Mild stress during development affects the
phenotype of great tit Parus major nestlings:
a challenge experiment
WILLEM TALLOEN
1
, LUC LENS
2
, STEFAN VAN DONGEN
1
, FRANK ADRIAENSEN
1
and
ERIK MATTHYSEN
1
*
1
Evolutionary Ecology Group, Department of Biology, Groenenborgerlaan 171, University of Antwerp,
B-2020 Antwerpen, Belgium
2
Terrestrial Ecology Unit, Department of Biology, Ledeganckstraat 35, Ghent University, B-9000
Ghent, Belgium
Received 13 July 2009; accepted for publication 17 December 2009
Conditions experienced during early development may affect both adult phenotype and performance later during
life. Phenotypic traits may hence be used to indicate past growing conditions and predict future survival
probabilities. Relationships between phenotypic markers and future survival are, however, highly heterogeneous,
possibly because poor- and high-quality individuals cannot be morphologically discriminated when developing
under good environmental conditions. Sub-optimal breeding conditions, in contrast, may unmask poor-quality
individuals in a measurable way at the morphological level. We thus predict stronger associations between
phenotype and performance under stress. In this field study, we test this hypothesis, experimentally challenging
the homeostasis of great tit (Parus major) nestlings by short-term deprivation of parental care, which had no
immediate effect on nestling fitness. The experiment was replicated during two subsequent breeding seasons with
contrasting ambient weather conditions. Experimental (short-term) stress affected tarsus growth but not residual
mass at fledging, whereas ambient (continuous) stress affected residual mass but not tarsus growth. Short-term
stress effects on tarsus length and tarsus fluctuating asymmetry were only apparent when ambient conditions were
unfavourable. Residual mass and hatching date, but none of the other phenotypic traits, predicted local survival,
whereby the strength of the relationship did not vary between both years. Because effects of stress on develop-
mental homeostasis are likely to be trait-specific and condition-dependent, studies on the use of phenotypic
markers for individual fitness should integrate multiple traits comprising different levels of developmental
complexity. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 103–110.
ADDITIONAL KEYWORDS: developmental instability – fitness – fluctuating asymmetry.
INTRODUCTION
Morphological traits, comprising the phenotypic end-
points in organisms with determinate growth, reflect
environmental conditions experienced during growth
and may predict long-term fitness consequences of
suboptimal developmental conditions (Lindström,
1999; Naguib & Gil, 2005). Morphological changes as
a result of adverse conditions during development are
considered to be primarily caused by a disruption of
developmental homeostasis (i.e. an organism’s prop-
erty to adjust itself to variable conditions such that
phenotypic variation is decreased) (Lerner, 1954).
Canalization decreases phenotypic variation between
environments (Waddington, 1959), and compensatory
growth and developmental stability decrease varia-
tion within an environment in trait size and develop-
mental noise, respectively (Nijhout & Davidowitz,
2003; Sibly & Calow, 1986; Van Valen, 1962). Rela-
tionships between phenotypic indices of homeostasis
and measures of environmental stress and individual
quality are typically heterogeneous (Bjorksten,
Fowler & Pomiankowski, 2000), possibly because
developmental rate and stability may remain unchal-
lenged under (near-)optimal conditions (Lens et al.,
2002; Van Dongen, 2006). Under this hypothesis, *Corresponding author. E-mail: erik.matthysen@ua.ac.be
Biological Journal of the Linnean Society, 2010, 100, 103–110. With 2 figures
© 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 103–110 103