Host genetic variation in feeding rate mediates a fecundity cost of parasite resistance in a Daphnia-parasite system

Organisms face numerous challenges over their lifetimes, including from competitors and parasites, and experience selection to maximise their fitness in the face of these various pressures. However, selection can rarely maximise individual ability to cope with all challenges, and trade-offs therefore emerge. One such trade-off is the cost of resisting parasitic infection, whereby hosts that have a high intrinsic capacity to resist parasitic infection have comparatively low fitness in the absence of the parasite, and spatio-temporal variation in the relative strength of parasite- and non parasite-mediated selection is thought to maintain diversity in host resistance. Here, we test for, and find, a simple cost of resistance in the freshwater host Daphnia magna and its sterilising bacterial parasite, Pasteuria ramosa that is shaped by ecology as opposed to immunity. We uncovered significant genetic variation in Daphnia feeding rate, and show that rapid-feeding Daphnia genotypes have high fecundity in the absence of the parasite, but are more likely to go on to suffer sterilising infection when exposed to the parasite. This feeding rate-mediated cost of resistance can explain the persistence of parasite-susceptible genotypes. Further, we found evidence of infection induced anorexia in Pasteuria-infected hosts. It follows that reduced feeding in infected hosts means that high parasite prevalence could result in greater host food availability; this could reduce intra-specific competition and mask the cost of resistance in nature. Summary statement Costs of Daphnia immunity to a sterilising bacterial parasite are mediated by feeding ecology and not immunity, and infection-induced anorexia can further alter the relative strength of parasitism and host-host competition.

[1]  M. Shocket,et al.  A paradox of parasite resistance: Disease-driven trophic cascades increase the cost of resistance, selecting for lower resistance with parasites than without them , 2021, bioRxiv.

[2]  S. Auld,et al.  Simulated climate change, epidemic size, and host evolution across host–parasite populations , 2017, Global change biology.

[3]  T. Day,et al.  Starvation reveals the cause of infection-induced castration and gigantism , 2014, Proceedings of the Royal Society B: Biological Sciences.

[4]  J. Kubanek,et al.  Poor resource quality lowers transmission potential by changing foraging behaviour , 2014 .

[5]  M. Duffy,et al.  Variation in costs of parasite resistance among natural host populations , 2013, Journal of evolutionary biology.

[6]  T. Little,et al.  Fecundity compensation and tolerance to a sterilizing pathogen in Daphnia , 2012, Journal of evolutionary biology.

[7]  S. Verhulst,et al.  Trade-off between growth and immune function: a meta-analysis of selection experiments , 2011 .

[8]  T. Little,et al.  Successfully resisting a pathogen is rarely costly in Daphnia magna , 2010, BMC Evolutionary Biology.

[9]  M. Duffy,et al.  Variation in Resource Acquisition and Use among Host Clones Creates Key Epidemiological Trade‐Offs , 2010, The American Naturalist.

[10]  N. Gerardo,et al.  Aphid reproductive investment in response to mortality risks , 2010, BMC Evolutionary Biology.

[11]  David S Schneider,et al.  The Role of Anorexia in Resistance and Tolerance to Infections in Drosophila , 2009, PLoS biology.

[12]  B. Lazzaro,et al.  Immunity in a variable world , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[13]  D. Ebert Host-parasite coevolution: Insights from the Daphnia-parasite model system. , 2008, Current opinion in microbiology.

[14]  D. Ebert,et al.  A quantitative test of the relationship between parasite dose and infection probability across different host–parasite combinations , 2008, Proceedings of the Royal Society B: Biological Sciences.

[15]  T. Little,et al.  A parasite-mediated life-history shift in Daphnia magna , 2005, Proceedings of the Royal Society B: Biological Sciences.

[16]  E. Decaestecker,et al.  The Evolution of Virulence When Parasites Cause Host Castration and Gigantism , 2004, The American Naturalist.

[17]  D. Ebert,et al.  Within–and between–population variation for resistance of Daphnia magna to the bacterial endoparasite Pasteuria ramosa , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[18]  H. Godfray,et al.  Trade–off associated with selection for increased ability to resist parasitoid attack in Drosophila melanogaster , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[19]  H. Godfray,et al.  Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster , 1997, Nature.

[20]  B. Sheldon,et al.  Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. , 1996, Trends in ecology & evolution.

[21]  Hans Toni Ratte,et al.  ADaM, an artificial freshwater for the culture of zooplankton , 1994 .

[22]  Paul H. Harvey,et al.  The evolution of virulence , 1993, Nature.

[23]  J. T. Jones,et al.  Increased oviposition and growth in immature Biomphalaria glabrata after exposure to Schistosoma mansoni , 1986, Parasitology.

[24]  B. Burnet,et al.  Genetic analysis of larval feeding behaviour in Drosophila melanogaster. , 1974, Genetical research.

[25]  S. Auld Immunology and Immunity , 2014 .

[26]  P. Schmid-Hempel,et al.  On the evolutionary ecology of specific immune defence , 2003 .

[27]  Steven A. Frank,et al.  Immunology and Evolution of Infectious Disease , 2002 .