Functional
Ecology 2006
20, 873–879
873
© 2006 The Authors.
Journal compilation
© 2006 British
Ecological Society
Blackwell Publishing Ltd
Immune challenge reduces reproductive output and growth
in a lizard
T. ULLER,*‡ C. ISAKSSON† and M. OLSSON*
*Institute for Conservation Biology, School of Biological Sciences, University of Wollongong, 2522 NSW, Australia,
and †Department of Zoology, Göteborg University, Medicinaregatan 18, 405 30 Göteborg, Sweden
Summary
1. A fundamental assumption in evolutionary immunology is that the immune system
is costly to develop, maintain or activate.
2. Two plausible costs of activation of the immune system are decreased resources for
growth and reproductive investment. However, few studies have estimated direct effects
of an immune challenge, in particular in ectotherm vertebrates. We studied the con-
sequences of an immune challenge in reproductive female dragons, Ctenophorus fordi,
and in their offspring by exposing lizards to bacterial lipopolysaccharides (LPS).
3. The immune challenge led to decreased reproductive investment in terms of egg
mass, but with no effect on probability of future reproduction.
4. Maternal immune challenge did not influence the response of their offspring to the
same challenge. However, juveniles that were induced to mount an immune response
had a higher thermal preference and showed reduced growth, but the magnitude of the
growth effect was dependent on the date of oviposition, indicating maternal effects on
offspring immunity.
5. Our results suggest that costs of immune activation may be important in shaping
growth and reproductive strategies in ectotherms.
Key-words: Cost, immune response, LPS, maternal effects
Functional Ecology (2006) 20, 873–879
doi: 10.1111/j.1365-2435.2006.01163.x
Introduction
The immune system is of fundamental importance for
an organism’s survival and therefore plays a central
role in evolutionary ecology (Sheldon & Verhulst 1996;
Lochmiller & Deerenberg 2000; Norris & Evans 2000;
Schmid-Hempel 2003). If immunity is costly, life-
history theory predicts that investment into the
immune system should be traded off against other
aspects of an individual’s fitness, such as reproductive
investment (Sheldon & Verhulst 1996). Expenditure
on immunity can be divided into three cost categories;
production, maintenance and usage (reviewed in
Klasing & Leshchinsky 1998; Lochmiller & Deerenberg
2000; Zuk & Stoehr 2002). Production costs imply
that ontogenetic development of the immune system
will interfere with resource allocation to growth
and development (Klasing 1998; Soler et al . 2003;
Brommer 2004; Jacot et al . 2005; Uller, Andersson &
Eklöf 2006). Maintenance costs imply that immunity
is paid for continuously and regardless of pathogen
exposure (although high exposure to pathogens
may lead to a higher up-regulation of the immune
defence and therefore a higher cost; Lochmiller &
Deerenberg 2000; Derting & Compton 2003). Finally,
usage costs are paid only when the immune system
is activated, and this magnitude should depend on the
level of the immune response (Derting & Compton
2003; Martin, Scheuerlein & Wikelski 2003; Jacot,
Scheuber & Brinkhof 2004). The relative importance
of these costs will determine to what extent specific
traits (e.g. reproductive investment) are traded off
against immunocompetence. Documentation of costs
of immune function is therefore central to our under-
standing of the role of immunity in life-history evolu-
tion (Ricklefs & Wikelski 2002; Schmid-Hempel 2003;
Viney, Riley & Buchanan 2005).
Providing strong evidence for direct costs of
immunity can be difficult since pathogen effects on
host health may confound costs of immunity per se .
Furthermore, allocation of resources among functions
other than the immune system may lead to similar pat-
terns as would a direct cost of mounting an immune
response. As a consequence, we still have a very limited
understanding of the importance of costs of immunity
at both the proximate (e.g. elevated metabolic rate) and
the ultimate (e.g. life-history decisions) level. However,
‡Author to whom correspondence should be addressed.
E-mail: uller@uow.ed.au