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Evolution of a costly immunity to cestode parasites is a pyrrhic victory

View ORCID ProfileJesse N. Weber, Natalie C. Steinel, Foen Peng, Kum Chuan Shim, Brian K. Lohman, Lauren Fuess, Stephen de Lisle, Daniel I. Bolnick
doi: https://doi.org/10.1101/2021.08.04.455160
Jesse N. Weber
1Department of Integrative Biology, University of Texas at Austin, Austin, TX 78712
2Department of Integrative Biology, University of Wisconsin-Madison, Madison, WI 53703
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  • ORCID record for Jesse N. Weber
  • For correspondence: jnweber2@wisc.edu
Natalie C. Steinel
1Department of Integrative Biology, University of Texas at Austin, Austin, TX 78712
3Department of Biological Sciences, University of Massachusetts Lowell, Lowell, MA 01854
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Foen Peng
4Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269
5Department of Biology, Haverford College, Haverford PA 19041
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Kum Chuan Shim
1Department of Integrative Biology, University of Texas at Austin, Austin, TX 78712
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Brian K. Lohman
1Department of Integrative Biology, University of Texas at Austin, Austin, TX 78712
6Eccles Institute of Human Genetics, Salt Lake City, UT, 84112
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Lauren Fuess
4Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269
7Department of Biology, Texas State University, San Marcos TX 78666
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Stephen de Lisle
4Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269
8Sölvegatan 37 Lund, 223 62 Sweden
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Daniel I. Bolnick
1Department of Integrative Biology, University of Texas at Austin, Austin, TX 78712
4Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT 06269
9Howard Hughes Medical Institute, Chevy Chase MD 02815
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Abstract

Parasites impose fitness costs on their hosts. Biologists therefore tend to assume that natural selection favors infection-resistant hosts. Yet, when the immune response itself is costly, theory suggests selection may instead favor loss of resistance. Immune costs are rarely documented in nature, and there are few examples of adaptive loss of resistance. Here, we show that when marine threespine stickleback colonized freshwater lakes they gained resistance to the freshwater-associated tapeworm, Schistocephalus solidus. Extensive peritoneal fibrosis and inflammation contribute to suppression of cestode growth and viability, but also impose a substantial cost of reduced fecundity. Combining genetic mapping and population genomics, we find that the immune differences between tolerant and resistant populations arise from opposing selection in both populations acting, respectively, to reduce and increase resistance consistent with divergent optimization.

One Sentence Summary Recently-evolved freshwater populations of stickleback frequently evolve increased resistance to tapeworms, involving extensive fibrosis that suppresses parasite growth; because this fibrosis greatly reduces fish fecundity, in some freshwater populations selection has favored an infection-tolerant strategy with fibrosis suppression.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
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Posted August 06, 2021.
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Evolution of a costly immunity to cestode parasites is a pyrrhic victory
Jesse N. Weber, Natalie C. Steinel, Foen Peng, Kum Chuan Shim, Brian K. Lohman, Lauren Fuess, Stephen de Lisle, Daniel I. Bolnick
bioRxiv 2021.08.04.455160; doi: https://doi.org/10.1101/2021.08.04.455160
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Evolution of a costly immunity to cestode parasites is a pyrrhic victory
Jesse N. Weber, Natalie C. Steinel, Foen Peng, Kum Chuan Shim, Brian K. Lohman, Lauren Fuess, Stephen de Lisle, Daniel I. Bolnick
bioRxiv 2021.08.04.455160; doi: https://doi.org/10.1101/2021.08.04.455160

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