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The macroparasite fauna of cichlid fish from Nicaraguan lakes, a model system for understanding host–parasite diversification and speciation

  • Price, P. W. Evolutionary Biology of Parasites (Princeton University Press, 1980).

    Google Scholar 

  • Lima, L. B., Bellay, S., Giacomini, H. C., Isaac, A. & Lima-Junior, D. P. Influence of host diet and phylogeny on parasite sharing by fish in a diverse tropical floodplain. Parasitology 143, 343–349 (2016).

    CAS 
    PubMed 

    Google Scholar 

  • Eizaguirre, C., Lenz, T. L., Kalbe, M. & Milinski, M. Rapid and adaptive evolution of MHC genes under parasite selection in experimental vertebrate populations. Nat. Commun. 3, 1–6 (2012).

    Google Scholar 

  • Bashey, F. Within-host competitive interactions as a mechanism for the maintenance of parasite diversity. Philos. Trans. R. Soc. B Biol. Sci. 370, 20140301 (2015).

    Google Scholar 

  • Jolles, J. W., Mazué, G. P. F., Davidson, J., Behrmann-Godel, J. & Couzin, I. D. Schistocephalus parasite infection alters sticklebacks’ movement ability and thereby shapes social interactions. Sci. Rep. 10, 12282 (2020).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Demandt, N. et al. Parasite-infected sticklebacks increase the risk-taking behaviour of uninfected group members. Proc. R. Soc. B Biol. Sci. 285, 20180956 (2018).

    Google Scholar 

  • Poulin, R. Parasite manipulation of host behavior: An update and frequently asked questions. Adv. Study Behav. 41, 151–186 (2010).

    Google Scholar 

  • Terui, A., Ooue, K., Urabe, H. & Nakamura, F. Parasite infection induces size-dependent host dispersal: Consequences for parasite persistence. Proc. R. Soc. B Biol. Sci. 284, 20171491 (2017).

    Google Scholar 

  • Raeymaekers, J. A. M. et al. Contrasting parasite communities among allopatric colour morphs of the Lake Tanganyika cichlid Tropheus. BMC Evol. Biol. 13, 41 (2013).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Meyer, B. S. et al. An exploration of the links between parasites, trophic ecology, morphology, and immunogenetics in the Lake Tanganyika cichlid radiation. Hydrobiologia 832, 215–233 (2019).

    PubMed 

    Google Scholar 

  • Gobbin, T. P. et al. Temporally consistent species differences in parasite infection but no evidence for rapid parasite-mediated speciation in Lake Victoria cichlid fish. J. Evol. Biol. 33, 556–575 (2020).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Karvonen, A., Wagner, C. E., Selz, O. M. & Seehausen, O. Divergent parasite infections in sympatric cichlid species in Lake Victoria. J. Evol. Biol. 31, 1313–1329 (2018).

    PubMed 

    Google Scholar 

  • Bush, S. E. et al. Host defense triggers rapid adaptive radiation in experimentally evolving parasites. Evol. Lett. 3, 120–128 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Waid, R. M., Raesly, R. L., Mckaye, K. R. & McCrary, J. Zoogeografía íctica de lagunas cratéricas de Nicaragua. Encuentro 51, 65–80 (1999).

    Google Scholar 

  • Barluenga, M., Stölting, K., Salzburger, W., Muschick, M. & Meyer, A. Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature 439, 719–723 (2006).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Elmer, K. R., Lehtonen, T. K., Fan, S. & Meyer, A. Crater lake colonization by neotropical cichlid fishes. Evolution 67, 281–288 (2012).

    PubMed 

    Google Scholar 

  • Kautt, A. F. et al. Contrasting signatures of genomic divergence during sympatric speciation. Nature 588, 106–111 (2020).

    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Elmer, K. R., Lehtonen, T. K., Kautt, A. F., Harrod, C. & Meyer, A. Rapid sympatric ecological differentiation of crater lake cichlid fishes within historic times. BMC Biol. 8, 1–15 (2010).

    Google Scholar 

  • Kautt, A. F., Machado-Schiaffino, G., Torres-Dowdall, J. & Meyer, A. Incipient sympatric speciation in Midas cichlid fish from the youngest and one of the smallest crater lakes in Nicaragua due to differential use of the benthic and limnetic habitats? Ecol. Evol. 6, 5342–5357 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Barluenga, M. & Meyer, A. Phylogeography, colonization and population history of the Midas cichlid species complex (Amphilophus spp.) in the Nicaraguan crater lakes. BMC Evol. Biol. 10, 326 (2010).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Elmer, K. R., Lehtonen, T. K. & Meyer, A. Color assortative mating contributes to sympatric divergence of neotropical cichlid fish. Evolution 63, 2750–2757 (2009).

    PubMed 

    Google Scholar 

  • Kautt, A. F., Machado-Schiaffino, G. & Meyer, A. Lessons from a natural experiment: Allopatric morphological divergence and sympatric diversification in the Midas cichlid species complex are largely influenced by ecology in a deterministic way. Evol. Lett. 2, 323–340 (2018).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Elmer, K. R., Kusche, H., Lehtonen, T. K. & Meyer, A. Local variation and parallel evolution: Morphological and genetic diversity across a species complex of neotropical crater lake cichlid fishes. Philos. Trans. R. Soc. B Biol. Sci. 365, 1763–1782 (2010).

    Google Scholar 

  • Elmer, K. R. et al. Parallel evolution of Nicaraguan crater lake cichlid fishes via non-parallel routes. Nat. Commun. 5, 1–8 (2014).

    Google Scholar 

  • Vanhove, M. P. M. et al. Cichlids: A host of opportunities for evolutionary parasitology. Trends Parasitol. 32, 820–832 (2016).

    PubMed 

    Google Scholar 

  • Choudhury, A. et al. Trematode diversity in freshwater fishes of the Globe II: ‘New World’. Syst. Parasitol. 93, 271–282 (2016).

    PubMed 

    Google Scholar 

  • Watson, D. E. Digenea of fishes from Lake Nicaragua. In Investigations of the Ichthyofauna of Nicaraguan Lakes Vol. 15 (ed. Thorson, T. B.) 251–260 (University of Nebraska Press, 1976).

    Google Scholar 

  • Aguirre-Macedo, M. L. et al. Larval helminths parasitizing freshwater fishes from the Atlantic coast of Nicaragua. Comp. Parasitol. 68, 42–51 (2001).

    Google Scholar 

  • Aguirre-Macedo, M. L. et al. Some adult endohelminths parasitizing freshwater fishes from the Atlantic Drainages of Nicaragua. Comp. Parasitol. 68, 190–195 (2001).

    Google Scholar 

  • Mendoza-Franco, E. F., Posel, P. & Dumailo, S. Monogeneans (Dactylogyridae: Ancyrocephalinae) of freshwater fishes from the Caribbean coast of Nicaragua. Comp. Parasitol. 70, 32–41 (2003).

    Google Scholar 

  • Andrade-Gómez, L., Pinacho-Pinacho, C. D. & García-Varela, M. Molecular, morphological, and ecological data of Saccocoelioides Szidat, 1954 (Digenea: Haploporidae) from Middle America supported the reallocation from Culuwiya cichlidorum to Saccocoelioides. J. Parasitol. 103, 257–267 (2017).

    PubMed 

    Google Scholar 

  • López-Jiménez, A., Pérez-Ponce de León, G. & García-Varela, M. Molecular data reveal high diversity of Uvulifer (Trematoda: Diplostomidae) in Middle America, with the description of a new species. J. Helminthol. 92, 725–739 (2018).

    PubMed 

    Google Scholar 

  • Vidal-Martínez, V. M., Scholz, T. & Aguirre-Macedo, M. L. Dactylogyridae of cichlid fishes from Nicaragua, Central America, with descriptions of Gussevia herotilapiae sp. n. and three new species of Sciadicleithrum (Monogenea: Ancyrocephalinae). Comp. Parasitol. 68, 76–86 (2001).

    Google Scholar 

  • de Chambrier, A. & Vaucher, C. Proteocephalus gaspari n. sp. (Cestoda: Proteocephalidae), parasite de Lepisosteus tropicus (Gill.) au Lac Managua (Nicaragua). Rev. suisse Zool. 91, 229–233 (1984).

    Google Scholar 

  • González-Solís, A. D. & Jiménez-García, M. I. Parasitic nematodes of freshwater fishes from two nicaraguan crater lakes. Comp. Parasitol. 73, 188–192 (2006).

    Google Scholar 

  • Santacruz, A., Morales-Serna, F. N., Leal-Cardín, M., Barluenga, M. & Pérez-Ponce de León, G. Acusicola margulisae n. sp. (Copepoda: Ergasilidae) from freshwater fishes in a Nicaraguan crater lake based on morphological and molecular evidence. Syst. Parasitol. 97, 165–177 (2020).

    PubMed 

    Google Scholar 

  • Santacruz, A., Barluenga, M. & Pérez-Ponce de León, G. Taxonomic assessment of the genus Procamallanus (Nematoda) in Middle American cichlids (Osteichthyes) with molecular data, and the description of a new species from Nicaragua and Costa Rica. Parasitol. Res. 120, 1965–1977 (2021).

    PubMed 

    Google Scholar 

  • Bush, A. O., Lafferty, K. D., Lotz, J. M. & Shostak, A. W. Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol. 83, 575–583 (1997).

    CAS 
    PubMed 

    Google Scholar 

  • Rózsa, L., Reiczigel, J. & Majoros, G. Quantifying parasites in samples of hosts. J. Parasitol. 86, 228–232 (2000).

    PubMed 

    Google Scholar 

  • Krebs, C. J. Species diversity measures. In Ecological Methodology (ed. Krebs, C. J.) (Addison-Wesley Educational Publishers, 2014).

    Google Scholar 

  • Dixon, P. VEGAN, a package of R functions for community ecology. J. Veg. Sci. 14, 927–930 (2003).

    Google Scholar 

  • R Core Team. A language and environment for statistical computing. R Found. Stat. Comput. (2018). https://www.R-project.org.

  • Wickham, H. Elegant Graphics for Data Analysis: ggplot2 (Springer, 2008).

    MATH 

    Google Scholar 

  • Hsieh, T. C., Ma, K. H. & Chao, A. iNEXT-package: Interpolation and extrapolation for species diversity. Methods Ecol. Evol. 7, 1451–1456 (2016).

    Google Scholar 

  • Chao, A. et al. Rarefaction and extrapolation with Hill numbers: A framework for sampling and estimation in species diversity studies. Ecol. Monogr. 84, 45–67 (2014).

    Google Scholar 

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

    PubMed 

    Google Scholar 

  • Salzburger, W. Understanding explosive diversification through cichlid fish genomics. Nat. Rev. Genet. 19, 705–717 (2018).

    CAS 
    PubMed 

    Google Scholar 

  • Barluenga, M. & Meyer, A. The Midas cichlid species complex: Incipient sympatric speciation in Nicaraguan cichlid fishes? Mol. Ecol. 13, 2061–2076 (2004).

    CAS 
    PubMed 

    Google Scholar 

  • Elmer, K. R. & Meyer, A. Adaptation in the age of ecological genomics: Insights from parallelism and convergence. Trends Ecol. Evol. 26, 298–306 (2011).

    PubMed 

    Google Scholar 

  • Pérez-Ponce de León, G. & Choudhury, A. Biogeography of helminth parasites of freshwater fishes in Mexico: The search for patterns and processes. J. Biogeogr. 32, 645–659 (2005).

    Google Scholar 

  • Blais, J. et al. MHC adaptive divergence between closely related and sympatric African cichlids. PLoS ONE 2, e734 (2007).

    ADS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pariselle, A. et al. The monogenean parasite fauna of cichlids: A potential tool for host biogeography. Int. J. Evol. Biol. 2011, 1–15 (2011).

    Google Scholar 

  • Aguilar-Aguilar, R., Salgado-Maldonado, G., Contreras-Medina, R. & Martínez-Aquino, A. Richness and endemism of helminth parasites of freshwater fishes in Mexico. Biol. J. Linn. Soc. 94, 435–444 (2008).

    Google Scholar 

  • Dogiel, V. A. Ecology of parasites of freshwater fish. In Parasitology of Fishes (eds Dogiel, V. A. et al.) 1–47 (Edinburgh Oliver & Boyd, 1961).

    Google Scholar 

  • Poulin, R. & Valtonen, E. T. The predictability of helminth community structure in space: A comparison of fish populations from adjacent lakes. Int. J. Parasitol. 32, 1235–1243 (2002).

    PubMed 

    Google Scholar 

  • Razo-Mendivil, U., Rosas-Valdez, R. & Pérez-Ponce de León, G. A new Cryptogonimid (Digenea) from the mayan cichlid, Cichlasoma urophthalmus (Osteichthyes: Cichlidae), in several localities of the Yucatán Peninsula, Mexico. J. Parasitol. 94, 1371–1378 (2009).

    Google Scholar 

  • Mendoza-Franco, E. F. et al. Occurrence of Sciadicleithrum mexicanum Kritsky, Vidal-Martinez et Rodríguez-Canul, 1994 (Monogenea: Dactylogyridae) in the Cichlid Cichlasoma urophthalmus from a flooded quarry in Yucatan, Mexico. Mem. Inst. Oswaldo Cruz 90, 319–324 (1995).

    Google Scholar 

  • Blasco-Costa, I. & Poulin, R. Host traits explain the genetic structure of parasites: A meta-analysis. Parasitology 140, 1316–1322 (2013).

    PubMed 

    Google Scholar 

  • Torchin, M. E., Lafferty, K. D., Dobson, A. P., McKenzie, V. J. & Kuris, A. M. Introduced species and their missing parasites. Nature 421, 628–630 (2003).

    ADS 
    CAS 
    PubMed 

    Google Scholar 

  • Salgado-Maldonado, G. et al. Helminth parasites of freshwater fishes of the Balsas River drainage basin of southwestern Mexico. Comp. Parasitol. 68, 196–203 (2001).

    Google Scholar 

  • McCrary, J. K., Murphy, B. R., Stauffer, J. R. & Hendrix, S. S. Tilapia (Teleostei: Cichlidae) status in Nicaraguan natural waters. Environ. Biol. Fishes 78, 107–114 (2007).

    Google Scholar 

  • García-Vásquez, A., Pinacho-Pinacho, C. D., Guzmán-Valdivieso, I., Calixto-Rojas, M. & Rubio-Godoy, M. Morpho-molecular characterization of Gyrodactylus parasites of farmed tilapia and their spillover to native fishes in Mexico. Sci. Rep. 11, 1–17 (2021).

    Google Scholar 

  • Paredes-Trujillo, A., Velázquez-Abunader, I., Torres-Irineo, E., Romero, D. & Vidal-Martínez, V. M. Geographical distribution of protozoan and metazoan parasites of farmed Nile tilapia Oreochromis niloticus (L.) (Perciformes: Cichlidae) in Yucatán, México. Parasit. Vectors 9, 66 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhang, S. et al. Monogenean fauna of alien tilapias (Cichlidae) in south China. Parasite 26, 4 (2019).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Outa, J. O., Dos Santos, Q. M., Avenant-Oldewage, A. & Jirsa, F. Parasite diversity of introduced fish Lates niloticus, Oreochromis niloticus and endemic Haplochromis spp. of Lake Victoria. Kenya. Parasitol. Res. 120, 1583 (2021).

    PubMed 

    Google Scholar 

  • Smit, N. J., Malherbe, W. & Hadfield, K. A. Alien freshwater fish parasites from South Africa: Diversity, distribution, status and the way forward. Int. J. Parasitol. Parasites Wildl. 6, 386–401 (2017).

    PubMed 
    PubMed Central 

    Google Scholar 

  • Pérez-Ponce de León, G., Lagunas-Calvo, O., García-Prieto, L., Briosio-Aguilar, R. & Aguilar-Aguilar, R. Update on the distribution of the co-invasive Schyzocotyle acheilognathi (= Bothriocephalus acheilognathi), the Asian fish tapeworm, in freshwater fishes of Mexico. J. Helminthol. 92, 279–290 (2018).

    PubMed 

    Google Scholar 

  • Scholz, T., Šimková, A., Razanabolana, J. R. & Kuchta, R. The first record of the invasive Asian fish tapeworm (Schyzocotyle acheilognathi) from an endemic cichlid fish in Madagascar. Helminthol. 55, 84–87 (2018).

    CAS 

    Google Scholar 

  • Acosta, A., Carvalho, E. & da Silva, R. First record of Lernaea cyprinacea (copepoda) in a native fish species from a Brazilian river. Neotrop. Helminthol. 7, 7–12 (2013).

    Google Scholar 

  • Choudhury, A. et al. The invasive asian fish tapeworm, Bothriocephalus acheilognathi Yamaguti, 1934, in the chagres river/panama canal drainage, Panama. BioInvas. Rec. 2, 99–104 (2013).

    Google Scholar 

  • Schatz, H. & Behan-Pelletier, V. Global diversity of oribatids (Oribatida: Acari: Arachnida). Hydrobiologia 595, 323–328 (2008).

    Google Scholar 

  • Choudhury, A., Hoffnagle, T. L. & Cole, R. A. Parasites of native and nonnative fishes of the Little Colorado River, Grand Canyon, Arizona. J. Parasitol. 90, 1042–1053 (2004).

    PubMed 

    Google Scholar 

  • Vanhove, M. P. M. Part 6: Evolutionary parasitology of African freshwater fishes—And its implications for the sustainable management of aquatic resources. In A Guide to the Parasites of African Freshwater Fishes (eds Scholz, T. et al.) 403–412 (Royal Belgian Institute of Natural Sciences, 2018).

    Google Scholar 

  • Catalano, S. R., Whittington, I. D., Donnellan, S. C. & Gillanders, B. M. Parasites as biological tags to assess host population structure: Guidelines, recent genetic advances and comments on a holistic approach. Int. J. Parasitol. Parasites Wildl. 3, 220–226 (2014).

    PubMed 

    Google Scholar 

  • Baldwin, R. E., Banks, M. A. & Jacobson, K. C. Integrating fish and parasite data as a holistic solution for identifying the elusive stock structure of Pacific sardines (Sardinops sagax). Rev. Fish Biol. Fish. 22, 137–156 (2011).

    Google Scholar 

  • Criscione, C. D. & Blouin, M. S. Parasite phylogeographical congruence with salmon host evolutionarily significant units: Implications for salmon conservation. Mol. Ecol. 16, 993–1005 (2007).

    CAS 
    PubMed 

    Google Scholar 

  • Vanhove, M. P. M. et al. Hidden biodiversity in an ancient lake: Phylogenetic congruence between Lake Tanganyika tropheine cichlids and their monogenean flatworm parasites. Sci. Rep. 5, 1–15 (2015).

    Google Scholar 

  • Matschiner, M., Böhne, A., Ronco, F. & Salzburger, W. The genomic timeline of cichlid fish diversification across continents. Nat. Commun. 11, 1–8 (2020).

    Google Scholar 

  • Choudhury, A., García-Varela, M. & Pérez-Ponce de León, G. Parasites of freshwater fishes and the Great American biotic interchange: A bridge too far? J. Helminthol. 91, 174–196 (2017).

    CAS 
    PubMed 

    Google Scholar 

  • Mendoza-Franco, E. F. & Vidal-Martínez, V. M. Phylogeny of species of Sciadicleithrum (Monogenoidea: Ancyrocephalinae), and their historical biogeography in the Neotropics. J. Parasitol. 91, 253–259 (2005).

    PubMed 

    Google Scholar 

  • de Chambrier, A., Pinacho-Pinacho, C. D., Hernández-Orts, J. S. & Scholz, T. T. A new genus and two new species of proteocephalidean tapeworms (Cestoda) from cichlid fish (Perciformes: Cichlidae) in the neotropics. J. Parasitol. 103, 83–94 (2017).

    PubMed 

    Google Scholar 

  • Mendoza-Palmero, C. A., Blasco-Costa, I., Hernández-Mena, D. & Pérez-Ponce de León, G. Parasciadicleithrum octofasciatum n. gen., n. sp. (Monogenoidea: Dactylogyridae), parasite of Rocio octofasciata (Regan) (Cichlidae: Perciformes) from Mexico characterised by morphological and molecular evidence. Parasitol. Int. 66, 152–162 (2017).

    PubMed 

    Google Scholar 

  • Pinacho-Pinacho, C. D., Hernández-Orts, J. S., Sereno-Uribe, A. L., Pérez-Ponce de León, G. & García-Varela, M. Mayarhynchus karlae n. g., n. sp. (Acanthocephala: Neoechinorhynchidae), a parasite of cichlids (Perciformes: Cichlidae) in southeastern Mexico, with comments on the paraphyly of Neoechynorhynchus Stiles & Hassall, 1905. Syst. Parasitol. 94, 351–365 (2017).

    PubMed 

    Google Scholar 

  • Razo-Mendivil, U., Vázquez-Domínguez, E., Rosas-Valdez, R., Pérez-Ponce de León, G. & Nadler, S. A. Phylogenetic analysis of nuclear and mitochondrial DNA reveals a complex of cryptic species in Crassicutis cichlasomae (Digenea: Apocreadiidae), a parasite of Middle-American cichlids. Int. J. Parasitol. 40, 471–486 (2010).

    CAS 
    PubMed 

    Google Scholar 

  • Razo-Mendivil, U., Rosas-Valdez, R., Rubio-Godoy, M. & Pérez-Ponce de León, G. The use of mitochondrial and nuclear sequences in prospecting for cryptic species in Tabascotrema verai (Digenea: Cryptogonimidae), a parasite of Petenia splendida (Cichlidae) in Middle America. Parasitol. Int. 64, 173–181 (2015).

    CAS 
    PubMed 

    Google Scholar 

  • Pinacho-Pinacho, C. D., García-Varela, M., Sereno-Uribe, A. L. & Pérez-Ponce de León, G. A hyper-diverse genus of acanthocephalans revealed by tree-based and non-tree-based species delimitation methods: Ten cryptic species of Neoechinorhynchus in Middle American freshwater fishes. Mol. Phylogenet. Evol. 127, 30–45 (2018).

    PubMed 

    Google Scholar 

  • Martínez-Aquino, A. et al. Detecting a complex of cryptic species within Neoechinorhynchus golvani (Acanthocephala: Neoechinorhynchidae) inferred from ITSs and LSU rDNA gene sequences. J. Parasitol. 95, 1040–1047 (2009).

    PubMed 

    Google Scholar 


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