Skip to main content
Erschienen in: Biodiversity and Conservation 13/2020

26.08.2020 | Original Paper

Endangered monoxenous trypanosomatid parasites: a lesson from island biogeography

verfasst von: Jan Votýpka, Petr Kment, Vyacheslav Yurchenko, Julius Lukeš

Erschienen in: Biodiversity and Conservation | Ausgabe 13/2020

Einloggen

Aktivieren Sie unsere intelligente Suche, um passende Fachinhalte oder Patente zu finden.

search-config
loading …

Abstract

Most remote and oceanic islands are important, yet highly vulnerable biodiversity hotspots, which host a significant proportion of endemic species. Along with iconic endangered or extinct animals and plants, the disappearance of their co-inhabitants, including protist parasites, gets usually unnoticed from the conservation perspective. Here, we examined insects from Madagascar, Reunion, and Mauritius for the presence of trypanosomatid parasites (Kinetoplastea). Out of 660 specimens of the true bugs (Heteroptera) belonging to 87 species and 18 families, 95 individuals of 30 species were found to be infected (14% prevalence) by at least one trypanosomatid species, here referred to as typing units (TUs). Out of 141 flies (Diptera), 19 (13%) were infected. High diversity of the host species correlated with a high diversity of detected TUs belonging to 11 trypanosomatid genera, and representatives of 7 genera (Angomonas, Blastocrithidia, Herpetomonas, ‘jaculum’, Leptomonas, Wallacemonas, and Zelonia) yielded axenic cultures. Of 39 detected TUs, more than half have not been encountered in other geographical regions and appear to be endemic. Altogether, 27 TUs, including 15 newly detected ones, were found exclusively in bugs, while flies hosted 11 TUs, out of which five were found exclusively on the studied islands. Only a single species, Leptomonas moramango, was found in both insect groups. Several new isolates have significantly extended the diversity of the plant-pathogenic Phytomonas. Geographically widespread as well as endemic TUs were detected in both widely distributed and (sub)endemic insects. The high proportion of endemic TUs suggests that the prominent role of islands in the global diversity of macroscopic organisms likely extends also to their protistan parasites and that the protection of macro-organisms in biodiversity hot spots can also protect the vast, yet mainly invisible, diversity of their parasitic companions.

Sie haben noch keine Lizenz? Dann Informieren Sie sich jetzt über unsere Produkte:

Springer Professional "Wirtschaft+Technik"

Online-Abonnement

Mit Springer Professional "Wirtschaft+Technik" erhalten Sie Zugriff auf:

  • über 102.000 Bücher
  • über 537 Zeitschriften

aus folgenden Fachgebieten:

  • Automobil + Motoren
  • Bauwesen + Immobilien
  • Business IT + Informatik
  • Elektrotechnik + Elektronik
  • Energie + Nachhaltigkeit
  • Finance + Banking
  • Management + Führung
  • Marketing + Vertrieb
  • Maschinenbau + Werkstoffe
  • Versicherung + Risiko

Jetzt Wissensvorsprung sichern!

Springer Professional "Technik"

Online-Abonnement

Mit Springer Professional "Technik" erhalten Sie Zugriff auf:

  • über 67.000 Bücher
  • über 390 Zeitschriften

aus folgenden Fachgebieten:

  • Automobil + Motoren
  • Bauwesen + Immobilien
  • Business IT + Informatik
  • Elektrotechnik + Elektronik
  • Energie + Nachhaltigkeit
  • Maschinenbau + Werkstoffe




 

Jetzt Wissensvorsprung sichern!

Anhänge
Nur mit Berechtigung zugänglich
Literatur
Zurück zum Zitat Barratt J, Ellis J, Stark D, Barratt J (2017a) The evolution of trypanosomatid taxonomy. Parasit Vector 10:287 Barratt J, Ellis J, Stark D, Barratt J (2017a) The evolution of trypanosomatid taxonomy. Parasit Vector 10:287
Zurück zum Zitat Barratt J, Kaufer A, Peters B, Craig D, Lawrence A, Roberts T, Lee R, McAuliffe G, Stark D, Ellis J (2017b) Isolation of novel trypanosomatid, Zelonia australiensis sp. nov (Kinetoplastida: Trypanosomatidae) provides support for a Gondwanan origin of dixenous parasitism in the Leishmaniinae. PLoS Negl Trop Dis 11:e0005215PubMedPubMedCentral Barratt J, Kaufer A, Peters B, Craig D, Lawrence A, Roberts T, Lee R, McAuliffe G, Stark D, Ellis J (2017b) Isolation of novel trypanosomatid, Zelonia australiensis sp. nov (Kinetoplastida: Trypanosomatidae) provides support for a Gondwanan origin of dixenous parasitism in the Leishmaniinae. PLoS Negl Trop Dis 11:e0005215PubMedPubMedCentral
Zurück zum Zitat Bianchi C, Kostygov AY, Kraeva N, Záhonová K, Horáková E, Sobotka R, Lukeš J, Yurchenko V (2019) An enigmatic catalase of Blastocrithidia. Mol Biochem Parasitol 232:111199PubMed Bianchi C, Kostygov AY, Kraeva N, Záhonová K, Horáková E, Sobotka R, Lukeš J, Yurchenko V (2019) An enigmatic catalase of Blastocrithidia. Mol Biochem Parasitol 232:111199PubMed
Zurück zum Zitat Borghesan TC, Ferreira RC, Takata CSA, Campaner M, Borda CC, Paiva F, Milder RV, Teixeira MMG, Camargo EP (2013) Molecular phylogenetic redefinition of Herpetomonas (Kinetoplastea, Trypanosomatidae), a genus of insect parasites associated with flies. Protist 164:129–152PubMed Borghesan TC, Ferreira RC, Takata CSA, Campaner M, Borda CC, Paiva F, Milder RV, Teixeira MMG, Camargo EP (2013) Molecular phylogenetic redefinition of Herpetomonas (Kinetoplastea, Trypanosomatidae), a genus of insect parasites associated with flies. Protist 164:129–152PubMed
Zurück zum Zitat Buckley TR, Palma RL, Johns PM, Gleeson DM, Heath ACG, Hitchmough RA, Stringer IAN (2012) The conservation status of small or less well known groups of New Zealand terrestrial invertebrates. NZ Entomol 35:137–143 Buckley TR, Palma RL, Johns PM, Gleeson DM, Heath ACG, Hitchmough RA, Stringer IAN (2012) The conservation status of small or less well known groups of New Zealand terrestrial invertebrates. NZ Entomol 35:137–143
Zurück zum Zitat Camargo EP, Kastelein P, Roitman I (1990) Trypanosomatid parasites of plants (Phytomonas). Parasitol Today 6:22–25PubMed Camargo EP, Kastelein P, Roitman I (1990) Trypanosomatid parasites of plants (Phytomonas). Parasitol Today 6:22–25PubMed
Zurück zum Zitat Chandler JA, James PM (2013) Discovery of trypanosomatid parasites in globally distributed Drosophila species. PLoS ONE 8:e61937PubMedPubMedCentral Chandler JA, James PM (2013) Discovery of trypanosomatid parasites in globally distributed Drosophila species. PLoS ONE 8:e61937PubMedPubMedCentral
Zurück zum Zitat d'Avila-Levy C, Boucinha C, Kostygov A, Santos HLC, Morelli KA, Grybchuk-Ieremenko A, Duval L, Votýpka J, Yurchenko V, Grellier P, Lukeš J (2015) Exploring environmental diversity of kinetoplastid flagellates in the high-throughput DNA sequencing era (Review). Mem Inst Oswaldo Cruz 110:956–965PubMedPubMedCentral d'Avila-Levy C, Boucinha C, Kostygov A, Santos HLC, Morelli KA, Grybchuk-Ieremenko A, Duval L, Votýpka J, Yurchenko V, Grellier P, Lukeš J (2015) Exploring environmental diversity of kinetoplastid flagellates in the high-throughput DNA sequencing era (Review). Mem Inst Oswaldo Cruz 110:956–965PubMedPubMedCentral
Zurück zum Zitat Dheilly NM, Martínez-Martínez J, Rosario K, Brindley PJ, Fichorova RN, Kaye JZ, Kohl K, Knoll LJ, Lukeš J, Perkins SL, Poulin R, Schriml L, Thompson LR (2019) Parasite microbiome project: grand challenges. PLoS Pathog 15:e1008028PubMedPubMedCentral Dheilly NM, Martínez-Martínez J, Rosario K, Brindley PJ, Fichorova RN, Kaye JZ, Kohl K, Knoll LJ, Lukeš J, Perkins SL, Poulin R, Schriml L, Thompson LR (2019) Parasite microbiome project: grand challenges. PLoS Pathog 15:e1008028PubMedPubMedCentral
Zurück zum Zitat Dobson A, Lafferty KD, Kuris AM, Hechinger RF, Jetz W (2008) Homage to Linnaeus: how many parasites? How many hosts? Proc Natl Acad Sci USA 105:11482–11489PubMed Dobson A, Lafferty KD, Kuris AM, Hechinger RF, Jetz W (2008) Homage to Linnaeus: how many parasites? How many hosts? Proc Natl Acad Sci USA 105:11482–11489PubMed
Zurück zum Zitat Dougherty ER, Carlson CJ, Bueno VM, Burgio KR, Cizauskas CA, Clements CF, Seidel DP, Harris NC (2015) Paradigms for parasite conservation. Conserv Biol 30:724–733PubMed Dougherty ER, Carlson CJ, Bueno VM, Burgio KR, Cizauskas CA, Clements CF, Seidel DP, Harris NC (2015) Paradigms for parasite conservation. Conserv Biol 30:724–733PubMed
Zurück zum Zitat Emerson BC (2002) Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process. Mol Ecol 11:951–966PubMed Emerson BC (2002) Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process. Mol Ecol 11:951–966PubMed
Zurück zum Zitat Espinosa OA, Camargo EP, Teixeira MMG, Shaw JJ (2018) An appraisal of the taxonomy and nomenclature of trypanosomatids presently classified as Leishmania and Endotrypanum. Parasitology 145:430–442PubMed Espinosa OA, Camargo EP, Teixeira MMG, Shaw JJ (2018) An appraisal of the taxonomy and nomenclature of trypanosomatids presently classified as Leishmania and Endotrypanum. Parasitology 145:430–442PubMed
Zurück zum Zitat França C (1920) La flagellose des euphorbes II. Ann l'Inst Pasteur, Paris 34:432–465 França C (1920) La flagellose des euphorbes II. Ann l'Inst Pasteur, Paris 34:432–465
Zurück zum Zitat Forthman M, Chłond D, Weirauch C (2016) Taxonomic monograph of the endemic millipede assassin bug fauna of Madagascar (Hemiptera: Reduviidae: Ectrichodiinae). Bull Am Mus Nat Hist 400:1–152 Forthman M, Chłond D, Weirauch C (2016) Taxonomic monograph of the endemic millipede assassin bug fauna of Madagascar (Hemiptera: Reduviidae: Ectrichodiinae). Bull Am Mus Nat Hist 400:1–152
Zurück zum Zitat Frolov AO, Malysheva MN, Yurchenko V, Kostygov AY (2016) Back to monoxeny: Phytomonas nordicus descended from dixe-nous plant parasites. Europ J Protistol 52:1–10 Frolov AO, Malysheva MN, Yurchenko V, Kostygov AY (2016) Back to monoxeny: Phytomonas nordicus descended from dixe-nous plant parasites. Europ J Protistol 52:1–10
Zurück zum Zitat Frolov AO, Malysheva MN, Ganyukova AI, Spodareva VV, Yurchenko V, Kostygov AY (2019) Development of Phytomonas lipae sp. n. (Kinetoplastea: Trypanosomatidae) in the true bug Coreus marginatus (Heteroptera: Coreidae) and insights into the evolution of life cycles in the genus Phytomonas. PLoS ONE 14:e0214484PubMedPubMedCentral Frolov AO, Malysheva MN, Ganyukova AI, Spodareva VV, Yurchenko V, Kostygov AY (2019) Development of Phytomonas lipae sp. n. (Kinetoplastea: Trypanosomatidae) in the true bug Coreus marginatus (Heteroptera: Coreidae) and insights into the evolution of life cycles in the genus Phytomonas. PLoS ONE 14:e0214484PubMedPubMedCentral
Zurück zum Zitat Frolov AO, Malysheva MN, Ganyukova AI, Spodareva VV, Králová J, Yurchenko V, Kostygov AY (2020) If host is refractory, insistent parasite goes berserk: trypanosomatid Blastocrithidia raabei in the true bug Coreus marginatus. PLoS ONE 15:e0227832PubMedPubMedCentral Frolov AO, Malysheva MN, Ganyukova AI, Spodareva VV, Králová J, Yurchenko V, Kostygov AY (2020) If host is refractory, insistent parasite goes berserk: trypanosomatid Blastocrithidia raabei in the true bug Coreus marginatus. PLoS ONE 15:e0227832PubMedPubMedCentral
Zurück zum Zitat Gómez A, Nichols E (2013) Neglected wild life: parasitic biodiversity as a conservation target. Int J Parasitol Parasites Wildl 2:222–227PubMedPubMedCentral Gómez A, Nichols E (2013) Neglected wild life: parasitic biodiversity as a conservation target. Int J Parasitol Parasites Wildl 2:222–227PubMedPubMedCentral
Zurück zum Zitat Grybchuk D, Akopyants NS, Kostygov AY, Konovalovas A, Lye L-F, Dobson DE, Zangger H, Fasel N, Butenko A, Frolov AO, Votýpka J, Avila-Levy CM, Kulich P, Moravcová J, Plevka P, Rogozin IB, Serva S, Lukeš J, Beverley SM, Yurchenko V (2018) Viral discovery and diversity in trypanosomatid protozoa with a focus on relatives of the human parasite Leishmania. Proc Natl Acad Sci USA 115:E506–E515PubMed Grybchuk D, Akopyants NS, Kostygov AY, Konovalovas A, Lye L-F, Dobson DE, Zangger H, Fasel N, Butenko A, Frolov AO, Votýpka J, Avila-Levy CM, Kulich P, Moravcová J, Plevka P, Rogozin IB, Serva S, Lukeš J, Beverley SM, Yurchenko V (2018) Viral discovery and diversity in trypanosomatid protozoa with a focus on relatives of the human parasite Leishmania. Proc Natl Acad Sci USA 115:E506–E515PubMed
Zurück zum Zitat Grybchuk-Ieremenko A, Losev A, Kostygov A, Lukeš J, Yurchenko V (2014) High prevalence of trypanosome co-infections in freshwater fishes. Folia Parasitol 61:495–504 Grybchuk-Ieremenko A, Losev A, Kostygov A, Lukeš J, Yurchenko V (2014) High prevalence of trypanosome co-infections in freshwater fishes. Folia Parasitol 61:495–504
Zurück zum Zitat Guilbert E (2020) New species of Tingidae (Insecta: Heteroptera) from Madagascar. Zootaxa 4759(3):391–404 Guilbert E (2020) New species of Tingidae (Insecta: Heteroptera) from Madagascar. Zootaxa 4759(3):391–404
Zurück zum Zitat Ishemgulova A, Butenko A, Kortišová L, Boucinha C, Grybchuk-Ieremenko A, Morelli KA, Tesařová M, Kraeva N, Grybchuk D, Pánek T, Flegontov P, Lukeš J, Votýpka J, Pavan MG, Opperdoes FR, Spodareva V, d'Avila-Levy CM, Kostygov AY, Yurchenko V (2017) Molecular mechanisms of thermal resistance of the insect trypanosomatid Crithidia thermophila. PLoS ONE 12:e0174165PubMedPubMedCentral Ishemgulova A, Butenko A, Kortišová L, Boucinha C, Grybchuk-Ieremenko A, Morelli KA, Tesařová M, Kraeva N, Grybchuk D, Pánek T, Flegontov P, Lukeš J, Votýpka J, Pavan MG, Opperdoes FR, Spodareva V, d'Avila-Levy CM, Kostygov AY, Yurchenko V (2017) Molecular mechanisms of thermal resistance of the insect trypanosomatid Crithidia thermophila. PLoS ONE 12:e0174165PubMedPubMedCentral
Zurück zum Zitat Jaskowska E, Butler C, Preston G, Kelly S (2015) Phytomonas: trypanosomatids adapted to plant environments. PLOS Pathog 11:e1004484PubMedPubMedCentral Jaskowska E, Butler C, Preston G, Kelly S (2015) Phytomonas: trypanosomatids adapted to plant environments. PLOS Pathog 11:e1004484PubMedPubMedCentral
Zurück zum Zitat Jirků M, Yurchenko VY, Lukeš J, Maslov DA (2012) New species of insect trypanosomatids from Costa Rica and the proposal for a new subfamily within the Trypanosomatidae. J Eukaryot Microbiol 59:537–547PubMed Jirků M, Yurchenko VY, Lukeš J, Maslov DA (2012) New species of insect trypanosomatids from Costa Rica and the proposal for a new subfamily within the Trypanosomatidae. J Eukaryot Microbiol 59:537–547PubMed
Zurück zum Zitat Kikuchi Y, Hosokawa T, Fukatsu T (2011) An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME J 5:446–460PubMed Kikuchi Y, Hosokawa T, Fukatsu T (2011) An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME J 5:446–460PubMed
Zurück zum Zitat Kment P (2013) Carduelicoris stehliki, a new genus and species of Pentatomidae (Hemiptera: Heteroptera) from Madagascar Acta Mus Moraviae. Sci Biol 98:415–432 Kment P (2013) Carduelicoris stehliki, a new genus and species of Pentatomidae (Hemiptera: Heteroptera) from Madagascar Acta Mus Moraviae. Sci Biol 98:415–432
Zurück zum Zitat Kment P, Hemala V, Baňař P (2016) Rhyparoclava pyrrhocoroides, a new genus and species of autapomorphic Rhyparochromidae with clavate antennae from Madagascar (Hemiptera: Heteroptera). Acta Entomol Mus Nat Pragae 56:517–545 Kment P, Hemala V, Baňař P (2016) Rhyparoclava pyrrhocoroides, a new genus and species of autapomorphic Rhyparochromidae with clavate antennae from Madagascar (Hemiptera: Heteroptera). Acta Entomol Mus Nat Pragae 56:517–545
Zurück zum Zitat Kostygov A, Dobáková E, Grybchuk-Ieremenko A, Váhala D, Maslov DA, Votýpka J, Lukeš J, Yurchenko V (2016) Novel trypanosomatid-bacterium association: evolution of endosymbiosis in action. mBio 7:e01985–e2015PubMedPubMedCentral Kostygov A, Dobáková E, Grybchuk-Ieremenko A, Váhala D, Maslov DA, Votýpka J, Lukeš J, Yurchenko V (2016) Novel trypanosomatid-bacterium association: evolution of endosymbiosis in action. mBio 7:e01985–e2015PubMedPubMedCentral
Zurück zum Zitat Kostygov A, Grybchuk-Ieremenko A, Malysheva M, Frolov A, Yurchenko V (2014) Molecular revision of the genus Wallaceina. Protist 165:594–604PubMed Kostygov A, Grybchuk-Ieremenko A, Malysheva M, Frolov A, Yurchenko V (2014) Molecular revision of the genus Wallaceina. Protist 165:594–604PubMed
Zurück zum Zitat Kostygov A, Yurchenko V (2017) Revised classification of the subfamily Leishmaniinae (Trypanosomatidae). Folia Parasitol 64:020 Kostygov A, Yurchenko V (2017) Revised classification of the subfamily Leishmaniinae (Trypanosomatidae). Folia Parasitol 64:020
Zurück zum Zitat Kozminsky E, Kraeva N, Ishemgulova A, Dobakova E, Lukeš J, Kment P, Yurchenko V, Votypka J, Maslov DA (2015) Host-specificity of monoxenous typanosomatids: statistical analysis of the distribution and transmission patterns of the parasites from Neotropical Heteroptera. Protist 166:551–568PubMed Kozminsky E, Kraeva N, Ishemgulova A, Dobakova E, Lukeš J, Kment P, Yurchenko V, Votypka J, Maslov DA (2015) Host-specificity of monoxenous typanosomatids: statistical analysis of the distribution and transmission patterns of the parasites from Neotropical Heteroptera. Protist 166:551–568PubMed
Zurück zum Zitat Králová J, Grybchuk-Ieremenko A, Votýpka J, Novotný V, Kment P, Lukeš J, Yurchenko V, Kostygov AY (2019) Insect trypanosomatids in Papua New Guinea: high endemism and diversity. Int J Parasitol 49:1075–1086PubMed Králová J, Grybchuk-Ieremenko A, Votýpka J, Novotný V, Kment P, Lukeš J, Yurchenko V, Kostygov AY (2019) Insect trypanosomatids in Papua New Guinea: high endemism and diversity. Int J Parasitol 49:1075–1086PubMed
Zurück zum Zitat Lafont A (1909) Sur la présence d’un parasite de la classe des flagellés dans le latex de l’Euphorbia pilulifera. CR Séances Soc Biol Ses Fil 66:1011–1013 Lafont A (1909) Sur la présence d’un parasite de la classe des flagellés dans le latex de l’Euphorbia pilulifera. CR Séances Soc Biol Ses Fil 66:1011–1013
Zurück zum Zitat Lafont A (1910) Sur la présence d’un Leptomonas, parasite de la classe des Flagellés, dans le latex de trois Euphorbiacées. Ann l'Inst Pasteur Paris 24:205–219 Lafont A (1910) Sur la présence d’un Leptomonas, parasite de la classe des Flagellés, dans le latex de trois Euphorbiacées. Ann l'Inst Pasteur Paris 24:205–219
Zurück zum Zitat Lafont A (1911) Sur la transmission du Leptomonas davidi des euphorbes par un hémiptère, Nysius euphorbiae. CR S Soc Biol Ses Fil 70:58–59 Lafont A (1911) Sur la transmission du Leptomonas davidi des euphorbes par un hémiptère, Nysius euphorbiae. CR S Soc Biol Ses Fil 70:58–59
Zurück zum Zitat Legros V, Gasnier S, Rochat J (2016) First general inventory of the terrestrial Heteroptera fauna and its specificity on the oceanic island of Reunion. Ann Soc Entomol Fr (N.S.) 52:311–342 Legros V, Gasnier S, Rochat J (2016) First general inventory of the terrestrial Heteroptera fauna and its specificity on the oceanic island of Reunion. Ann Soc Entomol Fr (N.S.) 52:311–342
Zurück zum Zitat Lipa JJ (1966) Blastocrithidia raabei sp. n., a flagellate parasite of Mesocerus marginatus L. (Hemiptera: Coreidae). Acta Protozool 4:19–23 Lipa JJ (1966) Blastocrithidia raabei sp. n., a flagellate parasite of Mesocerus marginatus L. (Hemiptera: Coreidae). Acta Protozool 4:19–23
Zurück zum Zitat Lukeš J, Votýpka J (2020) Field isolation and cultivation of trypanosomatids from insects. In: Michels P, Ginger M, Zilberstein D (eds) Trypanosomatids methods in molecular biology. Humana, New York, pp 3–21 Lukeš J, Votýpka J (2020) Field isolation and cultivation of trypanosomatids from insects. In: Michels P, Ginger M, Zilberstein D (eds) Trypanosomatids methods in molecular biology. Humana, New York, pp 3–21
Zurück zum Zitat Lukeš J, Butenko A, Hashimi H, Maslov DA, Votýpka J, Yurchenko V (2018) Trypanosomatids are much more than just trypanosomes: clues from the expanded family tree. Trends Parasitol 34:466–480PubMed Lukeš J, Butenko A, Hashimi H, Maslov DA, Votýpka J, Yurchenko V (2018) Trypanosomatids are much more than just trypanosomes: clues from the expanded family tree. Trends Parasitol 34:466–480PubMed
Zurück zum Zitat Lukeš J, Skalický T, Týč J, Votýpka J, Yurchenko V (2014) Evolution of parasitism in kinetoplastid flagellates. Mol Biochem Parasit 195:115–122 Lukeš J, Skalický T, Týč J, Votýpka J, Yurchenko V (2014) Evolution of parasitism in kinetoplastid flagellates. Mol Biochem Parasit 195:115–122
Zurück zum Zitat MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton, p 203 MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton, p 203
Zurück zum Zitat Maslov DA, Lukeš J, Jirků M, Simpson L (1996) Phylogeny of trypanosomes as inferred from the small and large subunit rRNAs: Implications for the evolution of parasitism in the trypanosomatid protozoa. Mol Biochem Parasitol 75:197–205PubMed Maslov DA, Lukeš J, Jirků M, Simpson L (1996) Phylogeny of trypanosomes as inferred from the small and large subunit rRNAs: Implications for the evolution of parasitism in the trypanosomatid protozoa. Mol Biochem Parasitol 75:197–205PubMed
Zurück zum Zitat Maslov DA, Westenberger SJ, Xu X, Campbell DA, Sturm NR (2007) Discovery and barcoding by analysis of spliced leader RNA gene sequences of new isolates of Trypanosomatidae from Heteroptera in Costa Rica and Ecuador. J Eukaryot Microbiol 54:57–65PubMed Maslov DA, Westenberger SJ, Xu X, Campbell DA, Sturm NR (2007) Discovery and barcoding by analysis of spliced leader RNA gene sequences of new isolates of Trypanosomatidae from Heteroptera in Costa Rica and Ecuador. J Eukaryot Microbiol 54:57–65PubMed
Zurück zum Zitat Maslov DA, Votýpka J, Yurchenko V, Lukeš J (2013) Diversity and phylogeny of insect trypanosomatids: all that is hidden shall be revealed. Trends Parasitol 29:43–52PubMed Maslov DA, Votýpka J, Yurchenko V, Lukeš J (2013) Diversity and phylogeny of insect trypanosomatids: all that is hidden shall be revealed. Trends Parasitol 29:43–52PubMed
Zurück zum Zitat Maslov DA, Opperdoes FR, Kostygov AY, Hashimi H, Lukeš J, Yurchenko V (2019) Recent advances in trypanosomatid research: genome organization, expression, metabolism, taxonomy and evolution. Parasitol 146:1–27 Maslov DA, Opperdoes FR, Kostygov AY, Hashimi H, Lukeš J, Yurchenko V (2019) Recent advances in trypanosomatid research: genome organization, expression, metabolism, taxonomy and evolution. Parasitol 146:1–27
Zurück zum Zitat Miyamoto S (1961) Comparative morphology of alimentary organs of Heteroptera, with phylogenetic consideration. Sieboldia 2:197–259 Miyamoto S (1961) Comparative morphology of alimentary organs of Heteroptera, with phylogenetic consideration. Sieboldia 2:197–259
Zurück zum Zitat Mihalca AD, Gherman CM, Cozma V (2011) Coendangered hard-ticks: threatened or threatening? Parasit Vector 4:71 Mihalca AD, Gherman CM, Cozma V (2011) Coendangered hard-ticks: threatened or threatening? Parasit Vector 4:71
Zurück zum Zitat Novotný V, Drozd P, Miller SE, Kulfan M, Janda M, Basset Y, Weiblen GD (2006) Why are there so many species of herbivorous insects in tropical rainforests? Science 313:1115–1118PubMed Novotný V, Drozd P, Miller SE, Kulfan M, Janda M, Basset Y, Weiblen GD (2006) Why are there so many species of herbivorous insects in tropical rainforests? Science 313:1115–1118PubMed
Zurück zum Zitat Ohbayashi T, Takeshita K, Kitagawa W, Nikoh N, Koga R, Meng XY, Tago K, Hori T, Hayatsu M, Asano K, Kamagata Y, Lee BL, Fukatsu T, Kikuchi Z (2015) Insect’s intestinal organ for symbiont sorting. Proc Natl Acad Sci USA 112:E5179–E5188PubMed Ohbayashi T, Takeshita K, Kitagawa W, Nikoh N, Koga R, Meng XY, Tago K, Hori T, Hayatsu M, Asano K, Kamagata Y, Lee BL, Fukatsu T, Kikuchi Z (2015) Insect’s intestinal organ for symbiont sorting. Proc Natl Acad Sci USA 112:E5179–E5188PubMed
Zurück zum Zitat Okamura B, Hartigan A, Naldoni J (2018) Extensive uncharted biodiversity: the parasite dimension. Integr Comp Biol 58:1132–1145PubMed Okamura B, Hartigan A, Naldoni J (2018) Extensive uncharted biodiversity: the parasite dimension. Integr Comp Biol 58:1132–1145PubMed
Zurück zum Zitat Pawlowski J, Audic S, Adl S, Bass D, Belbahri L, Berney C, Bowser SS, Čepička I, Decelle J, Dunthorn M, Fiore-Donno AM, Gile GH, Holzmann M, Jahn R, Jirku M, Keeling PJ, Kostka M, Kudryavtsev A, Lara E, Lukeš J, Mann DG, Mitchell EAD, Nitsche F, Romeralo M, Saunders GW, Simpson AGB, Smirnov AV, Spouge JL, Stern RF, StoeckT ZJ, Schindel D (2012) CBOL protist working group: barcoding eukaryotic richness beyond the animal, plant, and fungal kingdoms. PLoS Biol 10:e1001419PubMedPubMedCentral Pawlowski J, Audic S, Adl S, Bass D, Belbahri L, Berney C, Bowser SS, Čepička I, Decelle J, Dunthorn M, Fiore-Donno AM, Gile GH, Holzmann M, Jahn R, Jirku M, Keeling PJ, Kostka M, Kudryavtsev A, Lara E, Lukeš J, Mann DG, Mitchell EAD, Nitsche F, Romeralo M, Saunders GW, Simpson AGB, Smirnov AV, Spouge JL, Stern RF, StoeckT ZJ, Schindel D (2012) CBOL protist working group: barcoding eukaryotic richness beyond the animal, plant, and fungal kingdoms. PLoS Biol 10:e1001419PubMedPubMedCentral
Zurück zum Zitat Podlipaev S (1988) Blastocrithidia raabei rostrata subsp. n. (Mastigophora, Trypanosomamonadida) parasite of a bug Coreus marginatus. Zool Zh 67:1407–1411 (in Russian) Podlipaev S (1988) Blastocrithidia raabei rostrata subsp. n. (Mastigophora, Trypanosomamonadida) parasite of a bug Coreus marginatus. Zool Zh 67:1407–1411 (in Russian)
Zurück zum Zitat Podlipaev SA (1990) Catalogue of world fauna of Trypanosomatidae (Protozoa). Proc Zool Inst, Leningrad 144:1–178 (in Russian) Podlipaev SA (1990) Catalogue of world fauna of Trypanosomatidae (Protozoa). Proc Zool Inst, Leningrad 144:1–178 (in Russian)
Zurück zum Zitat Podlipaev SA, Sturm NR, Fiala I, Fernandes O, Westenberger SJ, Dollet M, Campbell DA, Lukeš J (2004) Diversity of insect trypanosomatids assessed from the spliced leader RNA and 5S rRNA genes and intergenic regions. J Eukaryot Microbiol 51:283–290PubMed Podlipaev SA, Sturm NR, Fiala I, Fernandes O, Westenberger SJ, Dollet M, Campbell DA, Lukeš J (2004) Diversity of insect trypanosomatids assessed from the spliced leader RNA and 5S rRNA genes and intergenic regions. J Eukaryot Microbiol 51:283–290PubMed
Zurück zum Zitat Poulin R (2014) Parasite biodiversity revisited: frontiers and constraints. Int J Parasitol 44:581–589PubMed Poulin R (2014) Parasite biodiversity revisited: frontiers and constraints. Int J Parasitol 44:581–589PubMed
Zurück zum Zitat Rocha CFD, Bergallo HG, Bittencourt EB (2016) More than just invisible inhabitants: parasites are important but neglected components of the biodiversity. Zoologia 33:e20150198 Rocha CFD, Bergallo HG, Bittencourt EB (2016) More than just invisible inhabitants: parasites are important but neglected components of the biodiversity. Zoologia 33:e20150198
Zurück zum Zitat Rózsa LA, Vas Z (2015) Co-extinct and critically co-endangered species of parasitic lice, and conservation-induced extinction: should lice be reintroduced to their hosts? Oryx 49:107–110 Rózsa LA, Vas Z (2015) Co-extinct and critically co-endangered species of parasitic lice, and conservation-induced extinction: should lice be reintroduced to their hosts? Oryx 49:107–110
Zurück zum Zitat Seward EA, Votýpka J, Kment P, Lukeš J, Kelly S (2017) Description of Phytomonas oxycareni n. sp. from the salivary glands of Oxycarenus lavaterae. Protist 168:71–79PubMed Seward EA, Votýpka J, Kment P, Lukeš J, Kelly S (2017) Description of Phytomonas oxycareni n. sp. from the salivary glands of Oxycarenus lavaterae. Protist 168:71–79PubMed
Zurück zum Zitat Schoener E, Uebleis SS, Cuk C, Nawratil M, Obwaller AG, Zechmeister T, Lebl K, Rádrová J, Zittra C, Votýpka J, Fuehrer H-P (2018) Trypanosomatid parasites in Austrian mosquitoes. PLoS ONE 13:e0196052PubMedPubMedCentral Schoener E, Uebleis SS, Cuk C, Nawratil M, Obwaller AG, Zechmeister T, Lebl K, Rádrová J, Zittra C, Votýpka J, Fuehrer H-P (2018) Trypanosomatid parasites in Austrian mosquitoes. PLoS ONE 13:e0196052PubMedPubMedCentral
Zurück zum Zitat Schwelm A, Badstöber J, Bulman S, Desoignies N, Etemadi M, Falloon RE, Gachon CMM, Legreve A, Lukeš J, Merz U, Nenarokova A, Strittmatter M, Sullivan BK, Neuhauser S (2018) Not in your usual Top 10: protists that infect plants and algae. Mol Plant Pathol 19:1029–1044PubMed Schwelm A, Badstöber J, Bulman S, Desoignies N, Etemadi M, Falloon RE, Gachon CMM, Legreve A, Lukeš J, Merz U, Nenarokova A, Strittmatter M, Sullivan BK, Neuhauser S (2018) Not in your usual Top 10: protists that infect plants and algae. Mol Plant Pathol 19:1029–1044PubMed
Zurück zum Zitat Stork NE, Lyal CHC (1993) Extinction or “co-extinction” rates? Nature 366:307 Stork NE, Lyal CHC (1993) Extinction or “co-extinction” rates? Nature 366:307
Zurück zum Zitat Strona G, Fattorini S (2014) Parasitic worms: how many really? Int J Parasitol 44:269–272PubMed Strona G, Fattorini S (2014) Parasitic worms: how many really? Int J Parasitol 44:269–272PubMed
Zurück zum Zitat Strona G (2015) Past, present and future of host–parasite coextinctions. Int J Parasitol Parasites Wildl 4:431–441PubMedPubMedCentral Strona G (2015) Past, present and future of host–parasite coextinctions. Int J Parasitol Parasites Wildl 4:431–441PubMedPubMedCentral
Zurück zum Zitat Teixeira MMG, Borghesan TC, Ferreira RC, Santos MA, Takata CSA, Campaner M, Nunes VLB, Milder RV, de Souza W, Camargo EP (2011) Phylogenetic validation of the genera Angomonas and Strigomonas of trypanosomatids harboring bacterial endosymbionts with the description of new species of trypanosomatids and of proteobacterial symbionts. Protist 162:503–524PubMed Teixeira MMG, Borghesan TC, Ferreira RC, Santos MA, Takata CSA, Campaner M, Nunes VLB, Milder RV, de Souza W, Camargo EP (2011) Phylogenetic validation of the genera Angomonas and Strigomonas of trypanosomatids harboring bacterial endosymbionts with the description of new species of trypanosomatids and of proteobacterial symbionts. Protist 162:503–524PubMed
Zurück zum Zitat Teixeira MMG, Takata CSA, Conchon I, Campaner M, Camargo EP (1997) Ribosomal and kDNA markers distinguish two subgroups of Herpetomonas among old species and new trypanosomatids isolated from flies. J Parasitol 83:58–65PubMed Teixeira MMG, Takata CSA, Conchon I, Campaner M, Camargo EP (1997) Ribosomal and kDNA markers distinguish two subgroups of Herpetomonas among old species and new trypanosomatids isolated from flies. J Parasitol 83:58–65PubMed
Zurück zum Zitat Turvey ST, Cheke AS (2008) Dead as a dodo: the fortuitous rise to fame of an extinction icon. Hist Biol 20:149–163 Turvey ST, Cheke AS (2008) Dead as a dodo: the fortuitous rise to fame of an extinction icon. Hist Biol 20:149–163
Zurück zum Zitat Týč J, Votýpka J, Klepetková H, Šuláková H, Jirků M, Lukeš J (2013) Growing diversity of trypanosomatid parasites of flies (Diptera: Brachycera): frequent cosmopolitism and moderate host specificity. Mol Phylogenet Evol 69:255–264PubMed Týč J, Votýpka J, Klepetková H, Šuláková H, Jirků M, Lukeš J (2013) Growing diversity of trypanosomatid parasites of flies (Diptera: Brachycera): frequent cosmopolitism and moderate host specificity. Mol Phylogenet Evol 69:255–264PubMed
Zurück zum Zitat Votýpka J, Maslov A, Yurchenko V, Jirků M, Kment P, Lun Z-R, Lukeš J (2010) Probing into the diversity of trypanosomatid flagellates parasitizing insect hosts in South-West China reveals both endemism and global dispersal. Mol Phylogenet Evol 54:243–253PubMed Votýpka J, Maslov A, Yurchenko V, Jirků M, Kment P, Lun Z-R, Lukeš J (2010) Probing into the diversity of trypanosomatid flagellates parasitizing insect hosts in South-West China reveals both endemism and global dispersal. Mol Phylogenet Evol 54:243–253PubMed
Zurück zum Zitat Votýpka J, Klepetková H, Jirků M, Kment P, Lukeš J (2012a) Phylogenetic relationships of trypanosomatids parasitizing true bugs (Insecta: Heteroptera) in sub-Saharan Africa. Int J Parasitol 42:489–500PubMed Votýpka J, Klepetková H, Jirků M, Kment P, Lukeš J (2012a) Phylogenetic relationships of trypanosomatids parasitizing true bugs (Insecta: Heteroptera) in sub-Saharan Africa. Int J Parasitol 42:489–500PubMed
Zurück zum Zitat Votýpka J, Klepetková H, Yurchenko V, Horák A, Lukeš J, Maslov A (2012b) Cosmopolitan distribution of a trypanosomatid Leptomonas pyrrhocoris. Protist 163:616–631PubMed Votýpka J, Klepetková H, Yurchenko V, Horák A, Lukeš J, Maslov A (2012b) Cosmopolitan distribution of a trypanosomatid Leptomonas pyrrhocoris. Protist 163:616–631PubMed
Zurück zum Zitat Votýpka J, Suková E, Kraeva N, Ishemgulova A, Duží I, Lukeš J, Yurchenko V (2013) Diversity of Trypanosomatids (Kinetoplastea: Trypanosomatidae) parasitizing fleas (Insecta: Siphonaptera) and description of a new genus Blechomonas gen. n. Protist 164:763–781PubMed Votýpka J, Suková E, Kraeva N, Ishemgulova A, Duží I, Lukeš J, Yurchenko V (2013) Diversity of Trypanosomatids (Kinetoplastea: Trypanosomatidae) parasitizing fleas (Insecta: Siphonaptera) and description of a new genus Blechomonas gen. n. Protist 164:763–781PubMed
Zurück zum Zitat Votýpka J, Kostygov AY, Kraeva N, Grybchuk-Ieremenko A, Tesařová M, Grybchuk D, Lukeš J, Yurchenko V (2014) Kentomonas gen. g., a new genus of endosymbiont-containing Trypanosomatids of Strigomonadinae subfam. n. Protist 165:825–838PubMed Votýpka J, Kostygov AY, Kraeva N, Grybchuk-Ieremenko A, Tesařová M, Grybchuk D, Lukeš J, Yurchenko V (2014) Kentomonas gen. g., a new genus of endosymbiont-containing Trypanosomatids of Strigomonadinae subfam. n. Protist 165:825–838PubMed
Zurück zum Zitat Votýpka J, d'Avila-Levy CM, Grellier P, Maslov DA, Lukeš J, Yurchenko V (2015) New approaches to systematics of Trypanosomatidae: criteria for taxonomic (re)description. Trends Parasitol 31:460–469PubMed Votýpka J, d'Avila-Levy CM, Grellier P, Maslov DA, Lukeš J, Yurchenko V (2015) New approaches to systematics of Trypanosomatidae: criteria for taxonomic (re)description. Trends Parasitol 31:460–469PubMed
Zurück zum Zitat Votýpka J, Pafčo B, Modrý D, Mbohli D, Tagg N, Petrželková KJ (2018) An unexpected diversity of trypanosomatids in fecal samples of great apes. Int J Parasitol Parasites Wildl 7:322–325PubMedPubMedCentral Votýpka J, Pafčo B, Modrý D, Mbohli D, Tagg N, Petrželková KJ (2018) An unexpected diversity of trypanosomatids in fecal samples of great apes. Int J Parasitol Parasites Wildl 7:322–325PubMedPubMedCentral
Zurück zum Zitat Votýpka J, Kment P, Kriegová E, Vermeij MJA, Keeling PJ, Yurchenko V, Lukeš J (2019) High prevalence and endemism of trypanosomatids on a small Caribbean island. J Eukaryot Microbiol 66:600–607PubMed Votýpka J, Kment P, Kriegová E, Vermeij MJA, Keeling PJ, Yurchenko V, Lukeš J (2019) High prevalence and endemism of trypanosomatids on a small Caribbean island. J Eukaryot Microbiol 66:600–607PubMed
Zurück zum Zitat Wallace FG (1966) The trypanosomatid parasites of insects and arachnids. Exp Parasitol 18:124–193PubMed Wallace FG (1966) The trypanosomatid parasites of insects and arachnids. Exp Parasitol 18:124–193PubMed
Zurück zum Zitat Warren BH, Simberloff D, Ricklefs RE, Aguilée R, Condamine FL, Gravel D, Morlon H, Mouquet N, Rosindell J, Casquet J, Conti E, Cornuault J, Fernández-Palacios JM, Hengl T, Norder SJ, Rijsdijk KF, Sanmartín I, Strasberg D, Triantis KA, Valente LM, Whittaker RJ, Gillespie RG, Emerson BC, Thébaud C (2015) Islands as model systems in ecology and evolution: prospects fifty years after MacArthur–Wilson. Ecol Lett 18:200–217PubMed Warren BH, Simberloff D, Ricklefs RE, Aguilée R, Condamine FL, Gravel D, Morlon H, Mouquet N, Rosindell J, Casquet J, Conti E, Cornuault J, Fernández-Palacios JM, Hengl T, Norder SJ, Rijsdijk KF, Sanmartín I, Strasberg D, Triantis KA, Valente LM, Whittaker RJ, Gillespie RG, Emerson BC, Thébaud C (2015) Islands as model systems in ecology and evolution: prospects fifty years after MacArthur–Wilson. Ecol Lett 18:200–217PubMed
Zurück zum Zitat Westenberger SJ, Sturm NR, Yanega D, Podlipaev SA, Zeledon R, Campbell DA, Maslov DA (2004) Trypanosomatid biodiversity in Costa Rica: genotyping of parasites from Heteroptera using the Spliced Leader RNA gene. Parasitology 129:537–547PubMed Westenberger SJ, Sturm NR, Yanega D, Podlipaev SA, Zeledon R, Campbell DA, Maslov DA (2004) Trypanosomatid biodiversity in Costa Rica: genotyping of parasites from Heteroptera using the Spliced Leader RNA gene. Parasitology 129:537–547PubMed
Zurück zum Zitat Wilfert L, Longdon B, Ferreira AG, Bayer F, Jiggins FM (2011) Trypanosomatids are common and diverse parasites of Drosophila. Parasitology 138:585–865 Wilfert L, Longdon B, Ferreira AG, Bayer F, Jiggins FM (2011) Trypanosomatids are common and diverse parasites of Drosophila. Parasitology 138:585–865
Zurück zum Zitat Windsor DA (1995) Equal rights for parasites. Conserv Biol 9:1–2 Windsor DA (1995) Equal rights for parasites. Conserv Biol 9:1–2
Zurück zum Zitat Windsor DA (1998) Most of species on Earth are parasites. Int J Parasitol 28:1939–1941PubMed Windsor DA (1998) Most of species on Earth are parasites. Int J Parasitol 28:1939–1941PubMed
Zurück zum Zitat Yurchenko V, Kostygov A, Havlová J, Grybchuk-Ieremenko A, Ševčíková T, Lukeš J, Ševčík J, Votýpka J (2016) Diversity of Trypanosomatids in cockroaches and the description of Herpetomonas tarakana sp. n. J Eukaryot Microbiol 63:198–209PubMed Yurchenko V, Kostygov A, Havlová J, Grybchuk-Ieremenko A, Ševčíková T, Lukeš J, Ševčík J, Votýpka J (2016) Diversity of Trypanosomatids in cockroaches and the description of Herpetomonas tarakana sp. n. J Eukaryot Microbiol 63:198–209PubMed
Zurück zum Zitat Yurchenko V, Votýpka J, Tesařová M, Klepetková H, Kraeva N, Jirků M, Lukeš J (2014) Ultrastructure and molecular phylogeny of four new species of monoxenous trypanosomatids from flies (Diptera: Brachycera) with redefinition of the genus Wallaceina. Folia Parasitol 61:97–112 Yurchenko V, Votýpka J, Tesařová M, Klepetková H, Kraeva N, Jirků M, Lukeš J (2014) Ultrastructure and molecular phylogeny of four new species of monoxenous trypanosomatids from flies (Diptera: Brachycera) with redefinition of the genus Wallaceina. Folia Parasitol 61:97–112
Zurück zum Zitat Yurchenko VY, Lukeš J, Jirků M, Zeledon R, Maslov DA (2006) Leptomonas costaricensis sp. n. (Kinetoplastea: Trypanosomatidae), a member of the novel phylogenetic group of insect trypanosomatids closely related to the genus Leishmania. Parasitology 133:537–546PubMed Yurchenko VY, Lukeš J, Jirků M, Zeledon R, Maslov DA (2006) Leptomonas costaricensis sp. n. (Kinetoplastea: Trypanosomatidae), a member of the novel phylogenetic group of insect trypanosomatids closely related to the genus Leishmania. Parasitology 133:537–546PubMed
Zurück zum Zitat Yurchenko V, Lukeš J (2018) Parasites and their (endo)symbiotic microbes. Parasitology 145:1261–1264PubMed Yurchenko V, Lukeš J (2018) Parasites and their (endo)symbiotic microbes. Parasitology 145:1261–1264PubMed
Zurück zum Zitat Záhonová K, Kostygov AY, Ševčíková T, Yurchenko V, Eliáš M (2016) An unprecedented non-canonical nuclear genetic code with all three termination codons reassigned as sense codons. Curr Biol 26:2364–2369PubMed Záhonová K, Kostygov AY, Ševčíková T, Yurchenko V, Eliáš M (2016) An unprecedented non-canonical nuclear genetic code with all three termination codons reassigned as sense codons. Curr Biol 26:2364–2369PubMed
Zurück zum Zitat Zhou Y-Y, Rédei D (2018) A new synonymy in East Asian Urostylididae (Hemiptera: Heteroptera). Zootaxa 4504:145–150PubMed Zhou Y-Y, Rédei D (2018) A new synonymy in East Asian Urostylididae (Hemiptera: Heteroptera). Zootaxa 4504:145–150PubMed
Metadaten
Titel
Endangered monoxenous trypanosomatid parasites: a lesson from island biogeography
verfasst von
Jan Votýpka
Petr Kment
Vyacheslav Yurchenko
Julius Lukeš
Publikationsdatum
26.08.2020
Verlag
Springer Netherlands
Erschienen in
Biodiversity and Conservation / Ausgabe 13/2020
Print ISSN: 0960-3115
Elektronische ISSN: 1572-9710
DOI
https://doi.org/10.1007/s10531-020-02041-2

Weitere Artikel der Ausgabe 13/2020

Biodiversity and Conservation 13/2020 Zur Ausgabe