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Parasitological research in the molecular age

Published online by Cambridge University Press:  18 June 2019

Christian Selbach Open the ORCID record for Christian Selbach [Opens in a new window] ,
Fátima Jorge Open the ORCID record for Fátima Jorge [Opens in a new window] ,
Eddy Dowle ,
Jerusha Bennett ,
Xuhong Chai ,
Jean-François Doherty ,
Alan Eriksson Open the ORCID record for Alan Eriksson [Opens in a new window] ,
Antoine Filion ,
Eleanor Hay  and
Ryan Herbison Open the ORCID record for Ryan Herbison [Opens in a new window]
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Christian Selbach*
Affiliation:
Department of Zoology, University of Otago, 340 Great King St, Dunedin, 9016, New Zealand
Fátima Jorge
Affiliation:
Department of Zoology, University of Otago, 340 Great King St, Dunedin, 9016, New Zealand
Eddy Dowle
Affiliation:
Department of Anatomy, University of Otago, 270 Great King St, Dunedin, 9016, New Zealand
Jerusha Bennett
Affiliation:
Department of Zoology, University of Otago, 340 Great King St, Dunedin, 9016, New Zealand
Xuhong Chai
Affiliation:
Department of Zoology, University of Otago, 340 Great King St, Dunedin, 9016, New Zealand
Jean-François Doherty
Affiliation:
Department of Zoology, University of Otago, 340 Great King St, Dunedin, 9016, New Zealand
Alan Eriksson
Affiliation:
Programa de Pós-Graduação em Ecologia e Conservação, Universidade Federal de Mato Grosso do Sul, 79070-900 Campo Grande, Mato Grosso do Sul, Brazil
Antoine Filion
Affiliation:
Department of Zoology, University of Otago, 340 Great King St, Dunedin, 9016, New Zealand
Eleanor Hay
Affiliation:
Department of Zoology, University of Otago, 340 Great King St, Dunedin, 9016, New Zealand
Ryan Herbison
Affiliation:
Department of Zoology, University of Otago, 340 Great King St, Dunedin, 9016, New Zealand
Jocelyn Lindner
Affiliation:
Department of Zoology, University of Otago, 340 Great King St, Dunedin, 9016, New Zealand
Eunji Park
Affiliation:
Department of Zoology, University of Otago, 340 Great King St, Dunedin, 9016, New Zealand
Bronwen Presswell
Affiliation:
Department of Zoology, University of Otago, 340 Great King St, Dunedin, 9016, New Zealand
Brandon Ruehle
Affiliation:
Department of Zoology, University of Otago, 340 Great King St, Dunedin, 9016, New Zealand
Paulo M. Sobrinho
Affiliation:
Programa de Pós-Graduação em Etnobiologia e Conservação da Natureza, Universidade Federal Rural de Pernambuco, Rua Dom Manuel de Medeiros, Dois Irmãos, 52171-900 Recife, PE, Brazil
Eleanor Wainwright
Affiliation:
Department of Zoology, University of Otago, 340 Great King St, Dunedin, 9016, New Zealand
Robert Poulin
Affiliation:
Department of Zoology, University of Otago, 340 Great King St, Dunedin, 9016, New Zealand
*
Author for correspondence: Christian Selbach, E-mail: chris.selbach@gmail.com
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Abstract

New technological methods, such as rapidly developing molecular approaches, often provide new tools for scientific advances. However, these new tools are often not utilized equally across different research areas, possibly leading to disparities in progress between these areas. Here, we use empirical evidence from the scientific literature to test for potential discrepancies in the use of genetic tools to study parasitic vs non-parasitic organisms across three distinguishable molecular periods, the allozyme, nucleotide and genomics periods. Publications on parasites constitute only a fraction (<5%) of the total research output across all molecular periods and are dominated by medically relevant parasites (especially protists), particularly during the early phase of each period. Our analysis suggests an increasing complexity of topics and research questions being addressed with the development of more sophisticated molecular tools, with the research focus between the periods shifting from predominantly species discovery to broader theory-focused questions. We conclude that both new and older molecular methods offer powerful tools for research on parasites, including their diverse roles in ecosystems and their relevance as human pathogens. While older methods, such as barcoding approaches, will continue to feature in the molecular toolbox of parasitologists for years to come, we encourage parasitologists to be more responsive to new approaches that provide the tools to address broader questions.

Keywords

Allozymegenomicsmolecular toolsnucleotide sequencingpublication trends
Type
Review Article
Information
Parasitology , Volume 146 , Issue 11 , September 2019 , pp. 1361 - 1370
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Copyright
Copyright © Cambridge University Press 2019 

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Footnotes

*

Authors contributed equally to this work.

References

Ahrends, A, Burgess, ND, Gereau, RE, Marchant, R, Bulling, MT, Lovett, JC, Platts, PJ, Kindemba, VW, Owen, N, Fanning, E and Rahbek, C (2011) Funding begets biodiversity. Diversity and Distributions 17, 191–200.Google Scholar
Alvar, J, Vélez, ID, Bern, C, Herrero, M, Desjeux, P, Cano, J, Jannin, J and den Boer, M (2012) Leishmaniasis worldwide and global estimates of its incidence. PLoS ONE 7, e35671.Google Scholar
Aria, M and Cuccurullo, C (2017) Bibliometrix: an R-tool for comprehensive science mapping analysis. Journal of Informetrics 11, 959–975.Google Scholar
Bass, D, Stentiford, GD, Littlewood, DTJ and Hartikainen, H (2015) Diverse applications of environmental DNA methods in parasitology. Trends in Parasitology 31, 499–513.Google Scholar
Bennett, S (2004) Solexa Ltd. Pharmacogenomics 5, 433–438.Google Scholar
Blasco-Costa, I, Poulin, R and Presswell, B (2016) Species of Apatemon szidat, 1928 and Australapatemon sudarikov, 1959 (Trematoda: Strigeidae) from New Zealand: linking and characterising life cycle stages with morphology and molecules. Parasitology Research 115, 271–289.Google Scholar
Carraro, L, Hartikainen, H, Jokela, J, Bertuzzo, E and Rinaldo, A (2018) Estimating species distribution and abundance in river networks using environmental DNA. Proceedings of the National Academy of Sciences 115, 11724–11729.Google Scholar
Dayrat, B (2005) Towards integrative taxonomy. Biological Journal of the Linnean Society 85, 407–415.Google Scholar
Dheilly, NM, Bolnick, D, Bordenstein, S, Brindley, PJ, Figuères, C, Holmes, EC, Martinez, JM, Phillips, AJ, Poulin, R and Rosario, K (2017) Parasite Microbiome Project: systematic investigation of microbiome dynamics within and across parasite-host interactions. mSystems 2, e00050–17.Google Scholar
Dobson, A, Lafferty, KD, Kuris, AM, Hechinger, RF and Jetz, W (2008) Homage to linnaeus: how many parasites? how many hosts? Proceedings of the National Academy of Sciences 105, 11482–11489.Google Scholar
Fellows, I (2018) wordcloud: Word Clouds. R package version 2.6. Available at https://CRAN.R-project.org/package=wordcloud.Google Scholar
Ferro e Silva, AM, Sobral-Souza, T, Vancine, MH, Muylaert, RL, de Abreu, AP, Pelloso, SM, de Barros Carvalho, MD, de Andrade, L, Ribeiro, MC and de Toledo, MJO (2018) Spatial prediction of risk areas for vector transmission of Trypanosoma cruzi in the State of Paraná, southern Brazil. PLoS Neglected Tropical Diseases 12, e0006907.Google Scholar
Furuse, Y (2019) Analysis of research intensity on infectious disease by disease burden reveals which infectious diseases are neglected by researchers. Proceedings of the National Academy of Sciences 116, 478–483.Google Scholar
GBD 2015 Disease and Injury Incidence and Prevalence Collaborators (2016) Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015. The Lancet 388, 1545–1602.Google Scholar
Gryseels, B, Polman, K, Clerinx, J and Kestens, L (2006) Human schistosomiasis. The Lancet 368, 1106–1118.Google Scholar
Hall, N (2013) After the gold rush. Genome Biology 14, 115.Google Scholar
Hatcher, MJ and Dunn, AM (2011) Parasites in Ecological Communities: From Interactions to Ecosystems. Cambridge, UK: Cambridge University Press.Google Scholar
Hendriks, IE and Duarte, CM (2008) Allocation of effort and imbalances in biodiversity research. Journal of Experimental Marine Biology and Ecology 360, 15–20.Google Scholar
Hering, D, Borja, A, Jones, JI, Pont, D, Boets, P, Bouchez, A, Bruce, K, Drakare, S, Hänfling, B, Kahlert, M, Leese, F, Meissner, K, Mergen, P, Reyjol, Y, Segurado, P, Vogler, A and Kelly, M (2018) Implementation options for DNA-based identification into ecological status assessment under the European Water Framework Directive. Water Research 138, 192–205.Google Scholar
Hubby, JL and Lewontin, RC (1966) A molecular approach to the study of genic heterozygosity in natural populations. I. The number of alleles at different loci in Drosophila pseudoobscura. Genetics 54, 577–594.Google Scholar
Hudson, PJ, Dobson, AP and Newborn, D (1998) Prevention of population cycles by parasite removal. Science 282, 2256–2258.Google Scholar
Huver, JR, Koprivnikar, J, Johnson, PTJ and Whyard, S (2015) Development and application of an eDNA method to detect and quantify a pathogenic parasite in aquatic ecosystems. Ecological Applications 25, 991–1002.Google Scholar
Jenkins, TP, Brindley, PJ, Gasser, RB and Cantacessi, C (2019) Helminth microbiomes: a hidden treasure trove? Trends in Parasitology 35, 13–22.Google Scholar
Jensen, K and Bullard, SA (2010) Characterization of a diversity of tetraphyllidean and rhinebothriidean cestode larval types, with comments on host associations and life-cycles. International Journal for Parasitology 40, 889–910.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.Google Scholar
Jourdan, PM, Lamberton, PHL, Fenwick, A and Addiss, DG (2018) Soil-transmitted helminth infections. The Lancet 391, 252–265.Google Scholar
Kuris, AM, Hechinger, RF, Shaw, JC, Whitney, KL, Aguirre-Macedo, L, Boch, CA, Dobson, AP, Dunham, EJ, Fredensborg, BL, Huspeni, TC, Lorda, J, Mabada, 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.Google Scholar
Lacoursière-Roussel, A, Howland, K, Normandeau, E, Grey, EK, Archambault, P, Deiner, K, Lodge, DM, Hernandez, C, Leduc, N and Bernatchez, L (2018) eDNA metabarcoding as a new surveillance approach for coastal Arctic biodiversity. International Journal of Business Innovation and Research 17, 7763–7777.Google Scholar
Lafferty, KD and Gerber, LR (2002) Good medicine for conservation biology: the intersection of epidemiology and conservation biology. Conservation Biology 16, 593–604.Google Scholar
Lafferty, KD, Allesina, S, Arim, M, Briggs, CJ, De Leo, G, Dobson, AP, Dunne, JA, Johnson, PTJ, Kuris, AM, Marcogliese, DJ, Martinez, ND, Memmott, J, Marquet, PA, McLaughlin, JP, Mordecai, EA, Pascual, M, Poulin, R and Thieltges, DW (2008) Parasites in food webs: the ultimate missing links. Ecology Letters 11, 533–546.Google Scholar
Litt, M and Luty, JA (1989) A hypervariable microsatellite revealed by in vitro amplification of a dinucleotide repeat within the cardiac muscle actin gene. American Journal of Human Genetics 44, 397–401.Google Scholar
Locke, SA, McLaughlin, JD, Dayanandan, S and Marcogliese, D (2010) Diversity and specificity in Diplostomum spp. metacercariae in freshwater fishes revealed by cytochrome c oxidase I and internal transcribed spacer sequences. International Journal for Parasitology 40, 333–343.Google Scholar
Locke, SA, McLaughlin, JD and Marcogliese, DJ (2013) Predicting the similarity of parasite communities in freshwater fishes using the phylogeny, ecology and proximity of hosts. Oikos 122, 73–83.Google Scholar
Martin, LJ, Blossey, B and Ellis, E (2012) Mapping where ecologists work: biases in the global distribution of terrestrial ecological observations. Frontiers in Ecology and the Environment 10, 195–201.Google Scholar
Mathies, RA and Huang, XC (1992) Capillary array electrophoresis: an approach to high-speed, high-throughput DNA sequencing. Nature 359, 167–169.Google Scholar
Metzker, ML (2005) Emerging technologies in DNA sequencing. Genome Research 15, 1767–1776.Google Scholar
Metzker, ML (2009) Sequencing technologies — the next generation. Nature Reviews Genetics 11, 31–46.Google Scholar
Møller, AP (2005) Parasitism and the regulation of host populations. In Thomas, F, Renaud, F and Guégan, J-F (eds), Parasitism and Ecosystems. Oxford, UK: Oxford University Press, pp. 43–53.Google Scholar
Mouritsen, KN and Poulin, R (2005) Parasites boost biodiversity and change animal community structure by trait-mediated indirect effects. Oikos 108, 344–350.Google Scholar
Muir, P, Li, S, Lou, S, Wang, D, Spakowicz, DJ, Salichos, L, Zhang, J, Weinstock, GM, Isaacs, F, Rozowsky, J and Gerstein, M (2016) The real cost of sequencing: scaling computation to keep pace with data generation. Genome Biology 17, 53.Google Scholar
National Human Genome Research Institute (2018) DNA Sequencing Costs: Data. Available at https://www.genome.gov/27541954/dna-sequencing-costs-data/.Google Scholar
Parker, PG, Snow, AA, Schug, MD, Booton, GC and Fuerst, PA (1998) What molecules can tell us about populations: choosing and using a molecular marker. Ecology 79, 361–382.Google Scholar
Pautasso, M (2014) The jump in network ecology research between 1990 and 1991 is a Web of Science artefact. Ecological Modelling 286, 11–12.Google Scholar
Pedersen, TL (2018) ggraph: An Implementation of Grammar of Graphics for Graphs and Networks. R package version 1.0.2. Available at https://CRAN.R-project.org/package=ggraph.Google Scholar
Poulin, R (2014) Parasite biodiversity revisited: frontiers and constraints. International Journal for Parasitology 44, 581–589.Google Scholar
Poulin, R and Leung, TLF (2010) Taxonomic resolution in parasite community studies: are things getting worse? Parasitology 137, 1967–1973.Google Scholar
Preston, DL, Mischler, JA, Townsend, AR and Johnson, PTJ (2016) Disease ecology meets ecosystem science. Ecosystems 19, 737–748.Google Scholar
R Core Team (2018) R: A Language and Environment for Statistical Computing. Vienna, Austria: R foundation for Statistical Computing. Available at http//www.R-project.org.Google Scholar
Richard, G-F, Kerrest, A and Dujon, B (2008) Comparative genomics and molecular dynamics of DNA repeats in eukaryotes. Microbiology and Molecular Biology Reviews 72, 686–727.Google Scholar
Rist, CL, Garchitorena, A, Ngonghala, CN, Gillespie, TR and Bonds, MH (2015) The burden of livestock parasites on the poor. Trends in Parasitology 31, 527–530.Google Scholar
Rusch, JC, Hansen, H, Strand, DA, Markussen, T, Hytterød, S and Vrålstad, T (2018) Catching the fish with the worm: a case study on eDNA detection of the monogenean parasite Gyrodactylus salaris and two of its hosts, Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss). Parasites and Vectors 11, 1–12.Google Scholar
Sanger, F, Air, GM, Barrell, BG, Brown, NL, Coulson, AR, Fiddes, JC, Hutchison, CA, Slocombe, PM and Smith, M (1977) Nucleotide sequence of bacteriophage φX174 DNA. Nature 265, 687–695.Google Scholar
Schlötterer, C (2004) The evolution of molecular markers – just a matter of fashion? Nature Reviews Genetics 5, 63–69.Google Scholar
Schuster, SC (2007) Next-generation sequencing transforms today's biology. Nature Methods 5, 16–18.Google Scholar
Selakovic, S, de Ruiter, PC and Heesterbeek, H (2014) Infectious disease agents mediate interaction in food webs and ecosystems. Proceedings of the Royal Society B 281, 20132709.Google Scholar
Selbach, C, Soldánová, M, Georgieva, S, Kostadinova, A and Sures, B (2015) Integrative taxonomic approach to the cryptic diversity of Diplostomum spp. in lymnaeid snails from Europe with a focus on the ‘Diplostomum mergi’ species complex. Parasites & Vectors 8, 300.Google Scholar
Sievert, C (2018) plotly for R. Available at https://plotly-book.cpsievert.me.Google Scholar
Smith, KF, Acevedo-Whitehouse, K and Pedersen, AB (2009) The role of infectious diseases in biological conservation. Animal Conservation 12, 1–12.Google Scholar
South, A (2011) Rworldmap: a New R package for Mapping Global Data. The R Journal 3, 35–43.Google Scholar
Stat, M, Huggett, MJ, Bernasconi, R, DiBattista, JD, Berry, TE, Newman, SJ, Harvey, ES and Bunce, M (2017) Ecosystem biomonitoring with eDNA: metabarcoding across the tree of life in a tropical marine environment. Scientific Reports 7, 12240.Google Scholar
Thomsen, PF and Willerslev, E (2015) Environmental DNA – an emerging tool in conservation for monitoring past and present biodiversity. Biological Conservation 183, 4–18.Google Scholar
Tompkins, DM, Dobson, AP, Arneberg, P, Begon, ME, Cattadori, IM, Greenman, JV, Heesterbeek, JAP, Hudson, PJ, Newborn, D, Pugliese, A, Rizzoli, AP, Rosà, R, Rosso, F and Wilson, K (2002) Parasites and host population dynamics. In Hudson, PJ, Rizzoli, A, Grenfell, BT, Heesterbeek, H and Dobson, AP (eds), The Ecology of Wildlife Diseases. Oxford, UK: Oxford University Press, pp. 45–62.Google Scholar
Torgerson, PR, Devleesschauwer, B, Praet, N, Speybroeck, N, Willingham, AL, Kasuga, F, Rokni, MB, Zhou, X-N, Fèvre, EM, Sripa, B, Gargouri, N, Fürst, T, Budke, CM, Carabin, H, Kirk, MD, Angulo, FJ, Havelaar, A and de Silva, N (2015) World Health Organization estimates of the global and regional disease burden of 11 foodborne parasitic diseases, 2010: a data synthesis. PLoS Medicine 12, e1001920.Google Scholar
UNESCO Institute for Statistics (UIS) (2019) How much does your country invest in R&D? Available at http://uis.unesco.org/apps/visualisations/research-and-development-spending/.Google Scholar
Van Helden, P (2012) The cost of research in developing countries. EMBO Reports 13, 395.Google Scholar
Wang, L-D, Guo, J-G, Wu, X-H, Chen, H-G, Wang, T-P, Zhu, S-P, Zhang, Z-H, Steinmann, P, Yang, G-J, Wang, S-P, Wu, Z-D, Wang, L-Y, Hao, Y, Bergquist, R, Utzinger, J and Zhou, XN (2009) China's new strategy to block Schistosoma japonicum transmission: experiences and impact beyond schistosomiasis. Tropical Medicine & International Health 14, 1475–1483.Google Scholar
Weinstein, SB and Kuris, AM (2016) Independent origins of parasitism in Animalia. Biology Letters 12, 20160324.Google Scholar
Wickham, H (2016) ggplot2: Elegant Graphics for Data Analysis. New York: Springer-Verlag.Google Scholar
Windsor, DA (1998) Most of the species on Earth are parasites. International Journal for Parasitology 28, 1939–1941.Google Scholar
Wood, CL, Byers, JE, Cottingham, KL, Altman, I, Donahue, MJ and Blakeslee, AMH (2007) Parasites alter community structure. Proceedings of the National Academy of Sciences 104, 9335–9339.Google Scholar
World Bank (2019) Research and development expenditure. Available at https://data.worldbank.org/indicator/GB.XPD.RSDV.GD.ZS.Google Scholar
Zhou, P, Chen, Z, Li, H-L, Zheng, H, He, S, Lin, R-Q and Zhu, X-Q (2011) Toxoplasma gondii infection in humans in China. Parasites & Vectors 4, 165.Google Scholar
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