Presence of a cryptic Onchocerca species in black flies of northern California, USA

Abstract Background Black flies (Diptera: Simuliidae) serve as arthropod vectors for various species of Onchocerca (Nematoda: Onchocercidae) that may be associated with disease in humans, domestic animals, and wildlife. The emergence of zoonotic Onchocerca lupi in North America and reports of cervid...

Full description

Bibliographic Details
Main Authors: Matthew Kulpa, Kimberly J. Nelson, Alana M. Morales, Bonnie M. Ryan, Michelle L. Koschik, Jamesina J. Scott, Guilherme G. Verocai
Format: Article
Language:English
Published: BMC 2021-09-01
Series:Parasites & Vectors
Subjects:
Online Access:https://doi.org/10.1186/s13071-021-04990-1
_version_ 1819122424991449088
author Matthew Kulpa
Kimberly J. Nelson
Alana M. Morales
Bonnie M. Ryan
Michelle L. Koschik
Jamesina J. Scott
Guilherme G. Verocai
author_facet Matthew Kulpa
Kimberly J. Nelson
Alana M. Morales
Bonnie M. Ryan
Michelle L. Koschik
Jamesina J. Scott
Guilherme G. Verocai
author_sort Matthew Kulpa
collection DOAJ
description Abstract Background Black flies (Diptera: Simuliidae) serve as arthropod vectors for various species of Onchocerca (Nematoda: Onchocercidae) that may be associated with disease in humans, domestic animals, and wildlife. The emergence of zoonotic Onchocerca lupi in North America and reports of cervid-associated zoonotic onchocerciasis by Onchocerca jakutensis highlight the need for increased entomological surveillance. In addition, there is mounting evidence that Onchocerca diversity in North America is far greater than previously thought, currently regarded as Onchocerca cervipedis species complex. This study reports new geographic records and black fly vector associations of an uncharacterized Onchocerca species. Methods To better understand the biodiversity and geographic distribution of Onchocerca, 485 female black flies (2015: 150, 2016: 335) were collected using CO2-baited traps from February to October 2015–2016 in Lake County, northern California, USA. Individual flies were morphologically identified and pooled (≤ 10 individuals) by species, collection date, and trap location. Black fly pools were processed for DNA extraction, and subsequent PCR and sequencing targeting of the NADH dehydrogenase subunit 5 gene of filarioids. Results Among the pools of black flies, there were 158 individuals of Simulium tescorum (2015: 57, 2016: 101), 302 individuals of Simulium vittatum (sensu lato [s.l.]) (2015: 82, 2016: 220), 16 individuals of Simulium clarum “black” phenotype (2015: 5, 2016: 11), and 13 individuals of S. clarum “orange” phenotype (2015: 6, 2016: 7). PCR analysis revealed the percentage of filarioid-positive pools were 7.50% (n = 3) for S. tescorum, 3.75% (n = 3) for S. vittatum (s.l., likely S. tribulatum), 7.69% (n = 1) for S. clarum “black” phenotype, and no positives for S. clarum “orange” phenotype. Genetic distance and phylogenetic analyses suggest that the northern California Onchocerca isolates belong to the same species reported in black flies from southern California (average pairwise comparison: 0.32%), and seem closely related to Onchocerca isolates of white-tailed deer from upstate New York (average pairwise comparison: 2.31%). Conclusion A cryptic Onchocerca species was found in Lake County, California, and may be a part of a larger, continentally distributed species complex rather than a single described species of North America. In addition, there are at least three putative vectors of black flies (S. clarum, S. tescorum, S. vittatum) associated with this cryptic Onchocerca species. A comprehensive reassessment of North American Onchocerca biodiversity, host, and geographic range is necessary. Graphical abstract
first_indexed 2024-12-22T06:52:15Z
format Article
id doaj.art-4d76a563472b45a28e96e89a97b49f98
institution Directory Open Access Journal
issn 1756-3305
language English
last_indexed 2024-12-22T06:52:15Z
publishDate 2021-09-01
publisher BMC
record_format Article
series Parasites & Vectors
spelling doaj.art-4d76a563472b45a28e96e89a97b49f982022-12-21T18:35:06ZengBMCParasites & Vectors1756-33052021-09-0114111010.1186/s13071-021-04990-1Presence of a cryptic Onchocerca species in black flies of northern California, USAMatthew Kulpa0Kimberly J. Nelson1Alana M. Morales2Bonnie M. Ryan3Michelle L. Koschik4Jamesina J. Scott5Guilherme G. Verocai6Department of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M UniversitySan Gabriel Valley Mosquito and Vector Control DistrictDepartment of Infectious Diseases, College of Veterinary Medicine, University of GeorgiaLake County Vector Control DistrictLake County Vector Control DistrictLake County Vector Control DistrictDepartment of Veterinary Pathobiology, College of Veterinary Medicine and Biomedical Sciences, Texas A&M UniversityAbstract Background Black flies (Diptera: Simuliidae) serve as arthropod vectors for various species of Onchocerca (Nematoda: Onchocercidae) that may be associated with disease in humans, domestic animals, and wildlife. The emergence of zoonotic Onchocerca lupi in North America and reports of cervid-associated zoonotic onchocerciasis by Onchocerca jakutensis highlight the need for increased entomological surveillance. In addition, there is mounting evidence that Onchocerca diversity in North America is far greater than previously thought, currently regarded as Onchocerca cervipedis species complex. This study reports new geographic records and black fly vector associations of an uncharacterized Onchocerca species. Methods To better understand the biodiversity and geographic distribution of Onchocerca, 485 female black flies (2015: 150, 2016: 335) were collected using CO2-baited traps from February to October 2015–2016 in Lake County, northern California, USA. Individual flies were morphologically identified and pooled (≤ 10 individuals) by species, collection date, and trap location. Black fly pools were processed for DNA extraction, and subsequent PCR and sequencing targeting of the NADH dehydrogenase subunit 5 gene of filarioids. Results Among the pools of black flies, there were 158 individuals of Simulium tescorum (2015: 57, 2016: 101), 302 individuals of Simulium vittatum (sensu lato [s.l.]) (2015: 82, 2016: 220), 16 individuals of Simulium clarum “black” phenotype (2015: 5, 2016: 11), and 13 individuals of S. clarum “orange” phenotype (2015: 6, 2016: 7). PCR analysis revealed the percentage of filarioid-positive pools were 7.50% (n = 3) for S. tescorum, 3.75% (n = 3) for S. vittatum (s.l., likely S. tribulatum), 7.69% (n = 1) for S. clarum “black” phenotype, and no positives for S. clarum “orange” phenotype. Genetic distance and phylogenetic analyses suggest that the northern California Onchocerca isolates belong to the same species reported in black flies from southern California (average pairwise comparison: 0.32%), and seem closely related to Onchocerca isolates of white-tailed deer from upstate New York (average pairwise comparison: 2.31%). Conclusion A cryptic Onchocerca species was found in Lake County, California, and may be a part of a larger, continentally distributed species complex rather than a single described species of North America. In addition, there are at least three putative vectors of black flies (S. clarum, S. tescorum, S. vittatum) associated with this cryptic Onchocerca species. A comprehensive reassessment of North American Onchocerca biodiversity, host, and geographic range is necessary. Graphical abstracthttps://doi.org/10.1186/s13071-021-04990-1CervidaeFilarial parasitesFilarioideaOnchocerciasisParasite biodiversityVector-borne diseases
spellingShingle Matthew Kulpa
Kimberly J. Nelson
Alana M. Morales
Bonnie M. Ryan
Michelle L. Koschik
Jamesina J. Scott
Guilherme G. Verocai
Presence of a cryptic Onchocerca species in black flies of northern California, USA
Parasites & Vectors
Cervidae
Filarial parasites
Filarioidea
Onchocerciasis
Parasite biodiversity
Vector-borne diseases
title Presence of a cryptic Onchocerca species in black flies of northern California, USA
title_full Presence of a cryptic Onchocerca species in black flies of northern California, USA
title_fullStr Presence of a cryptic Onchocerca species in black flies of northern California, USA
title_full_unstemmed Presence of a cryptic Onchocerca species in black flies of northern California, USA
title_short Presence of a cryptic Onchocerca species in black flies of northern California, USA
title_sort presence of a cryptic onchocerca species in black flies of northern california usa
topic Cervidae
Filarial parasites
Filarioidea
Onchocerciasis
Parasite biodiversity
Vector-borne diseases
url https://doi.org/10.1186/s13071-021-04990-1
work_keys_str_mv AT matthewkulpa presenceofacrypticonchocercaspeciesinblackfliesofnortherncaliforniausa
AT kimberlyjnelson presenceofacrypticonchocercaspeciesinblackfliesofnortherncaliforniausa
AT alanammorales presenceofacrypticonchocercaspeciesinblackfliesofnortherncaliforniausa
AT bonniemryan presenceofacrypticonchocercaspeciesinblackfliesofnortherncaliforniausa
AT michellelkoschik presenceofacrypticonchocercaspeciesinblackfliesofnortherncaliforniausa
AT jamesinajscott presenceofacrypticonchocercaspeciesinblackfliesofnortherncaliforniausa
AT guilhermegverocai presenceofacrypticonchocercaspeciesinblackfliesofnortherncaliforniausa