Presencia de una especie de malaria invasora en aves traficadas ilegalmente en la Amazonía Peruana

Resumen del trabajo presentado al XVIII Congreso Nacional y XV Iberoamericano de Etología y Ecología Evolutiva, celebrados en Badajoz (España) del 31 de octubre al 3 de noviembre de 2023.El tráfico ilegal de especies está clasificado como la tercera actividad delictiva más lucrativa y representa uno de los mayores peligros para la biodiversidad. Además, el comercio ilegal de vida silvestre puede aumentar la propagación de parásitos en todo el mundo, provocando la aparición de enfermedades que afectan a la fauna silvestre, los animales domésticos y los humanos. El orden Psittaciformes presenta la mayor proporción de especies en peligro de extinción entre todas las aves del mundo y es uno de los taxones más traficados en el comercio de mascotas. Sin embargo, la influencia del comercio ilegal de aves silvestres en la introducción de patógenos exóticos está poco investigada. Aquí examinamos la prevalencia y la diversidad genética de los parásitos hemosporidios en periquitos de alas amarillas (Brotogeris versicolorus) comercializados ilegalmente en la Amazonía peruana. El 18,5% de los periquitos estaban infectados por Plasmodium relictum GRW04, un parásito altamente invasor que provoca graves efectos negativos en el fitness de sus hospedadores e incluso la extinción de la avifauna nativa cuando se establece fuera de su área de distribución natural. Además, las aves infectadas con malaria tuvieron una peor condición corporal que las no infectados, lo que revela los efectos negativos de esta especie de malaria. Estos resultados resaltan que el comercio ilegal de fauna silvestre puede suponer un riesgo de brotes de enfermedades. Nuestros resultados también revelan conceptos epidemiológicos clave en la transmisión de enfermedades, como el papel de las especies de psitácidos poco estudiadas como reservorios naturales de haemosporidios. Estos hallazgos enfatizan la importancia las políticas y normativas que combatan el tráfico ilegal de vida silvestre y eviten la propagación de enfermedades.Peer reviewe

Molecular identification of the chitinase genes in Plasmodium relictum

Background: Malaria parasites need to synthesize chitinase in order to go through the peritrophic membrane, which is created around the mosquito midgut, to complete its life cycle. In mammalian malaria species, the chitinase gene comprises either a large or a short copy. In the avian malaria parasites Plasmodium gallinaceum both copies are present, suggesting that a gene duplication in the ancestor to these extant species preceded the loss of either the long or the short copy in Plasmodium parasites of mammals. Plasmodium gallinaceum is not the most widespread and harmful parasite of birds. This study is the first to search for and identify the chitinase gene in one of the most prevalent avian malaria parasites, Plasmodium relictum. Methods: Both copies of P. gallinaceum chitinase were used as reference sequences for primer design. Different sequences of Plasmodium spp. were used to build the phylogenetic tree of chitinase gene. Results: The gene encoding for chitinase was identified in isolates of two mitochondrial lineages of P. relictum (SGS1 and GRW4). The chitinase found in these two lineages consists both of the long (PrCHT1) and the short (PrCHT2) copy. The genetic differences found in the long copy of the chitinase gene between SGS1 and GRW4 were higher than the difference observed for the cytochrome b gene. Conclusion: The identification of both copies in P. relictum sheds light on the phylogenetic relationship of the chitinase gene in the genus Plasmodium. Due to its high variability, the chitinase gene could be used to study the genetic population structure in isolates from different host species and geographic regions

Stimuli Followed by Avian Malaria Vectors in Host-Seeking Behaviour

Vector-borne infectious diseases (e.g., malaria, dengue fever, and yellow fever) result from a parasite transmitted to humans and other animals by blood-feeding arthropods. They are major contributors to the global disease burden, as they account for nearly a fifth of all infectious diseases worldwide. The interaction between vectors and their hosts plays a key role driving vector-borne disease transmission. Therefore, identifying factors governing host selection by blood-feeding insects is essential to understand the transmission dynamics of vector-borne diseases. Here, we review published information on the physical and chemical stimuli (acoustic, visual, olfactory, moisture and thermal cues) used by mosquitoes and other haemosporidian vectors to detect their vertebrate hosts. We mainly focus on studies on avian malaria and related haemosporidian parasites since this animal model has historically provided important advances in our understanding on ecological and evolutionary process ruling vector-borne disease dynamics and transmission. We also present relevant studies analysing the capacity of feather and skin symbiotic bacteria in the production of volatile compounds with vector attractant properties. Furthermore, we review the role of uropygial secretions and symbiotic bacteria in bird–insect vector interactions. In addition, we present investigations examining the alterations induced by haemosporidian parasites on their arthropod vector and vertebrate host to enhance parasite transmission. Finally, we propose future lines of research for designing successful vector control strategies and for infectious disease management

Genomic advances in the study of the mosquito vector during avian malaria infection

Invertebrate host–parasite associations are one of the keystones in order to understand vector-borne diseases. The study of these specific interactions provides information not only about how the vector is affected by the parasite at the gene-expression level, but might also reveal mosquito strategies for blocking the transmission of the parasites. A very well-known vector for human malaria is Anopheles gambiae. This mosquito species has been the main focus for genomics studies determining essential key genes and pathways over the course of a malaria infection. However, to-date there is an important knowledge gap concerning other non-mammophilic mosquito species, for example some species from the Culex genera which may transmit avian malaria but also zoonotic pathogens such as West Nile virus. From an evolutionary perspective, these 2 mosquito genera diverged 170 million years ago, hence allowing studies in both species determining evolutionary conserved genes essential during malaria infections, which in turn might help to find key genes for blocking malaria cycle inside the mosquito. Here, we extensively review the current knowledge on key genes and pathways expressed in Anopheles over the course of malaria infections and highlight the importance of conducting genomic investigations for detecting pathways in Culex mosquitoes linked to infection of avian malaria. By pooling this information, we underline the need to increase genomic studies in mosquito–parasite associations, such as the one in Culex–Plasmodium, that can provide a better understanding of the infection dynamics in wildlife and reduce the negative impact on ecosystems

The Adaptive Host Manipulation Hypothesis: Parasites Modify the Behaviour, Morphology, and Physiology of Amphibians

Parasites have evolved different strategies to increase their transmission from one host to another. The Adaptive Host Manipulation hypothesis states that parasites induce modifications of host phenotypes that could maximise parasite fitness. There are numerous examples of parasite manipulation across a wide range of host and parasite taxa. However, the number of studies exploring the manipulative effects of parasites on amphibians is still scarce. Herein, we extensively review the current knowledge on phenotypic alterations in amphibians following parasite infection. Outcomes from different studies show that parasites may manipulate amphibian behaviours to favour their transmission among conspecifics or to enhance the predation of infected amphibians by a suitable definite host. In addition, parasites also modify the limb morphology and impair locomotor activity of infected toads, frogs, and salamanders, hence facilitating their ingestion by a final host and completing the parasite life cycle. Additionally, parasites may alter host physiology to enhance pathogen proliferation, survival, and transmission. We examined the intrinsic (hosts traits) and extrinsic (natural and anthropogenic events) factors that may determine the outcome of infection, where human-induced changes of environmental conditions are the most harmful stressors that enhance amphibian exposure and susceptibility to parasite

Avian malaria, haematocrit, and body condition in invasive wetland passerines settled in southwestern Spain

Avian malaria and related haemosporidian parasites can negatively impact fitness in many songbirds. Research on the malaria infection and its physiological costs on their avian hosts is heavily skewed toward native passerines, with exotic species underrepresented. However, introduced species may carry on and spread new pathogens to native species, and play a role on parasite transmission cycle in invaded bird communities as pathogen reservoir. Here, we molecularly assess the prevalence and diversity of haemosporidian parasites in three introduced wetland passerines (the Red Avadavat Amandava amandava, the Yellow-crowned Bishop Euplectes afer, and the Common Waxbill Estrilda astrild) captured during the same season in southwestern Spain. We also explored the relation between parasite infection, body condition, haematocrit, and uropygial gland volume. We detected an overall parasite prevalence of 3.55%, where Common Waxbills showed higher prevalence (6.94%) than Red Avadavats (1.51%). None Yellow-crowned Bishops were infected with haemosporidians. Almost 60% of infections were caused by Leucocytozoon, and about 40% by Plasmodium. We identified four unique lineages of Plasmodium and three of Leucocytozoon. Moreover, 91% of the identified host–parasite interactions represented new host records for these haemosporidian parasites. Parasite infection was not related to body condition, haematocrit, and uropygial gland volume of the wetland passerines. Haematocrit values varied seasonally among bird species. Additionally, haematocrit was positively related to body condition in the Yellow-crowned Bishops, but not in the other species. Red Avadavats had higher haematocrit levels than Yellow-crowned Bishops, whereas Common Waxbills showed the lower haematocrit values. The uropygial gland volume was positively correlated with body condition in all bird species. Common Waxbills showed higher uropygial gland volumes related to their body size than birds from other two species. These outcomes highlight the importance of exotic invasive species in the transmission dynamics of haemosporidian parasites.We are grateful to technical and human support provided by Facility of Bioscience Applied Techniques of SAIUEx (financed by UEX, Junta de Extremadura, MICINN, FEDER and FSE). This study was funded by Consejería de Economía e Infraestructura of the Junta de Extremadura and the European Regional Development Fund, a Way to Make Europe (research projects IB16121 and IB20089). JM was supported by a postdoctoral grant from the Juan de la Cierva Subprogram (FJCI 2017-34109, MICINN), and a postdoctoral contract for scientific excellence in the development of the Plan Propio de I ​+ ​D ​+ ​i of the UCLM (co-funded by the European Social Fund Plus (ESF+)).Peer reviewe

Detecting transmission areas of malaria parasites in a migratory bird species.

The identification of the regions where vector-borne diseases are transmitted is essential to study transmission patterns and to recognize future changes in environmental conditions that may potentially influence the transmission areas. SGS1, one of the lineages of Plasmodium relictum, is known to have active transmission in tropical Africa and temperate regions of Europe. Nuclear sequence data from isolates infected with SGS1 (based on merozoite surface protein 1 (MSP1) allelic diversity) have provided new insights on the distribution and transmission areas of these allelic variants. For example, MSP1 alleles transmitted in Africa differ from those transmitted in Europe, suggesting the existence of two populations of SGS1 lineages. However, no study has analysed the distribution of African and European transmitted alleles in Afro-Palearctic migratory birds. With this aim, we used a highly variable molecular marker to investigate whether juvenile house martins become infected in Europe before their first migration to Africa. We explored the MSP1 allelic diversity of P. relictum in adult and juvenile house martins. We found that juveniles were infected with SGS1 during their first weeks of life, confirming active transmission of SGS1 to house martins in Europe. Moreover, we found that all the juveniles and most of adults were infected with one European transmitted MSP1 allele, whereas two adult birds were infected with two African transmitted MSP1 alleles. These findings suggest that house martins are exposed to different strains of P. relictum in their winter and breeding quarters

Host-parasite interaction explains variation in the prevalence of avian haemosporidians at the community level

Parasites are a selective force that shape host community structure and dynamics, but host communities can also influence parasitism. Understanding the dual nature from host-parasite interactions can be facilitated by quantifying the variation in parasite prevalence among host species and then comparing that variation to other ecological factors that are known to also shape host communities. Avian haemosporidian parasites (e.g. Plasmodium and Haemoproteus) are abundant and widespread representing an excellent model for the study of host-parasite interactions. Several geographic and environmental factors have been suggested to determine prevalence of avian haemosporidians in bird communities. However, it remains unknown whether host and parasite traits, represented by phylogenetic distances among species and degree of specialization in host-parasite relationships, can influence infection status. The aims of this study were to analyze factors affecting infection status in a bird community and to test whether the degree of parasite specialization on their hosts is determined by host traits. Our statistical analyses suggest that infection status is mainly determined by the interaction between host species and parasite lineages where tolerance and/or susceptibility to parasites plays an essential role. Additionally, we found that although some of the parasite lineages infected a low number of bird individuals, the species they infected were distantly related and therefore the parasites themselves should not be considered typical host specialists. Infection status was higher for generalist than for specialist parasites in some, but not all, host species. These results suggest that detected prevalence in a species mainly results from the interaction between host immune defences and parasite exploitation strategies wherein the result of an association between particular parasite lineages and particular host species is idiosyncratic

Reciprocal positive effects on parasitemia between coinfecting haemosporidian parasites in house sparrows

Background: Hosts are often simultaneously infected with several parasite species. These co-infections can lead to within-host interactions of parasites, including mutualism and competition, which may affect both virulence and transmission. Birds are frequently co-infected with different haemosporidian parasites, but very little is known about if and how these parasites interact in natural host populations and what consequences there are for the infected hosts. We therefore set out to study Plasmodium and Haemoproteus parasites in house sparrows Passer domesticus with naturally acquired infections using a protocol where the parasitemia (infection intensity) is quantified by qPCR separately for the two parasites. We analysed infection status (presence/absence of the parasite) and parasitemia of parasites in the blood of both adult and juvenile house sparrows repeatedly over the season. Results: Haemoproteus passeris and Plasmodium relictum were the two dominating parasite species, found in 99% of the analyzed Sanger sequences. All birds were infected with both Plasmodium and Haemoproteus parasites during the study period. Seasonality explained infection status for both parasites in the adults: H. passeris was completely absent in the winter while P. relictum was present all year round. Among adults infected with H. passeris there was a positive effect of P. relictum parasitemia on H. passeris parasitemia and likewise among adults infected with P. relictum there was a positive effect of H. passeris parasitemia on P. relictum parasitemia. No such associations on parasitemia were seen in juvenile house sparrows. Conclusions: The reciprocal positive relationships in parasitemia between P. relictum and H. passeris in adult house sparrows suggests either mutualistic interactions between these frequently occurring parasites or that there is variation in immune responses among house sparrow individuals, hence some individuals suppress the parasitemia of both parasites whereas other individuals suppress neither. Our detailed screening of haemosporidian parasites over the season shows that co-infections are very frequent in both juvenile and adult house sparrows, and since co-infections often have stronger negative effects on host fitness than the single infection, it is imperative to use screening systems with the ability to detect multiple parasites in ecological studies of host-parasite interactions