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Title: Parasitaemia data and molecular characterization of Haemoproteus catharti from New World vultures (Cathartidae) reveals a novel clade of Haemosporida

Abstract

Background: New World vultures (Cathartiformes: Cathartidae) are obligate scavengers comprised of seven species in five genera throughout the Americas. Of these, turkey vultures (Cathartes aura) and black vultures (Coragyps atratus) are the most widespread and, although ecologically similar, have evolved differences in morphology, physiology, and behaviour. Three species of haemosporidians have been reported in New World vultures to date: Haemoproteus catharti, Leucocytozoon toddi and Plasmodium elongatum, although few studies have investigated haemosporidian parasites in this important group of species. In this study, morphological and molecular methods were used to investigate the epidemiology and molecular biology of haemosporidian parasites of New World vultures in North America. Methods: Blood and/or tissue samples were obtained from 162 turkey vultures and 95 black vultures in six states of the USA. Parasites were identified based on their morphology in blood smears, and sequences of the mitochondrial cytochrome b and nuclear adenylosuccinate lyase genes were obtained for molecular characterization. Results: No parasites were detected in black vultures, whereas 24% of turkey vultures across all sampling locations were positive for H. catharti by blood smear analysis and/or PCR testing. The phylogenetic analysis of cytochrome b gene sequences revealed that H. catharti is closely related to MYCAMH1, amore » yet unidentified haemosporidian from wood storks (Mycteria americana) in southeastern USA and northern Brazil. Haemoproteus catharti and MYCAMH1 represent a clade that is unmistakably separate from all other Haemoproteus spp., being most closely related to Haemocystidium spp. from reptiles and to Plasmodium spp. from birds and reptiles. Conclusions: Haemoproteus catharti is a widely-distributed parasite of turkey vultures in North America that is evolutionarily distinct from other haemosporidian parasites. These results reveal that the genetic diversity and evolutionary relationships of avian haemosporidians are still being uncovered, and future studies combining a comprehensive evaluation of morphological and life cycle characteristics with the analysis of multiple nuclear and mitochondrial genes will be useful to redefine the genus boundaries of these parasites and to re-evaluate the relationships amongst haemosporidians of birds, reptiles and mammals.« less

Authors:
ORCiD logo [1];  [2];  [3];  [1];  [4];  [1];  [1];  [5];  [6];  [7];  [1];  [1];  [8];  [9];  [10];  [4]
  1. Univ. of Georgia, Athens, GA (United States)
  2. Nelson Mandela University, Port Elizabeth (South Africa)
  3. National Zoological Park, Washington DC (United States); Univ. of Vermont, Burlington, VT (United States)
  4. Univ. of Georgia, Athens, GA (United States); Univ. of Georgia, Aiken, SC (United States); Savannah River Site (SRS), Aiken, SC (United States). Savannah River Ecology Lab. (SREL)
  5. American Museum of Natural History, New York, NY (United States)
  6. Yurok Tribe Wildlife Program, Klamath, CA (United States)
  7. Savannah River Site (SRS), Aiken, SC (United States). Savannah River Ecology Lab. (SREL); Univ. of Georgia, Aiken, SC (United States)
  8. Animal Diagnostic Laboratory, University Park, PA (United States)
  9. Wildlife Center of Virginia, Waynesboro, VA (United States)
  10. West Virginia Univ., Morgantown, WV (United States)
Publication Date:
Research Org.:
Univ. of Georgia, Athens (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1510292
Grant/Contract Number:  
FC09-07SR22506
Resource Type:
Accepted Manuscript
Journal Name:
Malaria Journal
Additional Journal Information:
Journal Volume: 17; Journal Issue: 1; Journal ID: ISSN 1475-2875
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Adenylosuccinate lyase; Avian parasite; Bird; Cytochrome b; Cathartidae; Evolution; Haemoproteidae; Malarial parasite; North America; Neotropical

Citation Formats

Yabsley, Michael J., Vanstreels, Ralph E. T., Martinsen, Ellen S., Wickson, Alexandra G., Holland, Amanda E., Hernandez, Sonia M., Thompson, Alec T., Perkins, Susan L., West, Christopher J., Bryan, A. Lawrence, Cleveland, Christopher A., Jolly, Emily, Brown, Justin D., McRuer, Dave, Behmke, Shannon, and Beasley, James C. Parasitaemia data and molecular characterization of Haemoproteus catharti from New World vultures (Cathartidae) reveals a novel clade of Haemosporida. United States: N. p., 2018. Web. doi:10.1186/s12936-017-2165-5.
Yabsley, Michael J., Vanstreels, Ralph E. T., Martinsen, Ellen S., Wickson, Alexandra G., Holland, Amanda E., Hernandez, Sonia M., Thompson, Alec T., Perkins, Susan L., West, Christopher J., Bryan, A. Lawrence, Cleveland, Christopher A., Jolly, Emily, Brown, Justin D., McRuer, Dave, Behmke, Shannon, & Beasley, James C. Parasitaemia data and molecular characterization of Haemoproteus catharti from New World vultures (Cathartidae) reveals a novel clade of Haemosporida. United States. doi:10.1186/s12936-017-2165-5.
Yabsley, Michael J., Vanstreels, Ralph E. T., Martinsen, Ellen S., Wickson, Alexandra G., Holland, Amanda E., Hernandez, Sonia M., Thompson, Alec T., Perkins, Susan L., West, Christopher J., Bryan, A. Lawrence, Cleveland, Christopher A., Jolly, Emily, Brown, Justin D., McRuer, Dave, Behmke, Shannon, and Beasley, James C. Mon . "Parasitaemia data and molecular characterization of Haemoproteus catharti from New World vultures (Cathartidae) reveals a novel clade of Haemosporida". United States. doi:10.1186/s12936-017-2165-5. https://www.osti.gov/servlets/purl/1510292.
@article{osti_1510292,
title = {Parasitaemia data and molecular characterization of Haemoproteus catharti from New World vultures (Cathartidae) reveals a novel clade of Haemosporida},
author = {Yabsley, Michael J. and Vanstreels, Ralph E. T. and Martinsen, Ellen S. and Wickson, Alexandra G. and Holland, Amanda E. and Hernandez, Sonia M. and Thompson, Alec T. and Perkins, Susan L. and West, Christopher J. and Bryan, A. Lawrence and Cleveland, Christopher A. and Jolly, Emily and Brown, Justin D. and McRuer, Dave and Behmke, Shannon and Beasley, James C.},
abstractNote = {Background: New World vultures (Cathartiformes: Cathartidae) are obligate scavengers comprised of seven species in five genera throughout the Americas. Of these, turkey vultures (Cathartes aura) and black vultures (Coragyps atratus) are the most widespread and, although ecologically similar, have evolved differences in morphology, physiology, and behaviour. Three species of haemosporidians have been reported in New World vultures to date: Haemoproteus catharti, Leucocytozoon toddi and Plasmodium elongatum, although few studies have investigated haemosporidian parasites in this important group of species. In this study, morphological and molecular methods were used to investigate the epidemiology and molecular biology of haemosporidian parasites of New World vultures in North America. Methods: Blood and/or tissue samples were obtained from 162 turkey vultures and 95 black vultures in six states of the USA. Parasites were identified based on their morphology in blood smears, and sequences of the mitochondrial cytochrome b and nuclear adenylosuccinate lyase genes were obtained for molecular characterization. Results: No parasites were detected in black vultures, whereas 24% of turkey vultures across all sampling locations were positive for H. catharti by blood smear analysis and/or PCR testing. The phylogenetic analysis of cytochrome b gene sequences revealed that H. catharti is closely related to MYCAMH1, a yet unidentified haemosporidian from wood storks (Mycteria americana) in southeastern USA and northern Brazil. Haemoproteus catharti and MYCAMH1 represent a clade that is unmistakably separate from all other Haemoproteus spp., being most closely related to Haemocystidium spp. from reptiles and to Plasmodium spp. from birds and reptiles. Conclusions: Haemoproteus catharti is a widely-distributed parasite of turkey vultures in North America that is evolutionarily distinct from other haemosporidian parasites. These results reveal that the genetic diversity and evolutionary relationships of avian haemosporidians are still being uncovered, and future studies combining a comprehensive evaluation of morphological and life cycle characteristics with the analysis of multiple nuclear and mitochondrial genes will be useful to redefine the genus boundaries of these parasites and to re-evaluate the relationships amongst haemosporidians of birds, reptiles and mammals.},
doi = {10.1186/s12936-017-2165-5},
journal = {Malaria Journal},
number = 1,
volume = 17,
place = {United States},
year = {2018},
month = {1}
}

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MrBayes 3: Bayesian phylogenetic inference under mixed models
journal, August 2003