Physiological Entomology (2017), DOI: 10.1111/phen.12186
The more, the merrier? Obligate symbiont density
changes over time under controlled environmental
conditions, yet holds no clear fitness consequences
JASMINE F. PARKINSON
1
, BRUNO GOBIN
2
and
WILLIAM O. H. HUGHES
1
1
Department of Evolution, Behaviour and Environment, School of Life Sciences, University of Sussex, Falmer, U.K. and
2
PCS-Ornamental Plant Research, Destelbergen, Belgium
Abstract. Symbiotic bacteria are highly diverse, play an important role in ecology and
evolution, and are also of applied relevance because many pest insects rely on them
for their success. However, the dynamics and regulation of symbiotic bacteria within
hosts is complex and still poorly understood outside of a few model systems. One of
the most intriguing symbiotic relationships is the obligate, tripartite nutritional mutu-
alism in sap-feeding, economically-destructive mealybugs (Hemiptera: Sternorrhyncha:
Pseudococcidae), which involves γ-proteobacteria hosted within β-proteobacteria hosted
within the mealybugs. The present study examines whether there is population variation
in symbiont density (i.e. infection intensity, or titre) in the citrus mealybug Planococcus
citri (Risso) and how this impacts host life-history. Symbiont density is found to differ
significantly between populations when reared under controlled environmental condi-
tions, indicating that the density of symbiont infections is influenced by host or symbiont
genotype. However, symbiont density changes in populations over multiple generations,
indicating that symbiont densities are dynamic. Surprisingly, given that the symbionts
are essential nutritional mutualists, the density of the symbionts does not correlate sig-
nificantly with either host fecundity or development. Higher levels of symbionts have
no clear benefit to hosts and therefore appear to be superfluous, at least under constant,
optimized environmental conditions. Excessive symbiont density may be an evolution-
ary artefact from a period of inefficient vertical transmission when the balance of conflict
between host and symbiont was still being established.
Key words. Endosymbionts, fecundity, Hemiptera, mealybug, Planococcus citri,
Proteobacteria, Pseudococcidae, qPCR reproduction, size.
Introduction
Symbiotic bacteria are now understood to be highly diverse and
influential players in eukaryotic ecology and evolution (Saffo,
1992; Moran, 2001; Douglas, 2009). They are fundamental to
many aspects of life, having given rise to mitochondria and
chloroplasts, as well as numerous other pivotal evolutionary
steps, such as nitrogen fixation and bioluminescence (Giobel,
1926; Yasaki, 1928; Schwartz & Dayhoff, 1978; Peix et al.,
Correspondence: Jasmine Parkinson, Department of Evolution,
Behaviour and Environment, School of Life Sciences, University
of Sussex, John Maynard Smith Building, North South Road,
Falmer, Brighton BN1 9RH, U.K. Tel.: +44 7540687532; e-mail:
jasmine.parkinson@gmail.com
2015). The impacts that symbionts have on their hosts can range
from mutualistic, to commensal, to parasitic. However, rather
than residing in strict categories, the relationships between hosts
and symbionts exist on a dynamic spectrum, and may often be
context-specific (Swain, 2012; Gerardo, 2015).
Each member in a symbiotic relationship will ultimately
evolve to maximize its own fitness rather than that of its partner,
so conflict between host and symbiont may often occur, even
in mutualistic associations (Bennett & Moran, 2015). The
maintenance of beneficial symbionts will still incur some cost
to the host, and the host should reduce symbiont density (i.e.
infection intensity) when it is in excess, whereas the symbiont
should seek to optimize its density to maximize the likelihood
of its own transmission to new hosts (Falkowski et al., 1993;
© 2017 The Royal Entomological Society 1