Genetic, individual, and group facilitation of disease resistance in honey bees (Apis mellifera) and two species of paper wasps (Polistes dominulus and P. fuscatus).
Abstract: Social insects are remarkable for their extreme form of group
living. This includes a reproductive division of labor, overlap of generations, and
cooperative care for the brood. The global success of social insects suggests that the
benefits of eusociality outweigh its costs. In this dissertation, I investigated how three
species of social insects resist disease at multiple levels of ... read morebiological organization. My
co-authors and I first present a comprehensive review of what is known about how social
insects resist disease, scaling up from genes to proteins and cells, to individual behavior
to groups and populations. Next, I provide the first critical test of the `haploid
susceptibility hypothesis' using naturally occurring genetic misfits in Polistes dominulus
populations. This hypothesis assumes that males are likely to have fewer disease resistance
alleles than females in haplodiploid species, and that this disparity has shaped the
evolution of social behavior. My co-authors and I show that this hypothesis is not a
significant contributor to the evolution of social behavior in P. dominulus. Instead, I
note strong ecological influences on immune function, including temporal-, sex-, and
caste-related factors. Time of emergence and behavioral role are the best predictors of
immune function in Polistes. I then scale up from individual genetics in paper wasps to
group genetics in honey bee hives. Interestingly, phenoloxidase activity and encapsulation
response are not influenced by colony-level genetic diversity. Therefore, the mechanistic
explanation linking genetic diversity to prior observations of increased disease resistance
in genetically diverse colonies remains elusive. A main theme throughout this work is the
use of empirical methods to quantify invertebrate immune function. I report results from a
set of experiments, performed with my co-authors, demonstrating the applicability of a
novel method for assaying the invertebrate encapsulation response. This method uses a nylon
monofilament coated with pathogen-associated membrane patterns (PAMPs). These implants,
termed "PAMPlants", now allow researchers to investigate questions relating to how
invertebrates mount an immune response against different classes of microbes. Following
this, I then report results from experiments documenting how cellular and humoral immune
function develops with honey bee ontogeny. I draw conclusions within the context of
behavioral differences between life stages, and also differences in pathogen pressure
across these stages. The final data chapter investigates a possible immune mechanism for
the noted success of the P. dominulus invasion into North America from Europe and Northern
Africa. My co-author and I compared multiple measures of immune function between P.
dominulus and its sympatric, native congener P. fuscatus. Surprisingly, P. dominulus had
lower immune function than P. fuscatus. I interpret these results within the context of the
enemy-release hypothesis as a putative explanation for the success of this non-native
population. My results present a comprehensive report of immune function in three species
of social insects, and provide important insights into past, present, and future methods
for testing immune function in these truly remarkable beasts.
Thesis (Ph.D.)--Tufts University, 2011.
Submitted to the Dept. of Biology.
Advisor: Philip Starks.
Committee: Juliet Fuhrman, Colin Orians, Sara Lewis, and Heather Mattila.
Keywords: Ecology, Entomology, and Immunology.read less