Phenotypic variation among individuals can be partitioned into three components, that are caused by genetic variation, environmental variation, and gene-environment interactions (Kozhara 1989, Lajus 1991, Lajus et al. 2003). The environmental component can be further subdivided into macro- and micro-environmental variation, maternal effects, and random developmental processes. The random developmental processes that contribute to phenotypic variation may be estimated by measuring deviations from perfect bilateral symmetry. Such random deviations are called fluctuating asymmetry. They arise from two sources: (1) developmental noise (at both molecular and cellular levels) and (2) the inherent nonlinearity of complex developmental processes, which give rise to morphogenetic oscillations, and perhaps chaos or near chaos (Emlen et al. 1993, Freeman et al. 1993, Graham et al. 1993).
Developmental noise represents variation arising inside the system (i.e. embryo) from perturbations that originate outside the system (i.e. environment). Deterministic chaos, on the other hand, arises entirely from within the system (i.e. it is part of the norm of reaction), but is often indistinguishable from developmental noise. Because such variation is part of the norm of reaction, it can be generated by either genetic or environmental variation (Graham et al. 1993).
A theory of developmental stability must
account for observed transitions from fluctuating asymmetry to either
directional asymmetry or antisymmetry. Directional asymmetry
(i.e. handedness, or laterality) occurs when most individuals are
either left or right dominant. Antisymmetry occurs when most
individuals are asymmetric, but it is random which side is
dominant. The transitions between fluctuating asymmetry and
directional asymmetry or antisymmetry can be easily modeled via the
Rashevsky-Turing
Reaction Diffusion Equations (Graham et al. 1993). But such phase
transitions
are a general property of complex dynamical systems (Nicolis and
Prigogine
1989). Thus, stress, which influences the feedback term in the
model,
should lead to both symmetry breaking (Graham et al. 1993) and
increased
developmental noise (Emlen et al. 1993). Antisymmetry then
involves
a phase transition leading to the breaking of bilateral symmetry
(Graham et al. 2003).
Directional
asymmetry, which also involves a breaking of bilateral symmetry, occurs
when
there is a slight developmental bias for one side. The slight
initial
bias is ultimately amplified into a large consistent difference (i.e.
directional
asymmetry).
Fluctuating asymmetry, directional asymmetry,
and antisymmetry are dynamically interrelated, and so it is important
to
estimate all three components of asymmetry. In particular,
fluctuating
asymmetry may be estimated from directionally asymmetric traits if the
additive
genetic component for directional asymmetry is nil (Graham et al
1998).
The fluctuating asymmetry variance is simply the residual variance in a
major-axis regression of one side on the other (say left on
right).
In some cases, it may even be possible to estimate the fluctuating
asymmetry
component of an antisymmetric trait, such as the claws of male fiddler
crabs.
Developmental trajectories for male and female
fiddler crabs, Uca urvillei. Females are open circles;
right-dominant males are closed circles; left dominant males are open
squares. From Graham et al. (1998)
The theory presented here can be extended
to include
the concepts of canalization and plasticity. Canalization is an
individual's
ability to produce a consistent phenotype under different environmental
and
genetic conditions, while plasticity is its converse. Plasticity
is
usually adaptive, but such adaptive plasticity cannot be explained by
neo-Darwinian
theory, because the adaptation occurs within the life-span of an
individual.
Emlen et al. (1998) show that adaptive plasticity is an unavoidable
emergent
property of complex organisms. This adaptation involves selection
for
the most energy-efficient physiological and developmental states, or
attractors.
In conclusion, a well-defined theory of
developmental stability may lead to a better understanding of bilateral
asymmetry in multicellular organisms.
Link: Ecotoxicological Applications of
Developmental Stability
Emlen, J. M., D. C. Freeman, and J. H. Graham. 1993. Nonlinear growth dynamics and the origin of fluctuating asymmetry. Genetica 89: 77-96.
Emlen, J. M., D. C. Freeman, A. Mills, J. H. Graham. 1998. How organisms do the right thing: the attractor hypothesis. Chaos 8: 717-726. (pdf)
Freeman, D. C., J. H. Graham, and J. M. Emlen. 1993.
Developmental stability in plants: symmetries, stress and
epigenesis. Genetica 89: 97-119
Graham, J. H., J. M. Emlen, and D. C. Freeman. 2003.
Nonlinear dynamics and developmental instability. Pages 35-50 In:
M. Polak (editor) Developmental Instability: Causes and Consequences.
Oxford University Press, New York.
Graham, J. H., J. M. Emlen, D. C. Freeman, L. J. Leamy, and J. A. Kieser. 1998. Directional asymmetry and the measurement of developmental instability. Biological Journal of the Linnean Society 64: 1-16.
Graham, J. H., D. C. Freeman, and J. M. Emlen. 1993. Antisymmetry, directional asymmetry, and dynamic morphogenesis. Genetica 89: 121-137.
Kozhara, A. V. 1989. On the ratio of components of phenotypic variances of bilateral characters in populations of some fishes. Genetika 25: 1508-1513. (in Russian)
Lajus, D. L. 1991. Analysis of fluctuating asymmetry as a method of population study of the White Sea herring. Proceedings of the Zoological Institute (Leningrad) 235: 113-121. (in Russian)
Lajus, D. L.,
J. H.
Graham, and A. V. Kozhara. 2003.
Developmental instability and the stochastic component of total
phenotypic
variance. Pages 343-363 In: M. Polak
(editor)
Developmental instability: causes and consequences.
Nicolis, G. and I. Prigogine. 1989. Understanding
Complexity.
Freeman, New York.
Zakharov, V. M. 1989. Future prospects for population
phenogenetics. Soviet Scientific Reviews F. Physiology and
General Biology 4: 1-79.
Last Updated 1 February 2008