Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-19T06:25:23.651Z Has data issue: false hasContentIssue false

The role of spore morphology in horizontal transmission of a microsporidium of Daphnia

Published online by Cambridge University Press:  16 March 2018

Hadas Urca
Affiliation:
School of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv 6997801, Israel
Frida Ben-Ami*
Affiliation:
School of Zoology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv 6997801, Israel
*
Author for correspondence: Frida Ben-Ami, E-mail: [email protected]

Abstract

The microsporidian parasite Hamiltosporidium tvaerminnensis can infect Daphnia magna both horizontally (through environmental spores) and vertically (through parthenogenetic and sexually produced eggs). The spores of H. tvaerminnensis come in three distinguishable morphologies, which are thought to have different roles in the transmission of the parasite. In this study, we examined the role of the two most common spore morphologies (i.e. oval-shaped spores and pear-shaped spores) in horizontal transmission of H. tvaerminnensis. To this end, we infected hosts with solutions consisting of either mostly oval- or mostly pear-shaped spores, and quantified infection rates, parasite-induced host mortality and mean number of parasite spores produced per host. We found that spore morphology by itself did not influence infection rates and parasite-induced host mortality. Instead, host clone and parasite isolate interacted with spore morphology in shaping infection outcome and mortality. Thus, there appear to be strong genotype-by-genotype (G × G) interactions in this system. While there is no dispute that H. tvaerminnensis can transmit both vertically and horizontally, our findings do not support theoretical predictions that different spore morphologies hold different roles in horizontal transmission of H. tvaerminnensis.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

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

Agnew, P and Koella, JC (1999) Life history interactions with environmental conditions in a host–parasite relationship and the parasite's mode of transmission. Evolutionary Ecology 13(1), 6791.Google Scholar
Antonovics, J, Wilson, AJ, Forbes, MR, Hauffe, HC, Kallio, ER, Leggett, HC, Longdon, B, Okamura, B, Sait, SM and Webster, JP (2017) The evolution of transmission mode. Philosophical Transactions of the Royal Society of London B: Biological Sciences 372(1719), 20160083.Google Scholar
Ben-Ami, F and Routtu, J (2013) The expression and evolution of virulence in multiple infections: the role of specificity, relative virulence and relative dose. BMC Evolutionary Biology 13, 97.Google Scholar
Ben-Ami, F, Mouton, L and Ebert, D (2008 a) The effects of multiple infections on the expression and evolution of virulence in a Daphnia-endoparasite system. Evolution 62(7), 17001711.Google Scholar
Ben-Ami, F, Regoes, RR and Ebert, D (2008 b) A quantitative test of the relationship between parasite dose and infection probability across different host–parasite combinations. Proceedings of the Royal Society of London B: Biological Sciences 275(1636), 853859.Google Scholar
Ben-Ami, F, Ebert, D and Regoes, RR (2010) Pathogen dose infectivity curves as a method to analyze the distribution of host susceptibility: a quantitative assessment of maternal effects after food stress and pathogen exposure. American Naturalist 175(1), 106115.Google Scholar
Carius, HJ, Little, TJ and Ebert, D (2001) Genetic variation in a host-parasite association: potential for coevolution and frequency-dependent selection. Evolution 55(6), 11361145.Google Scholar
Decaestecker, E, Declerck, S, De Meester, L and Ebert, D (2005) Ecological implications of parasites in natural Daphnia populations. Oecologia 144(3), 382390.Google Scholar
Duneau, D, Luijckx, P, Ben-Ami, F, Laforsch, C and Ebert, D (2011) Resolving the infection process reveals striking differences in the contribution of environment, genetics and phylogeny to host-parasite interactions. BMC Biology 9, 11.Google Scholar
Dunn, AM and Smith, JE (2001) Microsporidian life cycles and diversity: the relationship between virulence and transmission. Microbes and Infection 3(5), 381388.Google Scholar
Dunn, AM, Terry, RS and Smith, JE (2001) Transovarial transmission in the microsporidia. Advances in Parasitology 48, 57100.Google Scholar
Ebert, D (2013) The epidemiology and evolution of symbionts with mixed-mode transmission. Annual Review of Ecology, Evolution, and Systematics 44, 623643.Google Scholar
Ebert, D, Zschokke-Rohringer, CD and Carius, HJ (2000) Dose effects and density-dependent regulation of two microparasites of Daphnia magna. Oecologia 122(2), 200209.Google Scholar
Fine, PE (1975) Vectors and vertical transmission: an epidemiologic perspective. Annals of the New York Academy of Sciences 266(1), 173194.Google Scholar
Frank, SA (1996) Models of parasite virulence. Quarterly Review of Biology 71(1), 3778.Google Scholar
Goren, L and Ben-Ami, F (2013) Ecological correlates between cladocerans and their endoparasites from permanent and rain pools: patterns in community composition and diversity. Hydrobiologia 701(1), 1323.Google Scholar
Green, J (1974) Parasites and epibionts of Cladocera. The Transactions of the Zoological Society of London 32(6), 417515.Google Scholar
Haag, KL, Larsson, JR, Refardt, D and Ebert, D (2011) Cytological and molecular description of Hamiltosporidium tvaerminnensis gen. et sp. nov., a microsporidian parasite of Daphnia magna, and establishment of Hamiltosporidium magnivora comb. nov. Parasitology 138(4), 447462.Google Scholar
Haine, ER (2008) Symbiont-mediated protection. Proceedings of the Royal Society of London B: Biological Sciences 275(1633), 353361.Google Scholar
Hall, MD and Ebert, D (2012) Disentangling the influence of parasite genotype, host genotype and maternal environment on different stages of bacterial infection in Daphnia magna. Proceedings of the Royal Society of London B: Biological Sciences 279(1741), 31763183.Google Scholar
Ironside, JE, Smith, JE, Hatcher, MJ and Dunn, AM (2011) Should sex-ratio distorting parasites abandon horizontal transmission? BMC Evolutionary Biology 11, 370.Google Scholar
Iwano, H and Ishihara, R (1991) Dimorphism of spores of Nosema spp. in cultured cell. Journal of Invertebrate Pathology 57(2), 211219.Google Scholar
Iwano, H and Kurtti, TJ (1995) Identification and isolation of dimorphic spores from Nosema furnacalis (Microspora: Nosematidae). Journal of Invertebrate Pathology 65(3), 230236.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(7), 15351542.Google Scholar
Keeling, PJ and Fast, NM (2002) Microsporidia: biology and evolution of highly reduced intracellular parasites. Annual Review of Microbiology 56, 93116.Google Scholar
Koella, J, Agnew, P and Michalakis, Y (1998) Coevolutionary interactions between host life histories and parasite life cycles. Parasitology 116(S1), S47S55.Google Scholar
Lipsitch, M and Moxon, ER (1997) Virulence and transmissibility of pathogens: what is the relationship? Trends in Microbiology 5(1), 3137.Google Scholar
Lipsitch, M, Siller, S and Nowak, MA (1996) The evolution of virulence in pathogens with vertical and horizontal transmission. Evolution 50(5), 17291741.Google Scholar
Luijckx, P, Ben-Ami, F, Mouton, L, Du Pasquier, L and Ebert, D (2011) Cloning of the unculturable parasite Pasteuria ramosa and its Daphnia host reveals extreme genotype–genotype interactions. Ecology Letters 14(2), 125131.Google Scholar
Messenger, SL, Molineux, IJ and Bull, J (1999) Virulence evolution in a virus obeys a trade off. Proceedings of the Royal Society of London B: Biological Sciences 266(1417), 397404.Google Scholar
Refardt, D and Rainey, PB (2010) Tuning a genetic switch: experimental evolution and natural variation of prophage induction. Evolution 64(4), 10861097.Google Scholar
Regoes, RR, Ebert, D and Bonhoeffer, S (2002) Dose-dependent infection rates of parasites produce the Allee effect in epidemiology. Proceedings of the Royal Society of London B: Biological Sciences 269(1488), 271279.Google Scholar
Restif, O and Kaltz, O (2006) Condition-dependent virulence in a horizontally and vertically transmitted bacterial parasite. Oikos 114(1), 148158.Google Scholar
Stewart, AD, Logsdon, JM and Kelley, SE (2005) An empirical study of the evolution of virulence under both horizontal and vertical transmission. Evolution 59(4), 730739.Google Scholar
Stewart, FM and Levin, BR (1984) The population biology of bacterial viruses: why be temperate. Theoretical Population Biology 26(1), 93117.Google Scholar
Tintjer, T, Leuchtmann, A and Clay, K (2008) Variation in horizontal and vertical transmission of the endophyte Epichloe elymi infecting the grass Elymus hystrix. New Phytologist 179(1), 236246.Google Scholar
Turner, PE, Cooper, VS and Lenski, RE (1998) Tradeoff between horizontal and vertical modes of transmission in bacterial plasmids. Evolution 52(2), 315329.Google Scholar
Vávra, J and Lukeš, J (2013) Microsporidia and ‘the art of living together’. Advances in Parasitology 82, 253319.Google Scholar
Vizoso, DB and Ebert, D (2004) Within-host dynamics of a microsporidium with horizontal and vertical transmission: Octosporea bayeri in Daphnia magna. Parasitology 128(1), 3138.Google Scholar
Vizoso, DB, Lass, S and Ebert, D (2005) Different mechanisms of transmission of the microsporidium Octosporea bayeri: a cocktail of solutions for the problem of parasite permanence. Parasitology 130(5), 501509.Google Scholar
Williams, BAP (2009) Unique physiology of host–parasite interactions in microsporidia infections. Cellular Microbiology 11(11), 15511560.Google Scholar