EVOLUTIONARY ECOLOGY AND ADAPTIVENESS OF IMMUNE

Diss. ETH. No. 14278
EVOLUTIONARY ECOLOGY AND ADAPTIVENESS OF IMMUNE
DEFENSES OF THE SOCIAL INSECT BOMBUS TERRESTRIS (L.)
(HYMENOPTERA: APIDAE)
Adissertation submitted to the
SWISS FEDERAL INSTITUTE OF TECHNOLOGY
for the degree of Doctor ofNatural Seiences
Presented by
Yannick Moret
Diplöme d'Etudes Approfondies (D.E.A.) ofPopulation Biology, Genetics and
Eco-Ethology, University ofTours, France
Born February 5, 1973
From Montlucon, France.
Accepted on the recommendation
of
Prof. Dr. P. Schmid-Hempel, examiner
Prof. Dr. J. Koella, co-examiner

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1. RESUME
Les parasites et les pathogenes peuvent affecter la survie, la croissance et la reproduction
de leurs hötes.
Ces effets nefastes ont conduit, parmi les populations d'hötes, ala
selection de nombreux mecanismes de resistance, Parmi ceux-ci, le systeme immunitaire
des animaux est
l'un des plus repandu. Malgre l'importance de la pression de selection
exercee par les parasites, les populations d'hötes presentent des niveaux de resistance ou
d'immunocompetence tres varies. Pour expliquer cette grande variation, des discussions
recentes en ecologie et en evolution ont emis l'hypothese selon laquelle
l'immunite serait
coüteuse et contraindrait l'expression
d'autres composantes de la valeur selective (ou
fitness). Par consequent, la selection naturelle favoriserait I'accroissement de
l'immunocompetence uniquement lorsque celle-ci serait benefique,
Afin
d' examiner la veracite de cette hypothese, j' ai etudie, au cours de cette these, les
coüts sur la fitness associes äl'utilisation du systeme immunitaire. Cette etude aete
realisee sur le
bourdon Bambus terrestris (L.), un insecte social facile a elever en
laboratoire. B. terrestris est connu pour etre la cible de nombreux parasites et doit, par
consequent, solieiter tres frequement son systeme immunitaire. L'utilisation du systeme
immunitaire requiere des ressources (nutriments et energie) et pourrait imposer un coüt
capable d'affecter la fitness de l'höte, Dans cette etude, pour forcer les bourdons äactiver
leur systeme immunitaire, des ouvrieres ont ete exposees a des stimulations
immunogeniques standards. En fonction de la disponibilite de ressource, il a pu etre
dementre qu'une reponse immunitaire impose un coüt substantiel sur la survie des
ouvrieres. De plus, lorsque les ouvrieres utilisent leur fonetion immunitaire pendant une
periode prolongee du cycle de vie de la colonie, le succes reproducteur de cette derniere
est diminue. Des donnees supplementaires montrent que des compromis
d'allocation (ou
trade-offs) pourraient exister entre les composantes mernes du systeme immunitaire des
bourdons. Par consequent, les resultats presentes ici supportent l'hypothese mentionnee
plus
haut selon laquelle le coüt des defenses immunitaires pourrait contraindre
l'evolution de l'immunite.

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Cependant, cette etude montre aussi que des changements phenotypiques de 1'histoire de
vie des colonies de bourdons peuvent resulter de l' activation du systeme immunitaire.
Ces modifications de l'histoire de vie aideraient äreduire l'impact du coüt des defenses
immunitaires lorsque celles-ci sont necessaires, Ainsi, la combinaison du coüt de la
fonction immunitaire et de la necessite de se defendre contre les parasites pourrait avoir
conduit ala selection d'adaptations permettant le maintient d'un niveau
dimmunocompetence eleve mais avec un coüt attenue au mieux.

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2. SUMMARY
Parasites and pathogens can negatively affect the survival, growth and reproduction of
their hosts. These negative effects lead, in host populations, to selection for various
resistance mechanisms. Among these, the immune system
of animals is one of the most
widespread. Despite the strong selective pressure imposed by parasites, host populations
exhibit high natural variation in pathogen resistance or immunocompetence. To explain
this variation, recent discussion in evolutionary ecology entertained the hypothesis that
immunity might be costly and trade-off against other fitness components. Hence, natural
selection would favour enhanced immunocompetence only when it is beneficial.
To examine the extent to which this hypothesis could be supported Iinvestigated, in this
thesis, the fitness costs associated with the use
of the immune system. In this study, the
model system used was the bumblebee Bambus terrestris (L.), which can be easily bred
in the laboratory. B. terrestris is known to be targeted by many parasites and thus may
face frequent challenges to its immune system. Here, to induce bumblebees to use their
immune system, workers were exposed to standardised immunogenic challenges.
According to levels
of environmental stress (resource limitation) a substantial individual
cost
ofthe immune response was seen to decrease worker's survival. In addition, forcing
workers to use their immune system over prolonged periods
of time during the colony life
cycle resulted in a decrease in a colony's reproductive success. Furthermore, additional
data showed that trade-offs between components
of the immune system of bumblebees
exist. Therefore, the results presented here support the hypothesis above in which the cost
of the immune defences may constrain the evolution of immunity.
However, also in this study, adaptive phenotypic changes
of life history patterns were
observed due to the activation
of the immune system. These may help to decrease or
compensate for the cost
of immune defences. This suggests that the cost of immune
defences associated with the necessity
of defence against parasites may also select for
adaptations leading to an affordable, albeit costly immunity.