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Host specificity and the reproductive strategies of parasites

Published online by Cambridge University Press:  13 December 2021

Jean-François Doherty Open the ORCID record for Jean-François Doherty [Opens in a new window] ,
Marin Milotic ,
Antoine Filion  and
Alan Eriksson Open the ORCID record for Alan Eriksson [Opens in a new window]
Jean-François Doherty*
Affiliation:
Department of Zoology, University of Otago, Dunedin, New Zealand
Marin Milotic
Affiliation:
Department of Zoology, University of Otago, Dunedin, New Zealand
Antoine Filion
Affiliation:
Department of Zoology, University of Otago, Dunedin, New Zealand
Alan Eriksson
Affiliation:
Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, Campo Grande, Brazil
*
Author for correspondence: Jean-François Doherty, E-mail: [email protected]
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Abstract

Environmental stability can have profound impacts on life history trait evolution in organisms, especially with respect to development and reproduction. In theory, free-living species, when subjected to relatively stable and predictable conditions over many generations, should evolve narrow niche breadths and become more specialized. In parasitic organisms, this level of specialization is reflected by their host specificity. Here, we tested how host specificity impacts the reproductive strategies of parasites, a subject seldomly addressed for this group. Through an extensive review of the literature, we collated a worldwide dataset to predict, through Bayesian multilevel modelling, the effect of host specificity on the reproductive strategies of parasitic copepods of fishes or corals. We found that copepods of fishes with low host specificity (generalists) invest more into reproductive output with larger clutch sizes, whereas generalist copepods of corals invest less into reproductive output with smaller clutch sizes. The differences in host turnover rates through an evolutionary timescale could explain the contrasting strategies across species observed here, which should still favour the odds of parasites encountering and infecting a host. Ultimately, the differences found in this study reflect the unique evolutionary history that parasites share both intrinsically and extrinsically with their hosts.

Keywords

Host specificityhost–parasite interactionparasitic copepodr/K selectionreproductive strategy
Type
Research Article
Information
Parasitology , Volume 149 , Issue 4 , April 2022 , pp. 534 - 541
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Agosta, SJ, Janz, N and Brooks, DR (2010) How specialists can be generalists: resolving the ‘parasite paradox’ and implications for emerging infectious disease. Zoologia 27, 151–162.CrossRefGoogle Scholar
Bauer, G (1994) The adaptive value of offspring size among freshwater mussels (Bivalvia; Unionoidea). Journal of Animal Ecology 63, 933–944.CrossRefGoogle Scholar
Bertram, J and Masel, J (2019) Density-dependent selection and the limits of relative fitness. Theoretical Population Biology 129, 81–92.CrossRefGoogle ScholarPubMed
Blasco-Costa, I and Poulin, R (2013) Host traits explain the genetic structure of parasites: a meta-analysis. Parasitology 140, 1316–1322.CrossRefGoogle ScholarPubMed
Blasco-Costa, I, Waters, JM and Poulin, R (2012) Swimming against the current: genetic structure, host mobility and the drift paradox in trematode parasites. Molecular Ecology 21, 207–217.CrossRefGoogle ScholarPubMed
Bohnsack, JA (1983) Species turnover and the order versus chaos controversy concerning reef fish community structure. Coral Reefs 1, 223–228.CrossRefGoogle Scholar
Bonte, D, Van Dyck, H, Bullock, JM, Coulon, A, Delgado, M, Gibbs, M, Lehouck, V, Matthysen, E, Mustin, K, Saastamoinen, M, Schtickzelle, N, Stevens, VM, Vandewoestijne, S, Baguette, M, Barton, K, Benton, TG, Chaput-Bardy, A, Clobert, J, Dytham, C, Hovestadt, T, Meier, CM, Palmer, SCF, Turlure, C and Travis, JMJ (2012) Costs of dispersal. Biological Reviews 87, 290–312.CrossRefGoogle ScholarPubMed
Büchi, L and Vuilleumier, S (2016) Ecological strategies in stable and disturbed environments depend on species specialisation. Oikos 125, 1408–1420.CrossRefGoogle Scholar
Buckley, LB and Jetz, W (2008) Linking global turnover of species and environments. Proceedings of the National Academy of Sciences of the United States of America 105, 17836–17841.CrossRefGoogle ScholarPubMed
Bürkner, P-C (2017) brms: an R package for Bayesian multilevel models using Stan. Journal of Statistical Software 80, 1–28.CrossRefGoogle Scholar
Cavaleiro, FI and Santos, MJ (2014) Egg number-egg size: an important trade-off in parasite life history strategies. International Journal for Parasitology 44, 173–182.CrossRefGoogle ScholarPubMed
Cheng, YR and Dai, CF (2009) The infection process of the reef coral Stylophora pistillata by the parasitic copepod, Xarifia obesa. Coral Reefs 28, 681–681.CrossRefGoogle Scholar
Cheng, Y-R, Mayfield, AB, Meng, P-J, Dai, C-F and Huys, R (2016) Copepods associated with scleractinian corals: a worldwide checklist and a case study of their impact on the reef-building coral Pocillopora damicornis (Linnaeus, 1758) (Pocilloporidae). Zootaxa 4174, 291–345.CrossRefGoogle Scholar
Combes, C (1991) Evolution of parasite life-cycles. In Toft, CA, Aeschlimann, A and Bolis, L (eds), Parasite-Host Associations: Coexistence or Conflict? Oxford: Oxford Science, pp. 62–82.Google Scholar
Dallas, T, Huang, S, Nunn, C, Park, AW and Drake, JM (2017) Estimating parasite host range. Proceedings of the Royal Society B-Biological Sciences 284, 20171250. doi: 10.1098/rspb.2017.1250CrossRefGoogle ScholarPubMed
de Queiroz, K (2007) Species concepts and species delimitation. Systematic Biology 56, 879–886.CrossRefGoogle ScholarPubMed
Esch, GW, Hazen, TC and Aho, JM (1977) Parasitism and r- and K-selection. In Esch, GW (ed.), Regulation of Parasite Populations. New York, NY, USA: Academic Press, Inc., pp. 9–62.Google Scholar
Espirito-Santo, HMV, Rodriguez, MA and Zuanon, J (2013) Reproductive strategies of Amazonian stream fishes and their fine-scale use of habitat are ordered along a hydrological gradient. Freshwater Biology 58, 2494–2504.CrossRefGoogle Scholar
Futuyma, DJ and Moreno, G (1988) The evolution of ecological specialization. Annual Review of Ecology and Systematics 19, 207–233.CrossRefGoogle Scholar
Haubrock, PJ, Pilotto, F, Innocenti, G, Cianfanelli, S and Haase, P (2020) Two centuries for an almost complete community turnover from native to non-native species in a riverine ecosystem. Global Change Biology 27(3), 606–623. doi: 10.1111/gcb.15442CrossRefGoogle Scholar
Horton, T, Kroh, A, Ahyong, S, Bailly, N, Boyko, CB, Brandão, SN, Gofas, S, Hooper, JNA, Hernandez, F, Holovachov, O, Mees, J, Molodtsova, TN, Paulay, G, Decock, W, Dekeyzer, S, Lanssens, T, Vandepitte, L, Vanhoorne, B, Adlard, R, Adriaens, P, Agatha, S, Ahn, KJ, Akkari, N, Alvarez, B, Anderberg, A, Anderson, G, Angel, MV, Antic, D, Arango, C, Artois, T, Atkinson, S, Baldwin, BG, Bank, R, Barber, A, Barbosa, JP, Bartsch, I, Bellan-Santini, D, Bergh, N, Bernot, J, Berta, A, Bezerra, TN, Bieler, R, Blanco, S, Blasco-Costa, I, Blazewicz, M, Bock, P, Bonifacino de León, M, Böttger-Schnack, R, Bouchet, P, Boury-Esnault, N, Boxshall, G, Bray, R, Bruce, NL, Cairns, S, Calvo Casas, J, Carballo, JL, Cárdenas, P, Carstens, E, Chan, BK, Chan, TY, Cheng, L, Churchill, M, Coleman, CO, Collins, AG, Collins, GE, Corbari, L, Cordeiro, R, Cornils, A, Coste, M, Costello, MJ, Crandall, KA, Cremonte, F, Cribb, T, Cutmore, S, Dahdouh-Guebas, F, Daly, M, Daneliya, M, Dauvin, JC, Davie, P, De Broyer, C, De Grave, S, de Mazancourt, V, de Voogd, NJ, Decker, P, Decraemer, W, Defaye, D, d'Hondt, JL, Dippenaar, S, Dohrmann, M, Dolan, J, Domning, D, Downey, R, Ector, L, Eisendle-Flöckner, U, Eitel, M, Encarnação, SCd, Enghoff, H, Epler, J, Ewers-Saucedo, C, Faber, M, Feist, S, Figueroa, D, Finn, J, Fišer, C, Fordyce, E, Foster, W, Frank, JH, Fransen, C, Freire, S, Furuya, H, Galea, H, Gao, T, Garcia-Alvarez, O, Garcia-Jacas, N, Garic, R, Garnett, S, Gasca, R, Gaviria-Melo, S, Gerken, S, Gibson, D, Gibson, R, Gil, J, Gittenberger, A, Glasby, C, Glover, A, Gómez-Noguera, SE, González-Solís, D, Gordon, D, Gostel, M, Grabowski, M, Gravili, C, Guerra-García, JM, Guidetti, R, Guiry, MD, Gutierrez, D, Hadfield, KA, Hajdu, E, Hallermann, J, Hayward, BW, Heiden, G, Hendrycks, E, Herbert, D, Herrera Bachiller, A, Ho, JS, Hodda, M, Høeg, J, Hoeksema, B, Houart, R, Hughes, L, Hyžný, M, Iniesta, LFM, Iseto, T, Ivanenko, S, Iwataki, M, Janssen, R, Jarms, G, Jaume, D, Jazdzewski, K, Jersabek, CD, Jóźwiak, P, Kabat, A, Kantor, Y, Karanovic, I, Karthick, B, Katinas, L, Kim, YH, King, R, Kirk, PM, Klautau, M, Kociolek, JP, Köhler, F, Kolb, J, Kotov, A, Kremenetskaia, A, Kristensen, RM, Kulikovskiy, M, Kullander, S, Lambert, G, Lazarus, D, Le Coze, F, LeCroy, S, Leduc, D, Lefkowitz, EJ, Lemaitre, R, Liu, Y, Loeuille, B, Lörz, AN, Lowry, J, Ludwig, T, Lundholm, N, Macpherson, E, Madin, L, Mah, C, Mamo, B, Mamos, T, Manconi, R, Mapstone, G, Marck, I, Marek, PE, Marshall, B, Marshall, DJ, Martin, P, Mast, R, McFadden, C, McInnes, SJ, Meidla, T, Meland, K, Merrin, KL, Messing, C, Miljutin, D, Mills, C, Moestrup, Ø, Mokievsky, V, Monniot, F, Mooi, R, Morandini, AC, Moreira da Rocha, R, Morrow, C, Mortelmans, J, Mortimer, J, Musco, L, Nesom, G, Neubauer, TA, Neubert, E, Neuhaus, B, Ng, P, Nguyen, AD, Nguyen Thi My, Y, Nielsen, C, Nishikawa, T, Norenburg, J, O'Hara, T, Opresko, D, Osawa, M, Osigus, HJ, Ota, Y, Páll-Gergely, B, Panero, JL, Pasini, E, Patterson, D, Paxton, H, Pelser, P, Peña-Santiago, R, Perrier, V, Perrin, W, Petrescu, I, Picton, B, Pilger, JF, Pisera, AB, Polhemus, D, Poore, GC, Potapova, M, Pugh, P, Read, G, Reich, M, Reimer, JD, Reip, H, Reuscher, M, Reynolds, JW, Richling, I, Rimet, F, Ríos, P, Rius, M, Rogers, DC, Roque, N, Rosenberg, G, Rützler, K, Sabbe, K, Saiz-Salinas, J, Sala, S, Santagata, S, Santos, S, Sar, E, Satoh, A, Saucède, T, Schatz, H, Schierwater, B, Schilling, E, Schmidt-Rhaesa, A, Schneider, S, Schönberg, C, Schuchert, P, Senna, AR, Serejo, C, Shaik, S, Shamsi, S, Sharma, J, Shear, WA, Shenkar, N, Shinn, A, Short, M, Sicinski, J, Sierwald, P, Simmons, E, Sinniger, F, Sivell, D, Sket, B, Smit, H, Smit, N, Smol, N, Souza-Filho, JF, Spelda, J, Sterrer, W, Stienen, E, Stoev, P, Stöhr, S, Strand, M, Suárez-Morales, E, Summers, M, Suppan, L, Susanna, A, Suttle, C, Swalla, BJ, Taiti, S, Tanaka, M, Tandberg, AH, Tang, D, Tasker, M, Taylor, J, Taylor, J, Tchesunov, A, ten Hove, H, ter Poorten, JJ, Thomas, JD, Thuesen, EV, Thurston, M, Thuy, B, Timi, JT, Timm, T, Todaro, A, Turon, X, Tyler, S, Uetz, P, Uribe-Palomino, J, Urtubey, E, Utevsky, S, Vacelet, J, Vachard, D, Vader, W, Väinölä, R, Valls Domedel, G, Van de Vijver, B, van der Meij, SE, van Haaren, T, van Soest, RW, Vanreusel, A, Venekey, V, Vinarski, M, Vonk, R, Vos, C, Walker-Smith, G, Walter, TC, Watling, L, Wayland, M, Wesener, T, Wetzel, CE, Whipps, C, White, K, Wieneke, U, Williams, DM, Williams, G, Wilson, R, Witkowski, A, Witkowski, J, Wyatt, N, Wylezich, C, Xu, K, Zanol, J, Zeidler, W and Zhao, Z (2020) World Register of Marine Species (WoRMS). WoRMS Editorial Board. https://www.marinespecies.org (accessed July 2019).Google Scholar
Huelsenbeck, JP and Ronquist, F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics (Oxford, England) 17, 754–755.CrossRefGoogle ScholarPubMed
Humes, AG (1985) Cnidarians and copepods: a success story. Transactions of the American Microscopical Society 104, 313–320.CrossRefGoogle Scholar
Jennings, JB and Calow, P (1975) The relationship between high fecundity and the evolution of entoparasitism. Oecologia 21, 109–115.CrossRefGoogle ScholarPubMed
Kabata, Z (1981) Copepoda (Crustacea) parasitic on fishes: problems and perspectives. Advances in Parasitology 19, 1–71.Google Scholar
Khodami, S, McArthur, JV, Blanco-Bercial, L and Arbizu, PM (2017) Molecular phylogeny and revision of copepod orders (Crustacea: Copepoda). Scientific Reports 7, 9164. doi: 10.1038/s41598-017-06656-4CrossRefGoogle Scholar
Koprivnikar, J and Randhawa, HS (2013) Benefits of fidelity: does host specialization impact nematode parasite life history and fecundity? Parasitology 140, 587–597.CrossRefGoogle ScholarPubMed
Krasnov, BR, Shenbrot, GI, Khokhlova, IS, Mouillot, D and Poulin, R (2008) Latitudinal gradients in niche breadth: empirical evidence from haematophagous ectoparasites. Journal of Biogeography 35, 592–601.CrossRefGoogle Scholar
Krasnov, BR, Mouillot, D, Shenbrot, GI, Khokhlova, IS and Poulin, R (2011) Beta-specificity: the turnover of host species in space and another way to measure host specificity. International Journal for Parasitology 41, 33–41.CrossRefGoogle ScholarPubMed
MacArthur, RH and Wilson, EO (1967) The Theory of Island Biogeography. Princeton, NJ, USA: Princeton University Press.Google Scholar
McKinney, ML (1997) Extinction vulnerability and selectivity: combining ecological and paleontological views. Annual Review of Ecology and Systematics 28, 495–516.CrossRefGoogle Scholar
Molina-Venegas, R and Rodriguez, MA (2017) Revisiting phylogenetic signal; strong or negligible impacts of polytomies and branch length information? BMC Evolutionary Biology 17, 53. doi: 10.1186/s12862-017-0898-yCrossRefGoogle ScholarPubMed
Morand, S (1996) Life-history traits in parasitic nematodes: a comparative approach for the search of invariants. Functional Ecology 10, 210–218.CrossRefGoogle Scholar
Morris, DW (1987) Tests of density-dependent habitat selection in a patchy environment. Ecological Monographs 57, 269–281.CrossRefGoogle Scholar
Mueller, LD, Guo, PZ and Ayala, FJ (1991) Density-dependent natural selection and trade-offs in life history traits. Science (New York, N.Y.) 253, 433–435.CrossRefGoogle ScholarPubMed
Pandolfi, JM (2002) Coral community dynamics at multiple scales. Coral Reefs 21, 13–23.CrossRefGoogle Scholar
Pandolfi, JM and Jackson, JBC (2001) Community structure of Pleistocene coral reefs of Curacao, Netherlands Antilles. Ecological Monographs 71, 49–67.Google Scholar
Pandolfi, JM and Jackson, JBC (2006) Ecological persistence interrupted in Caribbean coral reefs. Ecology Letters 9, 818–826.CrossRefGoogle ScholarPubMed
Parry, GD (1981) The meanings of r- and K-selection. Oecologia 48, 260–264.CrossRefGoogle ScholarPubMed
Patrick, SC and Weimerskirch, H (2017) Reproductive success is driven by local site fidelity despite stronger specialisation by individuals for large-scale habitat preference. Journal of Animal Ecology 86, 674–682.CrossRefGoogle ScholarPubMed
Pianka, ER (1970) On r- and K-selection. American Naturalist 104, 592–597.CrossRefGoogle Scholar
Poulin, R (1995) Clutch size and egg size in free-living and parasitic copepods: a comparative analysis. Evolution 49, 325–336.CrossRefGoogle ScholarPubMed
Poulin, R (1996) The evolution of life history strategies in parasitic animals. In Baker, JR, Muller, R and Rollinson, D (eds), Advances in Parasitology, vol. 37. Amsterdam, Netherlands: Elsevier, pp. 107–134.Google Scholar
Poulin, R (2007) Evolutionary Ecology of Parasites. Princeton, NJ, USA: Princeton University Press.CrossRefGoogle Scholar
Poulin, R and Hamilton, WJ (1997) Ecological correlates of body size and egg size in parasitic Ascothoracida and Rhizocephala (Crustacea). Acta Oecologica-International Journal of Ecology 18, 621–635.CrossRefGoogle Scholar
Poulin, R and Mouillot, D (2003) Parasite specialization from a phylogenetic perspective: a new index of host specificity. Parasitology 126, 473–480.CrossRefGoogle ScholarPubMed
Poulin, R, Krasnov, BR and Mouillot, D (2011) Host specificity in phylogenetic and geographic space. Trends in Parasitology 27, 355–361.CrossRefGoogle ScholarPubMed
Quadros, AF, Caubet, Y and Araujo, PB (2009) Life history comparison of two terrestrial isopods in relation to habitat specialization. Acta Oecologica-International Journal of Ecology 35, 243–249.CrossRefGoogle Scholar
Reznick, D, Bryant, MJ and Bashey, F (2002) r- and K-selection revisited: the role of population regulation in life-history evolution. Ecology 83, 1509–1520.CrossRefGoogle Scholar
Roff, D (2002) Life History Evolution. Sunderland, MA, USA: Sinauer Associates Inc.Google Scholar
Rohde, K (1978) Latitudinal differences in host-specificity of marine Monogenea and Digenea. Marine Biology 47, 125–134.CrossRefGoogle Scholar
Schmidtmann, ET (1994) Ecologically based strategies for controlling ticks. In Sonenshine, DE and Mather, TN (eds), Ecological Dynamics of Tick-Borne Zoonoses. New York, NY, USA: Oxford University Press, pp. 240–280.Google Scholar
Stearns, SC (1977) The evolution of life history traits: a critique of the theory and a review of the data. Annual Review of Ecology and Systematics 8, 145–171.CrossRefGoogle Scholar
Stearns, SC (1992) The Evolution of Life Histories. New York, NY, USA: Oxford University Press.Google Scholar
Stock, JH (1988) Copepods associated with reef corals: a comparison between the Atlantic and the Pacific. Hydrobiologia 167, 545–547.CrossRefGoogle Scholar
Strona, G (2015) Past, present and future of host-parasite co-extinctions. International Journal for Parasitology: Parasites and Wildlife 4, 431–441.Google ScholarPubMed
Thomas, GH, Hartmann, K, Jetz, W, Joy, JB, Mimoto, A and Mooers, AO (2013) PASTIS: an R package to facilitate phylogenetic assembly with soft taxonomic inferences. Methods in Ecology and Evolution 4, 1011–1017.CrossRefGoogle Scholar
Vallee, V, Villanueva, MC and Blanchard, F (2019) Functional richness and turnover patterns reveal assembly rules structuring marine fish communities on the continental shelf of French Guiana. Marine Ecology Progress Series 630, 183–195.CrossRefGoogle Scholar
van Beest, FM, Uzal, A, Vander Wal, E, Laforge, MP, Contasti, AL, Colville, D and McLoughlin, PD (2014) Increasing density leads to generalization in both coarse-grained habitat selection and fine-grained resource selection in a large mammal. Journal of Animal Ecology 83, 147–156.CrossRefGoogle Scholar
Vázquez, DP and Stevens, RD (2004) The latitudinal gradient in niche breadth: concepts and evidence. American Naturalist 164, E1–E19.CrossRefGoogle ScholarPubMed
Vehtari, A, Gelman, A and Gabry, J (2017) Practical Bayesian model evaluation using leave-one-out cross-validation and WAIC. Statistics and Computing 27, 1413–1432.CrossRefGoogle Scholar
Whittington, ID (1997) Reproduction and host-location among the parasitic Platyhelminthes. International Journal for Parasitology 27, 705–714.CrossRefGoogle ScholarPubMed
Zuur, AF, Ieno, EN, Walker, NJ, Saveliev, AA and Smith, GM (2009) Mixed Effects Models and Extensions in Ecology with R. New York, NY: Spinger, pp. 209–243.CrossRefGoogle Scholar
Zuur, AF, Ieno, EN and Elphick, CS (2010) A protocol for data exploration to avoid common statistical problems. Methods in Ecology and Evolution 1, 3–14.CrossRefGoogle Scholar
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