Literature DB >> 27683366

Evolution of transgenerational immunity in invertebrates.

R Pigeault1, R Garnier2, A Rivero3, S Gandon4.   

Abstract

Over a decade ago, the discovery of transgenerational immunity in invertebrates shifted existing paradigms on the lack of sophistication of their immune system. Nonetheless, the prevalence of this trait and the ecological factors driving its evolution in invertebrates remain poorly understood. Here, we develop a theoretical host-parasite model and predict that long lifespan and low dispersal should promote the evolution of transgenerational immunity. We also predict that in species that produce both philopatric and dispersing individuals, it may pay to have a plastic allocation strategy with a higher transgenerational immunity investment in philopatric offspring because they are more likely to encounter locally adapted pathogens. We review all experimental studies published to date, comprising 21 invertebrate species in nine different orders, and we show that, as expected, longevity and dispersal correlate with the transfer of immunity to offspring. The validity of our prediction regarding the plasticity of investment in transgenerational immunity remains to be tested in invertebrates, but also in vertebrate species. We discuss the implications of our work for the study of the evolution of immunity, and we suggest further avenues of research to expand our knowledge of the impact of transgenerational immune protection in host-parasite interactions.
© 2016 The Author(s).

Keywords:  Drosophila; dispersal; eusocial insects; local adaptation; longevity; transgenerational immune effect

Year:  2016        PMID: 27683366      PMCID: PMC5046895          DOI: 10.1098/rspb.2016.1136

Source DB:  PubMed          Journal:  Proc Biol Sci        ISSN: 0962-8452            Impact factor:   5.349


  44 in total

1.  The evolution of resistance through costly acquired immunity.

Authors:  Michael Boots; Roger G Bowers
Journal:  Proc Biol Sci       Date:  2004-04-07       Impact factor: 5.349

2.  Trans-generational immune priming in a social insect.

Authors:  Ben M Sadd; Yvonne Kleinlogel; Regula Schmid-Hempel; Paul Schmid-Hempel
Journal:  Biol Lett       Date:  2005-12-22       Impact factor: 3.703

Review 3.  A practical guide to measuring local adaptation.

Authors:  François Blanquart; Oliver Kaltz; Scott L Nuismer; Sylvain Gandon
Journal:  Ecol Lett       Date:  2013-07-15       Impact factor: 9.492

4.  Linking immune defenses and life history at the levels of the individual and the species.

Authors:  Kelly A Lee
Journal:  Integr Comp Biol       Date:  2006-10-20       Impact factor: 3.326

5.  The evolutionary dynamics of within-generation immune priming in invertebrate hosts.

Authors:  Alex Best; Hannah Tidbury; Andy White; Mike Boots
Journal:  J R Soc Interface       Date:  2012-12-26       Impact factor: 4.118

6.  Where does innate immunity stop and adaptive immunity begin?

Authors:  Junaid Ziauddin; David S Schneider
Journal:  Cell Host Microbe       Date:  2012-10-18       Impact factor: 21.023

Review 7.  Dscam and pancrustacean immune memory - a review of the evidence.

Authors:  Sophie A O Armitage; Robert Peuss; Joachim Kurtz
Journal:  Dev Comp Immunol       Date:  2014-03-19       Impact factor: 3.636

8.  The effect of maternal and paternal immune challenge on offspring immunity and reproduction in a cricket.

Authors:  K B McNamara; E van Lieshout; L W Simmons
Journal:  J Evol Biol       Date:  2014-04-18       Impact factor: 2.411

9.  The evolutionary dynamics of timing of maternal immunity: evaluating the role of age-specific mortality.

Authors:  C J E Metcalf; J H Jones
Journal:  J Evol Biol       Date:  2015-02-26       Impact factor: 2.411

10.  Trans-generational Immune Priming Protects the Eggs Only against Gram-Positive Bacteria in the Mealworm Beetle.

Authors:  Aurore Dubuffet; Caroline Zanchi; Gwendoline Boutet; Jérôme Moreau; Maria Teixeira; Yannick Moret
Journal:  PLoS Pathog       Date:  2015-10-02       Impact factor: 6.823

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  13 in total

Review 1.  Recent advances in vertebrate and invertebrate transgenerational immunity in the light of ecology and evolution.

Authors:  Olivia Roth; Anne Beemelmanns; Seth M Barribeau; Ben M Sadd
Journal:  Heredity (Edinb)       Date:  2018-06-18       Impact factor: 3.821

Review 2.  Vector Immunity and Evolutionary Ecology: The Harmonious Dissonance.

Authors:  Dana K Shaw; Ann T Tate; David S Schneider; Elena A Levashina; Jonathan C Kagan; Utpal Pal; Erol Fikrig; Joao H F Pedra
Journal:  Trends Immunol       Date:  2018-10-06       Impact factor: 16.687

Review 3.  Balancing sensitivity, risk, and immunopathology in immune regulation.

Authors:  Brian P Lazzaro; Ann T Tate
Journal:  Curr Opin Insect Sci       Date:  2022-01-17       Impact factor: 5.254

4.  Pathogen-induced maternal effects result in enhanced immune responsiveness across generations.

Authors:  Rebeca B Rosengaus; Nicole Hays; Colette Biro; James Kemos; Muizz Zaman; Joseph Murray; Bruck Gezahegn; Wendy Smith
Journal:  Ecol Evol       Date:  2017-03-22       Impact factor: 2.912

5.  Grandparental immune priming in the pipefish Syngnathus typhle.

Authors:  Anne Beemelmanns; Olivia Roth
Journal:  BMC Evol Biol       Date:  2017-02-07       Impact factor: 3.260

6.  Bacterial microbiota of Aedes aegypti mosquito larvae is altered by intoxication with Bacillus thuringiensis israelensis.

Authors:  Guillaume Tetreau; Stéphanie Grizard; Chandrashekhar D Patil; Florence-Hélène Tran; Van Tran Van; Renaud Stalinski; Frédéric Laporte; Patrick Mavingui; Laurence Després; Claire Valiente Moro
Journal:  Parasit Vectors       Date:  2018-03-02       Impact factor: 3.876

Review 7.  Interaction between Insects, Toxins, and Bacteria: Have We Been Wrong So Far?

Authors:  Guillaume Tetreau
Journal:  Toxins (Basel)       Date:  2018-07-06       Impact factor: 4.546

Review 8.  Trans-generational Immune Priming in Invertebrates: Current Knowledge and Future Prospects.

Authors:  Guillaume Tetreau; Julien Dhinaut; Benjamin Gourbal; Yannick Moret
Journal:  Front Immunol       Date:  2019-08-14       Impact factor: 7.561

9.  Disentangling non-specific and specific transgenerational immune priming components in host-parasite interactions.

Authors:  Frida Ben-Ami; Christian Orlic; Roland R Regoes
Journal:  Proc Biol Sci       Date:  2020-02-12       Impact factor: 5.349

10.  Parental and offspring larval diets interact to influence life-history traits and infection with dengue virus in Aedes aegypti.

Authors:  Kylie Zirbel; Bradley Eastmond; Barry W Alto
Journal:  R Soc Open Sci       Date:  2018-07-18       Impact factor: 2.963

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