Not black and white
JERRY A. COYNE
Melanism: Evolution in Action
by Michael E. N. Majerus
Oxford University Press: 1998. 338 pp. £55, $105 (hbk), £23.95, $45 (pbk)
>From time to time, evolutionists re-examine a classic experimental study
and find, to their horror, that it is flawed or downright wrong. We no
longer use chromosomal polymorphism in Drosophila pseudoobscura to
demonstrate heterozygous advantage, flower-colour variation in Linanthus
parryae to illustrate random genetic drift, or the viceroy and monarch
butterflies to exemplify Batesian mimicry. Until now, however, the prize
horse in our stable of examples has been the evolution of 'industrial
melanism' in the peppered moth, Biston betularia, presented by most
teachers and textbooks as the paradigm of natural selection and evolution
occurring within a human lifetime. The re-examination of this tale is the
centrepiece of Michael Majerus's book, Melanism: Evolution in Action.
Depressingly, Majerus shows that this classic example is in bad shape, and,
while not yet ready for the glue factory, needs serious attention.
According to the standard textbook litany, before the mid-nineteenth
century, all B. betularia in England were white moths peppered with black
spots, a form called typica. Between 1850 and 1920, typica was largely
replaced by a pure black form (carbonaria) produced by a single dominant
allele, the frequency of which rose to nearly 100% in some areas. After
1950, this trend reversed, making carbonaria rare and typica again common.
These persistent and directional changes implied natural selection. In a
series of studies, this conclusion was verified by several investigators,
most prominently Bernard Kettlewell of Oxford.
According to these workers, the evolution of colour was caused by birds
eating the moths most conspicuous on their normal resting site -- tree
trunks. The increase in black moths was attributed to pollution
accompanying the rise of heavy industry. A combination of soot and acid
rain darkened trees by first killing the lichens that festooned them and
then blackening the naked trunks. The typica form, previously camouflaged
on lichens, thus became conspicuous
and heavily predated, while the less visible carbonaria enjoyed protection
and increased in frequency. After the passage of the Clean Air Acts in the
1950s, trees regained their former appearance, reversing the selective
advantage of the morphs. This conclusion was bolstered by a geographical
correlation between pollution levels and morph frequencies (carbonaria was
most common in industrial areas), and most prominently by Kettlewell's
famous experiments which showed that, after releasing typica and carbonaria
in both polluted and unpolluted woods, researchers recaptured many more of
the cryptic than of the conspicuous form. The differential predation was
supported by direct observation of birds eating moths placed on trees.
Finally, Kettlewell demonstrated in the laboratory that each form had a
behavioural preference to settle on backgrounds that matched its colour.
Criticisms of this story have circulated in samizdat for several years, but
Majerus summarizes them for the first time in print in an absorbing
two-chapter critique (coincidentally, a similar analysis [Sargent et al.,
Evol. Biol. 30, 299-322; 1998] has just appeared). Majerus notes that the
most serious problem is that B. betularia probably does not rest on tree
trunks -- exactly two
moths have been seen in such a position in more than 40 years of intensive
search. The natural resting spots are, in fact, a mystery. This alone
invalidates Kettlewell's release-recapture experiments, as moths were
released by placing them directly onto tree trunks, where they are highly
visible to bird predators. (Kettlewell also released his moths during the
day, while they
normally choose resting places at night.) The story is further eroded by
noting that the resurgence of typica occurred well before lichens
recolonized the polluted trees, and that a parallel increase and decrease
of the melanic form also occurred in industrial areas of the United States,
where there was no change in the abundance of the lichens that supposedly
play such an important role.
Finally, the results of Kettlewell's behavioural experiments were not
replicated in later studies: moths have no tendency to choose matching
backgrounds. Majerus finds many other flaws in the work, but they are too
numerous to list here. I unearthed additional problems when, embarrassed at
having taught the standard Biston story for years, I read Kettlewell's
papers for the first time.
Majerus concludes, reasonably, that all we can deduce from this story is
that it is a case of rapid evolution, probably involving pollution and bird
predation. I would, however, replace "probably" with "perhaps". B.
betularia shows the footprint of natural selection, but we have not yet
seen the feet. Majerus finds some solace in his analysis, claiming that the
true story is likely to be more complex and therefore more interesting, but
one senses that he is making a virtue of necessity. My own reaction
resembles the dismay attending my discovery, at the age of six, that it was
my father and not Santa who brought the presents on Christmas Eve.
Occupying a quarter of the book, the Biston analysis is necessary reading
for all evolutionists, as are the introductory chapters on the nature of
melanism, its distribution among animals, and its proposed causes. Majerus,
however, designed his book for both professional and lay readers, and this
causes some unevenness in the material. The Biston story is sandwiched
between less
compelling chapters, including long sections on the basic principles of
genetics and evolution, which can be skipped by evolutionists. Other
discussions, involving melanism in ladybirds and other Lepidoptera, as well
as the author's unpublished work on habitat selection, are full of
technical details that will overwhelm the lay reader. Unfortunately, most
of the work described is inconclusive; despite the widespread occurrence of
melanism, its evolutionary significance is nearly always unknown.
What can one make of all this? Majerus concludes with the usual call for
more research, but several lessons are already at hand. First, for the time
being we must discard Biston as a well-understood example of natural
selection in action, although it is clearly a case of evolution. There are
many studies more appropriate for use in the classroom, including the
classic work of Peter and Rosemary Grant on beak-size evolution in
Galapagos finches. It is also worth pondering why there has been general
and unquestioned acceptance of Kettlewell's work. Perhaps such powerful
stories discourage close scrutiny. Moreover, in evolutionary biology there
is little payoff in repeating other people's experiments, and, unlike
molecular biology, our field is not self-correcting because few studies
depend on the accuracy of earlier ones. Finally, teachers such as myself
often neglect original papers in favour of shorter textbook summaries,
which bleach the blemishes from complicated experiments.
It is clear that, as with most other work in evolutionary biology,
understanding selection in Biston will require much more information about
the animal's habits. Evolutionists may bridle at such a conclusion, because
ecological data are very hard to gather. Nevertheless, there is no other
way to unravel the forces changing a character. We must stop pretending
that we understand the course of natural selection as soon as we have
calculated the relative fitness of different traits.
Jerry A. Coyne is in the Department of Ecology and Evolution, University of
Chicago, 1101 E. 57 Street, Chicago, Illinois 60637, USA.