Folia Parasitologica 63:039 (2016) | DOI: 10.14411/fp.2016.039

A new R package and web application for detecting bilateral asymmetry in parasitic infections

Matthew T. Wayland1, James C. Chubb2
1 Department of Zoology, University of Cambridge, Cambridge, UK;
2 Department of Evolution, Ecology and Behaviour, Institute of Integrative Biology, University of Liverpool, Liverpool, UK

When parasites invade paired structures of their host non-randomly, the resulting asymmetry may have both pathological and ecological significance. To facilitate the detection and visualisation of asymmetric infections we have developed a free software tool, Analysis of Symmetry of Parasitic Infections (ASPI). This tool has been implemented as an R package (https://cran.r-project.org/package=aspi) and a web application (https://wayland.shinyapps.io/aspi). ASPI can detect both consistent bias towards one side, and inconsistent bias in which the left side is favoured in some hosts and the right in others. Application of ASPI is demonstrated using previously unpublished data on the distribution of metacercariae of species of Diplostomum von Nordmann, 1832 in the eyes of ruffe Gymnocephalus cernua (Linnaeus). Invasion of the lenses appeared to be random, with the proportion of metacercariae in the left and right lenses showing the pattern expected by chance. However, analysis of counts of metacercariae from the humors, choroid and retina revealed asymmetry between eyes in 38% of host fish.

Keywords: bilateral asymmetry, Trematoda, Diplostomum, fish, Gymnocephalus cernua, ruffe, software, statistical analysis

Received: July 3, 2016; Accepted: October 10, 2016; Published online: November 10, 2016  Show citation

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Wayland, M.T., & Chubb, J.C. (2016). A new R package and web application for detecting bilateral asymmetry in parasitic infections. Folia Parasitologica63, Article 2016.039. https://doi.org/10.14411/fp.2016.039


This article contains supporting information (Tables S1-S3) online at http://folia.paru.cas.cz/suppl/2016-63-039.pdf

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References

  1. Benjamini Y., Hochberg Y. 1995: Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. Roy. Stat. Soc. B 57: 289-300. Go to original source...
  2. Buchmann K. 1988: Spatial distribution of Pseudodactylogyrus anguillae and P. bini (Monogenea) on the gills of the European eel, Anguilla anguilla. J. Fish Biol. 32: 801-802. Go to original source...
  3. Chang W., Cheng J., Allaire J.J., Xie Y., McPherson J. 2016: shiny: Web Application Framework for R. R package version 0.13.2. https://CRAN.R-project.org/package=shiny
  4. Dorovskikh G.N. 1997: [Results of the study of fishes' parasites in river basins of the north-east of the European part of Russia. Trematodes (Trematoda).] Parazitologiya 21: 551-564. (In Russian.)
  5. Dwyer W.P., Smith C.E. 1989: Metacercariae of Diplostomum spathaceum in the eyes of fishes from Yellowstone Lake, Wyoming. J. Wildlife Dis. 25: 126-129. Go to original source... Go to PubMed...
  6. Dzika E. 1999: Microhabitats of Pseudodactylogyrus anguillae and P. bini (Monogenea: Dactylogyridae) on the gills of large-size European eel Anguilla anguilla from Lake Gaj, Poland. Folia Parasitol. 46: 33-36.
  7. Faulkner M. 1989: The application of sodium dodecyl sulphate-polyacrylamide gel electrophoresis to the taxonomic identification of the total body protein band profiles of Diplostomum spp. metacercariae (Digenea), parasites of fish eyes. Electrophoresis 10: 260-264. Go to original source... Go to PubMed...
  8. Georgieva S., Soldánová M., Pérez-del-Olmo A., Dangel D.R., Sitko J., Sures B., Kostadinova A. 2013: Molecular prospecting for European Diplostomum (Digenea: Diplostomidae) reveals cryptic diversity. Int. J. Parasitol. 43: 57-72. Go to original source... Go to PubMed...
  9. Graczyk T. 1991: Cases of bilateral asymmetry of Diplostomum pseudospathaceum Niewiadomska, 1984 metacercariae infections (Trematoda, Diplostomidae) in the eye lens of fish. Acta Parasitol. Pol. 36: 131-134.
  10. Graham J.H., Raz S., Hel-Or H., Nevo E. 2010: Fluctuating asymmetry: methods, theory and applications. Symmetry 2: 466-540. Go to original source...
  11. Holm S. 1979: A simple sequentially rejective multiple test procedure. Scand. J. Statistics 6: 65-70.
  12. Johnson P.T.J., Koprivnikar J., Orlofske S.A., Melbourne B.A., Lafonte B.E. 2014: Making the right choice: testing the drivers of asymmetric infections within hosts and their consequences for pathology. Oikos 123: 875-885. Go to original source...
  13. Karvonen A, Seppala O. 2008: Eye fluke infection and lens size reduction in fish: a quantitative analysis. Dis. Aquat. Org. 80: 21-26. Go to original source... Go to PubMed...
  14. Kearn G.C. 1984: The migration of the monogenean Entobdella soleae on the surface of its host, Solea solea. Int. J. Parasitol. 14: 63-69. Go to original source...
  15. King J.C., Dubay S.A., Huspeni T.C., VanLanen A.R., Gerhold R.W. 2010: Parasite infections in nestling red-shouldered hawks (Buteo lineatus) in northeast Wisonsin. J. Parasitol. 96: 535-540. Go to original source... Go to PubMed...
  16. Locke S.A., Al-Nasiri F.S., Caffara M., Drago F., Kalbe M., Lapierre A.R., McLaughlin J.D., Nie P., Overstreet R.M., Souza G.T., Takemoto R.M., Marcogliese D.J. 2015: Diversity, specificity and speciation in larval Diplostomidae (Platyhelminthes: Digenea) in the eyes of freshwater fish, as revealed by DNA barcodes. Int. J. Parasitol. 45: 841-855. Go to original source... Go to PubMed...
  17. McDonald J.H. 2014: Handbook of Biological Statistics. Third Edition. Sparky House Publishing, Baltimore, Maryland, 299 pp.
  18. R Core Team 2016. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, https://www.R-project.org/.
  19. Rau M.E., Gordon D.M., Curtis M.A. 1979: Bilateral asymmetry of Diplostomum infections in the eyes of lake whitefish Coregonus clupeaformis (Mitchell) and a computer simulation of the observed metacercarial distribution. J. Fish Dis. 2: 291-297. Go to original source...
  20. Rintamäki-Kinnunen P.A., Karvonen A., Anttila P., Valtonen E.T. 2004: Diplostomum spathaceum metacercarial infection and colour change in salmonid fish. Parasitol. Res. 93: 51-55. Go to original source... Go to PubMed...
  21. Rodrigues A.A., Saraiva A. 1996: Spatial distribution & seasonality of Pseudodactylogyrus anguillae & P. bini (Monogenea: Pseudodactylogyridae) on the gills of the European eel Anguilla anguilla from Portugal. Bull. Eur. Ass. Fish Pathol. 16: 85-88.
  22. Shigin A. A. 1986: [Trematode Fauna of USSR. Genus Diplostomum, metacercariae.] Nauka, Moscow, 253 pp. (In Russian.)
  23. Sokal R.R., Rohlf F.J. 1995: Biometry: the Principles and Practice of Statistics in Biological Research. Third Edition. Freeman, New York, 887 pp.
  24. Stumbo A.D., Poulin R. 2016: Possible mechanism of host manipulation resulting from a diel behaviour pattern of eye-dwelling parasites? Parasitology 143: 1261-1267. Go to original source... Go to PubMed...