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Endangered monoxenous trypanosomatid parasites: a lesson from island biogeography

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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.

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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).

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Authors and Affiliations

  1. Department of Parasitology, Faculty of Science, Charles University, Prague, Czech Republic

    Jan Votýpka

  2. Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice (Budweis), Czech Republic

    Jan Votýpka & Julius Lukeš

  3. Department of Entomology, National Museum, Prague, Czech Republic

    Petr Kment

  4. Faculty of Science, University of Ostrava, Ostrava, Czech Republic

    Vyacheslav Yurchenko

  5. Martsinovsky Institute of Medical Parasitology, Sechenov University, Moscow, Russia

    Vyacheslav Yurchenko

  6. Faculty of Sciences, University of South Bohemia, České Budějovice (Budweis), Czech Republic

    Julius Lukeš

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  1. Jan Votýpka
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  2. Petr Kment
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  3. Vyacheslav Yurchenko
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  4. Julius Lukeš
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Correspondence to Jan Votýpka or Julius Lukeš.

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Communicated by Nigel E. Stork.

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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.

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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

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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

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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

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