RESUMEN

A most interesting exception within the parasitic Apicomplexa is Nephromyces, an extracellular, probably mutualistic, endosymbiont found living inside molgulid ascidian tunicates (i.e., sea squirts). Even though Nephromyces is now known to be an apicomplexan, many other questions about its nature remain unanswered. To gain further insights into the biology and evolutionary history of this unusual apicomplexan, we aimed to 1) find the precise phylogenetic position of Nephromyces within the Apicomplexa, 2) search for the apicoplast genome of Nephromyces, and 3) infer the major metabolic pathways in the apicoplast of Nephromyces. To do this, we sequenced a metagenome and a metatranscriptome from the molgulid renal sac, the specialized habitat where Nephromyces thrives. Our phylogenetic analyses of conserved nucleus-encoded genes robustly suggest that Nephromyces is a novel lineage sister to the Hematozoa, which comprises both the Haemosporidia (e.g., Plasmodium) and the Piroplasmida (e.g., Babesia and Theileria). Furthermore, a survey of the renal sac metagenome revealed 13 small contigs that closely resemble the genomes of the nonphotosynthetic reduced plastids, or apicoplasts, of other apicomplexans. We show that these apicoplast genomes correspond to a diverse set of most closely related but genetically divergent Nephromyces lineages that co-inhabit a single tunicate host. In addition, the apicoplast of Nephromyces appears to have retained all biosynthetic pathways inferred to have been ancestral to parasitic apicomplexans. Our results shed light on the evolutionary history of the only probably mutualistic apicomplexan known, Nephromyces, and provide context for a better understanding of its life style and intricate symbiosis.

Asunto(s)

Apicomplexa/genética , Apicoplastos/genética , Genoma , Apicomplexa/clasificación , Núcleo Celular/genética , Redes y Vías Metabólicas/genética , Filogenia

RESUMEN

The class Hematozoa encompasses several clinically important genera, including Plasmodium, whose members cause the major life-threating disease malaria. Hence, a good understanding of the interrelationships of organisms from this class and reliable means for distinguishing them are of much importance. This study reports comprehensive phylogenetic and comparative analyses on protein sequences on the genomes of 28 hematozoa species to understand their interrelationships. In addition to phylogenetic trees based on two large datasets of protein sequences, detailed comparative analyses were carried out on the genomes of hematozoa species to identify novel molecular synapomorphies consisting of conserved signature indels (CSIs) in protein sequences. These studies have identified 79 CSIs that are exclusively present in specific groups of Hematozoa/Plasmodium species, also supported by phylogenetic analysis, providing reliable means for the identification of these species groups and understanding their interrelationships. Of these CSIs, six CSIs are specifically shared by all hematozoa species, two CSIs serve to distinguish members of the order Piroplasmida, five CSIs are uniquely found in all Piroplasmida species except B. microti and two CSIs are specific for the genus Theileria. Additionally, we also describe 23 CSIs that are exclusively present in all genome-sequenced Plasmodium species and two, nine, ten and eight CSIs which are specific for members of the Plasmodium subgenera Haemamoeba, Laverania, Vinckeia and Plasmodium (excluding P. ovale and P. malariae), respectively. Additionally, our work has identified several CSIs that support species relationships which are not evident from phylogenetic analysis. Of these CSIs, one CSI supports the ancestral nature of the avian-Plasmodium species in comparison to the mammalian-infecting groups of Plasmodium species, four CSIs strongly support a specific relationship of species between the subgenera Plasmodium and Vinckeia and three CSIs each that reliably group P. malariae with members of the subgenus Plasmodium and P. ovale within the subgenus Vinckeia, respectively. These results provide a reliable framework for understanding the evolutionary relationships among the Plasmodium/Piroplasmida species. Further, in view of the exclusivity of the described molecular markers for the indicated groups of hematozoa species, particularly large numbers of unique characteristics that are specific for all Plasmodium species, they provide important molecular tools for biochemical/genetic studies and for developing novel diagnostics and therapeutics for these organisms.

Asunto(s)

Piroplasmida/clasificación , Plasmodium/clasificación , Secuencia de Aminoácidos , Proteínas Bacterianas/genética , Evolución Biológica , Secuencia Conservada/genética , Mutación INDEL , Filogenia , Piroplasmida/genética , Plasmodium/genética , Plasmodium malariae/genética , Plasmodium ovale/genética , Theileria/genética

RESUMEN

Vertical transmission of blood parasites has been demonstrated in humans and some domestic species, but it has not been well documented in wild populations. We assessed whether Hepatozoon blood parasites are vertically transmitted in naturally infected individuals of the viviparous western terrestrial garter snake ( Thamnophis elegans ). Blood smears were taken from nine wild-caught gravid female snakes at capture, preparturition, and postparturition, and then from their laboratory-born offspring at age 2 mo and 1 yr. All infected offspring were born to four infected females, although not all offspring in a given litter were necessarily infected. Parasites were not detected in offspring born to the five uninfected mothers. The highest parasite loads were found in neonates at 2 mo of age. Parasite prevalence did not vary between sexes in offspring, but females showed higher loads than did males when 2 mo old. This study supports vertical transmission of Hepatozoon in naturally infected viviparous snakes and suggests that vertical transmission of hematozoan parasites might be an overlooked mode of transmission in wildlife.

Asunto(s)

Colubridae/parasitología , Animales , Animales Salvajes , Femenino , Transmisión Vertical de Enfermedad Infecciosa/veterinaria , Masculino

RESUMEN

A severely underweight alligator snapping turtle Macrochelys temminckii Troost in Harlan, 1835, was found near Tyler, Texas, and taken to the Caldwell Zoo. Blood films were submitted to Texas A&M University, College Station, Texas, for morphological and molecular identification of haemogregarine-like inclusions in the red blood cells. Intraerythrocytic Haemogregarina sp. forms were found on microscopic examination at a parasitemia of <1 %. The morphology and morphometric data for the forms indicate similarity to Haemogregarina macrochelysi n. sp. Telford et al., 2009, previously reported in alligator snapping turtles in Florida and Georgia, but two characteristic stage forms were not shared between H. macrochelysi n. sp. and the parasite found in this report. The haemogregarine 18S ribosomal RNA gene (1555-bp fragment) was amplified and cloned, and five clones sequenced. The sequences were deposited in the NCBI GenBank database. All five showed ∼96 % identity to Haemogregarina balli Paterson and Desser, 1976, Hepatozoon sp., and Hemolivia stellata Petit et al., 1990. A 774-bp segment shared 98-99 % identity with the corresponding Haemogregarina sp. rDNA sequence (KR006985) from Caspian turtles (Mauremys caspica McDowell, 1964) in Iran. A neighbor-joining phylogenetic tree generated from aligned sequences from the clones, 26 hematozoa, Adelina dimidiata Schneider, 1875, and Cryptosporidium serpentis Levine, 1980, revealed the cloned sequences clustered on their own branch within the Haemogregarina spp. clade. No genetic data are available for H. macrochelysi n. sp. at this time, so it remains unclear if this parasite in a Texas alligator snapping turtle is conspecific with H. macrochelysi n. sp.

Asunto(s)

Coccidiosis/veterinaria , Eucoccidiida/crecimiento & desarrollo , Eucoccidiida/aislamiento & purificación , Tortugas/parasitología , Animales , Coccidiosis/parasitología , ADN Ribosómico/genética , Eucoccidiida/clasificación , Eucoccidiida/genética , Datos de Secuencia Molecular , Parasitemia/parasitología , Parasitemia/veterinaria , Filogenia , ARN Ribosómico 18S/genética , Texas

RESUMEN

Infectious disease represents an emerging threat to natural populations, particularly when hosts are more susceptible to novel parasites (allopatric) than to parasites from the local area (sympatric). This pattern could arise through evolutionary processes (host populations become adapted to their local parasites and genetically differentiated from other populations at immune-related loci) and/or through ecological interactions (host individuals develop resistance to local parasites through previous exposure). The relative importance of these candidate mechanisms remains unclear. In jawed vertebrates, genes of the major histocompatibility complex (MHC) play a fundamental role in immunity and are compelling candidates for spatially varying selection. We recently showed that song sparrows (Melospiza melodia) are more susceptible to allopatric than to sympatric strains of malaria (Plasmodium). In the current study, to determine whether population differences at MHC explain this pattern, we characterized the peptide-binding regions of MHC (classes I and II) of birds that did or did not become infected in the previous experiment. We recovered up to 4 alleles per individual at class I, implying at least 2 loci, and up to 26 alleles per individual at class II, implying at least 13 loci. Individuals with more class I alleles were less likely to become infected by Plasmodium, consistent with parasite-mediated balancing selection. However, we found no evidence for population genetic differentiation at either class of MHC, based on 36 individuals sequenced. Resistance to sympatric parasites previously described for this system likely stems from individuals' prior immune experience, not from population differentiation and locally protective alleles at MHC.

Asunto(s)

Resistencia a la Enfermedad/genética , Genética de Población , Interacciones Huésped-Parásitos/genética , Complejo Mayor de Histocompatibilidad/genética , Gorriones/genética , Alelos , Animales , Resistencia a la Enfermedad/inmunología , Susceptibilidad a Enfermedades , Variación Genética , Heterocigoto , Interacciones Huésped-Parásitos/inmunología , Complejo Mayor de Histocompatibilidad/inmunología , Ontario , Selección Genética , Gorriones/inmunología , Gorriones/parasitología

RESUMEN

BACKGROUND: The epidemiology of avian hematozoa at high latitudes is still not well understood, particularly in sub-Arctic and Arctic habitats, where information is limited regarding seasonality and range of transmission, co-infection dynamics with parasitic and viral agents, and possible fitness consequences of infection. Such information is important as climate warming may lead to northward expansion of hematozoa with unknown consequences to northern-breeding avian taxa, particularly populations that may be previously unexposed to blood parasites. METHODS: We used molecular methods to screen blood samples and cloacal/oropharyngeal swabs collected from 1347 ducks of five species during May-August 2010, in interior Alaska, for the presence of hematozoa, Influenza A Virus (IAV), and IAV antibodies. Using models to account for imperfect detection of parasites, we estimated seasonal variation in prevalence of three parasite genera (Haemoproteus, Plasmodium, Leucocytozoon) and investigated how co-infection with parasites and viruses were related to the probability of infection. RESULTS: We detected parasites from each hematozoan genus in adult and juvenile ducks of all species sampled. Seasonal patterns in detection and prevalence varied by parasite genus and species, age, and sex of duck hosts. The probabilities of infection for Haemoproteus and Leucocytozoon parasites were strongly positively correlated, but hematozoa infection was not correlated with IAV infection or serostatus. The probability of Haemoproteus infection was negatively related to body condition in juvenile ducks; relationships between Leucocytozoon infection and body condition varied among host species. CONCLUSIONS: We present prevalence estimates for Haemoproteus, Leucocytozoon, and Plasmodium infections in waterfowl at the interface of the sub-Arctic and Arctic and provide evidence for local transmission of all three parasite genera. Variation in prevalence and molecular detection of hematozoa parasites in wild ducks is influenced by seasonal timing and a number of host traits. A positive correlation in co-infection of Leucocytozoon and Haemoproteus suggests that infection probability by parasites in one or both genera is enhanced by infection with the other, or that encounter rates of hosts and genus-specific vectors are correlated. Using size-adjusted mass as an index of host condition, we did not find evidence for strong deleterious consequences of hematozoa infection in wild ducks.

Asunto(s)

Enfermedades de las Aves/epidemiología , Patos/parasitología , Haemosporida/aislamiento & purificación , Virus de la Influenza A/aislamiento & purificación , Gripe Aviar/complicaciones , Infecciones Protozoarias en Animales/epidemiología , Alaska/epidemiología , Animales , Animales Salvajes , Anticuerpos Antivirales/sangre , Enfermedades de las Aves/diagnóstico , Enfermedades de las Aves/parasitología , Enfermedades de las Aves/transmisión , Cloaca/parasitología , Coinfección , Femenino , Haemosporida/genética , Especificidad del Huésped , Virus de la Influenza A/genética , Virus de la Influenza A/inmunología , Masculino , Orofaringe/parasitología , Plasmodium/genética , Plasmodium/aislamiento & purificación , Prevalencia , Infecciones Protozoarias en Animales/diagnóstico , Infecciones Protozoarias en Animales/parasitología , Infecciones Protozoarias en Animales/transmisión , Estaciones del Año

RESUMEN

Blue-winged teal (Anas discors) are abundant, small-bodied dabbling ducks that breed throughout the prairies of the northcentral USA and central Canada and that winter in the southern USA and northern Neotropics. Given the migratory tendencies of this species, it is plausible that blue-winged teal may disperse avian pathogens, such as parasites causing avian malaria, between spatially distant areas. To test the hypothesis that blue-winged teal play a role in the exchange of blood parasites between North America and areas further south, we collected information on migratory tendencies of this species and sampled birds at spatially distant areas during breeding and non-breeding periods to diagnose and genetically characterize parasitic infections. Using a combination of band recovery data, satellite telemetry, molecular diagnostics, and genetic analyses, we found evidence for (1) migratory connectivity of blue-winged teal between our sampling locations in the Canadian prairies and along the US Gulf Coast with areas throughout the northern Neotropics, (2) parasite acquisition at both breeding and non-breeding areas, (3) infection of blue-winged teal sampled in Canada and the USA with Plasmodium parasite lineages associated with the Neotropics, and (4) infection of blue-winged teal with parasites that were genetically related to those previously reported in waterfowl in both North America and South America. Collectively, our results suggest that blue-winged teal likely play a role in the dispersal of blood parasites between the Neotropics and North America, and therefore, the targeting of this species in surveillance programs for the early detection of Neotropical-origin avian pathogens in the USA may be informative.

Asunto(s)

Enfermedades de las Aves/epidemiología , Patos/parasitología , Malaria/epidemiología , Parasitemia/veterinaria , Plasmodium/aislamiento & purificación , Migración Animal , Animales , Enfermedades de las Aves/parasitología , Canadá/epidemiología , Geografía , Malaria/parasitología , América del Norte/epidemiología , Parasitemia/epidemiología , Parasitemia/parasitología , Filogenia , Plasmodium/genética , Estaciones del Año , América del Sur/epidemiología , Estados Unidos/epidemiología

RESUMEN

Habitats are rapidly changing across the planet and the consequences will have major and long-lasting effects on wildlife and their parasites. Birds harbor many types of blood parasites, but because of their relatively high prevalence and ease of diagnosis, it is the haemosporidians - Plasmodium, Haemoproteus, and Leucocytozoon - that are the best studied in terms of ecology and evolution. For parasite transmission to occur, environmental conditions must be permissive, and given the many constraints on the competency of parasites, vectors and hosts, it is rather remarkable that these parasites are so prevalent and successful. Over the last decade, a rapidly growing body of literature has begun to clarify how environmental factors affect birds and the insects that vector their hematozoan parasites. Moreover, several studies have modeled how anthropogenic effects such as global climate change, deforestation and urbanization will impact the dynamics of parasite transmission. This review highlights recent research that impacts our understanding of how habitat and environmental changes can affect the distribution, diversity, prevalence and parasitemia of these avian blood parasites. Given the importance of environmental factors on transmission, it remains essential that researchers studying avian hematozoa document abiotic factors such as temperature, moisture and landscape elements. Ultimately, this continued research has the potential to inform conservation policies and help avert the loss of bird species and threatened habitats.

RESUMEN

Information on the molecular detection of hematozoa from different tissue types and multiple years would be useful to inform sample collection efforts and interpret results of meta-analyses or investigations spanning multiple seasons. In this study, we tested blood and muscle tissue collected from northern pintails (Anas acuta) during autumn and winter of different years to evaluate prevalence and genetic diversity of Leucocytozoon, Haemoproteus, and Plasmodium infections in this abundant waterfowl species of the Central Valley of California. We first compared results for paired blood and wing muscle samples to assess the utility of different tissue types for molecular investigations of haemosporidian parasites. Second, we explored inter-annual variability of hematozoa infection in Central Valley northern pintails and investigated possible effects of age, sex, and sub-region of sample collection on estimated parasite detection probability and prevalence. We found limited evidence for differences between tissue types in detection probability and prevalence of Leucocytozoon, Haemoproteus, and Plasmodium parasites, which supports the utility of both sample types for obtaining information on hematozoan infections. However, we detected 11 haemosporidian mtDNA cyt b haplotypes in blood samples vs. six in wing muscle tissue collected during the same sample year suggesting an advantage to using blood samples for investigations of genetic diversity. Estimated prevalence of Leucocytozoon parasites was greater during 2006-2007 as compared to 2011-2012 and four unique haemosporidian mtDNA cyt b haplotypes were detected in the former sample year but not in the latter. Seven of 15 mtDNA cyt b haplotypes detected in northern pintails had 100% identity with previously reported hematozoa lineages detected in waterfowl (Haemoproteus and Leucocytozoon) or other avian taxa (Plasmodium) providing support for lack of host specificity for some parasite lineages.

RESUMEN

Parasites have the potential to decrease reproductive output of hosts by competing for nutrients or forcing hosts to invest in immune function. Conversely, reproductive output may affect parasite loads if hosts allocate resources to reproduction such that allocation to immune function is compromised. Both hypotheses implicitly have a temporal component, so we sampled parasites both before and after egg laying to examine the relationship between reproductive output (indexed using a combined measure of clutch size, egg volume, and initiation date) and blood parasite loads of American kestrels (Falco sparverius). Parasite loads measured prior to egg laying had no adverse effects on subsequent reproductive output. Females that previously had large reproductive outputs subsequently had lower parasite intensities than those whose outputs were smaller, suggesting that females were capable of allocating energy to both forming clutches and reducing parasite loads. Because male kestrels provide most of their mate's energetic needs before, during, and after egg laying, mate choice by females may have consequences for their parasite loads. Females choosing high-quality mates may not only have increased reproductive output, but may also obtain sufficient resources from their mates to enable them to reduce their parasite burdens. Males whose mates had large reproductive outputs were more likely to subsequently be parasitized and have more intense infections. For individual males sampled both before and after egg laying, those whose mates had larger reproductive outputs were also more likely to become parasitized, or remain parasitized, between sampling periods. Increased parasite loads of males may be one mechanism by which the costs of reproduction are paid.