Division of labor in disease resistance and causes of interindividual variability in the workforce 

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Phenotypic variability

Eusocial insects are able to generate worker phenotypes with distinct morphological, physiological and behavioral phenotypes from the same genome through a variety of nonmutually exclusive mechanisms. In social insects, immune defense varies at the colony and at the individual level and worker immune investment has important fitness consequences as it may affect colony disease rate and productivity (e.g. Evans and Pettis 2005; Baer and Schmid-Hempel 2006). Several immune components underlie plasticity, depending on environmental conditions and factors such as task performance, age, diet or parasite exposure (Rosengaus et al. 1998b; Jaccoud et al. 1999; Doums and Schmid-Hempel 2000; Amdam et al. 2005; Bocher et al. 2007; Castella et al. 2008, 2010; Simone et al. 2009; Walker and Hughes 2009; Kay et al. 2014). An individual’s degree of plasticity in response to these factors is determined by the level of heritability of a trait (including a potential effect of plasticity-regulating loci which exert environmentally-dependent control over structural gene expression: Schlichting and Pigliucci 1993). Factors leading to phenotypic variability among the workforce are dynamic and enable colonies to more rapidly adjust to changing internal and external conditions, compared to solely genetic trait determination (Passera et al. 1996; McGlynn and Owen 2002; Hughes et al. 2003; Bargum et al. 2004; Jeanson and Weidenmüller 2013).

Cataglyphis velox

The genus Cataglyphis (subfamily Formicinae) comprises more than 100 species occurring in arid habitats in Asia, Europe and Africa. Especially the Mediterranean C. bicolor, C. cursor and C. velox are valued model species to investigate the elaborate navigational abilities and thermal adaptations typical for this genus. One of the most polymorphic species is Cataglyphis velox, Santschi, 1929, with a continuous worker length range of 4.5 -12 mm (Cerdá and Retana 1997). This species is endemic to the Iberian Peninsula and found in an elevation range between 0 and 2400 m (Tinaut 1990) (Fig. 2). Colonies have small to medium size, containing from hundreds to a few thousands of workers and one to several queens (worker number = 1220 individuals/colony (range 230-3650); queen number = 5 queens/colony (range 1-14) in 25 field colonies).The colonies occupy an underground nest containing several chambers connected by tunnels (Fig. 2). Two colonies were observed to possess superficial chambers close to the soil surface, containing empty cocoon cases and cadavers. Waste dumps with cadavers were also found exterior to the colony, about 15 to 20 cm away from the nest exit (observation by C. Haussy).

Metarhizium robertsii

Insect parasitic fungi play an important role in agriculture and public health. Especially the entomoparasitic fungi Metarhizium spp. (Fig. 4) and Beauveria bassiana have been applied as biological pesticides to control insects classified as agricultural pests (e.g. locusts in Africa) or malaria-causing parasites in mosquitoes (reviewed in Thomas and Read 2007). The general insect pathogenic fungus Metarhizium robertsii (Bischoff et al. 2009) is a natural pathogen of ants (Rath et al. 1992; Keller et al. 2003; St. Leger et al. 2011) and occurs in soils worldwide (St. Leger et al. 2011). Entomopathogenic fungi invade hosts by direct penetration of the cuticle. When conidiospores of Metarhizium adhere to the cuticle, they germinate under highhumidity conditions and penetration occurs by a combination of physical force and cuticluladegrading enzymes after approximately 24 hours (Clarkson and Charnley 1996; Hajek and St. Leger 1994; Ugelvig et al. 2010).

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Groomings and transports received by cadavers

The number of groomings cadavers received did neither change over trial, nor was it affected by cadaver size or by the duration a cadaver stayed in the nest (LMM, Table 2). Cadavers were groomed more often if they elicited grooming in a higher number of different grooming individuals (Table 2, Fig. 2, LMM, coefficient = 0.331). The number of transports also significantly increased with an increasing number of transporting individuals (Table 2, Fig. 2, LMM, coefficient = 0.134). Trial, cadaver size and the duration a cadaver stayed in the nest did not affect the number of transports received (Table 2).
The number of workers which groomed cadavers increased with trial (Table 2, LMM, coefficient = 0.051) and with the duration a cadaver stayed in the nest (Table 2, LMM, coefficient = 0.001), but was not affected by cadaver size (Table 2, LMM). The number of individuals which engaged in cadaver transports was neither affected by trial, nor by the duration a cadaver stayed in the nest, but depended on cadaver size (Table 2, LMM). The largest and second smallest cadavers were transported by fewer individuals.

Table of contents :

1. ABSTRACT 
2. RÉSUMÉ 
3. INTRODUCTION 
3.1 Disease resistance in social insects
3.1.1 Individual physiological immune defenses
3.1.2 Collective immune defenses
3.2 Division of labor in social insect colonies
3.3 Division of labor in disease resistance and causes of interindividual variability in the workforce
3.3.1 Genetic variability
3.3.2 Phenotypic variability
3.4 Aims of the thesis
3.5 The study systems
3.5.1 Platythyrea punctata
3.5.2 Cataglyphis velox
3.5.3 Metarhizium robertsii
4. CHAPTER 1: Increased grooming after repeated brood care provides sanitary benefits in a clonal ant. 
5. CHAPTER 2: Necrophoresis is not everything: cadaver groomings and intranidal transports in the ant Cataglyphis velox. 
6. CHAPTER 3: Are worker size and phenoloxidase activity of Cataglyphis velox workers genetically determined? 
7. CONCLUSIONS AND PERSPECTIVES
7.1 What are the benefits of interindividual variation in immune investment?
7.1.1 Behavioral performance of sanitary tasks
3.1.2 Physiological immune investment
7.2 Potential costs of interindividual variation
7.3 The modulation of sanitary division of labor and the costs and benefits of helping
7.4 Who is expected to invest more heavily into immune defense?
7.5 Nature versus nurture: phenotypic plasticity in immune defense mechanisms
7.6 When is experience-modulated behavioral plasticity expected to occur?
7.7 Empirical difficulties to analyze proximate mechanisms contributing to interindividual variation in immune defense
8. REFERENCES
9. ACKNOWLEDGMENTS 
10. AFFIDAVIT

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