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Detecting shifts of transmission areas in avian blood parasites - A phylogenetic approach
Abstract
We investigated the degree of geographical shifts of transmission areas of vector-borne avian blood parasites (Plasmodium, Haemoproteus and Leucocytozoon) over ecological and evolutionary timescales. Of 259 different parasite lineages obtained from 5886 screened birds sampled in Europe and Africa, only two lineages were confirmed to have current transmission in resident bird species in both geographical areas. We used a phylogenetic approach to show that parasites belonging to the genera Haemoproteus and Leucocytozoon rarely change transmission area and that these parasites are restricted to one resident bird fauna over a long evolutionary time span and are not freely spread between the continents with the help of migratory birds. Lineages of the genus Plasmodium seem more freely spread between the continents. We suggest that such a reduced transmission barrier of Plasmodium parasites is caused by their higher tendency to infect migratory bird species, which might facilitate shifting of transmission area. Although vector-borne parasites of these genera apparently can shift between a tropical and a temperate transmission area and these areas are linked with an immense amount of annual bird migration, our data suggest that novel introductions of these parasites into resident bird faunas are rather rare evolutionary events.
... Unlike P. relictum SGS1, the records of GRW4 in Europe are only from migrant adult birds, i.e. birds that have returned from winter grounds in tropical Africa. There are no convincing cases of the lineage GRW4 from European resident or juvenile migrating birds that would indicate transmission outside the tropics (Beadell et al., 2006;Bensch et al., 2021Bensch et al., , 2007Hellgren et al., 2007;Ventim et al., 2012). Numerous studies have shown that the lineage GRW4 is transmitted in tropical or subtropical areas (Beadell et al., 2006;Bensch et al., 2007;Loiseau et al., 2012;Marzal et al., 2011;Ricklefs et al., 2004;Waldenström et al., 2002). ...
... Hence, the absence of transmission of this tropical parasite in northern Europe cannot be explained by the lack of competent vectors. The infection intensities with the lineage GRW4 in European long distance migrants after their return from the wintering ground are typically very low and often in co-infections with other haemosporidian parasites, including SGS1 (Asghar et al., 2011;Bensch et al., 2007;Hellgren et al., 2007;Ishtiaq et al., 2017;Zehtindjiev et al., 2008). In contrast to GRW4, the P. relictum lineage SGS1 causes heavy primary infections in many bird species in Europe (Palinauskas et al., 2009(Palinauskas et al., , 2008 and appear to be more virulent in the presence of other Plasmodium parasites . ...
... The lack of transmission of this lineage in Europe remains enigmatic, although, Valkiūnas et al. (2015) investigation proved that GRW4 obtained from experimentally infected Eurasian siskin is capable to successfully complete sporogony in Culex pipiens, which is the main vector of P. relictum lineages SGS1 and GRW11 in northern Europe (Kazlauskienė et al., 2013;Ž iegytė et al., 2014). However, the gametocytemia during Valkiūnas et al. (2015) study was much higher than the general parasitemia observed in a number of European migrants during chronic stage of P. relictum (GRW4) infection, especially in co-infected individuals (Asghar et al., 2011;Bensch et al., 2007;Hellgren et al., 2007), which might be too low to initiate sporogony. As Plasmodium parasites are sensitive to environmental temperatures, it is another factor playing an important role in the prevalence of malaria parasites. ...
Although co-infections and interactions of parasites are a very common phenomenon in the wild, information received from studies on avian Plasmodium spp. is scarce and fragmented due to its complex nature. Different interactions of parasites and domination of one parasite may have a detrimental effect on transmission success of another pathogen. Untangling these interactions and competitive behavior of malarial parasites may help understanding why some haemosporidian parasites are dominant in certain host species, while others are observed only occasionally.We investigated the development of Plasmodium relictum (genetic lineage GRW4) during single and co-infection with a closely related lineage SGS1, with the aim to determine whether co-infections affect parasite development and condition of experimentally infected Eurasian siskins (Spinus spinus). For the experimental study of these two closely related lineages, a new qPCR protocol was designed to accurately quantify the parasitemia, i.e. the amount of infected red blood cells, during the of blood stages of each of the lineages. Our results show that during co-infection, GRW4 parasitemia was transient and disappeared from peripheral blood during acute increases of SGS1. Health parameters of infected birds did not differ between the GRW4 single infected with GRW4 group and the co-infection group. GRW4 induced infection was outcompeted and suppressed by the presence of the lineage SGS1, which is broadly transmitted in Northern Europe. This suggests that Ddouble infections and dominating lineages in the area may influence the transmission success of some avian Plasmodium parasites.
... The introduction of pathogens by migrants to new localities might lead to changes to the local community structure or richness, depending on the susceptibility of resident species to infection (Altizer et al. 2011). Indeed, recent studies have demonstrated that migratory birds harbor a greater diversity of parasites than resident species (Koprivnikar andLeung 2015, Gutiérrez et al. 2019) and documented the influence of migratory birds on the spread of important pathogens (Morshed et al. 2005, Hellgren et al. 2007, Ricklefs et al. 2017 with some of these able to infect humans (Morshed et al. 2005, Poupon et al. 2006, Lindeborg et al. 2012. Thus, the migratory behavior of birds may directly influence host local richness and community structure, as well as the local richness of parasite species. ...
... Moreover, prevalence of Plasmodium, which is the most prevalent haemosporidian in this region, can be markedly different among South American regions (Braga et al. 2011). Plasmodium parasites present higher host-shifting rates than other bird haemosporidians (Hellgren et al. 2007), which could certainly result in their increased dissemination by migratory birds into new areas. Indeed, host-shifting of a Plasmodium species from domestic chicken to wild and native birds has already been reported in South America (Ferreira-Junior et al. 2018). ...
... The fact that most of our lineages were observed only in resident birds could explain the lack of a relationship between avian migrants and general haemosporidian prevalence, since the greatest haemosporidian diversity occurs in resident avian species. However, Hellgren et al. (2007) also suggest that new haemosporidian introductions into resident bird faunas are not common evolutionary events. ...
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.
... This may indicate a close relationship between these haplotypes and Corvidae, indicative of some level of host-parasite specificity, and by extension parasite specialization. Similar host-specificity appears evident for SYAT44, which has been only recorded from Sylvia atricapilla, both in Sardinia and Europe, for RBS3 which appears to parasitize only Lanius host species [59,60], for SYLMEL02 [52] and SYBOR07 [51,57,[60][61][62] which have only been found in Sylvia hosts, for PADOM23 found only in Passer hosts [51,53,63], for AEDVEX1 found only in Emberiza hosts [24] and for BRAM2 found only in Fringilla hosts [51,57,60]. Conversely, some haemosporidian lineages are less specific, and include SFC1 (Haemoproteus balmorali), which we only detected in Muscicapa tyrrhennica (a Muscicapidae), but which has also been observed in Turdidae and Paridae (MalAvi). ...
... This may indicate a close relationship between these haplotypes and Corvidae, indicative of some level of host-parasite specificity, and by extension parasite specialization. Similar host-specificity appears evident for SYAT44, which has been only recorded from Sylvia atricapilla, both in Sardinia and Europe, for RBS3 which appears to parasitize only Lanius host species [59,60], for SYLMEL02 [52] and SYBOR07 [51,57,[60][61][62] which have only been found in Sylvia hosts, for PADOM23 found only in Passer hosts [51,53,63], for AEDVEX1 found only in Emberiza hosts [24] and for BRAM2 found only in Fringilla hosts [51,57,60]. Conversely, some haemosporidian lineages are less specific, and include SFC1 (Haemoproteus balmorali), which we only detected in Muscicapa tyrrhennica (a Muscicapidae), but which has also been observed in Turdidae and Paridae (MalAvi). ...
... This may indicate a close relationship between these haplotypes and Corvidae, indicative of some level of host-parasite specificity, and by extension parasite specialization. Similar host-specificity appears evident for SYAT44, which has been only recorded from Sylvia atricapilla, both in Sardinia and Europe, for RBS3 which appears to parasitize only Lanius host species [59,60], for SYLMEL02 [52] and SYBOR07 [51,57,[60][61][62] which have only been found in Sylvia hosts, for PADOM23 found only in Passer hosts [51,53,63], for AEDVEX1 found only in Emberiza hosts [24] and for BRAM2 found only in Fringilla hosts [51,57,60]. Conversely, some haemosporidian lineages are less specific, and include SFC1 (Haemoproteus balmorali), which we only detected in Muscicapa tyrrhennica (a Muscicapidae), but which has also been observed in Turdidae and Paridae (MalAvi). ...
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 Eu-rope. 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 Leucocyto-zoon) 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 lin-eage diversity and distribution in insular environments and presents new insights on potential host-parasite associations.
... Each year, billions of migratory birds carry numerous species of avian haemosporidian parasites from wintering grounds to breeding areas (McClure, 1974;Valkiūnas, 2005). Although active transmission of these parasites is often found in temperate or tropical avifauna only (Hellgren et al., 2007), many species of haemosporidians usually are present in the blood of the migratory birds and are accessible for vectors during the summer months thus, can potentially be spread from one hemisphere to the other (Lapointe et al., 2012;Levin et al., 2013;Ricklefs et al., 2017). However, biotic (e.g., phylogenetic similarity of hosts or lack of specific vector species) and abiotic (e.g., divergent climatic conditions) factors create barriers that might affect the transmission of avian haemosporidians to new geographical areas (Valkiūnas, 2005;Hellgren et al., 2007;Sehgal, 2015;Ricklefs et al., 2017). ...
... Although active transmission of these parasites is often found in temperate or tropical avifauna only (Hellgren et al., 2007), many species of haemosporidians usually are present in the blood of the migratory birds and are accessible for vectors during the summer months thus, can potentially be spread from one hemisphere to the other (Lapointe et al., 2012;Levin et al., 2013;Ricklefs et al., 2017). However, biotic (e.g., phylogenetic similarity of hosts or lack of specific vector species) and abiotic (e.g., divergent climatic conditions) factors create barriers that might affect the transmission of avian haemosporidians to new geographical areas (Valkiūnas, 2005;Hellgren et al., 2007;Sehgal, 2015;Ricklefs et al., 2017). In terms of abiotic factors, various studies have shown that global warming can play an important role in opening new areas for parasite transmission (Garamszegi, 2011;Zamora-Vilchis et al., 2012;Loiseau et al., 2013;Pérez-Rodríguez et al., 2014). ...
... In terms of abiotic factors, various studies have shown that global warming can play an important role in opening new areas for parasite transmission (Garamszegi, 2011;Zamora-Vilchis et al., 2012;Loiseau et al., 2013;Pérez-Rodríguez et al., 2014). Thus, several abundant generalist haemosporidian parasites (i.e., some Plasmodium species) may extend and/or switch their transmission areas from tropical to temperate regions and threaten bird species, which are nonadapted to these infections (Hellgren et al., 2007;Sehgal, 2015;Dimitrov et al., 2018). However, long-term monitoring of haemosporidian parasites that have recently switched transmission areas is still needed to better understand the mechanism of such switches (Hellgren et al., 2007;Dimitrov et al., 2018). ...
Avian haemosporidians (Haemosporida) represent a globally distributed, species-rich multiparasite-multihost host-parasite system. Each year, many of these parasite lineages are carried between temperate and tropical regions by migratory birds. While several factors can limit the transmission of avian haemosporidians to new areas, recent studies have shown that some abundant parasites can sometimes disperse and be transmitted in new areas to become emerging infectious diseases. In this study, we investigated the prevalence and diversity of avian haemosporidian parasites in Sultan Marshes National Park (SMNP), a major stopover site in the eastern Mediterranean flyway, and we evaluated the potential for avian haemosporidians in SMNP to be transmitted to areas outside of their known distributions. We sampled a total of 565 migratory and resident birds belonging to 39 species and 23 families. We applied both molecular and microscopic methods to detect and identify avian haemosporidian infections and also quantified the frequency of potential abortive infections. We identified a total of 52 different mitochondrial cytochrome b (cyt b) parasite lineages belonging to the genera Plasmodium (N = 12), Haemoproteus (N = 31), and Leucocytozoon (N = 9) in 193 (34.2%) infected birds. Ten of the lineages were reported for the first time. Our findings show that numerous parasite lineages are actively transmitted among resident bird species of SMNP. Our findings also revealed new parasite-host interactions while considering the role of possible abortive infections. The relatively high frequency of presumed abortive infections suggests that analyses of datasets generated only by PCR-based methods should be interpreted with caution. We also compared the prevalence and distribution of avian haemosporidian infections in both resident and migratory bird species and showed that haemosporidian prevalence was related to bird migratory behavior. The results of this study contribute to a better understanding of the ecological and genetic adaptations associated with changes in transmission areas of avian haemosporidian parasites.
... R. Soc. B 290: 20231581 and vector switching typically faces fitness tradeoffs linked to specialization in utilization of particular host and vector species [73][74][75][76][77][78][79][80]; thus, we expect that a typical range expansion of MBP requires a longer intermediate phase than a directly transmitted pathogen. Evidence in support of such a slow process is found in the rare occasions in which avian plasmodia (and other haemosporidia) found in migrant birds can be established in resident birds in both the Northern and Southern Hemispheres [73,80]. ...
... B 290: 20231581 and vector switching typically faces fitness tradeoffs linked to specialization in utilization of particular host and vector species [73][74][75][76][77][78][79][80]; thus, we expect that a typical range expansion of MBP requires a longer intermediate phase than a directly transmitted pathogen. Evidence in support of such a slow process is found in the rare occasions in which avian plasmodia (and other haemosporidia) found in migrant birds can be established in resident birds in both the Northern and Southern Hemispheres [73,80]. During the intermediate phase, the number of vectors and host species slowly increase, facilitating a gradual enlargement of the geographical range of the MBP. ...
Mosquito-borne diseases (MBDs) threaten public health and food security globally. We provide the first biogeographic description of the African mosquito fauna (677 species) and the 151 mosquito-borne pathogens (MBPs) they transmit. While mosquito species richness agrees with expectations based on Africa's land surface, African arboviruses and mammalian plasmodia are more speciose than expected. Species assemblages of mosquitoes and MBPs similarly separate sub-Saharan Africa from North Africa, and those in West and Central Africa from eastern and southern Africa. Similarities between mosquitoes and MBPs in diversity and range size suggest that mosquitoes are key in delimiting the range of MBPs. With approximately 25% endemicity, approximately 50% occupying one to three countries and less than 5% occupying greater than 25 countries, the ranges of mosquitoes and MBPs are surprisingly small, suggesting that most MBPs are transmitted by a single mosquito species. Exceptionally widespread mosquito species feed on people and livestock, and most are high-altitude-windborne migrants. Likewise, widespread MBPs are transmitted among people or livestock by widespread mosquitoes, suggesting that adapting to people or livestock and to widespread mosquito species promote range expansion in MBPs. Range size may predict range expansion and emergence risk. We highlight key knowledge gaps that impede prediction and mitigation of future emergence of local and global MBDs.
... However, residents have stronger associations with their haemosporidian parasites than their migrant counterparts (Jenkins et al., 2012), resulting in higher associations of specialists (i.e. restricted to a single host species, or a small number of closely related host species) in residents than migrants (Hellgren et al., 2007). Understanding the current distribution of parasite species across host taxa (i.e. ...
... We also compared our results to other haemosporidian community surveys on both sky islands and non-sky islands from the region. We hypothesized that we would detect (1) Haemoproteus as the most abundant genus due to its high global prevalence (Hellgren et al., 2007;Clark et al., 2014); (2) higher parasite prevalence in migratory species; (3) similar prevalence rates and lineages to those detected in the sky islands of New Mexico; (4) a higher proportion of specialist lineages than generalist lineages in residents due to potential geographic isolation in the region; (5) a high number of novel lineages due to limited sampling in the region; and (6) a higher proportion of novel lineages in resident species than migrant species. ...
Avian haemosporidians are protozoan parasites transmitted by insect vectors that infect birds worldwide, negatively impacting avian fitness and survival. However, the majority of haemosporidian diversity remains undescribed. Quantifying this diversity is critical to determining parasite–host relationships and host-switching potentials of parasite lineages as climate change induces both host and vector range shifts. In this study, we conducted a community survey of avian haemosporidians found in breeding birds on the Davis Mountains sky islands in west Texas, USA. We determined parasite abundance and host associations and compared our results to data from nearby regions. A total of 265 birds were screened and infections were detected in 108 birds (40.8%). Most positive infections were identified as Haemoproteus (36.2%), followed by Plasmodium (6.8%) and Leucocytozoon (0.8%). A total of 71 haemosporidian lineages were detected of which 39 were previously undescribed. We found that regional similarity influenced shared lineages, as a higher number of lineages were shared with avian communities in the sky islands of New Mexico compared to south Texas, the Texas Gulf Coast and central Mexico. We found that migratory status of avian host did not influence parasite prevalence, but that host phylogeny is likely an important driver.
... Of over 1400 detected Leucocytozoon lineages [19], most are unidentified to the level of species or their species identity is questionable. This is unfortunate because the application of molecular markers can speed research on various aspects of haemosporidian biology, and is particularly valuable for the identification of various stages of the life cycle in avian hosts and vectors [18,21,76,86,93,105,184,[277][278][279][280][281]. Details about the use of molecular methods in studies of avian haemosporidian parasites were recently reviewed [282], including the description of the MalAvi database, the use of barcoding, species limits, the selection of primers, and the peculiarities of molecular work. ...
... Limited molecular ecology data on the distribution of Leucocytozoon lineages in wild passeriform birds suggest that novel introductions of parasites into resident birds during seasonal migrations are rather rare events [34,278,339]. However, as seen with the case of leucocytozoids in domesticated birds, the mechanisms preventing the spread of these pathogens globally remain insufficiently understood. ...
Blood parasites of the genus Leucocytozoon (Leucocytozoidae) only inhabit birds and represent a readily distinct evolutionary branch of the haemosporidians (Haemosporida, Apicomplexa). Some species cause pathology and even severe leucocytozoonosis in avian hosts, including poultry. The diversity of Leucocytozoon pathogens is remarkable, with over 1400 genetic lineages detected, most of which, however, have not been identified to the species level. At most, approximately 45 morphologically distinct species of Leucocytozoon have been described, but only a few have associated molecular data. This is unfortunate because basic information about named and morphologically recognized Leucocytozoon species is essential for a better understanding of phylogenetically closely related leucocytozoids that are known only by DNA sequence. Despite much research on haemosporidian parasites during the past 30 years, there has not been much progress in taxonomy, vectors, patterns of transmission, pathogenicity, and other aspects of the biology of these cosmopolitan bird pathogens. This study reviewed the available basic information on avian Leucocytozoon species, with particular attention to some obstacles that prevent progress to better understanding the biology of leucocytozoids. Major gaps in current Leucocytozoon species research are discussed, and possible approaches are suggested to resolve some issues that have limited practical parasitological studies of these pathogens.
... The house sparrow was recorded as new host species for the HIP2 lineage in this study. Previously, the SW4 lineage was reported in the paddyfield warbler (Acrocephalus agricola) and Sedge warbler (Acrocephalus schoenobaenus) [52,53]. The great reed warbler (Acrocephalus arundinaceus) and house sparrow were recorded as new host species for this lineage in the current study. ...
... The species identity of this parasite remains unclear. The lineage RS4 was recorded in the common redstart (Phoenicurus phoenicurus), Eurasian blackcap, common whitethroat (Sylvia communis), berthelot's pipit (Anthus berthelotii), bluethroat (Luscinia svecica), forest fody (Foudia omissa), African stonechat (Saxicola torquata) in previous studies [51,52,[54][55][56]. The house sparrow (Passer domesticus) and the yellowthroated sparrow were recorded as new host species for this lineage in this study. ...
Avian haemosporidians are widespread and diverse and are classified in the genera Plasmodium, Haemoproteus, Leucocytozoon, and Fallisia. These species are known to cause haemosporidiosis and decreased fitness of their hosts. Despite the high diversity of habitats and animal species in Iran, only few studies have addressed avian haemosporidians in this geographic area. This study was performed in the south and southeast of Iran during the bird breeding seasons in 2017 and 2018, with the aim to partly fill in this gap. Blood samples of 237 passerine birds belonging to 41 species and 20 families were collected. Parasite infections were identified using a nested PCR protocol targeting a 479-base-pair fragment of the mitochondrial cytochrome b (cytb) gene of Haemoproteus, Plasmodium and Leucocytozoon species. The overall prevalence of haemosporidian parasites was 51.1%, and 55 different lineages were identified, of which 15 cytb lineages were new globally. The lineages of Haemoproteus predominated (63.6% of all detected lineages), followed by Leucocytozoon and Plasmodium. Nineteen new host records of haemosporidian cytb lineages were identified, and the majority of them were found in resident bird species, indicating local transmission. Thirteen co-infections (9.8% of infected individuals) of Haemoproteus and Leucocytozoon parasites in seven host species were observed. This study shows the presence of active local transmission of parasites to resident bird species in the southeast of Iran and contributes to the knowledge on haemosporidian parasite biodiversity in this poorly studied region of the world.
... Despite the small sample sizes for some host species, some patterns were still apparent largely in the family Turdidae. One lineage, TURDUS2, infects many families of birds throughout Europe [60], Asia [61], and the United States [62], yet most detections have occurred in the Turdidae, including robins and other thrushes. Accordingly, American Robins, at our study site had the highest proportion of TURDUS2 detections compared to other species and may act as a reservoir for this parasite lineage. ...
... Accordingly, 2 of the 4 detections of this lineage at our study site were from American Robins, with one detection in a Lincoln Sparrow, and the other in a Warbling Vireo. The POETR01 lineage has been mainly detected in the Thrush family as well [61], and our one detection of this lineage was in an American Robin in agreement with previous detections. ...
Background - Prevalence of avian haemosporidian parasites and the factors influencing infection in the Colorado Rocky Mountains are largely unknown. With climate change expected to promote the expansion of vector and avian blood parasite distributions, baseline knowledge and continued monitoring of the prevalence and diversity of these parasites is needed.
Methods - Using an occupancy modeling framework, we conducted a survey of haemosporidian parasite species infecting an avian community in the Colorado Rocky Mountains in order to estimate prevalence and diversity of blood parasites and to investigate species-level and individual-level characteristics that may influence infection.
Results - We estimated prevalence and diversity of avian haemosporidia across 24 bird species, detecting 39 parasite haplotypes. We found that open cup nesters have higher Haemoproteus prevalence than cavity or ground nesters. Additionally, we found that male Ruby-crowned Kinglets, White-crowned Sparrows, and Wilson’s Warblers have higher Haemoproteus prevalence compared to other host species.
Conclusions - Our study presents baseline knowledge of haemosporidian parasite presence, prevalence, and diversity among avian species in the Colorado Rocky Mountains and adds to our knowledge of host-parasite relationships of blood parasites and their avian hosts.
... Despite the small sample sizes for some host species, some patterns were still apparent largely in the family Turdidae. One lineage, TURDUS2, infects many families of birds throughout Europe [60], Asia [61], and the United States [62], yet most detections have occurred in the Turdidae, including robins and other thrushes. Accordingly, American Robins, at our study site had the highest proportion of TURDUS2 detections compared to other species and may act as a reservoir for this parasite lineage. ...
... Accordingly, 2 of the 4 detections of this lineage at our study site were from American Robins, with one detection in a Lincoln Sparrow, and the other in a Warbling Vireo. The POETR01 lineage has been mainly detected in the Thrush family as well [61], and our one detection of this lineage was in an American Robin in agreement with previous detections. ...
Background - Prevalence of avian haemosporidian parasites and the factors influencing infection in the Colorado Rocky Mountains are largely unknown. With climate change expected to promote the expansion of vector and avian blood parasite distributions, baseline knowledge and continued monitoring of the prevalence and diversity of these parasites is needed.
Methods - Using an occupancy modeling framework, we conducted a survey of haemosporidian parasite species infecting an avian community in the Colorado Rocky Mountains in order to estimate prevalence and diversity of blood parasites and to investigate species-level and individual-level characteristics that may influence infection.
Results - We estimated prevalence and diversity of avian haemosporidia across 24 bird species, detecting 39 parasite haplotypes. We found that open cup nesters have higher Haemoproteus prevalence than cavity or ground nesters. Additionally, we found that male Ruby-crowned Kinglets, White-crowned Sparrows, and Wilson’s Warblers have higher Haemoproteus prevalence compared to other host species. Plasmodium prevalence was relatively low (5%), consistent with the idea that competent vectors may be rare at high altitudes.
Conclusions - Our study presents baseline knowledge of haemosporidian parasite presence, prevalence, and diversity among avian species in the Colorado Rocky Mountains and adds to our knowledge of host-parasite relationships of blood parasites and their avian hosts.
... Haemosporidian parasites can disperse widely across zoogeographical realms and infect distantly related host species (Pérez-Tris and Bensch, 2005;Hellgren et al., 2007b;Ellis et al., 2015;Ricklefs et al., 2017;Fecchio et al., 2018a, Fecchio et al., 2019a. Plasmodium is general considered an indiscriminate host-generalists capable of infecting an enormous diversity of host species in any given environment as demonstrated by the global distributions of several common and potentially invasive Plasmodium lineages (Bensch et al., 2009;Clark et al., 2015;Marzal et al., 2015;Ellis et al., 2018). ...
... are known to be more host-specific at least at the host order level in comparison to Plasmodium, but there are exceptions. For example, Haemoproteus palloris (genetic lineage hWW1) a common parasite of Passeriformes has also been reported from Anseriformes (Wood et al., 2013) and Bucerotiformes (Zehtindjiev et al., 2012) and Haemoproteus majoris (genetic lineage hWW2) another common parasite of Passeriformes, has been reported from both Piciformes (Nilsson et al., 2016;Hellgren et al., 2007b) and Gruiformes (Fourcade et al., 2014). ...
Haemosporidian parasites of the genera Plasmodium, Leucocytozoon, and Haemoproteus are one of the most prevalent and widely studied groups of parasites infecting birds. Plasmodium is the most well-known haemosporidian as the avian parasite Plasmodium relictum was the original transmission model for human malaria and was also responsible for catastrophic effects on native avifauna when introduced to Hawaii. The past two decades has seen a dramatic increase in research on avian haemosporidian parasites as a model system to understand evolutionary and ecological parasite-host relationships. Despite haemosporidians being one the best studied groups of avian parasites their specialization among avian hosts and variation in prevalence amongst regions and host taxa are not fully understood. In this review we focus on describing the current phylogenetic and morphological diversity of haemosporidian parasites, their specificity among avian and vector hosts, and identifying the determinants of haemosporidian prevalence among avian species. We also discuss how these parasites might spread across regions due to global climate change and the importance of avian migratory behavior in parasite dispersion and subsequent diversification.
... This seems plausible, since the immune system is not as suppressed by the long flight, as has always been assumed . With recent molecular techniques to study parasite lineages, it appears that 'hitchhiking' of parasites is not as common as previously thought (Hellgren et al. 2007). This study distinguished between parasite lineages on sub-morphological level of migratory and endemic birds in Africa and Europe, and showed that only one of the 65 encountered Plasmodium lineages were present in both Africa and Europe, meaning that the parasites from the migratory birds are hardly ever transmitted to European birds at stop-over or breeding sites. ...
... MalAvi (27), an online database for molecular lineages of avian hemosporidian parasites, can be used for comparative analysis of novel sequences. Various elements are accompanied by avian blood parasite prevalence in their hosts and vectors; ecological and biological factors such as geographical regions and sampling time; the availability of competent vectors (mosquitoes); host immunity strength; and other factors related to host-parasite-vector interactions (19,(28)(29)(30)(31)(32)(33)(34)(35). ...
Background: Plasmodium and Haemoproteus are common parasites transferred to birds by Culicidae, Ceratopogonidae, and Hippoboscidae vectors. These parasites are of particular concern to healthcare researchers and veterinarians due to their impact on avian malaria, association with other animals and humans, and phylogenetic link with human Plasmodium species. Methods: This bibliographic review article was designed to deliver a report on the avian malaria infections of Plasmodium spp. and Haemoproteus spp. in birds in Iran. Published reports in Google Scholar, PubMed, and Science Direct were used for this revision until April 2023. Results: The highest number of recorded infections with Haemoproteus spp. and Plasmodium spp. was found in Passeridae, as revealed by genetic analysis of Cytb DNA sequences. In this revision, following preceding investigations, the overall prevalence of Haemoproteus spp. was greater than that of Plasmodium spp. discovered by molecular techniques in Iran. Besides, the frequency of published genetic variants (lineages) of Haemoproteus is higher than that of Plasmodium. Our result indicated that the frequency of novel genetic variants Haemoproteus and Plasmodium in published reports was 38% and 12.5% of diagnosed lineages, respectively. Conclusion: The region needs more studies to detect parasites in unexplored hosts and vectors, as there is a lack of research. Understanding the prevalence, epidemiology, transmission approach, and vectors of avian blood parasites is crucial for pet health care, zoos, parks, aviaries, and rehabilitation facilities.
... Presently C. minimus shows an increased breeding and migratory prevalence and diversity of avian malaria, a blood parasite, but aspects of this relationship probably changed over the time scales involved (Pulgarín-R et al., 2019 ;Ricklefs et al., 2014 ). Avian migrants are more likely to be affected by blood parasites in ecological rather than evolutionary time, although the latter are also operating (Hellgren et al., 2007 ;Ricklefs et al., 2014 ). At the deeper times of avian families, seasonal migration is an important factor affecting blood parasite-host coevolution by breaking down the congruence of phylogenetic relationships between hosts and parasites, and there are also important differences among biting-fly vectors and their transmission of avian blood parasite hosts (Jenkins et al., 2011 ;Ricklefs et al., 2014 ). ...
Modern genomic methods enable estimation of a lineage’s long-term effective population sizes back to its origins. This ability allows unprecedented opportunities to determine how adoption of a major life-history trait affects lineages’ populations relative to those without the trait. We used this novel approach to study the population effects of the life-history trait of seasonal migration in evolutionary time. Seasonal migration is a common life-history strategy, but its effects on long-term population sizes relative to lineages that don’t migrate are largely unknown. Using whole-genome data, we estimated effective population sizes over millions of years in closely related seasonally migratory and resident lineages in a group of songbirds. Our main predictions were borne out: Seasonal migration is associated with larger effective population sizes (Ne), greater long-term variation in Ne, and a greater degree of initial population growth than among resident lineages. Initial growth periods showed phylogenetic signal, and their length (0.75-4.3 Myr) parallels the expansion and adaptation phases of taxon cycles, a framework of lineage expansion and eventual contraction over time encompassing biogeography and evolutionary ecology. Heterogeneity among lineages is noteworthy, despite geographic proximity (including overlap) and close relatedness. Seasonal migration imbues these lineages with fundamentally different population size attributes through evolutionary time compared to closely related resident lineages.
... Some studies found that generalist lineages reached lower intensities in their hosts than specialists did, because they are less adapted to certain host species but infected closely related host species more often than expected by chance ). Generalist parasites might also be the most prevalent parasites in their compatible hosts Drovetski et al. 2014) because these parasite species have strong immune evasion capabilities (Hellgren et al. 2007). ...
Haemosporidian blood parasites are widely used in evolutionary ecological research when exploring the effects of parasites on different life-history traits of their bird hosts. However, their roles in bird migration are less studied. If these parasites deteriorate the body condition of the birds strongly, they might negatively affect the whole migration phenology and the survival of the birds as well. In our study, we tested the relationships between infection for parasite genera ( Haemoproteus or Plasmodium ), the three most frequent parasite lineages and body condition (body mass, fat deposit), and the timing of autumn migration in the European Robin ( Erithacus rubecula ). We found that mean body mass and fat scores did not differ between parasitized and non-parasitized individuals, but infected juveniles arrived later than their non-infected counterparts. The difference in the arrival time of parasitized and non-parasitized birds was greater in the case of Haemoproteus infections. However, when we analysed the effects of the distinct parasite lineages separately, we found that prevalence of parasite lineages correlated with the body mass, fat storage, and timing of autumn migration of the birds in a different direction. Our results therefore emphasize the importance of testing the impacts of the different parasites individually, because possible lineage-specific effects on bird condition during migration might exist.
... vectors, intermediate hosts (Kamiya et al., 2014). Similarly, migration may bring hosts into contact with a larger diversity of parasites (Hellgren et al., 2007). The position of species along the slow-fast life-history continuum could also be a strong predictor of co-infection risk (Vaumourin et al., 2015;Valenzuela-Sánchez et al., 2021). ...
Understanding the drivers of infection risk helps us to detect the most at-risk species in a community and identify species whose intrinsic characteristics could act as potential reservoirs of pathogens. This knowledge is crucial if we are to predict the emergence and evolution of infectious diseases. To date, most studies have only focused on infections caused by a single parasite, leaving out co-infections. Yet, co-infections are of paramount importance in understanding the ecology and evolution of host-parasite interactions due to the wide range of effects they can have on host fitness and on the evolutionary trajectories of parasites. Here, we used a multinomial Bayesian phylogenetic modelling framework to explore the extent to which bird ecology and phylogeny impact the probability of being infected by one genus (hereafter single infection) or by multiple genera (hereafter co-infection) of haemosporidian parasites. We show that while nesting and migration behaviors influenced both the probability of being single- and co-infected, species position along the slow-fast life-history continuum and geographic range size were only pertinent in explaining variation in co-infection risk. We also found evidence for a phylogenetic conservatism regarding both single- and co-infections, indicating that phylogenetically related bird species tend to have similar infection patterns. This phylogenetic signal was four times stronger for co-infections than for single infections, suggesting that co-infections may act as a stronger selective pressure than single infections. Overall, our study underscores the combined influence of hosts' evolutionary history and attributes in determining infection risk in avian host communities. These results also suggest that co-infection risk might be under stronger deterministic control than single infection risk, potentially paving the way toward a better understanding of the emergence and evolution of infectious diseases.
... Plasmodium and Haemoproteus parasites may be dispersed through migration (Hellgren et al., 2007;de Angeli Dutra et al., 2021b). For instance, Waldenstrom et al. (2002) detected haemosporidian lineages in many African samples that had also been detected in populations of migratory birds that breed in Europe. ...
South America has different biomes with a high richness of wild bird species and Diptera vectors, representing an ideal place to study the influence of habitat on vector-borne parasites. In order to better understand how different types of habitats do or do not influence the prevalence of haemosporidians, we performed a new analysis of two published datasets comprising wild birds from the Brazilian Savanna (Cerrado) as well as wild birds from the Venezuelan Arid Zone. We investigated the prevalence and genetic diversity of haemosporidian parasites belonging to two genera: Plasmodium and Haemoproteus . We evaluated data from 676 wild birds from the Cerrado and observed an overall prevalence of 49%, whereas, in the Venezuelan Arid Zone, we analyzed data from 527 birds and found a similar overall prevalence of 43%. We recovered 44 lineages, finding Plasmodium parasites more prevalent in the Cerrado (15 Plasmodium and 12 Haemoproteus lineages) and Haemoproteus in the Venezuelan Arid Zone (seven Plasmodium and 10 Haemoproteus lineages). No difference was observed on parasite richness between the two biomes. We observed seven out of 44 haemosporidian lineages that are shared between these two distinct South American biomes. This pattern of parasite composition and prevalence may be a consequence of multiple factors, such as host diversity and particular environmental conditions, especially precipitation that modulate the vector’s dynamics. The relationship of blood parasites with the community of hosts in large and distinct ecosystems can provide more information about what factors are responsible for the variation in the prevalence and diversity of these parasites in an environment.
... These reports might belong to other closely related lineages of the same morphospecies. Five lineages differ from pTURDUS1 in one bp: pFALTIN14 from Falco tinnunculus (1) in China [11], pCIAE07 from Circus aeruginosus (1) in Austria, pPARUS67 from Parus major (1) and Poecile palustris (1) in Sweden [38,55], pSFC6 from Muscicapa striata (1) and Phoenicurus phoenicurus (1) in Sweden [56,57], and pBT7. ...
Background
The order Accipitriformes comprises the largest group of birds of prey with 260 species in four families. So far, 21 haemosporidian parasite species have been described from or reported to occur in accipitriform birds. Only five of these parasite species have been characterized molecular genetically. The first part of this study involved molecular genetic screening of accipitriform raptors from Austria and Bosnia-Herzegovina and the first chromogenic in situ hybridization approach targeting parasites in this host group. The aim of the second part of this study was to summarize the CytB sequence data of haemosporidian parasites from accipitriform raptors and to visualize the geographic and host distribution of the lineages.
Methods
Blood and tissue samples of 183 accipitriform raptors from Austria and Bosnia-Herzegovina were screened for Plasmodium , Haemoproteus and Leucocytozoon parasites by nested PCR, and tissue samples of 23 PCR-positive birds were subjected to chromogenic in situ hybridization using genus-specific probes targeting the parasites’ 18S rRNAs. All published CytB sequence data from accipitriform raptors were analysed, phylogenetic trees were calculated, and DNA haplotype network analyses were performed with sequences from clades featuring multiple lineages detected in this host group.
Results
Of the 183 raptors from Austria and Bosnia-Herzegovina screened by PCR and sequencing, 80 individuals (44%) were infected with haemosporidian parasites. Among the 39 CytB lineages detected, 18 were found for the first time in the present study. The chromogenic in situ hybridization revealed exo-erythrocytic tissue stages of Leucocytozoon parasites belonging to the Leucocytozoon toddi species group in the kidneys of 14 infected birds. The total number of CytB lineages recorded in accipitriform birds worldwide was 57 for Leucocytozoon , 25 for Plasmodium , and 21 for Haemoproteus .
Conclusion
The analysis of the DNA haplotype networks allowed identifying numerous distinct groups of lineages, which have not yet been linked to morphospecies, and many of them likely belong to yet undescribed parasite species. Tissue stages of Leucocytozoon parasites developing in accipitriform raptors were discovered and described. The majority of Leucocytozoon and Haemoproteus lineages are specific to this host group, but most Plasmodium lineages were found in birds of other orders. This might indicate local transmission from birds kept at the same facilities (raptor rescue centres and zoos), likely resulting in abortive infections. To clarify the taxonomic and systematic problems, combined morphological and molecular genetic analyses on a wider range of accipitriform host species are needed.
... In Europe, including the northern temperate regions, transmission of various Plasmodium species is common [5,[18][19][20]. Former studies have revealed the presence of tropical malarial parasites in blood of the long-distance migrants after their return from their wintering grounds in Africa and South Asia [20][21][22]. ...
The avian malaria parasite Plasmodium relictum (genetic lineage pGRW4) is known to cause severe pathology in nonadapted vertebrate hosts. This parasite is prevalent in some bird species in Northern Europe, however the records obtained are only from adult long-distance migrant birds after their return from the wintering grounds. A recent experimental study showed that this parasite completes sporogonic development in the local European vector Culex pipiens at a controlled mean temperature of 19 °C. Thereby, temperature limits for the transmission of this parasite in Northern Europe remain unknown. In this study, we took a step further and tested the impact of different temperature conditions, including some extreme fluctuations between 23 °C down to 7 °C, on the sporogonic development of P. relictum (pGRW4) in the vector Culex pipiens form molestus. Mosquitoes were exposed to infection and kept under different air-temperature conditions: (i) constant warm temperature, (ii) natural outdoor temperatures and (iii) temporary exposure to low temperatures. Plasmodium relictum (pGRW4) completed sporogony in mosquitoes of all experimental groups, however different patterns of the sporogonic development depending on temperature conditions were observed. Based on these results, we conclude that the cool air temperature of Northern Europe in summer is not a limiting factor in successful development of the parasite. However, delayed sporogony caused by low summer temperatures may have a detrimental impact on the active transmission of this parasite in Northern Europe.
... In general, haemosporidian parasites infect closely related host species, with frequent host switches among those related species (Clark and Clegg, 2017;Hellgren et al., 2007;Pulgarín-R et al., 2018;Ricklefs et al., 2014;Ricklefs and Fallon, 2002;Santiago-Alarcon et al., 2014). Nevertheless, host shifts of generalist parasites among more distant species, including species of different orders, have also been reported (Clark and Clegg, 2017;Ricklefs et al., 2014;Santiago-Alarcon et al., 2014). ...
Migratory birds are important carriers of pathogens such as viruses, bacteria and protozoa. Avian haemosporidia have been detected from many wild birds of Japan, but the infection status of migratory birds and transmission area are still largely unknown. Gallinago snipes are long-distance migratory shorebirds, and five species migrate to or through Japan, including Latham's snipe which is near threatened. Haemosporidian parasites in four snipe species were investigated to understand the role of migratory birds in the transmission of avian haemosporidia. Namely, this study aimed: i) to investigate differences in parasite prevalence and related factors explaining infection likelihood among these migratory species, ii) to explore the diversity in haemosporidian lineages and possible transmission areas, and iii) to assess the possibility of morphological effects of infection. Blood samples were collected from snipes caught in central and southwest Japan during migration. Parasites cytb gene DNA were detected via PCR-based testing, and detected lineages were phylogenetically analyzed. Additionally, factors related to prevalence and morphological effects of infection were statistically tested. 383 birds from four Gallinago snipe species were caught, showing higher overall prevalence of avian haemosporidia (17.8 %) than reported in other wader species in previous studies. This high infection rate is presumably due to increased contact with vector insects, resultant of environmental preferences. The prevalence of Plasmodium spp. Was higher in Swinhoe's snipes, while Haemoproteus spp. Was higher in Latham's snipes. These differences are thought to be related to ecological factors including habitat use, distribution and migratory route. Six lineages detected from juveniles indicate transmission between the breeding and sampling area. Contrary to expectations, a direct link between morphological features and haemosporidian parasite infection were not detected. These findings provide valuable information for conservation of this endangered migratory bird group. Further studies linking biological and parasitological research are anticipated to contribute to conservational actions.
... Therefore, it is possible that migratory birds are not suitable hosts for Parahaemoproteus lineages with which they geographically overlap during their annual cycle. This agrees with the study presented by Hellgren et al. (2007) showing that Haemoproteus and Leucocytozoon had a significant affiliation to a single resident bird fauna, while Plasmodium lineages showed a higher degree of infecting both resident and migratory bird species. If that is true in the studied bird community, migrants may be less likely to become infected by Haemoproteus in CLBI when compared to resident birds, due to the greater specificity this parasite presents concerning its local hosts. ...
Avian haemosporidians are parasites with great capacity to spread to new environments and new hosts, being considered a good model to host-parasite interactions studies. Here, we examine avian haemosporidian parasites in a protected area covered by Restinga vegetation in northeastern Brazil, to test the hypothesis that haemosporidian prevalence is related to individual-level traits (age and breeding season), species-specific traits (diet, foraging strata, period of activity, species body weight, migratory status, and nest shape), and climate factors (temperature and rainfall). We screened DNA from 1,466 birds of 70 species captured monthly from April 2013 to March 2015. We detected an overall prevalence ( Plasmodium / Haemoproteus infection) of 22% (44 host species) and parasite’s lineages were identified by mitochondrial cyt b gene. Our results showed that migration can be an important factor predicting the prevalence of Haemoproteus ( Parahaemoproteus ), but not Plasmodium , in hosts. Besides, the temperature, but not rainfall, seems to predict the prevalence of Plasmodium in this bird community. Neither individual-level traits analyzed nor the other species-specific traits tested were related to the probability of a bird becoming infected by haemosporidians. Our results point the importance of conducting local studies in particular environments to understand the degree of generality of factors impacting parasite prevalence in bird communities. Despite our attempts to find patterns of infection in this bird community, we should be aware that an avian haemosporidian community organization is highly complex and this complexity can be attributed to an intricate net of factors, some of which were not observed in this study and should be evaluated in future studies. We evidence the importance of looking to host-parasite relationships in a more close scale, to assure that some effects may not be obfuscated by differences in host life-history.
... Though Plasmodium also displayed the highest prevalence from May to June, members of this genus are known to infect many migratory passerines and experience transmission on breeding and tropical wintering grounds (Hellgren et al. 2007). This could explain why many chickadees carried Plasmodium infections through winter. ...
Within animal hybrid zones, parasites may determine competitive outcomes between host species and thus affect hybridization dynamics. We addressed this hypothesis by evaluating haemosporidian prevalence and community composition in a rapidly moving hybrid zone between Black-capped Chickadees (Poecile atricapillus) and Carolina Chickadees (P. carolinensis). Using molecular methods, we screened for haemosporidians in multiple chickadee populations across the hybrid zone and investigated whether parasite prevalence varied as a function of admixture among these birds. We identified 36 parasite lineages from 3 haemosporidian genera (Plasmodium, Haemoproteus, and Leucocytozoon) but found no genera or lineages more likely to infect any particular chickadee taxon. Instead, haemosporidian prevalence varied across sites and seasons: Leucocytozoon was more prevalent during chickadees’ breeding season, whereas Haemoproteus prevalence peaked during nonbreeding periods. Leucocytozoon infected proportionally fewer birds at the leading edge of the hybrid zone than near its center. However, haemosporidian communities were similar among chickadee populations, and evidence for parasite exchanges between chickadee taxa was lacking. These results underscore the complexity of bird–parasite relationships and suggest that haemosporidians are unlikely to play a major role in the ongoing movement of this hybrid zone.
... Bird migration also influences patterns of distribution and diversity of haemosporidia because it can facilitate transport of parasites and possible introduction of new parasitic lineages in populations of resident birds (Waldenström et al., 2002;Ramey et al., 2015). Previous studies suggest that these events of dispersion of parasites between biogeographic zones are slow evolution-ary processes and that they occur with greater frequency in the genus Plasmodium (Hellgren et al., 2007). We analyzed 85 species of birds, including two long-distance migratory species (Tachycineta meyeni and Elaenia albiceps). ...
The specialist versus generalist strategies of hemoparasites in relation to their avian host, as well as environmental factors, can influence their prevalence, diversity and distribution. In this paper we investigated the influence of avian host species, as well as the environmental and geographical factors, on the strategies of Haemoproteus and Plasmodium hemoparasites. We determined prevalence and diversity by targeting their cytochrome b (Cytb) in a total of 2,590 passerine samples from 138 localities of Central and South America, and analysed biogeographic patterns and host-parasite relationships. We found a total prevalence of 23.2%. Haemoproteus presented a higher prevalence (15.3%) than Plasmodium (4.3%), as well as a higher diversity and host specificity. We determined that Plasmodium and Haemoproteus prevalences correlated positively with host diversity (Shannon index) and were significantly influenced by bird diversity, demonstrating a possible “amplification effect”. We found an effect of locality and the avian family for prevalences of Haemoproteus and Plasmodium. These results suggest that Haemoproteus is more specialist than Plasmodium and could be mostly influenced by its avian host and the Andes Mountains.
... In this study, two PCR-based detection protocols (Beadell et al., 2004;Hellgren et al., 2004) were used for several reasons. First, the available information about patterns of the global geographical distribution of the lineages pSGS1 and pGRW04 was based on results obtained using mainly these protocols, which have been also extensively used in different haemosporidian parasite studies all over the world (Beadell et al., 2006;Bensch et al., 2007;Dimitrov et al., 2015;Ejiri et al., 2009;Ewen et al., 2012;Ferrer et al., 2012;Hellgren et al., 2007Hellgren et al., , 2015Huang et al., 2015;Inumaru et al., 2017;Jia et al., 2018;Marzal et al., 2011Marzal et al., , 2015Quillfeldt et al., 2011;Valkiūnas et al., 2015). Thus, it was important to test their sensitivity in distinguishing co-infections of these lineages. ...
Plasmodium relictum is the most common generalist avian malaria parasite, which was reported in over 300 bird species of different orders, particularly often in passerines. This malaria infection is often severe in non-accustomed avian hosts. Currently, five distinct cytochrome b gene lineages have been assigned to P. relictum, with the lineages pSGS1 and pGRW04 being the most common. Based on molecular screenings, the transmission of these two parasite lineages might occur in sympatry, particularly often in sub-Saharan Africa, but they also have been reported to have different areas of transmission globally, with the lineages pSGS1 and pGRW04 being of low (if at all) transmission in huge regions of Americas and Europe, respectively. It remains unclear why these lineages are more often reported in some geographical areas, even though their susceptible vertebrate hosts and vectors are present globally. Co-infections of malaria parasites and other haemosporidians belonging to different species and subgenera are prevalent and even predominate in many bird populations, however, PCR-based protocols using commonly used primers often do not read such co-infections. Because information about the sensitivity of these protocols to read co-infections of the lineages pSGS1 and pGRW04 is absent, this study aimed to unravel this issue experimentally. Blood samples of birds experimentally infected with the single parasite lineages pSGS1 and pGRW04 were used to prepare various combinations of mixes, which were tested by two PCR-based protocols, which have been often used in current avian malaria research. Single infections of the same lineages were used as controls. Careful examination of the sequence electropherograms showed the presence of clear double peaks on polymorphic sites, indicating co-infections. This experiment shows that the broadly used PCR-based protocols can readily distinguish co-infections of these parasite lineages. In other words, the available information about patterns of the geographical distribution of the P. relictum lineages pSGS1 and pGRW04 likely mirrors the existing epidemiological situation but is not a result of the bias due to preferable DNA amplification of one of these lineages during their possible co-infections. This calls for further ecological research aiming determination of factors associated with the transmission of the lineages pSGS1 and pGRW04 in different regions of the globe.
... This could be explained by the fact that residents and short-distance migrants travel between areas that are likely to be within a single transmission area, e.g. within a continent, and so are confronted with a single parasite fauna (Hellgren et al. 2007;Jenkins et al. 2012). In contrast, longdistance migrants move between vastly separated areas and thereby encounter different faunas of parasites (Waldenström et al. 2002). ...
Diseases can play a role in species decline. Among them, haemosporidian parasites, vector-transmitted protozoan parasites, are known to constitute a risk for different avian species. However, the magnitude of haemosporidian infection in wild columbiform birds, including strongly decreasing European turtle doves, is largely unknown. We examined the prevalence and diversity of haemosporidian parasites Plasmodium, Leucocytozoon and subgenera Haemoproteus and Parahaemoproteus in six species of the order Columbiformes during breeding season and migration by applying nested PCR, one-step multiplex PCR assay and microscopy. We detected infections in 109 of the 259 screened individuals (42%), including 15 distinct haemosporidian mitochondrial cytochrome b lineages, representing five H. (Haemoproteus), two H. (Parahaemoproteus), five Leucocytozoon and three Plasmodium lineages. Five of these lineages have never been described before. We discriminated between single and mixed infections and determined host species-specific prevalence for each parasite genus. Observed differences among sampled host species are discussed with reference to behavioural characteristics, including nesting and migration strategy. Our results support previous suggestions that migratory birds have a higher prevalence and diversity of blood parasites than resident or short-distance migratory species. A phylogenetic reconstruction provided evidence for H. (Haemoproteus) as well as H. (Parahaemoproteus) infections in columbiform birds. Based on microscopic examination, we quantified parasitemia, indicating the probability of negative effects on the host. This study provides a large-scale baseline description of haemosporidian infections of wild birds belonging to the order Columbiformes sampled in the northern hemisphere. The results enable the monitoring of future changes in parasite transmission areas, distribution and diversity associated with global change, posing a potential risk for declining avian species as the European turtle dove.
... Taylor and the other two mountain ranges. Long-distance migrants are expected to connect avian haemosporidian communities in breeding and wintering grounds, and greater connectivity between parasite faunas has been documented in the Americas (eastern North America and West Indies/northern South America) compared to the Euro-African migration system (Hellgren et al. 2007;Ricklefs et al. 2017). Other studies in the Americas, however, indicate that haemosporidian assemblages of migratory and resident birds sampled in the wintering grounds are distinct from each other, suggesting that migrants do not necessarily connect parasite communities on large biogeographic scales (Soares et al. 2020a, b). ...
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.
... Plasmodium typically are generalists regarding host species, while Haemoproteus and Leucocytozoon show considerable host specificity (Waldenström et al. 2002, Dimitrov et al. 2010, Mata et al. 2015. Within this specificity there are also vector species, which frequently take blood primarily or exclusively from a limited number of host species (Malmqvist et al. 2004), hence limiting the spread of parasites (Hellgren et al. 2007). Consequently, haemosporidians seem to show a diversity similar or even higher than that of their passerine hosts, and sometimes lineages differ by only in a single nucleotide , 2009. ...
We report a new analysis of haemosporidian occurrence in 392 Southern Grey Shrike Lanius meridionalis nestlings previously reported in Hernández et al. (2017. Haemosporidian prevalence in Southern Grey Shrike Lanius meridionalis nestlings: impact on body condition and geographic distribution in the Iberian Peninsula. Bird Study 64: 362–373). The previous findings have since been suspected of suffering from contamination by DNA samples from another species. The new analysis showed a prevalence of 1% with a single Leucocytozoon lineage (ENCIR02), distributed in two of the three populations studied.
... Recent studies support this view, but the picture is more heterogeneous. On the one hand, the European-African migratory route shows high degree of conservatism, where there is little viable parasite exchange between resident and migrant birds (i.e., many European bids are commonly infected with Haemoproteus and Plasmodium parasites in Africa, but many of those parasites are not transmitted at breeding grounds in Europe; Valkiūnas and Iezhova 1990;Hellgren et al. 2007;García-Longoria et al. 2015;Ricklefs et al. 2017). On the other hand, the North-South American migration route is less restrictive and has a higher degree of haemosporidian exchange between resident and migrant species, which also depends on the phylogenetic relatedness of the migrant and resident bird species (Ricklefs et al. 2017). ...
In 1884, only 5 years after A. Laveran discovered agents of human malaria, Vassily Danilewsky reported the first description of the pathological effects of avian malaria on their bird hosts. Shortly after, Sir Ronald Ross carried out the first investigation on the life cycle of avian Plasmodium parasites, being the first to show that the malaria parasite is transmitted by the bite of infected mosquitoes. Since its discovery until now, bird malaria parasites have played a major role as model organisms in human malaria research. Experiments with avian malaria have significantly contributed to the description of the life cycle of Plasmodium parasites and for early antimalaria drug screening. Avian malaria and related haemosporidian parasites are globally distributed; host diversity and environmental factors in the tropical regions favor the prevalence and diversity of this group of parasites. Thus, a large number of studies on bird haemosporidians during the last century, particularly taxonomic descriptions, were conducted in a wide range of tropical birds, mainly in African countries. Although the number of publications on this topic was not big during the first half of the last century, it significantly increased from late 1970s, reaching a maximum on early 1990s. During these periods, internationally recognized researchers such as G.F. Bennett, M.A. Peirce, and R.A. Earlé, among others, published a number of studies reporting data of avian haemosporidian infections in many host taxa covering many tropical regions, as well as the descriptions of 134 novel species. During the last three decades, important contributions by G. Valkiūnas have organized and enriched the knowledge on the taxonomy of this group of protozoans. Here, we have conducted an extensive search for avian haemosporidians publications in the Web of Science Core Collection and a bibliometric analysis of the found documents during the period of 1909–2000. In this chapter, we present an extensive synthesis of research conducted on avian malaria and related haemosporidian parasites across the different tropical regions (America, Africa, Asia, Australia, and Oceania).
... Additionally, sequences of haemosporidia from the continental Americas were also included to detect lineages shared between the islands and the mainland. Previous studies indicate that haemosporidia do not disperse easily across continents and many of them are confined to one host or suit of hosts (Valkiūnas 2005;Hellgren et al. 2007;Ricklefs et al. 2017;Pulgarín-R et al. 2018); thus, lineages from other geographic regions were not used. ...
Islands have provided numerous examples of unique biological patterns and also have been fundamental in the development of the theory of island biogeography and the identification of putative processes to explain the presence and numbers of species on islands. The equilibrium model explaining species richness on islands has been at the center of this theory. We conducted exploratory analyses of avian blood parasites (Haemosporida) in three Neotropical insular regions (West Indies, Galapagos, and the Revillagigedo Archipelago), aiming to contribute to the development of the theory of island biogeography for this group of parasites. To explore and synthesize current knowledge, we compiled published mtDNA cyt b sequences and geographical information. We discarded short sequences with less than 300 bp and those that did not coincide with the MalAvi reference sequences. We generated two matrices, the first with sequences of the genus Haemoproteus (n = 366, 346 bp) and the second with Plasmodium (n = 228, 443 bp) sequences, including sequences from the continental Americas as reference. We used lineages representing unique sequence haplotypes with at least one different base pair. We found a positive nonsignificant trend between the number of lineages and island size when including all islands in the study; it was significant only for the Haemoproteus genus in the West Indies. Taxon cycles are recognizable patterns resulting from processes by which taxa adapt to local and specialized conditions leading to restricted distribution and specialization of older taxa. Although Haemoproteus and Plasmodium in the West Indies showed a trend consistent with a taxon cycle-older lineages in a reduced number of islands — general linear model analyses were not significant. The small island effect (SIE) must be revised to understand what factors allow islands, such as Montserrat, Nevis or Socorro, to host disproportionately more lineages than expected from their size. The opposite pattern, where larger islands such as Santa Cruz and Fernandina host fewer lineages than expected also deserves study. Microorganisms, such as haemosporidian parasites, require comprehensive sampling on islands in a wider geographical range.
... The small sample sizes obtained for many host species limit us from determining host speci city of the obtained lineages; however, some patterns were still apparent and most of these centered on the family Turdidae. One lineage, TURDUS2, infects many families of birds throughout Europe (Hellgren et al. 2007a), Asia (Hellgren et al. 2007b), and the United States (Oakgrove et al. 2014), yet most detections have occurred in the Turdidae (Thrush family). Accordingly, American Robins, a member of the Turdidae, at our study site had the highest proportion of TURDUS2 detections compared to other species. ...
Background - Prevalence of avian haemosporidian parasites and the factors influencing infection in the Colorado Rocky Mountains are largely unknown. With climate change expected to promote the expansion of vector and avian blood parasite distributions, baseline knowledge and continued monitoring of the prevalence and diversity of these parasites is needed.
Methods - Using an occupancy modeling framework, we conducted a survey of haemosporidian parasite species infecting an avian community in the Colorado Rocky Mountains in order to estimate prevalence and diversity of blood parasites and to investigate species-level and individual-level characteristics that may influence infection.
Results - We estimated prevalence and diversity of avian haemosporidia across 24 bird species, detecting 39 parasite haplotypes. We found that open cup nesters have higher Haemoproteus prevalence than cavity or ground nesters. Additionally, we found that male Ruby-crowned Kinglets, White-crowned Sparrows, and Wilson’s Warblers have higher Haemoproteus prevalence compared to other host species.
Conclusions - Our study presents baseline knowledge of haemosporidian parasite presence, prevalence, and diversity among avian species in the Colorado Rocky Mountains and adds to our knowledge of host-parasite relationships of blood parasites and their avian hosts.
... Evolutionary studies on host-parasite associations are essential for understanding when, where and to what extent parasites can infect certain hosts, in order to further predict outbreaks of infectious disease (Brooks et al., 2014). Avian haemosporidian parasites constitute a diverse group of protozoan parasites transmitted by dipteran insects that has become an important model system for ecological and evolutionary studies on host-parasite associations (Bensch et al., 2000;Ricklefs and Fallon, 2002;Hellgren et al., 2007;Asghar et al., 2011;Rivero and Gandon, 2018). ...
Infection patterns of avian haemosporidians result from the evolution of their associations with hosts, and can be shaped by multiple biotic factors. However, at the level of parasite species, few studies have investigated the details of the temporal dynamics of infection patterns in wild bird communities. We hereby studied a wild bird community in southern Sweden to investigate two generalist parasites (cyt b lineages PARUS1 and WW2) of the morphological species Haemoproteus majoris in their main host species (tits and warblers, respectively) to look for seasonal (spring to autumn) and age class related variation in infection patterns. For both lineages, we detected a similar temporal pattern in prevalence and infection intensity, with peak levels during the main nesting season in adults and a few weeks later in juveniles. Infections in juveniles were detected as soon as they started to be caught by mist nets, implying that they became infected when still in the nest or during the first weeks post-fledging. The initially high intensities in juveniles were followed by a significant decrease during the hatching year, emphasizing the importance of studying haemosporidian infections in nestlings and fledglings. Both prevalence and infection intensity in adults increased from spring to early summer, either due to spring relapses or new infections. Both prevalence and infection intensity declined in adults at the time when independent juveniles of the respective species started to appear, suggesting that the rate of parasite withdrawal from blood exceeded the rates of new infections gained and relapses of previous infections. Prevalence in both juveniles and adults approached zero towards the end of the summer.
... Plasmodium parasites were identified within 24 h by microscopic examination for sparrow blood smears and all the positive ones were used for genomic DNA extraction and PCR amplification as follows: approximately 50 μL whole blood of the infected sparrows were drawn from the brachial vein into heparinized microcapillaries and stored in SET-buffer (0.015 M NaCl, 0.05 M Tris, 0.25 M EDTA, pH 8.0) and stored at −20°C for molecular analysis (Hellgren et al., 2007). The standard ammonium-acetate protocol was used for genomic DNA extraction from avian blood and Culex whole body after 4 and 6 days of infection (Sambrook et al., 1989). ...
Avian malaria is a mosquito-borne disease caused by Plasmodium spp. protozoa. Although these parasites have been extensively studied in North America and Eurasia, knowledge on the diversity of Plasmodium , its vectors and avian hosts in Africa is scarce. In this study, we report on natural malarial infections in free-ranging sparrows ( Passer domesticus ) sampled at Giza Governorate, Egypt. Parasites were morphologically characterized as Plasmodium cathemerium based on the examination of thin blood smears from the avian host. Sequencing a fragment of the mitochondrial cytochrome b gene showed that the parasite corresponded to lineage PADOM02. Phylogenetic analysis showed that this parasite is closely related to the lineages SERAU01 and PADOM09, both of which are attributed to P. cathemerium . Experimental infection of Culex pipiens complex was successful, with ookinetes first detected at 1-day post infection (dpi), oocysts at 4 dpi and sporozoites at 6 dpi. The massive infection of the salivary glands by sporozoites corroborates that Cx. pipiens complex is a competent vector of PADOM02. Our findings confirm that Plasmodium lineage PADOM02 infects sparrows in urban areas along the Nile River, Egypt, and corroborate that Cx. pipiens complex is a highly competent vector for these parasites. Furthermore, our results demonstrate that this lineage corresponds to the morphospecies P. cathemerium and not P. relictum as previously believed.
... Differential reproductive allocation between clonal and sexual life-stages of haemosporidian parasites is expected in temperate regions, where vector abundance is highly seasonal, but it is unclear whether similar patterns would be observed in tropical regions. Seasonal relapse and transmission of parasite lineages have presumably evolved to match cycles of host movement in and out of transmission areas, which is supported by patterns of prevalence in populations of migratory hosts (Hellgren et al. 2007;Pérez-Rodríguez et al. 2015;Ricklefs et al. 2017). For example, despite wintering in sympatry, individual dark-eyed juncos (Junco hyemalis) from migratory populations presented lower prevalence of haemosporidian infections than individuals from sedentary populations (Slowinski et al. 2018). ...
In temperate regions, some avian haemosporidian parasites have evolved seasonal transmission strategies, with chronic infections relapsing during spring and transmission peaking during the hosts’ breeding season. Because lineages with seasonal transmission strategies are unlikely to produce gametocytes in winter, we predicted that (1) resident birds living within wintering areas of Neotropical migrants would unlikely be infected with North American parasite lineages; and (2) if infected, wintering migratory birds would be more likely to harbor Plasmodium spp. rather than Parahaemoproteus spp. or Haemoproteus spp. parasites in their bloodstreams, as only Plasmodium produces life stages, other than gametocytes, that infect red blood cells. To test these predictions, we used molecular detection and microscopy to compare the diversity and prevalence of haemosporidian parasites among year-round residents and wintering migratory birds during February 2016, on three islands of The Bahamas archipelago, i.e., Andros, Grand Bahama, and Great Abaco. Infection prevalence was low and comparable between migratory (15/111) and resident (15/129) individuals, and it did not differ significantly among islands. Out of the 12 lineages detected infecting migratory birds, five were transmitted in North America; four lineages could have been transmitted during breeding, wintering, or migration; and three lineages were likely transmitted in The Bahamas. Resident birds mostly carried lineages endemic to the Caribbean region. All North American–transmitted parasite lineages detected among migratory birds were Plasmodium spp. Our findings suggest that haemosporidian parasites of migrants shift resource allocation seasonally, minimizing the production of gametocytes during winter, with low risk of infection spillover to resident birds.
... Most parasites of both plants and animals show host specificity (Little et al., 2006;Norton and Carpenter, 1998). With global warming, many parasites and their hosts can expand their geographic ranges, which likely affects host-parasite interactions (Hellgren et al., 2007;Pickles et al., 2013;Polley and Thompson, 2009). For example, parasites may infect closely related host species when introduced into new habitats, as they share similar immune defenses and physiological traits as the original host (Norton & Carpenter, 1998;Davies & Pedersen, 2008;Poulin et al., 2011). ...
Many parasites are constrained to only one or a few hosts, showing host specificity. It remains unclear why some parasites are specialists and other parasites are generalists. The parasite Ophryocystis elektroscirrha (OE) is a neogregarine protozoan thought to be restricted to monarch butterflies, Danaus plexippus (Nymphaliae) and D. gilippus. Recently, we found OE-like spores in other Lepidoptera, specifically in three noctuid moths: Helicoverpa armigera, H. assulta and H. punctigera, as well as another nymphalid, Parthenos sylvia. To our knowledge, this is the first report of OE-like parasite infections in species other than the genus Danaus. In sequencing 558 bp of 18S rRNA, we found the genetic similarity between OE from D. plexippus and OE-like parasite from the moths H. armigera and H. punctigera to be 95.2%. When we conducted cross-species infection experiments, we could not infect the moths with OE from D. plexippus, but OE-like parasite from H. armigera did infect D. plexippus and a closely related moth species Heliothis virescens. Interestingly, we did not find OE-like parasite in the H. armigera population from Spain. Inter-population infection experiments with H. armigera demonstrated a higher sensitivity to OE-like infection in the population from Spain compared to the populations from Australia and China. These results suggest geographic variation in OE-like susceptibility and coevolution between parasite and host. Our findings give important new insights into the prevalence and host specificity of OE and OE-like parasites, and provide opportunities to study parasite transmission over spatial and temporal scales.
... Although ca. 1,800 bird species undertake seasonal migrations (Rolland, Jiguet, Jonsson, Condamine, & Morlon, 2014), we know little about whether migratory birds disperse parasites from breeding to wintering areas, as well as the extent to which migratory birds acquire parasite infections during winter (Altizer, Bartel, & Han, 2001;Hellgren et al., 2007;Piersma, 1997;Ricklefs et al., 2017). Here, we ascertain whether North American migratory birds introduce malaria parasites to resident bird assemblages on the wintering grounds, and the extent to which migratory and resident birds share parasite infections during winter. ...
Aim
We compared the parasite assemblages of over‐wintering migratory birds and permanent residents on the wintering grounds. We determined whether parasite sharing between migratory and resident birds is influenced by host phylogenetic relatedness. We then inferred whether migratory birds transport haemosporidian parasite lineages between the breeding and wintering grounds.
Location
Sierra de Bahoruco National Park, Dominican Republic, Hispaniola.
Taxa
Migratory and resident birds (primarily Aves: Passeriformes) and their haemosporidian parasites (order Haemosporida, Plasmodium , Haemoproteus and Parahaemoproteus ).
Methods
We used mist nets to capture birds in thorn scrub, broadleaf dry forests and pine forests during midwinter. We used molecular methods to recognize haemosporidian parasites in blood samples, and genotyped infections based on the nucleotide differences in a region of the parasite cytochrome b gene.
Results and Main Conclusion
We identified 505 infections by 32 haemosporidian parasite lineages in 1,780 blood samples from 37 resident species, and in 901 blood samples from 14 overwintering migratory species, over five years at the same sites. Infection prevalence varied among migratory species from zero to 13%, whereas infection prevalence among resident species ranged up to 77%. Host relatedness did not predict parasite assemblage similarity. We discuss four hypotheses for the rarity of haemosporidian infections in migratory birds during winter, and for the infrequency of parasite sharing between migratory and resident birds: (a) relative abundance and host preferences of dipteran vectors lower parasite transmission to migratory birds; (b) parasite lineages adapted to infect endemic Caribbean hosts are unable to infect migratory species; (c) the physiology of migratory birds after migration and during winter reduces parasite survival; and (d) infected individuals suffer more pronounced mortality rates during migration. We highlight the link between host–parasite coevolution and the physiological adaptations associated with avian seasonal migration.
Parasites are a key driving force behind many ecological and evolutionary processes. Prevalence and diversity of parasites, as well as their effects on hosts, are not uniform across host species. As such, the potential parasite spillover between species can significantly influence outcomes of interspecific interactions. We screened two species of Luscinia nightingales for haemosporidian blood parasites (Plasmodium, Leucocytozoon and Haemoproteus) along an approximately 3,000 km transect in Europe, incorporating areas of host distant allopatry, close allopatry and sympatry. We found significant differences in infection rates between the two host species, with common nightingales having much lower parasite prevalence than thrush nightingales (36.7% versus 83.8%). This disparity was mostly driven by Haemoproteus prevalence, which was significantly higher in thrush nightingales while common nightingales had a small, but significantly higher, Plasmodium prevalence. Furthermore, we found no effect of proximity to the contact zone on infection rate in either host species. Despite having lower infection prevalence, common nightingales were infected with a significantly higher diversity of parasite lineages than thrush nightingales, and lineage assemblages differed considerably between the two species, even in sympatry. This pattern was mostly driven by the large diversity of comparatively rare lineages, while the most abundant lineages were shared between the two host species. This suggests that, despite the close evolutionary relationships between the two nightingales, there are significant differences in parasite prevalence and diversity, regardless of the distance from the contact zone. This suggests that spillover of haemosporidian blood parasites is unlikely to contribute towards interspecific interactions in this system.
Modern genomic methods enable estimation of a lineage's long-term effective population sizes back to its origins. This ability allows unprecedented opportunities to determine how adoption of a major life-history trait affects lineages' populations relative to those without the trait. We used this novel approach to study the population effects of the life-history trait of seasonal migration in evolutionary time. Seasonal migration is a common life-history strategy, but its effects on long-term population sizes relative to lineages that don't migrate are largely unknown. Using whole-genome data, we estimated effective population sizes over millions of years in closely related seasonally migratory and resident lineages in a group of songbirds. Our main predictions were borne out: Seasonal migration is associated with larger effective population sizes (Ne), greater long-term variation in Ne, and a greater degree of initial population growth than among resident lineages. Initial growth periods showed phylogenetic signal, and their length (0.75-4.3 Myr) parallels the expansion and adaptation phases of taxon cycles, a framework of lineage expansion and eventual contraction over time encompassing biogeography and evolutionary ecology. Heterogeneity among lineages is noteworthy, despite geographic proximity (including overlap) and close relatedness. Seasonal migration imbues these lineages with fundamentally different population size attributes through evolutionary time compared to closely related resident lineages.
Avian blood parasites, from the genera Plasmodium, Haemoproteus and Leucocytozoon, are predicted to alter their range and prevalence as global temperatures change, and host and vector ranges shift. Understanding large-scale patterns in the prevalence and diversity of avian malaria and malaria-like parasites is important due to an incomplete understanding of their effects in the wild, where studies suggest even light parasitaemia can potentially cause rapid mortality, especially in naïve populations. We conducted phylogenetically controlled analyses to test for differences in prevalence and lineage diversity of haemoparasite infection (for Plasmodium, Haemoproteus and Leucocytozoon) in and between resident and migratory species along the African-Eurasian flyway. To test whether migratory strategy or range size drives differences in parasite prevalence and diversity between resident and migrant species, we included three categories of resident species: Eurasian only (n=36 species), African only (n=41), and species resident on both continents (n=17), alongside intercontinental migrants (n=64), using a subset of data from the MalAvi database comprising 27,861 individual birds. We found that species resident on both continents had a higher overall parasite diversity than all other categories. Eurasian residents had lower Plasmodium diversity than all other groups, and both migrants and species resident on both continents had higher Haemoproteus diversity than both African and Eurasian residents. Leucocytozoon diversity did not differ between groups. Prevalence patterns were less clear, with marked differences between genera. Both Plasmodium and Leucocytozoon prevalence was higher in species resident on both continents and African residents than in migrants and Eurasian residents. Haemoproteus prevalence was lower in Eurasian residents than species resident on both continents. Our findings contrast with previous findings in the North-South American flyway, where long-distance migrants had higher parasite diversity than residents and short-distance migrants, although we found contrasting patterns for parasite diversity to those seen for parasite prevalence. Crucially, our results suggest that geographic range may be more important than migratory strategy in driving parasite diversity within species along the African-Palaearctic flyway. Our findings differ between the three parasite genera included in our analysis, suggesting that vector ecology may be important in determining these large-scale patterns. Our results add to our understanding of global patterns in parasite diversity and abundance, and highlight the need to better understand the influence of vector ecology to understand the drivers of infection risk and predict responses to environmental change.
This datasheet on leucocytozoonosis covers Identity, Overview, Associated Diseases, Pests or Pathogens, Distribution, Hosts/Species Affected, Diagnosis, Pathology, Epidemiology, Impacts, Prevention/Control, Further Information.
This datasheet on Plasmodium relictum covers Identity, Overview, Distribution, Dispersal, Hosts/Species Affected, Vectors & Intermediate Hosts, Environmental Requirements, Impacts, Further Information.
This datasheet on Plasmodium relictum infection covers Identity, Overview, Associated Diseases, Pests or Pathogens, Distribution, Hosts/Species Affected, Diagnosis, Pathology, Epidemiology, Impacts, Prevention/Control, Further Information.
The evolution of host–parasite interactions as host lineages colonize new geographic regions and diversify over evolutionary time is poorly understood. To assess whether haemosporidian parasite diversity has changed during the diversification of an avian host, we surveyed the diversity and prevalence of blood parasite lineages (genera Plasmodium, Haemoproteus, and Leucocytozoon) across the range of the songbird genus Junco, which has diversified recently as it recolonized North America following the last glacial maximum ~18,000 years ago. We report the diversity and prevalence of parasites in junco taxa sampled from Costa Rica to Canada, and examine the influence of local avian species richness in the prevalence and diversity of parasites in junco samples. We screened for parasites in each individual by sequencing a fragment of their cytochrome b gene, identifying the different lineages, and quantifying the prevalence per junco taxon and locality. Of 304 juncos sampled, 178 tested positive for 1 or more parasite genera (58.5% overall prevalence). We found high parasite diversity in genera Haemoproteus and Leucocytozoon and much lower diversity in Plasmodium. Among the 63 parasite lineages detected, 32 of which have not been previously described, we found generalist lineages with widespread but low prevalence in Junco, but also some that appear to have remained specialized on this genus as it diversified across North America over thousands of years. Our results suggest a range of parasitic strategies, ranging from specialized to generalist lineages within single parasite genera.
We describe Leucocytozoon polynuclearis n. sp. (Haemosporida: Leucocytozoidae) from two North American woodpeckers, the northern flicker (Colaptes auratus Linnaeus) and white-headed woodpecker (Dryobates albolarvatus Boie, 1826), based on the morphology of its blood stages and portions of the mitochondrial cytochrome b gene. The most distinctive features of Leucocytozoon polynuclearis n. sp. development are the triangular-shaped host cell nuclei and position of host cell nuclei above gametocytes. This parasite inhabits thrombocytes. Leucocytozoon squamatus Nandi, 1986, the only other Leucocytozoon species detected from Picidae birds, lacks features that are commonly found with L. polynuclearis n. sp. infections. Phylogenetic analysis identified DNA lineages associated with L. polynuclearis n. sp. and showed that this parasite is more closely related to other North American Leucocytozoon species than to L. squamatus, whose initial description was from infected Old World Picidae species. Although there are reports of L. squamatus in North American Picidae species, these detections were based only on microscopic examinations, remain genetically non-characterized, and might be misidentifications with regards to L. polynuclearis n. sp. Available parasite distribution data indicate that L. polynuclearis n. sp. infects Picidae species throughout North America and L. squamatus distribution probably is restricted to Old World Piciformes birds.
Haemoproteus species are widespread avian blood parasites belonging to Haemoproteidae (Haemosporida). Blood stages of these pathogens have been relatively well-investigated, though exo-erythrocytic (tissue) stages remain unidentified for the majority of species. However, recent histopathological studies show that haemoproteins markedly affect bird organs during tissue merogony. This study investigated the exo-erythrocytic development of Haemoproteus (Parahaemoproteus) attenuatus (lineage hROBIN1), the common parasite of flycatchers (Muscicapidae). Naturally infected European robins Erithacus rubecula were examined. Parasite species and lineage were identified using microscopic examination of blood stages and DNA sequence analysis. Parasitaemia intensity varied between 0.8 and 26.5% in seven host individuals. Organs of infected birds were collected and processed for histological examination. Tissues stages (meronts) were seen in six birds and were present only in the lungs. The parasites were usually located in groups and were at different stages of maturation, indicating asynchronous exo-erythrocytic development. In most parasitized individuals, 100 meronts were observed in 1 cm2 section of lungs. The largest meronts reached 108 µm in length. Mature meronts contained numerous roundish merozoites of approximately 0.8 µm in diameter. Megalomeronts were not observed. Massive merogony and resulting damage of lungs is a characteristic feature during H. attenuatus infections and might occur in related parasite lineages, causing haemoproteosis.
Leucocytozoonosis is a vector-borne infection of birds, caused by members of the haemosporidian genus Leucocytozoon. The clinical presentation may range from asymptomatic to severe disease. Consequences of Leucocytozoon infection on blood profiles remain to be described, especially for different host species in the wild. In the current study, the prevalence of Leucocytozoon infection was determined in wild nestlings of three European raptor species, the common buzzard (Buteo buteo, n = 464), red kite (Milvus milvus, n = 46) and northern goshawk (Accipiter gentilis, n = 18). Among 528 nestlings, 51.9% (n = 274) were infected with Leucocytozoon spp., whereby the highest prevalence was found in common buzzards (54.9%), followed by red kites (32.6%) and northern goshawks (22.2%). For a subset of 87 individuals (50 common buzzards, 29 red kites, 8 northern goshawks), a detailed analysis of differential leukocyte counts and several blood chemistry parameters in response to infection was conducted: AP (alkaline phosphatase), AST (aspartate aminotransferase), GLDH (glutamate dehydrogenase), LDH (lactate dehydrogenase), GGT (gamma glutamyl transferase), CK (creatine kinase), BuChE (butyrylcholinesterase), BA (bile acids), ALB (albumin) and TP (total protein). Even though in the physiological range, infected nestlings displayed significantly increased levels of heterophils, aspartate aminotransferase, lactate dehydrogenase, bile acids and butyrylcholinesterase, but decreased lymphocyte and monocyte values compared to uninfected ones. Furthermore, significant species differences with regard to blood parameters, but no sex differences were found. Overall, obtained results show a high prevalence, but a low pathogenicity of Leucocytozoon spp. in wild raptor chicks, presumably resulting from coevolutionary adaptation, but show signatures of infection in the haematological and blood chemistry profiles.
Background
The prevalence of avian haemosporidian parasites and the factors influencing infection in the Colorado Rocky Mountains are largely unknown. With climate change expected to promote the expansion of vector and avian blood parasite distributions, baseline knowledge and continued monitoring of the prevalence and diversity of these parasites is needed.
Methods
Using an occupancy modeling framework, we conducted a survey of haemosporidian parasite species infecting an avian community in the Colorado Rocky Mountains in order to estimate the prevalence and diversity of blood parasites and to investigate species-level and individual-level characteristics that may influence infection.
Results
We estimated the prevalence and diversity of avian Haemosporidia across 24 bird species, detecting 39 parasite haplotypes. We found that open-cup nesters have higher Haemoproteus prevalence than cavity or ground nesters. Additionally, we found that male Ruby-crowned Kinglets, White-crowned Sparrows, and Wilson’s Warblers have higher Haemoproteus prevalence compared to other host species. Plasmodium prevalence was relatively low (5%), consistent with the idea that competent vectors may be rare at high altitudes.
Conclusions
Our study presents baseline knowledge of haemosporidian parasite presence, prevalence, and diversity among avian species in the Colorado Rocky Mountains and adds to our knowledge of host–parasite relationships of blood parasites and their avian hosts.
In order to be able to understand the ecological and evolutionary processes involved in the emergence of infectious diseases, one needs to comprehend how parasites arrive at new geographical areas and how they manage to maintain viable populations and even expand their ranges. We discuss host specificity in avian haemosporidians and how encounter and compatibility filters affect the dispersal of avian haemosporidians, and how these filters affect avian haemosporidian assemblages at different spatial and evolutionary scales. There are at least three important barriers to the dispersal of avian haemosporidians: (i) geographic barriers, (ii) environmental barriers, and (iii) interspecies barriers. In this chapter, we discuss the factors involved in these barriers and their effects on the structure of avian haemosporidian assemblages. Host specificity plays an important role in parasite dispersal, and in the case of avian haemosporidians that are vector-borne parasites, it needs to be evaluated both at the vector and bird host levels. Understanding the effects of these factors on host–vector–parasite dynamics is important to unravel the dispersal and diversification mechanisms of avian haemosporidians. We end this chapter reviewing host specialization in avian haemosporidians of tropical regions, discussing the mechanisms involved in the dispersal and specialization of these parasites and point out important research gaps that need attention.
During the last two decades, molecular methods to study mitochondrial DNA sequence variation have become an important part in the studies of avian haemosporidians. Up until recently, these methods have primarily been used for identification of the parasites and for tentative phylogenetic reconstructions, allowing researchers not trained in traditional parasitology to compare data across the globe. However, with the introduction of genome and transcriptome sequencing, studies are emerging that go deeper into the genetics and molecular biology of the parasites. In this chapter, we describe and summarize the common methods used for genetic barcoding of the parasites and give an introduction of what to take into account when designing a molecular study of avian haemosporidians. This chapter further discusses why nuclear genetic data are needed in order to answer several important ecological and evolutionary questions and which methods to use in order to overcome the obstacles of obtaining nuclear data of the parasites. Finally, this chapter highlights the challenges and opportunities that come with the use of molecular methods, such as how to study and interpret prevalence, the challenge of aborted developments, and how to obtain data for more robust phylogenies and population structure studies of the parasites.
Migration plays a significant role in the ecology and evolution of hosts and – consequently – their parasites. Migratory birds have evolved to cope with physiological and ecological demands of long-distance migration. While migrant hosts are expected to harbor a large diversity of parasites and thus facilitate cross-species transmission, migration allows hosts to escape parasites by moving away from high parasite pressure habitats during crucial stages of the migration cycle. In the context of vector-borne parasites, three factors play an important role in successful parasite transmission – the level of parasite host-specificity, the ecological and phylogenetic similarities with current and potential hosts, and parasite biology. Parasites with extremely high host-specificity are naturally limited in their ability to switch to new hosts compared to more generalist parasites. However, having closer phylogenetic relationships among hosts increases the likelihood that parasites are shared. Hence, if the migrant host belongs to a phylogenetic group represented in the wintering range, there may be more opportunity for both generalist and specialist parasites to expand their host range, whether from the wintering grounds to the breeding grounds or vice versa. Much of the literature is focused on bird movement and the exchange of parasites between regions, but we need a more in-depth study on the phenology (seasonal timing) of vector emergence and quantifying host and vector abundances, which in turn determines the interactions across taxa. Such data will help to develop a model to identify ecological factors associated with migration that influence host–parasite dynamics, which can further predict the spread of disease with climate change.
Avian Plasmodium is of special interest to health care scientists and veterinarians due to the potency of causing avian malaria in non-adapted birds and their evolutionary phylogenetic relationship with human malaria species. This article aimed to provide a comprehensive list of the common avian Plasmodium parasites in the birds and mosquitoes, to specify the common Plasmodium species and lineages in the selected regions of West of Asia, East of Europe, and North of Africa/Middle East, and to determine the contribution of generalist and host-specific Plasmodium species and lineages. The final list of published infected birds includes 146 species, among which Passer domesticus was the most prevalent in the studied areas. The species of Acrocephalus arundinaceus and Sylvia atricapilla were reported as common infected hosts in the examined regions of three continents. The highest numbers of common species of infected birds between continent pairs were from Asia and Europe, and no common record was found from Europe and Africa. The species of Milvus migrans and Upupa epops were recorded as common species from Asia and Africa. The lineage of GRW11 and species of P. relictum were the most prevalent parasites among all the infection records in birds. The most prevalent genus of vectors of avian malaria belonged to Culex and species of Cx. pipiens. The lineage SGS1 with the highest number of occurrence has been found in various vectors comprising Cx. pipiens, Cx. modestus, Cx. theileri, Cx. sasai, Cx. perexiguus, Lutzia vorax, and Culicoides alazanicus. A total of 31 Plasmodium species and 59 Plasmodium lineages were recorded from these regions. SGS1, GRW04, and GRW11, and P. relictum and P. vaughani are specified as common generalist avian malaria parasites from these three geographic areas. The presence of avian Plasmodium parasites in distant geographic areas and various hosts may be explained by the movement of the infected birds through the migration routes. Although most recorded lineages were from Asia, investigating the distribution of lineages in some of the countries has not been done. Thus, the most important outcome of this review is the determination of the distribution pattern of parasite and vector species that shed light on gaps requiring further studies on the monitoring of avian Plasmodium and common vectors extension. This task could be achieved through scientific field and laboratory networking, performing active surveillance and designing regional/continental control programs of birds' malaria and other zoonotic diseases.
With its theoretical basis firmly established in molecular evolutionary and population genetics, the comparative DNA and protein sequence analysis plays a central role in reconstructing the evolutionary histories of species and multigene families, estimating rates of molecular evolution, and inferring the nature and extent of selective forces shaping the evolution of genes and genomes. The scope of these investigations has now expanded greatly owing to the development of high-throughput sequencing techniques and novel statistical and computational methods. These methods require easy-to-use computer programs. One such effort has been to produce Molecular Evolutionary Genetics Analysis (MEGA) software, with its focus on facilitating the exploration and analysis of the DNA and protein sequence variation from an evolutionary perspective. Currently in its third major release, MEGA3 contains facilities for automatic and manual sequence alignment, web-based mining of databases, inference of the phylogenetic trees, estimation of evolutionary distances and testing evolutionary hypotheses. This paper provides an overview of the statistical methods, computational tools, and visual exploration modules for data input and the results obtainable in MEGA.
Laboratory and field experiments were conducted on the island of Hawaii from 1977-1980 in an effort to determine the impact of avian malaria on the forest birds. At 16 study sites from sea level to tree line in mesic and xeric habitat, birds were captured and bled to determine the host and altitudinal distribution of blood parasites. In the laboratory, six bird species were challenged with malarial parasites to measure host susceptibility. Distributions, activity cycles, and transmission potentials of malarial parasite vectors were also analyzed. One species of Plasmodium was present from sea level to tree line, concentrated in the mid-elevational ranges in the ecotonal area where vectors and native birds had the greatest overlap. Native forest birds were: (a) more susceptible to malaria than were introduced species; (b) most likely to have malaria during the nonbreeding, wet season; (c) found ranging lower in xeric than in mesic forests; and (d) found to have a lower prevalence of malaria in xeric forests. Temporal as well as elevational differences in prevalence and parasitemia levels of wild birds were apparent throughout the annual cycle, a result of differing host and parasite responses to biotic and abiotic factors. Avian malaria probably did not reach epizootic proportions on Hawaii until after @?1920. However, since that time it has had a negative impact on the population dynamics of the native forest birds and is today a major limiting factor, restricting both abundance and distribution of these species on the island. In response, a number of native bird species have developed immunogenetic and behavioral responses that reduce the impact of the parasite on host populations.
The outbreak of highly pathogenic avian influenza of the H5N1 subtype in Asia, which has subsequently spread to Russia, the Middle East, Europe, and Africa, has put increased focus on the role of wild birds in the persistence of influenza viruses. The ecology, epidemiology, genetics, and evolution of pathogens cannot be fully understood without taking into account the ecology of their hosts. Here, we review our current knowledge on global patterns of influenza virus infections in wild birds, discuss these patterns in the context of host ecology and in particular birds' behavior, and identify some important gaps in our current knowledge.
The program MRBAYES performs Bayesian inference of
phylogeny using a variant of Markov chain Monte Carlo.
Availability: MRBAYES, including the source code, documentation,
sample data files, and an executable, is available at http://brahms.biology.rochester.edu/software.html.
Contact: johnh{at}brahms.biology.rochester.edu
To evaluate the role of migratory birds in the long-distance dispersal of Ixodes dammini ticks and in the spread of Lyme disease, a 6-year study of migrating birds to an offshore New England island was conducted
during 1989–1994. I. dammini are not endemic on this island, therefore allowing assessment of long-distance tick dispersal rather than local infestation.
Of 11,324 spring migrants examined, 1.2% were infested with I. dammini. Of 8607 fall migrants examined, 0.2% were infested. Of nymphal ticks examined, 20% were infected with Borrelia burgdorferi. OspB DNA sequencing of 6 B. burgdorferi isolates was identical to sequences of 2 strains common in coastal Maine. It is evident that bird migration allows for long-distance
dispersal of I. dammini from areas where they are endemic to areas where they are not and that a few bird species account for the majority of tick
dispersal. The likelihood of establishment of enzootic Lyme disease by this mechanism is discussed.
We report a phylogenetic analysis of primate malaria parasites based on the gene encoding the cytochrome b protein from the mitochondrial genome. We have studied 17 species of Plasmodium, including 14 parasitic in primates. In our analysis, four species were used for rooting the Plasmodium phylogenetic tree: two from closely related genera (Hepatocystis sp. and Haemoproteus columbae) and two other Apicomplexa (Toxoplasma gondii and Theileria parva). We found that primate malaria parasites form a monophyletic group, with the only exception being the Plasmodium falciparum-Plasmodium reichenowi lineage. Phylogenetic analyses that include two species of non-Plasmodium Haemosporina suggest that the genus Plasmodium is polyphyletic. We conclude that the biologic traits, such as periodicity and the capacity to relapse, have limited value for assessing the phylogenetic relationships among Plasmodium species. For instance, we found no evidence that would link virulence with the age of the host-parasite association. Our studies also reveal that the primate malaria parasites originated in Africa, which contradicts the presently held opinion of Southeast Asia as their center of origin. We propose that the radiation of Asian monkey parasites is a recent event where several life history traits, like differences in periodicity, appeared de novo.
The program MODELTEST uses log likelihood scores to establish the model of DNA evolution that best fits the data.
AVAILABILITY: The MODELTEST package, including the source code and some documentation is available at http://bioag.byu. edu/zoology/crandall_lab/modeltest.html.
Leucocytozoon spp. and Trypanosoma spp. blood parasites in the redstart (Phoenicurus phoenicurus) were studied during spring migration 1994 in southern Finland (53 individuals) and the breeding season 1992-1994 in northern Finland (69). Parasite prevalence was higher during the breeding season (48%) than during the migration period (13%), with no age or sex differences in the breeding site birds. In both periods, redstarts were infected by the same blood parasites Leucocytozoon shaartusicum (46% prevalence at the breeding site and 71% during the migration period) and Trypanosoma avium, complex (58% and 43%, respectively). One individual at the breeding site had contracted L. dubreuili and one at the stop-over site had T. everetti. Our results may support the assumption that tissue-hidden parasites relapse during the breeding season when birds may have diminished immune response related to egg production and brood rearing. Another explanation could be that the high abundance of ornithophilic vectors enhance parasite transmission during breeding season in northern Finland.
A fragment of the mitochondrial cytochrome b gene of avian malaria (genera Haemoproteus and Plasmodium) was amplified from blood samples of 12 species of passerine birds from the genera Acrocephalus, Phylloscopus and Parus. By sequencing 478 nucleotides of the obtained fragments, we found 17 different mitochondrial haplotypes of Haemoproteus or Plasmodium among the 12 bird species investigated. Only one out of the 17 haplotypes was found in more than one host species, this exception being a haplotype detected in both blue tits (Parus caeruleus) and great tits (Parus major). The phylogenetic tree which was constructed grouped the sequences into two clades, most probably representing Haemoproteus and Plasmodium, respectively. We found two to four different parasite mitochondrial DNA (mtDNA) haplotypes in four bird species. The phylogenetic tree obtained from the mtDNA of the parasites matched the phylogenetic tree of the bird hosts poorly. For example, the two tit species and the willow warbler (Phylloscopus trochilus) carried parasites differing by only 0.6% sequence divergence, suggesting that Haemoproteus shift both between species within the same genus and also between species in different families. Hence, host shifts seem to have occurred repeatedly in this parasite host system. We discuss this in terms of the possible evolutionary consequences for these bird species.
The switching of parasitic organisms to novel hosts, in which they may cause the emergence of new diseases, is of great concern to human health and the management of wild and domesticated populations of animals. We used a phylogenetic approach to develop a better statistical assessment of host switching in a large sample of vector-borne malaria parasites of birds (Plasmodium and Haemoproteus) over their history of parasite-host relations. Even with sparse sampling, the number of parasite lineages was almost equal to the number of avian hosts. We found that strongly supported sister lineages of parasites, averaging 1.2% sequence divergence, exhibited highly significant host and geographical fidelity. Event-based matching of host and parasite phylogenetic trees revealed significant cospeciation. However, the accumulated effects of host switching and long distance dispersal cause these signals to disappear before 4% sequence divergence is achieved. Mitochondrial DNA nucleotide substitution appears to occur about three times faster in hosts than in parasites, contrary to findings on other parasite-host systems. Using this mutual calibration, the phylogenies of the parasites and their hosts appear to be similar in age, suggesting that avian malaria parasites diversified along with their modern avian hosts. Although host switching has been a prominent feature over the evolutionary history of avian malaria parasites, it is infrequent and unpredictable on time scales germane to public health and wildlife management.
MrBayes 3 performs Bayesian phylogenetic analysis combining information from different data partitions or subsets evolving under different stochastic evolutionary models. This allows the user to analyze heterogeneous data sets consisting of different data types—e.g. morphological, nucleotide, and protein—and to explore a wide variety of structured models mixing partition-unique and shared parameters. The program employs MPI to parallelize Metropolis coupling on Macintosh or UNIX clusters.
Availability: http://morphbank.ebc.uu.se/mrbayes
Contact: fredrik.ronquist@ebc.uu.se
*
To whom correspondence should be addressed.
Recently, several polymerase chain reaction (PCR)-based methods for detection and genetic identification of haemosporidian parasites in avian blood have been developed. Most of these have considerably higher sensitivity compared with traditional microscope-based examinations of blood smears. These new methods have already had a strong impact on several aspects of research on avian blood parasites. In this study, we present a new nested PCR approach, building on a previously published PCR method, which has significantly improved performance. We compare the new method with some existing assays and show, by sequence-based data, that the higher detection rate is mainly due to superior detection of Plasmodium spp. infections, which often are of low intensity and, therefore, hard to detect with other methods.
With its theoretical basis firmly established in molecular evolutionary and population genetics, the comparative DNA and protein
sequence analysis plays a central role in reconstructing the evolutionary histories of species and multigene families, estimating
rates of molecular evolution, and inferring the nature and extent of selective forces shaping the evolution of genes and genomes.
The scope of these investigations has now expanded greatly owing to the development of high-throughput sequencing techniques
and novel statistical and computational methods. These methods require easy-to-use computer programs. One such effort has
been to produce Molecular Evolutionary Genetics Analysis (MEGA) software, with its focus on facilitating the exploration and
analysis of the DNA and protein sequence variation from an evolutionary perspective. Currently in its third major release,
MEGA3 contains facilities for automatic and manual sequence alignment, web-based mining of databases, inference of the phylogenetic
trees, estimation of evolutionary distances and testing evolutionary hypotheses. This paper provides an overview of the statistical
methods, computational tools, and visual exploration modules for data input and the results obtainable in MEGA.
Variation in the prevalence of blood parasites among species of birds has been used to test hypotheses about the effects of sexual selection and parental investment on disease resistance, and how vector abundance influences infection. However, the factors causing this variation are still poorly understood. We assessed the statistical effects of biogeographic, plumage-related and life-history traits on the prevalence of the blood parasites Plasmodium, Haemoproteus, Leucocytozoon and Trypanosoma in European passerine birds. Most of the variation in parasite prevalence occurred at low taxonomic levels. Brighter male plumage and greater host body mass were associated with higher prevalence, explaining 32% of the total variation. Male plumage brightness remained a significant factor when we controlled for phylogenetic effects. These relationships were driven primarily by simuliid-transmitted parasites (Leucocytozoon, Trypanosoma), which were more frequent in species with northern distributions. Host species with greater maximum longevity and shorter nestling periods had higher prevalences of Plasmodium; however, the effect was not stable after controlling for phylogeny using pairwise contrasts. Coevolution between hosts and parasites appears to create temporal and spatial variation that disconnects haematozoan prevalence from evolutionarily conservative life-history traits while creating some positive associations with traits that are phylogenetically labile. Clearly, ecologists should be cautious in relating patterns of variation in haematozoan prevalence to particular host traits.
Many bird species host several lineages of apicomplexan blood parasites (Protista spp., Haemosporida spp.), some of which are shared across different host species. To understand such complex systems, it is essential to consider the fact that different lineages, species, and families of parasites can occur in the same population, as well as in the same individual bird, and that these parasites may compete or interact with each other. In this study, we present a new polymerase chain reaction (PCR) protocol that, for the first time, enables simultaneous typing of species from the 3 most common avian blood parasite genera (Haemoproteus, Plasmodium, and Leucocytozoon). By combining the high detection rate of a nested PCR with another PCR step to separate species of Plasmodium and Haemoproteus from Leucocytozoon, this procedure provides an easy, rapid, and accurate method to separate and investigate these parasites within a blood sample. We have applied this method to bird species with known infections of Leucocytozoon spp., Plasmodium spp., and Haemoproteus spp. To obtain a higher number of parasite lineages and to test the repeatability of the method, we also applied it to blood samples from bluethroats (Luscinia svecica), for which we had no prior knowledge regarding the blood parasite infections. Although only a small number of different bird species were investigated (6 passerine species), we found 22 different parasite species lineages (4 Haemoproteus, 8 Plasmodium, and 10 Leucocytozoon).
Mosquito-borne flaviviruses provide some of the most important examples of emerging and resurging diseases of global significance. Here, we describe three of them: the resurgence of dengue in tropical and subtropical areas of the world, and the spread and establishment of Japanese encephalitis and West Nile viruses in new habitats and environments. These three examples also illustrate the complexity of the various factors that contribute to their emergence, resurgence and spread. Whereas some of these factors are natural, such as bird migration, most are due to human activities, such as changes in land use, water impoundments and transportation, which result in changed epidemiological patterns. The three examples also show the ease with which mosquito-borne viruses can spread to and colonize new areas, and the need for continued international surveillance and improved public health infrastructure to meet future emerging disease threats.
The introduction of avian malaria (Plasmodium relictum) to Hawaii has provided a model system for studying the influence of exotic disease on naive host populations. Little is known, however, about the origin or the genetic variation of Hawaii's malaria and traditional classification methods have confounded attempts to place the parasite within a global ecological and evolutionary context. Using fragments of the parasite mitochondrial gene cytochrome b and the nuclear gene dihydrofolate reductase-thymidylate synthase obtained from a global survey of greater than 13000 avian samples, we show that Hawaii's avian malaria, which can cause high mortality and is a major limiting factor for many species of native passerines, represents just one of the numerous lineages composing the morphological parasite species. The single parasite lineage detected in Hawaii exhibits a broad host distribution worldwide and is dominant on several other remote oceanic islands, including Bermuda and Moorea, French Polynesia. The rarity of this lineage in the continental New World and the restriction of closely related lineages to the Old World suggest limitations to the transmission of reproductively isolated parasite groups within the morphological species.
Unlabelled:
A key element to a successful Markov chain Monte Carlo (MCMC) inference is the programming and run performance of the Markov chain. However, the explicit use of quality assessments of the MCMC simulations-convergence diagnostics-in phylogenetics is still uncommon. Here, we present a simple tool that uses the output from MCMC simulations and visualizes a number of properties of primary interest in a Bayesian phylogenetic analysis, such as convergence rates of posterior split probabilities and branch lengths. Graphical exploration of the output from phylogenetic MCMC simulations gives intuitive and often crucial information on the success and reliability of the analysis. The tool presented here complements convergence diagnostics already available in other software packages primarily designed for other applications of MCMC. Importantly, the common practice of using trace-plots of a single parameter or summary statistic, such as the likelihood score of sampled trees, can be misleading for assessing the success of a phylogenetic MCMC simulation.
Availability:
The program is available as source under the GNU General Public License and as a web application at http://ceb.scs.fsu.edu/awty.
When studying the effects of parasites on natural populations, the avian haematozoa fulfills many of the specifications of an ideal model. Featuring a multitude of tables and illustrations, Avian Malaria Parasites and Other Haemosporidia summarizes more than a century of research on bird haemosporidians. For a long time, bird blood parasites served as important models in studying human diseases. Although now largely replaced, a wealth of data and research remain. With chapters addressing life cycles and morphology, pathogenicity, ultrastructure, geographical distribution, and illustrated keys to all known species of the parasites, this book is a masterful assessment of the biology of bird haemosporidian parasites.
The importance and abundance of cryptic species among invertebrate taxa is well documented. Nowadays, taxonomic, phylogenetic and conservation biological studies frequently use molecular markers to delineate cryptic taxa. Such studies, however, often face the problem of the differential resolution of the molecular markers and techniques involved. This issue is explored in the present study of cryptic taxa within the terrestrial slug complex Arion subfuscus/fuscus in continental north-west Europe. To this end, morphological, allozyme and mitochondrial 16S rDNA sequence data have been jointly evaluated. Using allozyme data and gonad type, two distinct groups were consistently delineated, even under sympatric conditions. The 16S rDNA data strongly supported both those groups and even suggested the presence of three distinct taxa within one of them. However, in view of: (1) the allopatric distribution of three OTUs, (2) the lack of allozyme or morphological differentiation, and (3) the extremely high degree of intraspecific mtDNA variation reported in pulmonate gastropods, they are, for the time being, not regarded as valid species under the biological species concept. By means of 16S rDNA and allozyme data, the position of type and topotype material of A. subfuscus s.s. and A. fuscus relative to the newly defined OTUs was determined, thus clarifying the nomenclature of this species complex. Additionally, gonad type proved to be a useful character for distinguishing the two species in north-west Europe. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83, 23–38.
Mitochondrial control region sequences from European populations of the blue tit Parus caeruleus were used to reveal the Pleistocene history and the post-glacial recolonization of Europe by the species. The southern subspecies, P. c. ogliastrae was found to represent a stable population with isolation-by-distance structure harboring a lot of genetic variation, and the northern subspecies P. c. caeruleus a recently bottlenecked and expanded population. We suggest that after the last Ice Ages, the subspecies have colonized Europe from two different southern refuges following previously proposed general recolonization routes from the Balkans to northern and Central Europe, and from the Iberian Peninsula north- and eastwards. The two subspecies form a wide secondary contact zone extending from southern Spain to southern France.
The relationships between dispersal and local transmission rate of parasites are essential to understanding host–parasite coevolution and the emergence and spread of novel disease threats. Here we show that year-round transmission, as opposed to summer transmission, has repeatedly evolved in malarial parasites (genera Plasmodium and Haemoproteus) of a migratory bird. Year-round transmission allows parasites to spread in sympatric host's wintering areas, and hence to colonize distantly located host's breeding areas connected by host-migration movements. Widespread parasites had higher local prevalence, revealing increased transmission, than geographically restricted parasites. Our results show a positive relationship between dispersal and local transmission of malarial parasites that is apparently mediated by frequent evolutionary changes in parasite transmission dynamics, which has important implications for the ecology and evolution of infectious diseases.
Abstract Analyses of mitochondrial cytochrome b diversity among avian blood parasites of the genera Haemoproteus and Plasmodium suggest that there might be as many lineages of parasites as there are species of birds. This is in sharp contrast to the approximately 175 parasite species described by traditional methods based on morphology using light microscopy. Until now it has not been clear to what extent parasite mitochondrial DNA lineage diversity reflects intra- or interspecific variation. We have sequenced part of a fast-evolving nuclear gene, dihydrofolate reductase-thymidylate synthase (DHFR-TS), and demonstrate that most of the parasite mitochondrial DNA lineages are associated with unique gene copies at this locus. Although these parasite lineages sometimes coexist in the same host individual, they apparently do not recombine and could therefore be considered as functionally distinct evolutionary entities, with independent evolutionary potential. Studies examining parasite virulence and host immune systems must consider this remarkable diversity of avian malaria parasites.
A total of 86 adult bluethroats (Luscinia svecica) from nine different localities, covering the full length of the Fennoscandian mountain range, were screened for blood parasites of the three genera Haemoproteus, Plasmodium and Leucocytozoon using a recently developed polymerase chain reaction method. The overall occurrence of infection was 59.3%. Prevalence of Leucocytozoon spp. (47.7%), Plasmodium spp. (23.3%) and Haemoproteus spp. (1.2%) was detected. Of the infected birds, 15.1% carried mixed infections. Five different mitochondrial DNA-lineages of Leucocytozoon spp., eight lineages of Plasmodium spp. and one lineage of Haemoproteus spp. were found. Due to large sequence divergence these corresponded to at least five different species, but with the possibility of all 14 being independent evolutionary units with the potential of evolving different effects on the host. Of the lineages of Leucocytozoon spp., the most common was found throughout the range. The occurrence of the second most common lineage of Leucocytozoon spp. showed significant variation in prevalence between sites. The data also showed molecular evidence of one lineage of Leucocytozoon sp. existing in more than one species of avian host, thus challenging the use of host taxon as a taxonomic character when distinguishing between different species leucocytozoids.
We studied the phylogeny of avian haemosporidian parasites, Haemoproteus and Plasmodium, in a number of African resident and European migratory songbird species sampled during spring and autumn in northern Nigeria. The phylogeny of the parasites was constructed through sequencing part of their mitochondrial cytochrome b gene. We found eight parasite lineages, five Haemoproteus and three Plasmodium, infecting multiple host species. Thus, 44% of the 18 haemospiridian lineages found in this study were detected in more than one host species, indicating that host sharing is a more common feature than previously thought. Furthermore, one of the Plasmodium lineages infected species from different host families, Sylviidae and Ploceidae, expressing exceptionally large host range. We mapped transmission events, e.g. the occurrence of the parasite lineages in resident bird species in Europe or Africa, onto a phylogenetic tree. This yielded three clades, two Plasmodium and one Haemoproteus, in which transmission seems to occur solely in Africa. One Plasmodium clade showed European transmission, whereas the remaining two Haemoproteus clades contained mixes of lineages of African, European or unknown transmission. The mix of areas of transmission in several branches of the phylogenetic tree suggests that transmission of haemosporidian parasites to songbirds has arisen repeatedly in Africa and Europe. Blood parasites could be viewed as a cost of migration, as migratory species in several cases were infected with parasite lineages from African resident species. This cost of migration could have considerable impact on the evolution of migration and patterns of winter distribution in migrating birds.
Analyses of mitochondrial cytochrome b diversity among avian blood parasites of the genera Haemoproteus and Plasmodium suggest that there might be as many lineages of parasites as there are species of birds. This is in sharp contrast to the approximately 175 parasite species described by traditional methods based on morphology using light microscopy. Until now it has not been clear to what extent parasite mitochondrial DNA lineage diversity reflects intra- or interspecific variation. We have sequenced part of a fast-evolving nuclear gene, dihydrofolate reductase-thymidylate synthase (DHFR-TS), and demonstrate that most of the parasite mitochondrial DNA lineages are associated with unique gene copies at this locus. Although these parasite lineages sometimes coexist in the same host individual, they apparently do not recombine and could therefore be considered as functionally distinct evolutionary entities, with independent evolutionary potential. Studies examining parasite virulence and host immune systems must consider this remarkable diversity of avian malaria parasites.
The degree to which widespread avian blood parasites in the genera Plasmodium and Haemoproteus pose a threat to novel hosts depends in part on the degree to which they are constrained to a particular host or host family. We examined the host distribution and host-specificity of these parasites in birds from two relatively understudied and isolated locations: Australia and Papua New Guinea. Using polymerase chain reaction (PCR), we detected infection in 69 of 105 species, representing 44% of individuals surveyed (n = 428). Across host families, prevalence of Haemoproteus ranged from 13% (Acanthizidae) to 56% (Petroicidae) while prevalence of Plasmodium ranged from 3% (Petroicidae) to 47% (Ptilonorhynchidae). We recovered 78 unique mitochondrial lineages from 155 sequences. Related lineages of Haemoproteus were more likely to derive from the same host family than predicted by chance at shallow (average LogDet genetic distance = 0, n = 12, P = 0.001) and greater depths (average distance = 0.014, n = 11, P < 0.001) within the parasite phylogeny. Within two major Haemoproteus subclades identified in a maximum likelihood phylogeny, host-specificity was evident up to parasite genetic distances of 0.029 and 0.007 based on logistic regression. We found no significant host relationship among lineages of Plasmodium by any method of analysis. These results support previous evidence of strong host-family specificity in Haemoproteus and suggest that lineages of Plasmodium are more likely to form evolutionarily-stable associations with novel hosts.
Based on specific sequencing, we found that a Borrelia garinii strain from a rodent in Fukui Prefecture, Japan was highly similar to the unique Borrelia strains (pattern R'/R) isolated in northeastern China and Korea, and to strains from ticks feeding on migratory birds in Fukui Prefecture. These findings indicate that the Borrelia with this unique pattern may be locally naturalized to the epizootic transmission cycle in Japan, and that Borrelia is dispersed from the Asian Continent to Japan via migratory birds.
Research on contact zones has paid relatively little attention to host-parasite interactions, although these situations have important but different implications depending on whether one considers the host or the parasite's perspective. We investigated both the role of a host contact zone in parasite expansion and whether parasites could influence contact zone dynamics. We studied the diversity and the patterns of parasite exchange (genera Haemoproteus and Plasmodium) infecting two parapatric sibling passerines meeting at a moving contact zone in western Europe. We amplified and sequenced a fragment of the parasite cytochrome b gene. The expanding host harboured more diverse parasites, which might indicate a superior ability to face a diverse parasite fauna than the receding host. Prevalence was very high in both hosts, due to the frequent occurrence of two sister Haemoproteus lineages. Despite the recent movement of the contact zone, these two parasites fitted almost perfectly to the geographic range of their main host species. Yet, we found several cases of cross-species infection in sympatric areas and evidences of asymmetrical spreading of parasites from the expanding host towards the receding host. Altogether, our results suggest that the host contact zone mainly acts as a barrier to parasite expansion even if recurrent host shifts are observed. Besides, they also support the idea that parasite-mediated competition might contribute to the displacement of hosts' contact zones, thereby emphasizing the role of parasitism on the population dynamics of sympatric species.
Introduction to general state-space Markov chain theory. In W. R. Gilks, S. Richardson, and D. J. Spiegelhalter (Eds.), Markov Chain Monte Carlo in Practice, Chapter 4, pp. 59-74. London: Chapman and Hall. Yang, Z., R. Nielsen, N. Goldman, and A.-M. K. Pedersen (2000). Codon- substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155, 431-449. Yang, Z. and B. Rannala (1997). Bayesian phylogenetic inference using DNA sequences: A Markov chain Monte Carlo method. Molecular Biology and Evolution 1, 717-724. Yang, Z. H. (1993). Maximum-likelihood-estimation of phylogeny from DNA- sequences when substitution rates differ over sites. Molecular Biology and Evolution I0(6), 1396-1401. Zuckerkandl, E. (1987). On the molecular evolutionary clock. Journal of Molec- ular Evolution 26, 34-46. Zuckerkandl, E. and L. Pauling (1962). Molecular disease, evolution, and genic heterogeneity. In M. Kasha and B. Pullman (Eds.), Horizons in Biochem- istry, pp. 189-225. Ne
Identification Guide to European Passerines, 4 edn
- L Svensson
Svensson L (1992) Identification Guide to European Passerines, 4 edn.
Lars Svensson, Stockholm, Sweden.
Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds
- S Bensch
- M Stjernman
- D Hasselquist
Bensch S, Stjernman M, Hasselquist D et al. (2000) Host specificity
in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proceedings of the
Royal Society of London. Series B, Biological Sciences, 267, 1583 –1589.
Wintering Areas of Migrants Trapped at Ottenby Bird Observatory, Special report from Ottenby Bird observatory
- J Pettersson
- A Sandström
- K Johansson
Pettersson J, Sandström A, Johansson K (1986) Wintering Areas of
Migrants Trapped at Ottenby Bird Observatory, Special report from
Ottenby Bird observatory No. 6.
Der Zug Europäischer Singvögel, Ein Atlas der Wiederfunde Beringter Vögel. band III, AULA-verlag GmbH
- G Zink
Zink G (1995) Der Zug Europäischer Singvögel, Ein Atlas der Wiederfunde Beringter Vögel. band III, AULA-verlag GmbH, Wiesbaden.
Birds of Western Africa
- N Borrow
- R Demey
Borrow N, Demey R (2001) Birds of Western Africa, Christopher
Helm, London.
Migrants and their parasites; a bridge between two worlds
- Re Ricklefs
- Sm Fallon
- Sc Latta
- Bl Swanson
- E Bermingham
Ricklefs RE, Fallon SM, Latta SC, Swanson BL, Bermingham E (2005)
Migrants and their parasites; a bridge between two worlds.
- R Greenberg
- Pp Marra
In: Birds of Two Worlds; the Ecology and Evolution of Migration (eds
© 2007 The Authors
Journal compilation © 2007 Blackwell Publishing Ltd
Greenberg R, Marra PP), pp. 210 – 221. The Johns Hopkins University Press, Baltimore.
Wintering Areas of Migrants Trapped at Ottenby Bird Observatory
- J Pettersson
- K Sandström A Johansson
Wintering Areas of Migrants Trapped at Ottenby Bird Observatory Special report from Ottenby Bird observatory
- Johanssonk Petterssonj Sandströma
AWTY: a system for graphical exploration of MCMC convergence in Bayesian phylogenetic inference
- Swofforddl Wilgenbuschjc Warrendl