Macroevolutionary foundations of a recently evolved innate immune defense

. 2021 Oct ; 75 (10) : 2600-2612. [epub] 20210815

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, Research Support, U.S. Gov't, Non-P.H.S.

Perzistentní odkaz   https://www.medvik.cz/link/pmid34347301

Grantová podpora
R01 AI123659 NIAID NIH HHS - United States

Antagonistic interactions between hosts and parasites may drive the evolution of novel host defenses, or new parasite strategies. Host immunity is therefore one of the fastest evolving traits. But where do the novel immune traits come from? Here, we test for phylogenetic conservation in a rapidly evolving immune trait-peritoneal fibrosis. Peritoneal fibrosis is a costly defense against a specialist tapeworm, Schistocephalus solidus (Cestoda), expressed in some freshwater populations of threespine stickleback fish (Gasterosteus aculeatus, Perciformes). We asked whether stickleback fibrosis is a derived species-specific trait or an ancestral immune response that was widely distributed across ray-finned fish (Actinopterygii) only to be employed by threespine stickleback against the specialist parasite. We combined literature review on peritoneal fibrosis with a comparative experiment using either parasite-specific, or nonspecific, immune challenge in deliberately selected species across fish tree of life. We show that ray-finned fish are broadly, but not universally, able to induce peritoneal fibrosis when challenged with a generic stimulus (Alum adjuvant). The experimental species were, however, largely indifferent to the tapeworm antigen homogenate. Peritoneal fibrosis, thus, appears to be a common and deeply conserved fish immune response that was co-opted by stickleback to adapt to a new selective challenge.

Zobrazit více v PubMed

Abdelsalam, M. , Abdel‐Gaber R., Mahmoud M. A., Mahdy O. A., Khafaga N. I. M., and Warda M.. 2016. Morphological, molecular and pathological appraisal of Callitetrarhynchus gracilis plerocerci (Lacistorhynchidae) infecting Atlantic little tunny (Euthynnus alletteratus) in Southeastern Mediterranean. J. Adv. Res. 7:317–326. PubMed PMC

Allen, J. E. , and Maizels R. M.. 2011. Diversity and dialogue in immunity to helminths. Nat. Rev. Immunol. 11:375–388. PubMed

Arme, C. , and Owen R. W.. 1967. Infections of the three‐spined stickleback, Gasterosteus aculeatus L., with the plerocercoid larvae of Schistocephalus solidus (Müller, 1776), with special reference to pathological effects. Parasitology 57:301–314. PubMed

Barber, I. , and Scharsack J. P.. 2010. The three‐spined stickleback‐Schistocephalus solidus system: an experimental model for investigating host‐parasite interactions in fish. Parasitology 137:411–424. PubMed

Colquhoun, D. J. , Skjerve E., and Poppe T. T.. 1998. Pseudomonas fluorescens, infectious pancreatic necrosis virus and environmental stress as potential factors in the development of vaccine related adhesions in Atlantic Salmon, Salmo salar L. J. Fish Dis. 21:355–364.

Christensen, R. H. B. 2019. ordinal ‐ regression models for ordinal data. R package version 2019.12‐10. Available via https://CRAN.R‐project.org/package=ordinal.

De Lisle, S. P. , and Bolnick D. I.. 2021. Male and female reproductive fitness costs of an immune response in natural populations. Evolution. 10.1111/evo.14266. PubMed DOI PMC

Flajnik, M. F. , and Du Pasquier L.. 2004. Evolution of innate and adaptive immunity: can we draw a line? Trends Immunol. 25:640–644. PubMed

Fuess, L. , Weber J. N., Den Haan S., Steinel N. C., Shim K. C., and Bolnick D. I.. 2020. A test of the Baldwin Effect: differences in both constitutive expression and inducible responses to parasites underlie variation in host response to a parasite. bioRxiv. 10.1101/2020.07.29.216531. DOI

Gause, W. C. , Wynn T. A., and Allen J. E.. 2013. Type 2 immunity and wound healing: evolutionary refinement of adaptive immunity by helminths. Nat. Rev. Immunol. 13:607–614. PubMed PMC

Herpin, A. , Lelong C., and Favrel P.. 2004. Transforming growth factor‐β‐related proteins: an ancestral and widespread superfamily of cytokines in metazoans. Dev. Comp. Immunol. 28:461–485. PubMed

Hoffman, G. L. 1975. Lesions due to internal helminths of freshwater fishes. Pp. 151–188 in Ribelin W. E. and Migaki G., eds. The pathology of fishes. Univ. of Wisconsin Press, Madison, WI.

Hughes, L. C. , Ortí G., Huang Y., Sun Y., Baldwin C. C., Thompson A. W., Arcila D., Betancur‐Rodriguez R., Li C., Becker L., et al. 2018. Comprehensive phylogeny of ray‐finned fishes (Actinopterygii) based on transcriptomic and genomic data. Proc. Natl. Acad. Sci. USA 115:6249–6254. PubMed PMC

Hund, A. K. , Fuess L. E., Kenney M. L., Maciejewski M. F., Marini J. M., Shim K. C., and Bolnick D. I.. 2020. Rapid evolution of parasite resistance via improved recognition and accelerated immune activation and deactivation. bioRxiv. 10.1101/2020.07.03.186569. DOI

Kool, M. , Fierens K., and Lambrecht B. N.. 2012. Alum adjuvant: some of the tricks of the oldest adjuvant. J. Med. Microbiol. 61:927–934. PubMed

Lazzaro, B. , and Clark A.. 2012. Rapid evolution of innate immune response genes. Pp. 203–222 in Singh R. S., Xu J., and Kulathinal R. J., eds. Rapidly evolving genes and genetic systems. Oxford Univ. Press, Oxford, U.K.

Litman, G. W. , and Cooper M. D.. 2007. Why study the evolution of immunity? Nat. Immunol. 8:547–548. PubMed PMC

Litman, G. W. , Cannon J. P., and Dishaw L. J.. 2005. Reconstructing immune phylogeny: new perspectives. Nat. Rev. Immunol. 5:866–879. PubMed PMC

Lohman, B. K. , Steinel N. C., Weber J. N., and Bolnick D. I.. 2017. Gene expression contributes to the recent evolution of host resistance in a model host parasite system. Front. Immunol. 8:1071. PubMed PMC

Malmstrøm, M. , Jentoft S., Gregers T. F., and Jakobsen K. S.. 2013. Unraveling the evolution of the Atlantic cod's (Gadus morhua L.) alternative immune strategy. PLoS ONE 8:1–9. PubMed PMC

Malmstrøm, M. , Matschiner M., Tørresen O. K., Star B., Snipen L. G., Hansen T. F., Baalsrud H. T., Nederbragt A. J., Hanel R., Salzburger W., et al. 2016. Evolution of the immune system influences speciation rates in teleost fishes. Nat. Genet. 48:1204–1210. PubMed

Mangan, B. P. 1998. Long‐term retention of a radio transmitter by a muskellunge. J. Freshw. Ecol. 13:485–487.

Peuß, R. , Box A. C., Chen S., Wang Y., Tsuchiya D., Persons J. L., Kenzior A., Maldonado E., Krishnan J., Scharsack J. P., et al. 2020. Adaptation to low parasite abundance affects immune investment and immunopathological responses of cavefish. Nat. Ecol. Evol. 4:1416–1430. PubMed PMC

Pinheiro, J. , Bates D., DebRoy S., Sarkar D., and R.re. Team . 2018. nlme: linear and nonlinear mixed effects models. R package version 3.1‐137. Available via https://CRAN.R‐project.org/package=nlme.

Polačik, M. , Blažek R., and Reichard M.. 2016. Laboratory breeding of the short‐lived annual killifish Nothobranchius furzeri . Nat. Protoc. 11:1396–1413. PubMed

R Core Team . 2020. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available via https://www.R‐project.org/.

Rabosky, D. L. , Chang J., Title P. O., Cowman P. F., Sallan L., Friedman M., Kaschner K., Garilao C., Near T. J., Coll M., et al. 2018. An inverse latitudinal gradient in speciation rate for marine fishes. Nature 559:392–395. PubMed

Radwan, J. , Babik W., Kaufman J., Lenz T. L., and Winternitz J.. 2020. Advances in the evolutionary understanding of MHC polymorphism. Trends Genet. 36:298–311. PubMed

Rahn, A. K. , Eßer E., Reher S., Ihlow F., MacColl A. D. C., and Bakker T. C. M.. 2016. Distribution of common stickleback parasites on North Uist, Scotland, in relation to ecology and host traits. Zoology 119:395–402. PubMed

Revell, L. J. 2012. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3:217–223.

Rijkers, G. T. , Frederix‐Wolters E. M., and van Muiswinkel W. B.. 1980. The immune system of cyprinid fish. Kinetics and temperature dependence of antibody‐producing cells in carp (Cyprinus carpio). Immunology 41:91–97. PubMed PMC

Ritter, M. , Kalbe M., and Henrich T.. 2017. Virulence in the three‐spined stickleback specific parasite Schistocephalus solidus is inherited additively. Exp. Parasitol. 180:133–140. PubMed

Simon, V. , Elleboode R., Mahé K., Legendre L., Ornelas‐Garcia P., Espinasa L., and Rétaux S.. 2017. Comparing growth in surface and cave morphs of the species Astyanax mexicanus: insights from scales. Evodevo 8:23. PubMed PMC

Slodkowicz, G. , and Goldman N.. 2020. Integrated structural and evolutionary analysis reveals common mechanisms underlying adaptive evolution in mammals. Proc. Natl. Acad. Sci. USA 117:5977–5986. PubMed PMC

Solbakken, M. H. , Voje K. L., Jakobsen K. S., and Jentoft S.. 2017. Linking species habitat and past palaeoclimatic events to evolution of the teleost innate immune system. Proc. R. Soc. B Biol. Sci. 284:20162810. PubMed PMC

Thannickal, V. J. , Zhou Y., Gaggar A., and Duncan S. R.. 2014. Fibrosis: ultimate and proximate causes. J. Clin. Invest. 124:4673–4677. PubMed PMC

Velová, H. , Gutowska‐Ding M. W., Burt D. W., and Vinkler M.. 2018. Toll‐like receptor evolution in birds: gene duplication, pseudogenization, and diversifying selection. Mol. Biol. Evol. 35:2170–2184. PubMed PMC

Vrtílek, M. , and Bolnick D. I.. 2021. Macroevolutionary foundations of a recently‐evolved innate immune defense (data). Dryad. 10.5061/dryad.d2547d83c. PubMed DOI PMC

Weber, J. N. , Kalbe M., Shim K. C., Erin N. I., Steinel N. C., Ma L., and Bolnick D. I.. 2017a. Resist globally, infect locally: a transcontinental test of adaptation by stickleback and their tapeworm parasite. Am. Nat. 189:43–57. PubMed

Weber, J. N. , Steinel N. C., Shim K. C., and Bolnick D. I.. 2017b. Recent evolution of extreme cestode growth suppression by a vertebrate host. Proc. Natl. Acad. Sci. USA 114:6575–6580. PubMed PMC

Weber, M. G. , and Agrawal A. A.. 2012. Phylogeny, ecology, and the coupling of comparative and experimental approaches. Trends Ecol. Evol. 27:394–403. PubMed

Weber, J. N. , Steinel N. C., Peng F., Shim K. Ch., Lohman B. K., Fuess L. E., De Lisle S. P., and Bolnick D. I.. 2021. Evolution of a costly immunity to cestode parasites is a pyrrhic victory. bioRxiv. https://www.biorxiv.org/content/10.1101/2021.08.04.455160v1. DOI

Zobrazit více v PubMed

Dryad
10.5061/dryad.d2547d83c

figshare
10.6084/m9.figshare.12619367

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...