Download Book Review Mutation Driven Evolution

Journal of Heredity, 2015, 420
doi:10.1093/jhered/esv032
Book Review
Book Review
Mutation Driven Evolution
Masatoshi Nei, Oxford: Oxford University Press, 2014
Masatoshi Nei has been a major contributor to the field of molecular
evolution. In this important book, he argues for, among other things,
the end of “beanbag genetics,” finding the mathematical formulations that describe the effects of selection and drift on single genes
wanting. He casts serious doubt on natural selection as the primary
driving force in evolution, arguing instead that mutation is the major
determinant of evolutionary change.
Given his preeminence in the field, Nei’s assertions must be taken
seriously. In addition to the substantial role he has played in the
birth and maturation of molecular evolution (e.g., the widely used
neighbor-joining phylogenetic algorithm and the development of
dn and ds to measure divergence between homologous sequences),
Nei is an exceptionally clear thinker and writer (as demonstrated in
this book), for example, “evolution by omnipotent natural selection
is similar to creationism, in which natural selection is replaced by
God.”
When it comes to his criticisms of “beanbag genetics,” Nei is
not a naive iconoclast. In Chapter 2 and in an appendix, he very
clearly presents the mathematical theories of population genetics
but finds them essentially meaningless, for example, models with
just two alleles or models assuming constant fitness. He points out
how difficult it is to estimate selection coefficients, and, in discussing Fisher’s fundamental theorem of natural selection, Nei concludes
that “for the theories to be biologically meaningful, the fitness of all
genotypes must remain the same in all generations though allele frequencies may change. But this assumption obviously does not hold,
because genotype fitness depends on environmental condition, and
this condition varies with generation.” Nei finds other simplifying
assumptions behind the mathematical formulations of population
geneticists, including large population sizes, constant (and uncertain)
selection coefficients, constant environmental effects, and no gene
interactions. Hence, “The important problem in the study of evolution is to understand the molecular basis of formation of phenotypic
characters rather than the mathematical basis of increase of population fitness.”
So where does Nei see mutation having a major effect on molecular evolution?
First, in its role in producing gene duplications and pseudogenes
(Chapter 5). In this context, he discusses how the birth and death
model underlies processes of concerted evolution in multigene families. This chapter is richly illustrated with descriptions of multigene
families, for example, immune systems, homeobox genes, and genes
involved in flower development.
Second, in Chapter 6, Nei describes how mutations underlie phenotypic evolution through their effects on gene regulation.
Again, this chapter contains a wealth of examples of systems in
which mutations, including horizontal gene transfers, have resulted
in phenotypic changes in both physiological and morphological
characters.
A third place where Nei sees mutation playing an important
role is speciation (Chapter 7). Obviously, chromosomal mutations
such as polyploidization can lead to immediate speciation but less
obvious are the potential effects of gene mutations on speciation.
Nei discusses two models in detail, the Oka model involving mutations in duplicate genes and the Dobzhansky–Muller model in which
mutations in different genes in different populations can lead to speciation. Heterochromatin-associated effects, segregation distortion,
and even “passive processes” that can lead to speciation are also
considered in Chapter 7.
In Chapter 8, Nei discusses instances where mutations underlie
the origin of adaptations. This chapter examines “simple” adaptations such as wing polymorphisms, asymmetric morphologies,
and blindness in cave fish, as well as multigene systems such as
sex determination and dosage compensation. Even adaptations in
behavioral genes are considered. In these systems, the importance
of newly arising mutations in regulatory genes is emphasized, and
in this chapter in particular, the clarity of Nei’s writing can be
appreciated.
Nei does not deny the existence of natural selection. Indeed, he
points out that purifying selection operates on most genes and recognizes the role of selective sweeps of single nucleotide polymorphisms
in populations. But he does not see natural selection as a creative
force in evolution, dismissing that kind of thinking as teleological.
Given the abundance of selectively neutral or nearly neutral mutations in molecular evolution, he views mutations (broadly defined to
include nucleotide substitutions, indels, gene and genome duplications, and transpositions) as relatively more (perhaps much more?)
important than natural selection in evolution.
Ross MacIntyre
Cornell University
Ithaca, NY
© The American Genetic Association. 2015. All rights reserved. For permissions, please e-mail: [email protected]
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