The Proximate and Ultimate Bases of Regulation of Lifespan And

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The Proximate and Ultimate Bases of Regulation of Lifespan And The proximate and ultimate bases of regulation of lifespan and reproduction in ants Dissertation Zur Erlangung des Grades Doktor der Naturwissenschaften Fachbereich Biologie Johannes-Gutenberg Universität Mainz Matteo Negroni geb. am 20. Juni 1991 in Paris, Frankreich Mainz 2019 Dekan: Prof. Dr. NA 1. Berichterstatterin: Prof. Dr. NA 2. Berichterstatter: Dr. NA Tag der mündlichen Prüfung: 26.09.2019 TABLE OF CONTENTS SUMMARY……………………….………………………………………………………………………………....2 GENERAL INTRODUCTION...................................................................................................... 4 CHAPTER 1 ............................................................................................................................. 22 LIFE HISTORY EVOLUTION IN SOCIAL INSECTS: A FEMALE PERSPECTIVE .......................................... 22 CHAPTER 2 ............................................................................................................................. 34 SOCIAL ORGANISATION AND THE EVOLUTION OF LIFE-HISTORY TRAITS IN TWO QUEEN MORPHS OF THE ANT TEMNOTHORAX RUGATULUS 34 CHAPTER 3 ............................................................................................................................. 58 POSITIVE EFFECT OF FOOD INTAKE ON SEQUESTOSOME-1 EXPRESSION AND A POSITIVE LINK BETWEEN FERTILITY AND DNA REPAIR IN TEMNOTHORAX RUGATULUS ANT QUEENS ........................................ 58 CHAPTER 4 ............................................................................................................................. 76 LONG-LIVED TEMNOTHORAX ANT QUEENS SWITCH FROM INVESTMENT IN IMMUNITY TO ANTIOXIDANT PRODUCTION WITH AGE ................................................................................................................ 76 CHAPTER 5 ........................................................................................................................... 102 INTRINSIC WORKER MORTALITY DEPENDS ON BEHAVIORAL CASTE AND THE QUEENS’ PRESENCE IN A SOCIAL INSECT .......................................................................................................................... 102 CHAPTER 6 ........................................................................................................................... 116 IMMUNE-CHALLENGE DIMINISHES GUT MICROBIOME DIVERSITY AND TRIGGERS FERTILITY- AND LONGEVITY-DEPENDENT TRANSCRIPTOMIC RESPONSES IN AN ANT ................................................ 116 GENERAL DISCUSSION ....................................................................................................... 150 ACKNOWLEDGEMENTS ...................................................................................................... 166 REFERENCES ....................................................................................................................... 168 Chapter 2 Summary Understanding why and how organisms age and die is a major topic in biology, medicine and is of universal interest. The proximate causes of aging are even less well understood than why aging evolved in the first place. One possibility is that aging results from the accumulation of molecular damage due to incomplete somatic repair. Longevity and fecundity are traded-off in most organisms and the negative association between these two traits involves conserved molecular pathways. Social insects are an exception, as fertile individuals live longer, but the mechanisms underlying this positive association are unknown. We are still far from understanding the interactions between environment, genotype, and the molecular pathways determining variation in longevity both within and between species. Social insects are ideal models, not only because they exhibit strong intra- specific variation in lifespan and reproduction with extreme values recorded in queens, but also because this variation can arise from the same genome. I investigated here the ultimate and proximate bases of the regulation of lifespan and reproduction and their reversal association in social insects, using Temnothorax ants as a study system. I first review ultimate factors underlying variation in life-history strategies in female social insects. I highlight in chapter 1 the importance of colony size, colony founding strategy and social structure (number of queens in the colony) for the evolution of lifespan, reproduction, and body size in queens and workers. Social insects with large colony sizes and independent colony foundation exhibit the longest queen lifespans. In chapter 2, I experimentally tested the effect of colony size, body size and social structure, on egg production in ant queens. I show that colony size and social structure, but not body size, determine queen fecundity. While in most solitary insects, female body size is strongly linked to fecundity, this life-history parameter appears to be replaced by colony size in social insects. Next, I investigated the link between fertility and somatic maintenance within castes, as well as the role of other factors for the regulation of lifespan and reproduction. By connecting phenotypic 25 Summary results to gene expression data, I shed light on the molecular basis of this regulation as well as the proximate mechanisms underlying the reshaping of the longevity/fecundity trade-off. In chapter 3 I investigate how longevity and fecundity are linked, and show that both egg removal and nutrient intake have a positive effect on queen fertility, but also activate body maintenance mechanisms. These results contrast with findings on solitary organisms, suggesting an alteration of molecular pathways in our species. Chapter 4 reveals that queens switch from investment into immunity to the production of antioxidants with age and increasing fertility, suggesting a role of immunity in the reversal of the longevity/fecundity trade-off. Focussing then on workers, I show in chapter 5 that behavioural castes differ in their rate of intrinsic mortality, where foragers that performed risky tasks outside the nest survive shorter than nurses. The removal of the queen induces worker fertility but also extends their lifespan. I thus investigated in chapter 6 the molecular basis of this fertility induction and lifespan extension in relation with immunity and the gut microbiome composition. I demonstrate that fertile workers upregulated repair mechanisms, explaining their extended longevity. Fertile workers respond differently to an immune challenge than non-fertile ones. Results suggest that lifespan extension is linked to a better stability of the immune response but unlikely linked to the gut microbiome. In conclusion, this dissertation sheds light on the molecular bases of aging and the regulation of lifespan in social insects, but also reveals how social life reshapes the association of life-history traits. I bring evidence for an alteration of certain pathways in our focal social species compared to solitary ones and identify a number of candidate genes and pathways for the reshaping of the trade- off between lifespan and reproduction. Finally, I point to an important role of immunity and nutrients in the regulation of lifespan and reproduction in social insects. 36 Chapter 2 General Introduction Matteo Negroni “We are survival machines - robot vehicles blindly programmed to preserve the selfish molecules known as genes. This is a truth which still fills me with astonishment.” ― Richard Dawkins General Introduction As death is our primal fear, immortality is one of the most ancient dreams of humanity. Humans tried to answer the question why we age and die in mythological tales and by religion. Understanding why and how something as detrimental for an organism as senescence and death evolved is also one of the major challenges for evolutionary biology. The concept “survival of the fittest” seems to suggest at first that senescence, is strongly selected against, yet it occurs in almost all multicellular organisms. The evolution of senescence Senescence is omnipresent in the animal, fungal and plant kingdom and is characterized by a decline in biological functions, including reproduction and a reduction in survival with age (Box. 1). This deteriorating process has been termed an evolutionary paradox, as it represents a clear cost to individual fitness (Stearn 1992) raising the question: why do organisms not live forever? This intriguing problem has puzzled researchers for a long time leading to the development of evolutionary theories of aging (Medawar 1952, Williams 1957, Kirkwood 1977). Box. 1 The definition of the terms senescence and aging are used in a quite inconsistent manner throughout the literature. While senescence is used only to describe the age-related deterioration of the body (biological aging), aging describes the fact of simply growing older (chronological aging; Medaward 1957). Other authors have frequently ignored this distinction using either senescence, or aging, or in some cases both, to define the same concept: the age-related deterioration of the body (Kirkwood and Rose 1991, Lucas and Keller 2014). In this thesis I decided not to make the distinction between the two, and use senescence and aging equally as defined by a persistent decline in the age-specific fitness components of an organism due to internal physiological deterioration (Rose 1991). 5 General Introduction An early theory, the “programmed death” theory advised first by Weismann (1891) proposed that senescence is programmed and adaptive allowing to limit population size or accelerate the turnover of generations,
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