Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-28T05:47:01.782Z Has data issue: false hasContentIssue false
  • English
  • Français

Phenotypic plasticity more essential to maintaining variation in host-attachment behaviour than evolutionary trade-offs in a facultatively parasitic mite

Published online by Cambridge University Press:  08 May 2019

Emily S. Durkin Open the ORCID record for Emily S. Durkin [Opens in a new window]  and
Lien T. Luong
Emily S. Durkin*
Affiliation:
Department of Biological Sciences, University of Alberta, CW405, Biological Sciences Bldg., Edmonton, Alberta T6G 2E9
Lien T. Luong
Affiliation:
Department of Biological Sciences, University of Alberta, CW405, Biological Sciences Bldg., Edmonton, Alberta T6G 2E9
*
Author for correspondence: Emily S. Durkin, E-mail: edurkin@ufl.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

A prevailing hypothesis for the evolution of parasitism posits that the fitness benefits gained from parasitic activity results in selection for and fixation of parasitic strategies. Despite the potential fitness advantage of parasitism, facultative parasites continue to exhibit genetic variation in parasitic behaviour in nature. We hypothesized that evolutionary trade-offs associated with parasitic host-attachment behaviour maintain natural variation observed in attachment behaviour. In this study, we used replicate lines of a facultatively parasitic mite, previously selected for increased host-attachment behaviour to test whether increased attachment trades off with mite fecundity and longevity, as well as the phenotypic plasticity of attachment. We also tested for potential correlated changes in mite morphology. To test for context-dependent trade-offs, mite fecundity and longevity were assayed in the presence or absence of a host. Our results show that selected and control mites exhibited similar fecundities, longevities, attachment plasticities and morphologies, which did not provide evidence for life history trade-offs associated with increased attachment. Surprisingly, phenotypic plasticity in attachment was maintained despite directional selection on the trait, which suggests that phenotypic plasticity likely plays an important role in maintaining attachment variation in natural populations of this facultative parasite.

Keywords

Drosophila hydeiectoparasitic miteinfection variationMacrocheles muscaedomesticaenegative genetic correlationparasite evolutionparasite life-historyphenotypic plasticity
Type
Research Article
Information
Parasitology , Volume 146 , Issue 10 , September 2019 , pp. 1289 - 1295
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abo-Taka, M, Heikal, H and Abd El-Raheem, A (2014) Macrochelid Mite, Macrocheles muscaedomesticae (Acarina: Macrochelidae) as a Biological Control Agent Against House Fly, Musca domestica (Diptera: Muscidae) in Egypt. International Journal of Zoological Research 10, 30–36.Google Scholar
Baldwin, JM (1896) A new factor in evolution. The American Naturalist 30, 441–451.Google Scholar
Birget, PLG, Repton, C, O'Donnell, AJ, Schneider, P and Reece, SE (2017) Phenotypic plasticity in reproductive effort: malaria parasites respond to resource availability. Proceedings of the Royal Society B: Biological Sciences 284, 20171229.Google Scholar
Boots, M (2011) The evolution of resistance to a parasite is determined by resources. The American Naturalist 178, 214–220.Google Scholar
Campbell, EO and Luong, LT (2016) Mite choice generates sex- and size-biased infection in Drosophila hydei. Parasitology 143, 787–793.Google Scholar
Castagnone-Sereno, P, Mulet, K and Iachia, C (2015) Tracking changes in life-history traits related to unnecessary virulence in a plant-parasitic nematode. Ecology and Evolution 5, 3677–3686.Google Scholar
Chamberlain, SA, Bronstein, JL and Rudgers, JA (2014) How context dependent are species interactions? Ecology Letters 17, 881–890.Google Scholar
Crispo, E (2007) The Baldwin effect and genetic assimilation: revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity. Evolution 61, 2469–2479.Google Scholar
Crossan, J, Paterson, S and Fenton, A (2007) Host availability and the evolution of parasite life-history strategies. Evolution 61, 675–684.Google Scholar
Darwin, C and Wallace, A (1858) On the tendency of species to form varieties. Zoological Journal of the Linnean Society 3, 45–62.Google Scholar
Dowling, APG (2015) The evolution of parasitism and host associations in mites. In Morand, S, Krasnov, BR and Littlewood, DTJ (ed.), Parasite Diversity and Diversification: Evolutionary Ecology Meets Phylogenetics. Cambridge, UK: Cambridge University Press, pp. 265–288.Google Scholar
Durkin, ES and Luong, LT (2018) Experimental evolution of infectious behaviour in a facultative ectoparasite. Journal of Evolutionary Biology 31, 362–370.Google Scholar
Farish, DJ and Axtell, RC (1971) Phoresy redefined and examined in Macrocheles muscaedomesticae (Acarina:Macrochelidae). Acarologia 13, 16–29.Google Scholar
Garland, T (2014) Trade-offs. Current Biology 24, R60–R61.Google Scholar
Gilbert, SF and Epel, D (2015) Ecological Developmental Biology, 2nd Edn. Sunderland, MA: Sinauer Associates.Google Scholar
Huang, W, Traulsen, A, Werner, B, Hiltunen, T and Becks, L (2017) Dynamical trade-offs arise from antagonistic coevolution and decrease intraspecific diversity. Nature Communications 8, 2059.Google Scholar
Jalil, M and Rodriguez, JG (1970) Studies of behavior of Macrocheles muscaedomesticae (Acarina: Macrochelidae) with emphasis on its attraction to the house fly. Annals of the Entomological Society of America 63, 738–744.Google Scholar
Kaltz, O and Koella, JC (2003) Host growth conditions regulate the plasticity of horizontal and vertical transmission in Holospora undulata, a bacterial parasite of the protozoan Paramecium caudatum. Evolution 57, 1535–1542.Google Scholar
Krantz, GW (1998) Reflections on the biology, morphology and ecology of the Macrochelidae. Experimental and Applied Acarology 22, 125–137.Google Scholar
Lagrue, C and Poulin, R (2009) Life cycle abbreviation in trematode parasites and the developmental time hypothesis: is the clock ticking? Journal of Evolutionary Biology 22, 1727–1738.Google Scholar
Leggett, HC, Benmayor, R, Hodgson, DJ and Buckling, A (2013) Experimental evolution of adaptive phenotypic plasticity in a parasite. Current Biology 23, 139–142.Google Scholar
Luong, LT and Polak, M (2007) Costs of resistance in the Drosophila-Macrocheles system: a negative genetic correlation between ectoparasite resistance and reproduction. Evolution 61, 1391–1402.Google Scholar
Luong, LT and Subasinghe, D (2017) A facultative ectoparasite attains higher reproductive success as a parasite than its free-living conspecifics. Experimental and Applied Acarology 71, 63–70.Google Scholar
Luong, LT, Penoni, LR, Horn, CJ and Polak, M (2015) Physical and physiological costs of ectoparasitic mites on host flight endurance. Ecological Entomology 40, 518–524.Google Scholar
Luong, LT, Brophy, T, Stolz, E and Chan, SJ (2017) State-dependent parasitism by a facultative parasite of fruit flies. Parasitology 144, 1468–1475.Google Scholar
Lynch, M and Gabriel, W (1987) Environmental tolerance. American Naturalist 129, 283–303.Google Scholar
Manning, MJ and Halliday, RB (1994) Biology and reproduction of some Australian species of Macrochelidae. Australian Entomology 21, 89–94.Google Scholar
Nussey, DH, Postma, E, Gienapp, P and Visser, ME (2005) Evolution: selection on heritable phenotypic plasticity in a wild bird population. Science 310, 304–306.Google Scholar
Paterson, S and Barber, R (2007) Experimental evolution of parasite life-history traits in Strongyloides ratti (Nematoda). Proceedings of the Royal Society B 274, 1467–1474.Google Scholar
Pigliucci, M (2006) Phenotypic plasticity and evolution by genetic assimilation. Journal of Experimental Biology 209, 2362–2367.Google Scholar
Poulin, R (1995) Evolution of parasite life history traits: myths and reality. Parasitology Today 11, 342–345.Google Scholar
Poulin, R (2001) Progenesis and reduced virulence as an alternative transmission strategy in a parasitic trematode. Parasitology 123, 623–630.Google Scholar
Poulin, R (2007) Evolutionary Ecology of Parasites. Princeton, NJ: Princeton University Press.Google Scholar
Poulin, R and Morand, S (1997) Parasite body size distributions: interpreting patterns of skewness. International Journal for Parasitology 27, 959–964.Google Scholar
R Core Team (2017) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org.Google Scholar
Reece, SE, Ramiro, RS and Nussey, DH (2009) Plastic parasites: sophisticated strategies for survival and reproduction? Evolutionary Applications 2, 11–23.Google Scholar
Renaud, F, Clayton, D and De Meeos, T (1996) Biodiversity and evolution in host-parasite associations. Biodiversity and Conservation 5, 963–974.Google Scholar
Rothschild, M and Clay, T (1953) Fleas, Flukes and Cuckoos: A Study of Bird Parasites. London: Collins.Google Scholar
Scheiner, SM and Lyman, RF (1991) The genetics of phenotypic plasticity. II. Response to selection. Journal of Evolutionary Biology 4, 23–50.Google Scholar
Schlichting, CD and Pigliucci, M (1993) Control of phenotypic plasticity. American Naturalist 142, 366–370.Google Scholar
Schmid-Hempel, P (2013) Evolutionary Parasitology: The Integrated Study of Infections, Immunology, Ecology and Genetics. Oxford, UK: Oxford University Press.Google Scholar
Searle, CL, Ochs, JH, Caceres, CE, Chiang, SL, Gerardo, NM, Hall, SR and Duffy, MA (2015) Plasticity, not genetic variation, drives infection success of a fungal parasite. Parasitology 142, 839–848.Google Scholar
Sgrò, C and Hoffmann, A (2004) Genetic correlations, tradeoffs and environmental variation. Heredity 93, 241–248.Google Scholar
Stankiewicz, M (1996) Observations on the biology of free-living stages of parastrongyloides trichosuri (Nematoda, Rhabditoidea). Acta Parasitologica 41, 38–42.Google Scholar
Stasiuk, SJ, Scott, MJ and Grant, WN (2012) Developmental plasticity and the evolution of parasitism in an unusual nematode, Parastrongyloides trichosuri. EvoDevo 3, 1–14.Google Scholar
Stearns, SC (1992) The Evolution of Life Histories. Oxford, UK: Oxford University Press.Google Scholar
Suzuki, Y and Nijhout, F (2006) Evolution of a polyphenism by genetic accommodation. Science 311, 650–652.Google Scholar
Thomas, F, Brown, SP, Sukhdeo, M and Renaud, F (2002) Understanding parasite strategies: a state-dependent approach? Trends in Parasitology 18, 387–390.Google Scholar
Valladares, F, Sanchez-Gomez, D and Zavala, MA (2006) Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. Journal of Ecology 94, 1103–1116.Google Scholar
Waddington, CH (1942) Canalization of development and the inheritance of acquired characters. Nature 150, 563–565.Google Scholar
Wade, C (1961) Life history of Macrocheles muscaedomesticae (Acarina: Macrochelidae), a predator of the house fly. Annals of the Entomological Society of America 54, 776–781.Google Scholar
Supplementary material: File

Durkin and Luong supplementary material

Durkin and Luong supplementary material 1

Download Durkin and Luong supplementary material(File)
File 423.9 KB