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Biting midges (Culicoides, Diptera) transmit Haemoproteus parasites of owls: evidence from sporogony and molecular phylogeny.

Bukauskaitė D, Žiegytė R, Palinauskas V, Iezhova TA, Dimitrov D, Ilgūnas M, Bernotienė R, Markovets MY, Valkiūnas G - Parasit Vectors (2015)

Bottom Line: Gametes and ookinetes of both species readily developed in vitro.Culicoides nubeculosus and C. impunctatus are vectors of H. noctuae and H. syrnii.Phylogenies based on cytochrome b gene indicate parasite-vector relationships, and we recommend using them in predicting possible parasite-vector relationships and planning research on avian Haemoproteus spp. vectors in wildlife.

View Article: PubMed Central - PubMed

Affiliation: Institute of Ecology, Nature Research Centre, Akademijos 2, Vilnius 21, LT-09412, Lithuania. dovilebu7@gmail.com.

ABSTRACT

Background: Haemoproteus parasites are widespread, and several species cause diseases both in birds and blood-sucking insects. These pathogens are transmitted by dipterans belonging to the Ceratopogonidae and Hippoboscidae, however certain vector species remain unknown for the majority of Haemoproteus spp. Owls are often infected by Haemoproteus parasites, but experimental studies on vectors of these infections are lacking. The aim of this study was to investigate sporogonic development of two widespread Haemoproteus parasites of owls, H. noctuae and H. syrnii in experimentally infected biting midges Culicoides impunctatus and Culicoides nubeculosus. We also followed in vitro sporogonic development of these infections and determined their phylogenetic relationships with Haemoproteus spp., for which vectors have been identified.

Methods: Wild-caught C. impunctatus and laboratory reared C. nubeculosus were infected experimentally by allowing them to take blood meals on one individual long-eared owl (Asio otus) and one tawny owl (Strix aluco) harbouring mature gametocytes of H. noctuae (lineage hCIRCUM01) and H. syrnii (hCULCIB01), respectively. The engorged insects were maintained in the laboratory at 16-18 °C, and dissected at intervals in order to follow the development of ookinetes, oocysts and sporozoites. We also observed in vitro development of sexual stages of both parasites by exposure of infected blood to air. The parasite lineages were determined by polymerase chain reaction-based methods. Bayesian phylogeny was constructed in order to determine the relationships of owl parasites with other avian Haemoproteus spp., for which vectors have been identified.

Results: Both H. noctuae and H. syrnii completed sporogony in C. nubeculosus, and H. noctuae completed sporogony in C. impunctatus. Ookinetes, oocysts and sporozoites of these parasites were reported and described. Gametes and ookinetes of both species readily developed in vitro. In accordance with sporogony data, the phylogenetic analysis placed both parasite lineages in a clade of Culicoides spp.-transmitted avian Haemoproteus (Parahaemoproteus) spp.

Conclusions: Culicoides nubeculosus and C. impunctatus are vectors of H. noctuae and H. syrnii. Phylogenies based on cytochrome b gene indicate parasite-vector relationships, and we recommend using them in predicting possible parasite-vector relationships and planning research on avian Haemoproteus spp. vectors in wildlife.

No MeSH data available.


Related in: MedlinePlus

Bayesian phylogeny of 16 Haemoproteus (Parahaemoproteus) spp., 5 H. (Haemoproteus) spp. and 3 Plasmodium spp. based on cytochrome b gene sequences of 479 bp lengths. One Leucocytozoon sp. sequence was used as outgroup. Nodal support values indicate Bayesian posterior probabilities. The scale bar shows the expected substitutions per site. Parasite lineage codes are given according to MalAvi database [17]; they are followed by GenBank accession numbers of sequences and parasite species names. Vertical bars (a–c) indicate groups of closely related species belonging to the subgenus Parahaemoproteus (a) and Haemoproteus (b); lineages of owl parasites are marked by bar C. Parasite lineages used in this study are given in bold font
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Fig4: Bayesian phylogeny of 16 Haemoproteus (Parahaemoproteus) spp., 5 H. (Haemoproteus) spp. and 3 Plasmodium spp. based on cytochrome b gene sequences of 479 bp lengths. One Leucocytozoon sp. sequence was used as outgroup. Nodal support values indicate Bayesian posterior probabilities. The scale bar shows the expected substitutions per site. Parasite lineage codes are given according to MalAvi database [17]; they are followed by GenBank accession numbers of sequences and parasite species names. Vertical bars (a–c) indicate groups of closely related species belonging to the subgenus Parahaemoproteus (a) and Haemoproteus (b); lineages of owl parasites are marked by bar C. Parasite lineages used in this study are given in bold font

Mentions: Phylogenetic analysis placed all Culicoides spp.-transmitted avian haemoproteids in a well-supported clade A (Fig. 4), which contains Parahaemoproteus parasites. One H. noctuae lineage and five H. syrnii lineages, including those used in this study (Fig. 4, clade C), appeared in the clade A. That is in accordance with our sporogony study, which showed complete sporogonic development of these parasites in Culicoides biting midges (Fig. 2e–j). Lineages of hippoboscid-transmitted parasites of the subgenus Haemoproteus were placed in a separate well-supported clade B, which is the sister to clade A (Fig. 4).Fig. 4


Biting midges (Culicoides, Diptera) transmit Haemoproteus parasites of owls: evidence from sporogony and molecular phylogeny.

Bukauskaitė D, Žiegytė R, Palinauskas V, Iezhova TA, Dimitrov D, Ilgūnas M, Bernotienė R, Markovets MY, Valkiūnas G - Parasit Vectors (2015)

Bayesian phylogeny of 16 Haemoproteus (Parahaemoproteus) spp., 5 H. (Haemoproteus) spp. and 3 Plasmodium spp. based on cytochrome b gene sequences of 479 bp lengths. One Leucocytozoon sp. sequence was used as outgroup. Nodal support values indicate Bayesian posterior probabilities. The scale bar shows the expected substitutions per site. Parasite lineage codes are given according to MalAvi database [17]; they are followed by GenBank accession numbers of sequences and parasite species names. Vertical bars (a–c) indicate groups of closely related species belonging to the subgenus Parahaemoproteus (a) and Haemoproteus (b); lineages of owl parasites are marked by bar C. Parasite lineages used in this study are given in bold font
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4469425&req=5

Fig4: Bayesian phylogeny of 16 Haemoproteus (Parahaemoproteus) spp., 5 H. (Haemoproteus) spp. and 3 Plasmodium spp. based on cytochrome b gene sequences of 479 bp lengths. One Leucocytozoon sp. sequence was used as outgroup. Nodal support values indicate Bayesian posterior probabilities. The scale bar shows the expected substitutions per site. Parasite lineage codes are given according to MalAvi database [17]; they are followed by GenBank accession numbers of sequences and parasite species names. Vertical bars (a–c) indicate groups of closely related species belonging to the subgenus Parahaemoproteus (a) and Haemoproteus (b); lineages of owl parasites are marked by bar C. Parasite lineages used in this study are given in bold font
Mentions: Phylogenetic analysis placed all Culicoides spp.-transmitted avian haemoproteids in a well-supported clade A (Fig. 4), which contains Parahaemoproteus parasites. One H. noctuae lineage and five H. syrnii lineages, including those used in this study (Fig. 4, clade C), appeared in the clade A. That is in accordance with our sporogony study, which showed complete sporogonic development of these parasites in Culicoides biting midges (Fig. 2e–j). Lineages of hippoboscid-transmitted parasites of the subgenus Haemoproteus were placed in a separate well-supported clade B, which is the sister to clade A (Fig. 4).Fig. 4

Bottom Line: Gametes and ookinetes of both species readily developed in vitro.Culicoides nubeculosus and C. impunctatus are vectors of H. noctuae and H. syrnii.Phylogenies based on cytochrome b gene indicate parasite-vector relationships, and we recommend using them in predicting possible parasite-vector relationships and planning research on avian Haemoproteus spp. vectors in wildlife.

View Article: PubMed Central - PubMed

Affiliation: Institute of Ecology, Nature Research Centre, Akademijos 2, Vilnius 21, LT-09412, Lithuania. dovilebu7@gmail.com.

ABSTRACT

Background: Haemoproteus parasites are widespread, and several species cause diseases both in birds and blood-sucking insects. These pathogens are transmitted by dipterans belonging to the Ceratopogonidae and Hippoboscidae, however certain vector species remain unknown for the majority of Haemoproteus spp. Owls are often infected by Haemoproteus parasites, but experimental studies on vectors of these infections are lacking. The aim of this study was to investigate sporogonic development of two widespread Haemoproteus parasites of owls, H. noctuae and H. syrnii in experimentally infected biting midges Culicoides impunctatus and Culicoides nubeculosus. We also followed in vitro sporogonic development of these infections and determined their phylogenetic relationships with Haemoproteus spp., for which vectors have been identified.

Methods: Wild-caught C. impunctatus and laboratory reared C. nubeculosus were infected experimentally by allowing them to take blood meals on one individual long-eared owl (Asio otus) and one tawny owl (Strix aluco) harbouring mature gametocytes of H. noctuae (lineage hCIRCUM01) and H. syrnii (hCULCIB01), respectively. The engorged insects were maintained in the laboratory at 16-18 °C, and dissected at intervals in order to follow the development of ookinetes, oocysts and sporozoites. We also observed in vitro development of sexual stages of both parasites by exposure of infected blood to air. The parasite lineages were determined by polymerase chain reaction-based methods. Bayesian phylogeny was constructed in order to determine the relationships of owl parasites with other avian Haemoproteus spp., for which vectors have been identified.

Results: Both H. noctuae and H. syrnii completed sporogony in C. nubeculosus, and H. noctuae completed sporogony in C. impunctatus. Ookinetes, oocysts and sporozoites of these parasites were reported and described. Gametes and ookinetes of both species readily developed in vitro. In accordance with sporogony data, the phylogenetic analysis placed both parasite lineages in a clade of Culicoides spp.-transmitted avian Haemoproteus (Parahaemoproteus) spp.

Conclusions: Culicoides nubeculosus and C. impunctatus are vectors of H. noctuae and H. syrnii. Phylogenies based on cytochrome b gene indicate parasite-vector relationships, and we recommend using them in predicting possible parasite-vector relationships and planning research on avian Haemoproteus spp. vectors in wildlife.

No MeSH data available.


Related in: MedlinePlus