TY - JOUR
T1 - Variation in Immune Defense Shapes Disease Outcomes in Laboratory and Wild Daphnia
AU - Stewart Merrill, Tara E.
AU - Hall, Spencer R.
AU - Merrill, Loren
AU - Cáceres, Carla E.
N1 - Funding Information:
This material is based upon work supported by the National Science Foundation under Grant Numbers DGE 1144245 (awarded to T.E.S.M.), DGE 1069157 (awarded to Andrew Suarez), NSF 1354407 and 1655665 (awarded to C.E.C.), NSF 1701515 (awarded to T.E.S.M. and C.E.C.), and NSF 1655656 (awarded to S.R.H.). Any opinion, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation.
Funding Information:
Thanks to Grace Abernathy Pixton whose undergraduate thesis provided insight on the importance of the Daphnia gut for infection. The authors thank the Divisions of Ecoimmunology and Disease Ecology, Comparative Endocrinology, Animal Behavior, and Ecology and Evolution of the Society for Integrative and Comparative Biology as well as the Macroecology of Infectious Disease Research Coordination Network (NSF DEB 1316223) for financial support of the symposium “The Scale of Sickness: How Immune Variation across Space and Species Affects Infectious Disease Dynamics.” Thanks also to symposium organizers D. Becker, C. Downs, L. Martin, and L. Schoenle.
Publisher Copyright:
© 2019 The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved.
PY - 2019/11/1
Y1 - 2019/11/1
N2 - Host susceptibility may be critical for the spread of infectious disease, and understanding its basis is a goal of ecological immunology. Here, we employed a series of mechanistic tests to evaluate four factors commonly assumed to influence host susceptibility: parasite exposure, barriers to infection, immune responses, and body size. We tested these factors in an aquatic host-parasite system (Daphnia dentifera and the fungal parasite, Metschnikowia bicuspidata) using both laboratory-reared and field-collected hosts. We found support for each factor as a driver of infection. Elevated parasite exposure, which occurs through consumption of infectious fungal spores, increased a host's probability of infection. The host's gut epithelium functioned as a barrier to infection, but in the opposite manner from which we predicted: thinner anterior gut epithelia were more resistant to infectious spores than thick epithelia. This relationship may be mediated by structural attributes associated with epithelial cell height. Fungal spores that breached the host's gut barrier elicited an intensity-dependent hemocyte response that decreased the probability of infection for some Daphnia. Although larger body sizes were associated with increased levels of spore ingestion, larger hosts also had lower frequencies of parasite attack, less penetrable gut barriers, and stronger hemocyte responses. After investigating which mechanisms underlie host susceptibility, we asked: do these four factors contribute equally or asymmetrically to the outcome of infection? An information-theoretic approach revealed that host immune defenses (barriers and immune responses) played the strongest roles in mediating infection outcomes. These two immunological traits may be valuable metrics for linking host susceptibility to the spread of infectious disease.
AB - Host susceptibility may be critical for the spread of infectious disease, and understanding its basis is a goal of ecological immunology. Here, we employed a series of mechanistic tests to evaluate four factors commonly assumed to influence host susceptibility: parasite exposure, barriers to infection, immune responses, and body size. We tested these factors in an aquatic host-parasite system (Daphnia dentifera and the fungal parasite, Metschnikowia bicuspidata) using both laboratory-reared and field-collected hosts. We found support for each factor as a driver of infection. Elevated parasite exposure, which occurs through consumption of infectious fungal spores, increased a host's probability of infection. The host's gut epithelium functioned as a barrier to infection, but in the opposite manner from which we predicted: thinner anterior gut epithelia were more resistant to infectious spores than thick epithelia. This relationship may be mediated by structural attributes associated with epithelial cell height. Fungal spores that breached the host's gut barrier elicited an intensity-dependent hemocyte response that decreased the probability of infection for some Daphnia. Although larger body sizes were associated with increased levels of spore ingestion, larger hosts also had lower frequencies of parasite attack, less penetrable gut barriers, and stronger hemocyte responses. After investigating which mechanisms underlie host susceptibility, we asked: do these four factors contribute equally or asymmetrically to the outcome of infection? An information-theoretic approach revealed that host immune defenses (barriers and immune responses) played the strongest roles in mediating infection outcomes. These two immunological traits may be valuable metrics for linking host susceptibility to the spread of infectious disease.
UR - http://www.scopus.com/inward/record.url?scp=85069198862&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85069198862&partnerID=8YFLogxK
U2 - 10.1093/icb/icz079
DO - 10.1093/icb/icz079
M3 - Article
C2 - 31141120
AN - SCOPUS:85069198862
SN - 1540-7063
VL - 59
SP - 1203
EP - 1219
JO - Integrative and comparative biology
JF - Integrative and comparative biology
IS - 5
ER -