history of these parasites, discovering that, although year-round transmission has appeared multiple independent times and it is an ecologically successful strategy, it is not as successful as seasonal transmission in the long run. Finally, by examining the parasitic communities of the blackcaps inhabiting the archipelagos of the Canay Islands and Madeira, we found out that host-parasite relationships are compromised in insular environments, and that insular syndromes (low richness, host switching and host generalism) develop among parasites even before the development of full isolation.Los efectos negativos que los parásitos tienen sobre la eficacia biológica de sus hospedadores hacen del parasitismo uno de los principales agentes evolutivos. Por esta razón, conocer los factores que determinan la distribución espacial y temporal del impacto de los parásitos es crítico para anticiparnos a los problemas que las enfermedades emergentes pueden provocar en un contexto de cambio climático. Esta tesis emplea la curruca capirotada Sylvia atricapilla (Aves: Sylviidae) y sus parásitos sanguíneos hemosporidios (géneros Plasmodium, Haemoproteus y Leucocytozoon; Apicomplexa) como modelo de estudio para examinar cómo diversas fuentes de variación ambiental determinan las diferencias en el impacto de los parásitos. Se identificaron primero qué variables tienen mayor importancia en un contexto ibérico como determinantes de la diversidad de parásitos, encontrándose que si bien las variables ambientales (temperatura principalmente) son las más importantes, los modelos mejoran significativamente si se incluyen variables orográficas. Se usaron luego estos datos para examinar la distribución actual y la esperada a finales del S. XXI bajo tres escenarios de cambio climático de las zonas sujetas a un mayor impacto de estos parásitos en la Península, evidenciándose una reestructuración futura del mosaico actual de relaciones entre parásitos y hospedadores. Se realizó también una reconstrucción de cómo han evolucionado diferentes estrategias de transmisión estacional (transmisión estival, transmisión estival expandida y transmisión continua) a lo largo de la historia evolutiva de estos parásitos, encontrándose que paradójicamente la estructura ecológicamente más exitosa (transmisión continua) no es la más exitosa a largo plazo (transmisión estival). Finalmente, examinando las comunidades de parásitos de las currucas de Canarias y Madeira se descubrió que las relaciones parásito-hospedador habituales se ven comprometidas en ambientes insulares, y de que los síndromes insulares del parasitismo (riqueza baja, frecuentes cambios de hospedador y tendencia al generalismo) pueden desarrollarse incluso en la ausencia de aislamiento completo.Depto. de Biodiversidad, Ecología y EvoluciónFac. de Ciencias BiológicasTRUEunpu

Host life-history traits predict haemosporidian parasite prevalence in tanagers (Aves: Thraupidae)

Vector-borne parasites are important ecological drivers influencing life-history evolution in birds by increasing host mortality or susceptibility to new diseases. Therefore, understanding why vulnerability to infection varies within a host clade is a crucial task for conservation biology and for understanding macroecological life-history patterns. Here, we studied the relationship of avian life-history traits and climate on the prevalence of Plasmodium and Parahaemoproteus parasites. We sampled 3569 individual birds belonging to 53 species of the family Thraupidae. Individuals were captured from 2007 to 2018 at 92 locations. We created 2 phylogenetic generalized least-squares models with Plasmodium and Parahaemoproteus prevalence as our response variables, and with the following predictor variables: climate PC1, climate PC2, body size, mixed-species flock participation, incubation period, migration, nest height, foraging height, forest cover, and diet. We found that Parahaemoproteus and Plasmodium prevalence was higher in species inhabiting open habitats. Tanager species with longer incubation periods had higher Parahaemoproteus prevalence as well, and we hypothesize that these longer incubation periods overlap with maximum vector abundances, resulting in a higher probability of infection among adult hosts during their incubation period and among chicks. Lastly, we found that Plasmodium prevalence was higher in species without migratory behaviour, with mixed-species flock participation, and with an omnivorous or animal-derived diet. We discuss the consequences of higher infection prevalence in relation to life-history traits in tanagers.Fil: Aguiar de Souza Penha, Victor. Universidade Federal do Paraná; BrasilFil: Maia Chaves Bicalho Domingos, Fabricius. Universidade Federal do Paraná; BrasilFil: Fecchio, Alan. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte. Centro de Investigación Esquel de Montaña y Estepa Patagónica. Universidad Nacional de la Patagonia "San Juan Bosco". Centro de Investigación Esquel de Montaña y Estepa Patagónica; ArgentinaFil: Bell, Jeffrey A.. University of South Dakota; Estados UnidosFil: Weckstein, Jason D.. No especifíca;Fil: Ricklefs, Robert E.. University of Missouri; Estados UnidosFil: Martins Braga, Erika. Universidade Federal de Minas Gerais; BrasilFil: de Abreu Moreira, Patrícia. Universidade Federal de Ouro Preto; BrasilFil: Soares, Leticia. University of Western Australia; AustraliaFil: Latta, Steven. No especifíca;Fil: Tolesano Pascoli, Graziela. Universidade do Brasília; BrasilFil: Alquezar, Renata Duarte. Universidade do Brasília; BrasilFil: Del Claro, Kleber. Universidade Federal de Uberlandia; BrasilFil: Tonelli Manica, Lilian. Universidade Federal do Paraná; Brasi