High mitochondrial sequence divergence in synanthropic flea species (Insecta

Siphonaptera) from Europe and the Mediterranean

Sándor Hornok, Relja Beck, R. Farkas, Andrea Grima, Domenico Otranto, Jeno Kontschán, Nóra Takács, Gábor Horváth, Krisztina Szoke, Sándor Szekeres, Gábor Majoros, Alexandra Juhász, Harold Salant, Regina Hofmann-Lehmann, Michal Stanko, Gad Baneth

Research output: Contribution to journalArticle

1 Citation (Scopus)

Abstract

Background: Adult fleas are haematophagous ectoparasites of warm-blooded vertebrates, particularly mammals. Among them, the cat flea (Ctenocephalides felis) and the human flea (Pulex irritans) have high veterinary-medical significance, owing to their cosmopolitan distribution and role in the transmission of important vector-borne pathogens. While the taxonomy of Ct. felis has been investigated on a morphological basis during the past decades, its molecular-phylogenetic analyses have been only recently conducted. This study expands the knowledge on Ct. felis from hitherto less studied geographical regions, and includes representatives from additional flea families, less investigated with molecular approaches. Methods: Fleas were collected in four countries of the Mediterranean Basin (Croatia, Italy, Malta and Israel), as well as in Hungary, from domestic and wild carnivores, rodents and humans. The DNA extracts of representative fleas (n = 148), belonging to ten species of eight genera, were used for PCR amplification of part of their cytochrome c oxidase subunits 1, 2 (cox1, cox2) and 18S rRNA genes, followed by sequencing and phylogenetic analyses. Results: The majority (65.6%) of Ct. felis felis cox2 sequences showed 99.4-100% similarity to each other (haplogroup A), whereas those from Malta and Israel had 98.1-98.7% sequence similarity (haplogroup B), and a third sequence from Israel (haplotype C) had as low as 96.3% sequence similarity in comparison with a reference sequence from group "A". Except for the shape of the head, no consistent morphological differences (e.g. in chaetotaxy) were found between haplogroups "A" and "C". Haplotypes of Ct. canis were genetically more homogenous, with 99.6-100% sequence similarity to each other. However, when P. irritans collected from humans was compared to those from three species of wild carnivores, these only had 96.6% cox2 similarity. The mouse flea, Leptopsylla segnis and the northern rat flea, Nosopsyllus fasciatus were both shown to have haplotypes with low intraspecific cox2 similarities (96.2 and 94.4%, respectively). Taken together, differences between mitochondrial lineages within four flea species exceeded that observed between two Chaetopsylla spp. (which had 97.3% cox2 similarity). The topologies of cox1 and cox2 phylogenetic trees were in line with relevant sequence comparisons. Conversely, 18S rRNA gene analyses only resolved differences above the species level. Conclusions: Ctenocephalides felis felis, P. irritans, L. segnis and N. fasciatus were shown to have such a high level of mitochondrial gene heterogeneity, that the uniformity of these flea taxa should be reconsidered. Although the present results are limited (especially in the case of L. segnis and N. fasciatus), there appears to be no geographical or host restriction, which could explain the divergence of these genetic lineages.

Original languageEnglish
Article number221
JournalParasites and Vectors
Volume11
Issue number1
DOIs
Publication statusPublished - Apr 2 2018

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Siphonaptera
Ctenocephalides
Insects
Israel
Malta
Felis
Haplotypes
rRNA Genes
Croatia
Mitochondrial Genes
Hungary
Electron Transport Complex IV
Italy
Vertebrates
Mammals
Rodentia
Head
Polymerase Chain Reaction

ASJC Scopus subject areas

  • Parasitology
  • Infectious Diseases

Cite this

High mitochondrial sequence divergence in synanthropic flea species (Insecta : Siphonaptera) from Europe and the Mediterranean. / Hornok, Sándor; Beck, Relja; Farkas, R.; Grima, Andrea; Otranto, Domenico; Kontschán, Jeno; Takács, Nóra; Horváth, Gábor; Szoke, Krisztina; Szekeres, Sándor; Majoros, Gábor; Juhász, Alexandra; Salant, Harold; Hofmann-Lehmann, Regina; Stanko, Michal; Baneth, Gad.

In: Parasites and Vectors, Vol. 11, No. 1, 221, 02.04.2018.

Research output: Contribution to journalArticle

Hornok, S, Beck, R, Farkas, R, Grima, A, Otranto, D, Kontschán, J, Takács, N, Horváth, G, Szoke, K, Szekeres, S, Majoros, G, Juhász, A, Salant, H, Hofmann-Lehmann, R, Stanko, M & Baneth, G 2018, 'High mitochondrial sequence divergence in synanthropic flea species (Insecta: Siphonaptera) from Europe and the Mediterranean', Parasites and Vectors, vol. 11, no. 1, 221. https://doi.org/10.1186/s13071-018-2798-4
Hornok, Sándor ; Beck, Relja ; Farkas, R. ; Grima, Andrea ; Otranto, Domenico ; Kontschán, Jeno ; Takács, Nóra ; Horváth, Gábor ; Szoke, Krisztina ; Szekeres, Sándor ; Majoros, Gábor ; Juhász, Alexandra ; Salant, Harold ; Hofmann-Lehmann, Regina ; Stanko, Michal ; Baneth, Gad. / High mitochondrial sequence divergence in synanthropic flea species (Insecta : Siphonaptera) from Europe and the Mediterranean. In: Parasites and Vectors. 2018 ; Vol. 11, No. 1.
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abstract = "Background: Adult fleas are haematophagous ectoparasites of warm-blooded vertebrates, particularly mammals. Among them, the cat flea (Ctenocephalides felis) and the human flea (Pulex irritans) have high veterinary-medical significance, owing to their cosmopolitan distribution and role in the transmission of important vector-borne pathogens. While the taxonomy of Ct. felis has been investigated on a morphological basis during the past decades, its molecular-phylogenetic analyses have been only recently conducted. This study expands the knowledge on Ct. felis from hitherto less studied geographical regions, and includes representatives from additional flea families, less investigated with molecular approaches. Methods: Fleas were collected in four countries of the Mediterranean Basin (Croatia, Italy, Malta and Israel), as well as in Hungary, from domestic and wild carnivores, rodents and humans. The DNA extracts of representative fleas (n = 148), belonging to ten species of eight genera, were used for PCR amplification of part of their cytochrome c oxidase subunits 1, 2 (cox1, cox2) and 18S rRNA genes, followed by sequencing and phylogenetic analyses. Results: The majority (65.6{\%}) of Ct. felis felis cox2 sequences showed 99.4-100{\%} similarity to each other (haplogroup A), whereas those from Malta and Israel had 98.1-98.7{\%} sequence similarity (haplogroup B), and a third sequence from Israel (haplotype C) had as low as 96.3{\%} sequence similarity in comparison with a reference sequence from group {"}A{"}. Except for the shape of the head, no consistent morphological differences (e.g. in chaetotaxy) were found between haplogroups {"}A{"} and {"}C{"}. Haplotypes of Ct. canis were genetically more homogenous, with 99.6-100{\%} sequence similarity to each other. However, when P. irritans collected from humans was compared to those from three species of wild carnivores, these only had 96.6{\%} cox2 similarity. The mouse flea, Leptopsylla segnis and the northern rat flea, Nosopsyllus fasciatus were both shown to have haplotypes with low intraspecific cox2 similarities (96.2 and 94.4{\%}, respectively). Taken together, differences between mitochondrial lineages within four flea species exceeded that observed between two Chaetopsylla spp. (which had 97.3{\%} cox2 similarity). The topologies of cox1 and cox2 phylogenetic trees were in line with relevant sequence comparisons. Conversely, 18S rRNA gene analyses only resolved differences above the species level. Conclusions: Ctenocephalides felis felis, P. irritans, L. segnis and N. fasciatus were shown to have such a high level of mitochondrial gene heterogeneity, that the uniformity of these flea taxa should be reconsidered. Although the present results are limited (especially in the case of L. segnis and N. fasciatus), there appears to be no geographical or host restriction, which could explain the divergence of these genetic lineages.",
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TY - JOUR

T1 - High mitochondrial sequence divergence in synanthropic flea species (Insecta

T2 - Siphonaptera) from Europe and the Mediterranean

AU - Hornok, Sándor

AU - Beck, Relja

AU - Farkas, R.

AU - Grima, Andrea

AU - Otranto, Domenico

AU - Kontschán, Jeno

AU - Takács, Nóra

AU - Horváth, Gábor

AU - Szoke, Krisztina

AU - Szekeres, Sándor

AU - Majoros, Gábor

AU - Juhász, Alexandra

AU - Salant, Harold

AU - Hofmann-Lehmann, Regina

AU - Stanko, Michal

AU - Baneth, Gad

PY - 2018/4/2

Y1 - 2018/4/2

N2 - Background: Adult fleas are haematophagous ectoparasites of warm-blooded vertebrates, particularly mammals. Among them, the cat flea (Ctenocephalides felis) and the human flea (Pulex irritans) have high veterinary-medical significance, owing to their cosmopolitan distribution and role in the transmission of important vector-borne pathogens. While the taxonomy of Ct. felis has been investigated on a morphological basis during the past decades, its molecular-phylogenetic analyses have been only recently conducted. This study expands the knowledge on Ct. felis from hitherto less studied geographical regions, and includes representatives from additional flea families, less investigated with molecular approaches. Methods: Fleas were collected in four countries of the Mediterranean Basin (Croatia, Italy, Malta and Israel), as well as in Hungary, from domestic and wild carnivores, rodents and humans. The DNA extracts of representative fleas (n = 148), belonging to ten species of eight genera, were used for PCR amplification of part of their cytochrome c oxidase subunits 1, 2 (cox1, cox2) and 18S rRNA genes, followed by sequencing and phylogenetic analyses. Results: The majority (65.6%) of Ct. felis felis cox2 sequences showed 99.4-100% similarity to each other (haplogroup A), whereas those from Malta and Israel had 98.1-98.7% sequence similarity (haplogroup B), and a third sequence from Israel (haplotype C) had as low as 96.3% sequence similarity in comparison with a reference sequence from group "A". Except for the shape of the head, no consistent morphological differences (e.g. in chaetotaxy) were found between haplogroups "A" and "C". Haplotypes of Ct. canis were genetically more homogenous, with 99.6-100% sequence similarity to each other. However, when P. irritans collected from humans was compared to those from three species of wild carnivores, these only had 96.6% cox2 similarity. The mouse flea, Leptopsylla segnis and the northern rat flea, Nosopsyllus fasciatus were both shown to have haplotypes with low intraspecific cox2 similarities (96.2 and 94.4%, respectively). Taken together, differences between mitochondrial lineages within four flea species exceeded that observed between two Chaetopsylla spp. (which had 97.3% cox2 similarity). The topologies of cox1 and cox2 phylogenetic trees were in line with relevant sequence comparisons. Conversely, 18S rRNA gene analyses only resolved differences above the species level. Conclusions: Ctenocephalides felis felis, P. irritans, L. segnis and N. fasciatus were shown to have such a high level of mitochondrial gene heterogeneity, that the uniformity of these flea taxa should be reconsidered. Although the present results are limited (especially in the case of L. segnis and N. fasciatus), there appears to be no geographical or host restriction, which could explain the divergence of these genetic lineages.

AB - Background: Adult fleas are haematophagous ectoparasites of warm-blooded vertebrates, particularly mammals. Among them, the cat flea (Ctenocephalides felis) and the human flea (Pulex irritans) have high veterinary-medical significance, owing to their cosmopolitan distribution and role in the transmission of important vector-borne pathogens. While the taxonomy of Ct. felis has been investigated on a morphological basis during the past decades, its molecular-phylogenetic analyses have been only recently conducted. This study expands the knowledge on Ct. felis from hitherto less studied geographical regions, and includes representatives from additional flea families, less investigated with molecular approaches. Methods: Fleas were collected in four countries of the Mediterranean Basin (Croatia, Italy, Malta and Israel), as well as in Hungary, from domestic and wild carnivores, rodents and humans. The DNA extracts of representative fleas (n = 148), belonging to ten species of eight genera, were used for PCR amplification of part of their cytochrome c oxidase subunits 1, 2 (cox1, cox2) and 18S rRNA genes, followed by sequencing and phylogenetic analyses. Results: The majority (65.6%) of Ct. felis felis cox2 sequences showed 99.4-100% similarity to each other (haplogroup A), whereas those from Malta and Israel had 98.1-98.7% sequence similarity (haplogroup B), and a third sequence from Israel (haplotype C) had as low as 96.3% sequence similarity in comparison with a reference sequence from group "A". Except for the shape of the head, no consistent morphological differences (e.g. in chaetotaxy) were found between haplogroups "A" and "C". Haplotypes of Ct. canis were genetically more homogenous, with 99.6-100% sequence similarity to each other. However, when P. irritans collected from humans was compared to those from three species of wild carnivores, these only had 96.6% cox2 similarity. The mouse flea, Leptopsylla segnis and the northern rat flea, Nosopsyllus fasciatus were both shown to have haplotypes with low intraspecific cox2 similarities (96.2 and 94.4%, respectively). Taken together, differences between mitochondrial lineages within four flea species exceeded that observed between two Chaetopsylla spp. (which had 97.3% cox2 similarity). The topologies of cox1 and cox2 phylogenetic trees were in line with relevant sequence comparisons. Conversely, 18S rRNA gene analyses only resolved differences above the species level. Conclusions: Ctenocephalides felis felis, P. irritans, L. segnis and N. fasciatus were shown to have such a high level of mitochondrial gene heterogeneity, that the uniformity of these flea taxa should be reconsidered. Although the present results are limited (especially in the case of L. segnis and N. fasciatus), there appears to be no geographical or host restriction, which could explain the divergence of these genetic lineages.

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