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concerted evolution: selection and drift suffice

arlin at ac.dal.ca arlin at ac.dal.ca
Thu Dec 5 14:37:04 EST 1991

The explanation for concerted evolution was recently discussed here by
Dover and Felsenstein, who expressed opposing views.  Both seem to
have a similar conception of the observed *phenomenon* to be
explained, concerted evolution. They also seem to agree on the
importance of unequal crossing over and gene conversion in any
*mechanistic explanation* of concerted evolution. However, to explain
concerted evolution, Dover posits a "force" or process of genetic
change called "molecular drive" that he says is distinct from
selection and drift, while Felsenstein suggests that:

>The above mechanisms [gene conversion, crossing over, etc] having
>already been known, and under active investigation as explanations
>for concerted evolution, it seems of no utility to declare the
>discovery of a new evolutionary force [i.e., molecular drive] which
>consists of these forces.

Although it is true George P. Smith and others modelled concerted
evolution by "crossover fixation" in 1973 (see the CSH Symposium of
Quantitative Biology) without invoking "molecular drive," this
historical matter does not answer the question of whether "crossover
fixation" or "molecular drive" (or whatever the mechanism is to be
called) is fundamentally different from allele replacements by
selection or drift.

That the mechanism at the heart of this issue is distinct from
selection and drift acting through organismal reproduction is easily
shown by the fact that we can remove both deterministic and stochastic
differences in organismal reproduction, and still get allele
replacements by what Dover calls "molecular drive."  Consider a
population of 100 individuals, 25 BB, 50 Bb, and 25 bb.  We can
consider a case of no deterministic differences in reproduction: each
type has the same fitness, and thus the same expected number of
offspring.  And we can further stipulate no stochastic differences:
each type not only has the same *expected* number of offspring, they
each have exactly the same *realized* number of offspring.  Thus, each
generation, each of 100 individuals has a number of offspring such
that exactly 1 survives to reproduce in the next generation, which
will also number 100 individuals.

Can the frequencies of alleles B and b ever change?  Indeed they can,
though they cannot change due to differences in organismal
reproduction, since we have excluded this possibility. If something
like gene conversion is allowed to happen, at some time a Bb can
become a BB: thus a small change in allele frequencies. It matters not
whether the conversion is biased-- changes in allelic frequencies will
still occur (either deterministically or stochastically) and may
eventually lead to an allele replacement, given enough time.

The above example shows clearly that there is a mechanism for genetic
change that is distinct from selection and drift acting through
organismal reproduction.  Oddly enough, this observation does not
necessitate the establishment of any "force" other than selection and
drift.  What Dover calls "molecular drive" is really selection and
drift acting through reproductive differences that are not differences
in *organismal* reproduction, but rather differences in reproduction
at a *sub-organismal* level.

Thus, concerted evolution cannot be treated as a problem of selection
and drift acting solely on the basis of organismal reproduction.
Rather, differences (both stochastic and deterministic, for unbiased
and biased mechanisms, respectively) in the reproduction of sequences
within an individual must also be included.  Dover is to be credited
for having the savvy to feel a certain dissonance when the mechanism
of concerted evolution is mistakenly treated as a problem of mutation
+ selection + drift acting solely at the population level.  However,
Dover's answer to this anomaly misses the mark: THE PROBLEM IS NOT THE
AND DRIFT CAN ACT ON REPRODUCTION.  Concerted evolution requires
selection or drift at the level of suborganismal reproduction (and
probably always also involves selection or drift at the level of
organismal reproduction.)

The real problem at hand is this: how to formulate an evolutionary
genetics theory/terminology with the sophistication to account for the
effects of differential reproduction at diverse levels of biological
organization (chromosome, individual, population).  This evolutionary
genetics must be able to deal with concerted evolution, which is the
combined result of selection/drift at two or more different levels of
a reproductive hierarchy (the hierarchy consists of the fact that
individuals reproduce only if individuals' chromosomes reproduce, only
if chromosomes' sequences reproduce: but the three processes do not
occur in lock-step).

For a simple case involving gene conversion at a single locus, we can
describe each diploid organism as a population of 2 chromosomes.
Within each such tiny population, an allele replacement (Bb to BB, for
example) can take place by gene conversion in a single generation.
Considering the larger population, allele frequency changes at the B
locus will result from the dual processes of 1) selection/drift among
chromosomes of individuals by gene conversion; and 2) selection/drift
among individuals through reproductive differences.

I am personally unable to give an adequate representation of more
complicated examples: multilocus cases with gene conversion, unequal
crossing over, slippage, etc. (others may feel free to try). However,
I hereby forego and forfend the use of the term "molecular drive"
(which I have used in the past) and I encourage others to do the same.
Let's think hierarchically, rather than propose new forces. There lies
the answer to concerted evolution, and perhaps to other interesting
evolutionary phenomena.

Arlin Stoltzfus

Arlin at ac.dal.ca

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