Background. Organisms use a variety of mechanisms to protect themselves
against perturbations. For example, repair mechanisms fix damage, feedback
loops keep homeostatic systems at their setpoints, and biochemical filters
distinguish signal from noise. Such buffering mechanisms are often discussed in
terms of robustness, which may be measured by reduced sensitivity of
performance to perturbations. Methodology/Principal Findings. I use a
mathematical model to analyze the evolutionary dynamics of robustness in order
to understand aspects of organismal design by natural selection. I focus on two
characters: one character performs an adaptive task; the other character
buffers the performance of the first character against perturbations. Increased
perturbations favor enhanced buffering and robustness, which in turn decreases
sensitivity and reduces the intensity of natural selection on the adaptive
character. Reduced selective pressure on the adaptive character often leads to
a less costly, lower performance trait. Conclusions/Significance. The paradox
of robustness arises from evolutionary dynamics: enhanced robustness causes an
evolutionary reduction in the adaptive performance of the target character,
leading to a degree of maladaptation compared to what could be achieved by
natural selection in the absence of robustness mechanisms. Over evolutionary
time, buffering traits may become layered on top of each other, while the
underlying adaptive traits become replaced by cheaper, lower performance
components. The paradox of robustness has widespread implications for
understanding organismal design
