Skip to main content

Endangered monoxenous trypanosomatid parasites: a lesson from island biogeography

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Barratt J, Ellis J, Stark D, Barratt J (2017a) The evolution of trypanosomatid taxonomy. Parasit Vector 10:287

    Google Scholar 

  • 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:e0005215

    PubMed  PubMed Central  Google Scholar 

  • 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 232:111199

    CAS  PubMed  Google Scholar 

  • 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 164:129–152

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Camargo EP, Kastelein P, Roitman I (1990) Trypanosomatid parasites of plants (Phytomonas). Parasitol Today 6:22–25

    CAS  PubMed  Google Scholar 

  • Carlson CJ, Phillips AJ, Dallas TA, Alexander LW, Phelan A, Bansal S (2020) What would it take to describe the global diversity of parasites? Proc Natl Acad Sci USA. https://doi.org/10.1101/815902

    Article  PubMed  Google Scholar 

  • Chandler JA, James PM (2013) Discovery of trypanosomatid parasites in globally distributed Drosophila species. PLoS ONE 8:e61937

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 110:956–965

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e1008028

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 105:11482–11489

    CAS  PubMed  Google Scholar 

  • Dougherty ER, Carlson CJ, Bueno VM, Burgio KR, Cizauskas CA, Clements CF, Seidel DP, Harris NC (2015) Paradigms for parasite conservation. Conserv Biol 30:724–733

    PubMed  Google Scholar 

  • Emerson BC (2002) Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process. Mol Ecol 11:951–966

    CAS  PubMed  Google Scholar 

  • 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 145:430–442

    CAS  PubMed  Google Scholar 

  • França C (1920) La flagellose des euphorbes II. Ann l'Inst Pasteur, Paris 34:432–465

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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:e0214484

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e0227832

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gómez A, Nichols E (2013) Neglected wild life: parasitic biodiversity as a conservation target. Int J Parasitol Parasites Wildl 2:222–227

    PubMed  PubMed Central  Google Scholar 

  • Graham N, Gruner D, Lim J, Gillespie RG (2017) Island ecology and evolution: challenges in the Anthropocene. Environ Conserv. https://doi.org/10.1017/S0376892917000315

    Article  Google Scholar 

  • 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–E515

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Guilbert E (2020) New species of Tingidae (Insecta: Heteroptera) from Madagascar. Zootaxa 4759(3):391–404

    Google Scholar 

  • 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:e0174165

    PubMed  PubMed Central  Google Scholar 

  • Jaskowska E, Butler C, Preston G, Kelly S (2015) Phytomonas: trypanosomatids adapted to plant environments. PLOS Pathog 11:e1004484

    PubMed  PubMed Central  Google Scholar 

  • 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 59:537–547

    PubMed  Google Scholar 

  • Kikuchi Y, Hosokawa T, Fukatsu T (2011) An ancient but promiscuous host-symbiont association between Burkholderia gut symbionts and their heteropteran hosts. ISME J 5:446–460

    PubMed  Google Scholar 

  • Kment P (2013) Carduelicoris stehliki, a new genus and species of Pentatomidae (Hemiptera: Heteroptera) from Madagascar Acta Mus Moraviae. Sci Biol 98:415–432

    Google Scholar 

  • 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

    Google Scholar 

  • 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–e2015

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kostygov A, Grybchuk-Ieremenko A, Malysheva M, Frolov A, Yurchenko V (2014) Molecular revision of the genus Wallaceina. Protist 165:594–604

    CAS  PubMed  Google Scholar 

  • Kostygov A, Yurchenko V (2017) Revised classification of the subfamily Leishmaniinae (Trypanosomatidae). Folia Parasitol 64:020

    Google Scholar 

  • 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 166:551–568

    PubMed  Google Scholar 

  • 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 49:1075–1086

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Lipa JJ (1966) Blastocrithidia raabei sp. n., a flagellate parasite of Mesocerus marginatus L. (Hemiptera: Coreidae). Acta Protozool 4:19–23

    Google Scholar 

  • 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

    Google Scholar 

  • 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 34:466–480

    PubMed  Google Scholar 

  • Lukeš J, Skalický T, Týč J, Votýpka J, Yurchenko V (2014) Evolution of parasitism in kinetoplastid flagellates. Mol Biochem Parasit 195:115–122

    Google Scholar 

  • MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton, p 203

    Google Scholar 

  • 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 75:197–205

    CAS  PubMed  Google Scholar 

  • 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 54:57–65

    CAS  PubMed  Google Scholar 

  • Maslov DA, Votýpka J, Yurchenko V, Lukeš J (2013) Diversity and phylogeny of insect trypanosomatids: all that is hidden shall be revealed. Trends Parasitol 29:43–52

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Miyamoto S (1961) Comparative morphology of alimentary organs of Heteroptera, with phylogenetic consideration. Sieboldia 2:197–259

    Google Scholar 

  • Mihalca AD, Gherman CM, Cozma V (2011) Coendangered hard-ticks: threatened or threatening? Parasit Vector 4:71

    Google Scholar 

  • 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 313:1115–1118

    PubMed  Google Scholar 

  • 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–E5188

    CAS  PubMed  Google Scholar 

  • Okamura B, Hartigan A, Naldoni J (2018) Extensive uncharted biodiversity: the parasite dimension. Integr Comp Biol 58:1132–1145

    PubMed  Google Scholar 

  • 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:e1001419

    CAS  PubMed  PubMed Central  Google Scholar 

  • Podlipaev S (1988) Blastocrithidia raabei rostrata subsp. n. (Mastigophora, Trypanosomamonadida) parasite of a bug Coreus marginatus. Zool Zh 67:1407–1411 (in Russian)

    Google Scholar 

  • Podlipaev SA (1990) Catalogue of world fauna of Trypanosomatidae (Protozoa). Proc Zool Inst, Leningrad 144:1–178 (in Russian)

    Google Scholar 

  • 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 51:283–290

    CAS  PubMed  Google Scholar 

  • Poulin R (2014) Parasite biodiversity revisited: frontiers and constraints. Int J Parasitol 44:581–589

    PubMed  Google Scholar 

  • Rocha CFD, Bergallo HG, Bittencourt EB (2016) More than just invisible inhabitants: parasites are important but neglected components of the biodiversity. Zoologia 33:e20150198

    Google Scholar 

  • 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

    Google Scholar 

  • 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 168:71–79

    PubMed  Google Scholar 

  • 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:e0196052

    PubMed  PubMed Central  Google Scholar 

  • 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 19:1029–1044

    PubMed  Google Scholar 

  • Stork NE, Lyal CHC (1993) Extinction or “co-extinction” rates? Nature 366:307

    Google Scholar 

  • Strona G, Fattorini S (2014) Parasitic worms: how many really? Int J Parasitol 44:269–272

    PubMed  Google Scholar 

  • Strona G (2015) Past, present and future of host–parasite coextinctions. Int J Parasitol Parasites Wildl 4:431–441

    PubMed  PubMed Central  Google Scholar 

  • 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 162:503–524

    PubMed  Google Scholar 

  • 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 83:58–65

    CAS  PubMed  Google Scholar 

  • Turvey ST, Cheke AS (2008) Dead as a dodo: the fortuitous rise to fame of an extinction icon. Hist Biol 20:149–163

    Google Scholar 

  • 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 69:255–264

    PubMed  Google Scholar 

  • 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 54:243–253

    PubMed  Google Scholar 

  • 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 42:489–500

    PubMed  Google Scholar 

  • Votýpka J, Klepetková H, Yurchenko V, Horák A, Lukeš J, Maslov A (2012b) Cosmopolitan distribution of a trypanosomatid Leptomonas pyrrhocoris. Protist 163:616–631

    PubMed  Google Scholar 

  • 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 164:763–781

    PubMed  Google Scholar 

  • 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 165:825–838

    PubMed  Google Scholar 

  • 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 31:460–469

    PubMed  Google Scholar 

  • 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 7:322–325

    PubMed  PubMed Central  Google Scholar 

  • 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 66:600–607

    PubMed  Google Scholar 

  • Wallace FG (1966) The trypanosomatid parasites of insects and arachnids. Exp Parasitol 18:124–193

    CAS  PubMed  Google Scholar 

  • 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 18:200–217

    PubMed  Google Scholar 

  • 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 129:537–547

    CAS  PubMed  Google Scholar 

  • Wilfert L, Longdon B, Ferreira AG, Bayer F, Jiggins FM (2011) Trypanosomatids are common and diverse parasites of Drosophila. Parasitology 138:585–865

    Google Scholar 

  • Windsor DA (1995) Equal rights for parasites. Conserv Biol 9:1–2

    Google Scholar 

  • Windsor DA (1998) Most of species on Earth are parasites. Int J Parasitol 28:1939–1941

    CAS  PubMed  Google Scholar 

  • 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 63:198–209

    PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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 133:537–546

    CAS  PubMed  Google Scholar 

  • Yurchenko V, Lukeš J (2018) Parasites and their (endo)symbiotic microbes. Parasitology 145:1261–1264

    PubMed  Google Scholar 

  • 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 26:2364–2369

    PubMed  Google Scholar 

  • Zhou Y-Y, Rédei D (2018) A new synonymy in East Asian Urostylididae (Hemiptera: Heteroptera). Zootaxa 4504:145–150

    PubMed  Google Scholar 

Download references

Acknowledgements

We thank all specialists who helped to identify the insect host species: Harry Brailovsky (Instituto de Biología, Universidad Nacional Autónoma de México, Mexico), Frederic Chérot (Département de l’Etude du Milieu naturel et agricole, Service public de Wallonie, Gembloux, Belgium), Dominik Chłond (Department of Zoology, Faculty of Biology and Environmental Protection, University of Silesia, Katowice, Poland), Előd Kondorosy (Department of Animal Sciences, Georgikon Faculty, University of Pannonia, Keszthely, Hungary), Nico Nieser and Pingping Chen (Tiel, the Netherlands), and the late Jaroslav L. Stehlík (Moravian Museum, Brno, Czech Republic). We thank Eva Kriegová and Bethaney Gulla-Dewaney (Biology Centre) for help with sequencing. This work was supported by the ERD Funds of the Czech Ministry of Education 16_019/0000759, Czech Grant Agency Grants 20-07186S and 18-15962S, ERC CZ Grant LL1601, and the Czech Ministry of Culture (DKRVO 2019–2023/5.I.b, 00023272).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Jan Votýpka or Julius Lukeš.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by Nigel E. Stork.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10531_2020_2041_MOESM1_ESM.pdf

Supplementary file1 (PDF 104 kb). Fig. S1 The map of the islands with depicted collection sites (red dots). The numbers of wide/endemic/subendemic genera and species are presented for all (∑) and infected-only (I) true bugs (Heteroptera) studied for the presence of trypanosomatid parasites in their guts. The numbers of detected trypanosomatid species in true bugs and flies are listed in the following genus order (for more information see Tab. 2): Leptomonas/Zelonia/Blastocrithidia/’jaculum’/Phytomonas/Herpetomonas/Lafontella/Wallacemonas/new clade II/Angomonas/Kentomonas.

10531_2020_2041_MOESM2_ESM.pdf

Supplementary file2 (PDF 193 kb). Supplementary Table 1 (S1) Summarized information about all trypanosomatid-positive insect host species and studied parasites (including parasite morphotype (Type) and localization and intensity (Int) of the infection in the host intestine) from Madagascar, Reunion, and Mauritius. Source: envi, parasite DNA extracted from an infected host intestine; cult, parasite DNA extracted from an axenic culture; Localization of the infection in the host intestine: AMG, abdominal midgut; HG, hindgut; MG, midgut; MT, Malpighian tubules; RA, Rectal ampulla; TMG, thoracic midgut; Intensity of the infection based on the approximate estimation of parasite cells (solitary [0.1], dozens [1], hundreds [2], and thousands [3]) in host insect intestinal; morphotypes (Types) of the flagellates: S, short choanomastigotes; M, medium promastigotes; L, long slender leptomonads; and the typing units (TUs), to which the detected flagellates belong (* TU newly detected in this study). Distribution of Species and Genus of the insect host was sorted into the following categories: ENDE = taxon endemic for the particular island; SUBE = taxon sub-endemic, distributed in Madagascar, the Mascarene Islands, the Comoro Islands, and Seychelles; and WIDE = widely distributed taxa, including other biogeographic realms, such as the studied island(s) plus continental Africa, and/or beyond. MIX: a simultaneous infection by two (or even more) different trypanosomatid species detected based on the sequencing data obtained from the dissected intestine (envi) or by the comparison of data from the intestine and axenic culture (cult) derived from the same specimens

10531_2020_2041_MOESM3_ESM.pdf

Supplementary file3 (PDF 112 kb). Supplementary Table 2 (S2) List of all sequences publically available in the GenBank database (https://www.ncbi.nlm.nih.gov/genbank/) which were used for the phylogenetic analyses are indicated in the table: trypanosomatid species names, or name of the strains/isolates and/or Typing Unit (TU) and the Accession Numbers

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Votýpka, J., Kment, P., Yurchenko, V. et al. Endangered monoxenous trypanosomatid parasites: a lesson from island biogeography. Biodivers Conserv 29, 3635–3667 (2020). https://doi.org/10.1007/s10531-020-02041-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-020-02041-2

Keywords

  • Biodiversity loss
  • Conservation
  • Endemic
  • Host specificity
  • Coevolution
  • Phytomonas
  • Heteroptera