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Broad but restricted detection of malacosporeans in a Neotropical cradle of diversification

Published online by Cambridge University Press:  10 December 2020

Juliana Naldoni Open the ORCID record for Juliana Naldoni [Opens in a new window] ,
Beth Okamura Open the ORCID record for Beth Okamura [Opens in a new window] ,
Hanna Hartikainen ,
Lincoln L. Corrêa Open the ORCID record for Lincoln L. Corrêa [Opens in a new window]  and
Edson A. Adriano
Juliana Naldoni*
Affiliation:
Departamento de Ciências Biológicas, Universidade Federal de São Paulo (UNIFESP), Diadema, SP, Brazil
Beth Okamura
Affiliation:
Department of Life Sciences, Natural History Museum, Cromwell Road, LondonSW7 5BD, UK
Hanna Hartikainen
Affiliation:
School of Life Sciences, University of Nottingham, University Park, NottinghamNG7 2RD, UK
Lincoln L. Corrêa
Affiliation:
Instituto de Ciências e Tecnologia das Águas, Universidade Federal do Oeste do Pará (UFOPA), Santarém, PA, Brazil
Edson A. Adriano
Affiliation:
Departamento de Ciências Biológicas, Universidade Federal de São Paulo (UNIFESP), Diadema, SP, Brazil Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, SP, Brazil
*
Author for correspondence: Juliana Naldoni, E-mail: [email protected]
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Abstract

This study undertook the first investigation of malacosporean infections in Neotropical fish. We used polymerase chain reaction detection with a primer set generally targeting known malacosporeans to assay for infection in the kidney of 146 fish in 21 species belonging to 12 families collected from two areas in the Amazon Basin. Infections were found in 13 fish variously belonging to seven species in six families and included the first identification of a malacosporean infection in cartilaginous fish (a freshwater stingray). Based on ssrDNA, all infections represented a single Buddenbrockia species (Buddenbrockia sp. E) that demonstrates an exceptionally broad range of fish species infected, and countered our expectations of high Neotropical malacosporean diversity. Infections were characterized at varying and often high prevalences in fish species but sample sizes were small. Ascertaining whether highly divergent malacosporeans have not been detected by current primers, and more comprehensive sampling may reveal whether malacosporeans are truly as species poor in the Amazon Basin as present data suggest. Our results prompt speculations about evolutionary scenarios including introduction via marine incursions and patterns of host use over time.

Keywords

Cartilaginous fish hostevolutionary scenariosfreshwater bryozoansmarine incursionssampling biasssrDNA phylogeny
Type
Research Article
Information
Parasitology , Volume 148 , Issue 5 , April 2021 , pp. 511 - 518
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Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

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References

Altschul, SF, Madden, TL, Schaffer, AA, Zhang, J, Zhang, Z, Miller, W and Lipman, DJ (1997) Gapped BLASTn and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.CrossRefGoogle Scholar
Atkinson, SD, Bartošová-Sojková, P, Whipps, CM and Bartholomew, JL (2015) Approaches for characterising Myxozoan species. In Okamura, B, Gruhl, A and Bartholomew, JL (eds), Myxozoan Evolution, Ecology and Development. Switzerland: Springer International Publishing Cham, p 111–124.CrossRefGoogle Scholar
Bartošová-Sojková, P, Hrabcová, M, Pecková, H, Patra, S, Kodádková, A, Jurajda, P, Tyml, T and Sibylle, HA (2014) Hidden diversity and evolutionary trends in malacosporean parasites (Cnidaria: Myxozoa) identified using molecular phylogenetics. International Journal for Parasitology 44, 565–577.CrossRefGoogle ScholarPubMed
Bloom, DD and Lovejoy, NR (2017) On the origins of marine-derived freshwater fishes in South America. Journal of Biogeography 44, 1927–1938.CrossRefGoogle Scholar
Borgwardt, F, Unfer, G, Auer, S, Waldner, K, El-Matbouli, M and Bechter, T (2020) Direct and indirect climate change impacts on brown trout in central Europe: how thermal regimes reinforce physiological stress and support the emergence of diseases. Frontiers in Environmental Science 8, 59.CrossRefGoogle Scholar
Carlson, CJ, Burgio, KR, Dougherty, ER, Phillips, AJ, Bueno, VM, Clements, CF, Castaldo, G, Dallas, TA, Cizauskas, CA, Cumming, GS, Doña, J, Harris, NC, Jovani, R, Mironov, S, Muellerklein, OC, Proctor, HC and Getz, WM (2017) Parasite biodiversity faces extinction and redistribution in a changing climate. Science advances 3, e1602422.CrossRefGoogle Scholar
Carlson, CJ, Hopkins, S, Bell, KC, Doña, J, Godfrey, SS, Kwak, ML, Lafferty, KD, Moir, ML, Speer, KA, Strona, G, Torchin, M and Wood, CL (2020) A global parasite conservation plan. Biological Conservation 250, 108596.CrossRefGoogle Scholar
Choudhury, A and Dick, TA (2000) Richness and diversity of helminth communities in tropical freshwater fishes: empirical evidence. Journal of Biogeography 27, 935–956.CrossRefGoogle Scholar
Dallas, T, Huang, S, Nunn, C, Park, AW and Drake, JM (2017) Estimating parasite host range. Proceedings of the Royal Society B 284, 20171250.CrossRefGoogle ScholarPubMed
De Baets, K, Dentzien-Dias, P, Upeniece, I, Verneaujj, O and Donoghue, PCJ (2015) Constraining the deep origin of parasitic flatworms and host-interactions with fossil evidence. Advances in Parasitology 90, 93–135.CrossRefGoogle ScholarPubMed
Dobson, A, Lafferty, KD, Kuris, AM, Hechinger, RF and Jetz, W (2008) Homage to Linnaeus: how many parasites? How many hosts?. Dobson, Andy et al. ‘Colloquium paper: homage to Linnaeus: how many parasites? How many hosts?’. Proceedings of the National Academy of Sciences of the USA 105, 11482–11489.CrossRefGoogle Scholar
Dougherty, ER, Carlson, CJ, Bueno, VM, Burgio, KR, Cizauskas, CA, Clements, CF, Seidel, DP and Harris, NC (2016) Paradigms for parasite conservation. Conservation Biology 30, 724–733.CrossRefGoogle ScholarPubMed
Dudgeon, D, Arthington, AH, Gessner, MO, Kawabata, Z, Knowler, DJ, Lévêque, C, Naiman, RJ, Prieur-Richard, AH, Soto, D, Stiassny, ML and Sullivan, CA (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biological Reviews of the Cambridge Philosophical Society 81, 163–182.CrossRefGoogle ScholarPubMed
Dunn, RR, Harris, NC, Colwell, RK, Koh, LP and Sodhi, NS (2009) The sixth mass coextinction: are most endangered species parasites and mutualists? Proceedings of the Royal Society B 276, 3037–3045.CrossRefGoogle ScholarPubMed
Fiala, I, Bartošová-Sojková, P, Okamura, B and Hartikainen, H (2015) Adaptive radiation and evolution. In Okamura, B, Gruhl, A and Bartholomew, JL (eds), Myxozoan Evolution, Ecology and Development. Switzerland: Springer International Publishing Cham, p 69–84. doi: 10.1007/978-3-319-14753-6_4.CrossRefGoogle Scholar
Froese, R and Pauly, D (2013) FishBase. http://www.fishbase.org (Accessed May 2020).Google Scholar
Gibson, AK, Baffoe-Bonnie, H, Penley, MJ, Lin, J, Owens, R, Khalid, A and Morran, LT (2020) The evolution of parasite host range in heterogeneous host populations. Journal of Evolutionary Biology 33, 773–782.CrossRefGoogle ScholarPubMed
Giribet, G and Edgecombe, GD (2020) The Invertebrate Tree of Life. Princeton, USA: Princeton University Press.CrossRefGoogle Scholar
Grabner, DS and El-Matbouli, M (2010) Experimental transmission of malacosporean parasites from bryozoans to common carp (Cyprinus carpio) and minnow (Phoxinus phoxinus). Parasitology 137, 629–639.CrossRefGoogle Scholar
Guindon, S, Dufayard, JF, Lefort, V, Anisimova, M, Hordijk, W and Gascuel, O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307–321.CrossRefGoogle ScholarPubMed
Hall, TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hallett, SL, Atkinson, SD, Bartholomew, JL and Székely, C (2015) Myxozoans exploiting homeotherms. In Okamura, B, Gruhl, A and Bartholomew, J (eds), Myxozoan Evolution, Ecology and Development. Cham, Switzerland: Springer International Publishing, pp. 125–135.CrossRefGoogle Scholar
Harmon, A, Littlewood, DTJ and Wood, CL (2019) Parasites lost: using natural history collections to track disease change across deep time. Frontiers in Ecology and the Environment 17, 157–166.CrossRefGoogle Scholar
Hartigan, A, Wilkinson, M, Gower, DJ, Streicher, JW, Holzer, AS and Okamura, B (2016) Myxozoan infections of caecilians demonstrate broad host specificity and indicate a link with human activity. International Journal for Parasitology 46, 375–381.CrossRefGoogle ScholarPubMed
Hartikainen, H, Gruhl, A and Okamura, B (2014) Diversification and repeated morphological transitions in endo-parasitic cnidarians (Myxozoa: Malacosporea). Molecular Phylogenetics and Evolution 76, 261–269.CrossRefGoogle Scholar
Hartikainen, H, Bass, D, Briscoe, AG, Knipe, H, Green, AJ and Okamura, B (2016) Assessing myxozoan presence and diversity using environmental DNA. International Journal for Parasitology 46, 781–792.CrossRefGoogle ScholarPubMed
Hedrick, RP, MacConnell, E and de Kinkelin, P (1993) Proliferative kidney disease of salmonid fish. Annual Review of Fish Diseases 3, 277–290.CrossRefGoogle Scholar
Holzer, AS, Bartošová-Sojková, P, Born-Torrijos, A, Lövy, A, Hartigan, A and Fiala, I (2018) The joint evolution of the Myxozoa and their alternate hosts: a cnidarian recipe for success and vast biodiversity. Molecular Ecology 27, 1651–1666.CrossRefGoogle ScholarPubMed
Hudson, PJ, Dobson, AP and Lafferty, KD (2006) Is a healthy ecosystem one that is rich in parasites? Trends in Ecology & Evolution 21, 381–385.Google Scholar
[IUCN] International Union for Conservation of Nature (2019) The IUCN Red List of Threatened Species, version 2019-1. IUCN. http://www.iucnredlist.org.Google Scholar
Jorge, F and Poulin, R (2018) Poor geographical match between the distributions of host diversity and parasite discovery effort. Proceedings of the Royal Society B Biological Sciences 285, 20180072.CrossRefGoogle ScholarPubMed
Kamiya, T, O'Dwyer, K, Nakagawa, S and Poulin, R (2014) Host diversity drives parasite diversity: meta analytical insights into patterns and causal mechanisms. Ecography 37, 689–697.CrossRefGoogle Scholar
Kodádková, A, Bartošová-Sojková, P, Holzer, AS and Fiala, I (2015) Bipteria vetusta n. sp. – an old parasite in an old host: tracing the origin of myxosporean parasitism in vertebrates. International Journal for Parasitology 45, 269–276. doi: 10.1016/j.ijpara.2014.12.004CrossRefGoogle Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0. Molecular Biology and Evolution 33, 1870–1874.CrossRefGoogle ScholarPubMed
Kuris, AM, Hechinger, RF, Shaw, JC, Whitney, KL, Aguirre-Macedo, L, Boch, CA, Dobson, AP, Dunham, EJ, Fredensborg, BL, Huspeni, TC, Lorda, J, Mababa, L, Mancini, FT, Mora, AB, Pickering, M, Talhouk, NL, Torchin, ME and Lafferty, KD (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454, 515–518.CrossRefGoogle ScholarPubMed
Lisnerová, M, Fiala, I, Cantatore, D, Irigoitia, M, Timi, J, Pecková, H, Bartošová-Sojková, P, Sandoval, CM, Luer, C, Morris, J and Holzer, AS (2020) Mechanisms and drivers for the establishment of life cycle complexity in Myxozoan parasites. Biology 9, 10.CrossRefGoogle ScholarPubMed
Marcus, E (1941) Sobre Bryozoa do Brasil. Boletim Faculdade de Filosofia, Ciencias e Letras, Universidade de São Paulo. Serie Zoologia 10, 3–207.Google Scholar
Massard, J and Geimer, G (2008) Global diversity of bryozoans (Bryozoa or Ectoprocta) in freshwater: an update. Bulletin de la Société des Naturalists Luxembourbeois 109, 139–148.Google Scholar
Murphy, CA, Gerth, W, Pauk, K, Konstantinidis, P and Arismendi, I (2020) Hiding in plain sight: historical fish collections aid contemporary parasite research. Fisheries Magazine 45, 263–270.CrossRefGoogle Scholar
Naldoni, J, Adriano, EA, Hartigan, A, Sayer, C and Okamura, B (2019) Malacosporean myxozoans exploit a diversity of fish hosts. Parasitology 146, 968–978. doi: 10.1017/S0031182019000246CrossRefGoogle ScholarPubMed
Okamura, B and Gruhl, A (2020) Evolution, origins and diversification of parasitic cnidarians. EcoEvoRxiv. August 17. doi: 10.32942/osf.io/qdpje.CrossRefGoogle Scholar
Okamura, B, Hartikainen, H, Schmidt-Posthaus, H and Wahli, T (2011) Life cycle complexity, environmental change and the emerging status of salmonid proliferative kidney disease. Freshwater Biology 56, 735–753.CrossRefGoogle Scholar
Okamura, B, Hartigan, A and Naldoni, J (2018) Extensive uncharted biodiversity: the parasite dimension. Integrative and Comparative Biology 58, 1132–1145. doi: 10.1093/icb/icy039Google ScholarPubMed
Patra, S, Hartigan, A, Morris, DJ, Kodádková, A and Holzer, AS (2017) Description and experimental transmission of Tetracapsuloides vermiformis n. sp. (Cnidaria: Myxozoa) and guidelines for describing malacosporean species including reinstatement of Buddenbrockia bryozoides n. comb. (syn. Tetracapsula bryozoides). Parasitology 144, 497–511.CrossRefGoogle Scholar
Pérez, A and Fabré, NN (2009) Seasonal growth and life history of the catfish Calophysus macropterus (Lichtenstein, 1819) (Siluriformes: Pimelodidae) from the Amazon floodplain. Journal of Applied Ichthyology 25, 343–349.CrossRefGoogle Scholar
Poulin, R (2014) Parasite biodiversity revisited: frontiers and constraints. International Journal for Parasitology 44, 581–589.CrossRefGoogle ScholarPubMed
Rambaut, A (2008) FigTree v1.1.1: Tree Figure Drawing Tool. http://tree.bio.ed.ac.uk/software/figtree/ (Accessed May 2020).Google Scholar
Reis, RE, Albert, JS, Di Dario, F, Mincarone, MM, Petry, P and Rocha, LA (2016) Fish biodiversity and conservation in South America. Journal of Fish Biology 89, 12–47.CrossRefGoogle Scholar
Ruppert, EE, Fox, RS and Barnes, RD (2004) Invertebrate Zoology. A Functional Evolutionary Approach, 7th Edn. Belmont: Thomson Brooks/Cole.Google Scholar
Santos, GM, Ferreira, EJG and Zuanon, JAS (2006) Peixes comerciais de Manaus. Ibama/AM: Provárzea, p. 144.Google Scholar
Schmeller, DS, Courchamp, F and Killeen, G (2020) Biodiversity loss, emerging pathogens and human health risks. Biodiversity and Conservation 29, 3095–3102.CrossRefGoogle Scholar
Skovgaard, A and Buchmann, K (2012) Tetracapsuloides bryosalmonae and PKD in juvenile wild salmonids in Denmark. Diseases of Aquatic Organisms 101, 33–42.CrossRefGoogle ScholarPubMed
Stephens, PR, Altizer, S, Smith, KF, Alonso Aguirre, A, Brown, JH, Budischak, SA, Byers, JE, Dallas, TA, Jonathan Davies, T, Drake, JM, Ezenwa, VO, Farrell, MJ, Gittleman, JL, Han, BA, Huang, S, Hutchinson, RA, Johnson, P, Nunn, CL, Onstad, D, Park, A, Vazquez-Prokopec, GM, Schmidt, JP and Poulin, R (2016) The macroecology of infectious diseases: a new perspective on global-scale drivers of pathogen distributions and impacts. Ecology Letters 19, 1159–1171.CrossRefGoogle ScholarPubMed
Stinson, M, Atkinson, SD and Bartholomew, JL (2018) Widespread distribution of Ceratonova shasta (Cnidaria: Myxosporea) genotypes indicates evolutionary adaptation to its salmonid fish hosts. The Journal of Parasitology 104, 645–650.CrossRefGoogle ScholarPubMed
Wood, TS and Okamura, O (2017) New species, genera, families, and range extensions of freshwater bryozoans in Brazil: the tip of the iceberg? Zootaxa 4306, 383–400.CrossRefGoogle Scholar
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