Structural Constraints, Spandrels, and Exaptation 1243
not only play a refractive role in the lens, but they have important non-refractive
functions within and outside of the eye."
Vertebrate crystallins have been divided into two groups (Wistow, 1993; Lee et
al., 1994): the structural stress-proteins of the alpha and beta/gamma crystallin group
found in most vertebrate lenses; and the highly diverse, so-called "taxon specific"
crystallins, generally found in more restricted lineages, and exapted from enzymes
that continue to operate in their earlier manner elsewhere in the body (and often in the
lens as well).
The structural proteins of the first group also represent exaptations, rather than
direct adaptations, for vision. This cascade of reinterpretation began in the early
1980's with the discovery that alpha crystallins are homologs of the small heat shock
proteins of Drosophila. One of the two alpha crystallin genes continues to produce a
heat shock protein (Piatigorsky et al., 1994), while the other has become more
specialized for lens functions, although both also continue to act as molecular
chaperones. The beta/gamma crystallins (Piatigorsky and Wistow, 1991) are more
distantly related to microbial dormancy proteins, also inducible by osmotic shock and
other stresses.
But the second group of «taxon specific» crystallins shows far more diversity in
their multiple routes of exaptation from previous functions (often still retained) as
enzymes. For example, delta crystallin of chickens is arginino-succinate lyase;
epsilon crystallin of ducks is identical with the metabolic enzyme lactate
dehydrogenase; tau crystallin of turtles is alpha-enolase; and mu crystallin, found in
many marsupials, is ornithine cyclodeaminase (Piatigorsky, 1993b). In a proof of
multiple recruitability in independent events across great phyletic distances, the eta
crystallin that constitutes more than 25 percent of soluble proteins in the lens of
elephant shrews is the enzyme cytoplasmic aldehyde dehydrogenase (Piatigorsky and
Wistow, 1991), whereas the omega crystallin of octopuses has also been exapted
from aldehyde dehydrogenase in a separate cephalopod event (Piatigorsky et al.,
1994). The theme of lens proteins as exapted enzymes then extends to further
phyletic diversity, for the major lens component of squid S crystallin, is related to the
detoxification enzyme glutathione S-transferase.
Piatigorsky (1993a, p. 284) summarizes the dominant role of exaptation for the
origin and status of lens crystallins: "A number of the crystallins have been shown to
be expressed outside of the lens and to possess its original nonrefractive activity.
Indeed, a hallmark of an enzyme-crystallin is that it is expressed at high
concentration in the refractive lens and at a much lower concentration in other
tissues, where it has at least one other non-refractive role."
Since examples of exaptation always raise the structuralist theme of
preconditions for recruitment, we must ask what common properties of proteins and
enzymes in this large array of highly disparate sources prompts or facilitates
cooptation as lens crystallins. Some evident requirements—with transparency as the
most obvious property—probably represent merely incidental and nonadaptive
consequences of molecular structures evolved for other reasons, in the same evident
sense that natural selection did not make our blood