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Fungal infection alters collective nutritional intake of ant colonies

生物 蚂蚁 动物 生态学
作者
Enikő Csata,Alfonso Pérez‐Escudero,Emmanuel Laury,Hanna Leitner,Gérard Latil,Jürgen Heınze,Stephen J. Simpson,Sylvia Cremer,Audrey Dussutour
出处
期刊:Current Biology [Elsevier BV]
卷期号:34 (4): 902-909.e6 被引量:3
标识
DOI:10.1016/j.cub.2024.01.017
摘要

In animals, parasitic infections impose significant fitness costs. 1 Hurd H. Evolutionary drivers of parasite-induced changes in insect life-history traits From theory to underlying mechanisms. Adv. Parasitol. 2009; 68: 85-110 Crossref PubMed Scopus (0) Google Scholar ,2 Csata E. Erős K. Markó B. Effects of the ectoparasitic fungus Rickia wasmannii on its ant host Myrmica scabrinodis: changes in host mortality and behavior. Insect. Soc. 2014; 61: 247-252 Crossref Scopus (33) Google Scholar ,3 Bos N. Kankaanpää-Kukkonen V. Freitak D. Stucki D. Sundström L. Comparison of twelve ant species and their susceptibility to fungal infection. Insects. 2019; 10: 271 Crossref PubMed Scopus (13) Google Scholar ,4 Lochmiller R.L. Deerenberg C. Trade-offs in evolutionary immunology: just what is the cost of immunity?. Oikos. 2000; 88: 87-98 Crossref Google Scholar ,5 Schmid-Hempel P. Variation in immune defence as a question of evolutionary ecology. Proc. Biol. 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Wilson K. Can the protein costs of bacterial resistance be offset by altered feeding behaviour?. J. Anim. Ecol. 2009; 78: 437-446 Crossref PubMed Scopus (179) Google Scholar ,11 Ponton F. Wilson K. Cotter S.C. Raubenheimer D. Simpson S.J. Nutritional immunology: a multi-dimensional approach. PLoS Pathog. 2011; 7e1002223 Crossref PubMed Scopus (131) Google Scholar ,12 Kay A.D. Bruning A.J. van Alst A. Abrahamson T.T. Hughes W.O.H. Kaspari M. A carbohydrate-rich diet increases social immunity in ants. Proc. Biol. Sci. 2014; 281: 20132374 PubMed Google Scholar but parasites can manipulate animal foraging behavior to their own benefits. 13 de Bekker C. Beckerson W.C. Elya C. Mechanisms behind the madness: how do zombie-making fungal entomopathogens affect host behavior to increase transmission?. mBio. 2021; 12: e0187221 Crossref PubMed Scopus (8) Google Scholar ,14 Csata E. Billen J. Barbu-Tudoran L. Markó B. Inside Pandora’s box: Development of the lethal myrmecopathogenic fungus Pandora formicae within its ant host. Fungal Ecol. 2021; 50: 101022 Crossref Scopus (4) Google Scholar ,15 Hall S.R. Knight C.J. Becker C.R. Duffy M.A. Tessier A.J. Cáceres C.E. Quality matters: resource quality for hosts and the timing of epidemics. Ecol. Lett. 2009; 12: 118-128 Crossref PubMed Scopus (116) Google Scholar ,16 Vale P.F. Choisy M. Little T.J. Host nutrition alters the variance in parasite transmission potential. Biol. Lett. 2013; 9: 20121145 Crossref PubMed Scopus (0) Google Scholar How nutrition influences host-parasite interactions is not well understood, as studies have mainly focused on the host and less on the parasite. 9 Lee K.P. Cory J.S. Wilson K. Raubenheimer D. Simpson S.J. Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proc. Biol. Sci. 2006; 273: 823-829 Crossref PubMed Scopus (319) Google Scholar ,12 Kay A.D. Bruning A.J. van Alst A. Abrahamson T.T. Hughes W.O.H. Kaspari M. A carbohydrate-rich diet increases social immunity in ants. Proc. Biol. Sci. 2014; 281: 20132374 PubMed Google Scholar ,17 Moret Y. Schmid-Hempel P. Survival for immunity: the price of immune system activation for bumblebee workers. Science. 2000; 290: 1166-1168 Crossref PubMed Scopus (879) Google Scholar ,18 Triggs A.M. Knell R.J. Parental diet has strong transgenerational effects on offspring immunity. Funct. Ecol. 2012; 26: 1409-1417 Crossref Scopus (0) Google Scholar ,19 Castelli L. Branchiccela B. Garrido M. Invernizzi C. Porrini M. Romero H. Santos E. Zunino P. Antúnez K. Impact of nutritional stress on honeybee gut microbiota, immunity, and Nosema ceranae infection. Microb. Ecol. 2020; 80: 908-919 Crossref PubMed Scopus (55) Google Scholar ,20 Gómez-Moracho T. Durand T. Pasquaretta C. Heeb P. Lihoreau M. Artificial diets modulate infection rates by Nosema ceranae in bumblebees. Microorganisms. 2021; 9: 158 Crossref PubMed Scopus (7) Google Scholar ,21 Ayres J.S. Schneider D.S. The role of anorexia in resistance and tolerance to infections in Drosophila. PLoS Biol. 2009; 7e1000150 Crossref PubMed Scopus (245) Google Scholar ,22 Ponton F. Wilson K. Holmes A.J. Cotter S.C. Raubenheimer D. Simpson S.J. Integrating nutrition and immunology: a new frontier. J. Insect Physiol. 2013; 59: 130-137 Crossref PubMed Scopus (107) Google Scholar ,23 Cotter S.C. Al Shareefi E. Nutritional ecology, infection and immune defence - exploring the mechanisms. Curr. Opin. Insect Sci. 2022; 50: 100862 Crossref PubMed Scopus (12) Google Scholar We used the nutritional geometry framework 24 Simpson S.J. Raubenheimer D. The Nature of Nutrition: a Unifying Framework from Animal Adaptation to Human Obesity. Princeton University Press, 2012: 256 Google Scholar to investigate the role of amino acids (AA) and carbohydrates (C) in a host-parasite system: the Argentine ant, Linepithema humile, and the entomopathogenic fungus, Metarhizium brunneum. First, using 18 diets varying in AA:C composition, we established that the fungus performed best on the high-amino-acid diet 1:4. Second, we found that the fungus reached this optimal diet when given various diet pairings, revealing its ability to cope with nutritional challenges. Third, we showed that the optimal fungal diet reduced the lifespan of healthy ants when compared with a high-carbohydrate diet but had no effect on infected ants. Fourth, we revealed that infected ant colonies, given a choice between the optimal fungal diet and a high-carbohydrate diet, chose the optimal fungal diet, whereas healthy colonies avoided it. Lastly, by disentangling fungal infection from host immune response, we demonstrated that infected ants foraged on the optimal fungal diet in response to immune activation and not as a result of parasite manipulation. Therefore, we revealed that infected ant colonies chose a diet that is costly for survival in the long term but beneficial in the short term—a form of collective self-medication.
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