A POPULATION GENETIC THEORY OF CANALIZATION (original) (raw)
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Center for Computational Ecology Department of Ecology and Evolutionary Biology Yale University New Haven Connecticut 06520‐8041
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Center for Computational Ecology Department of Ecology and Evolutionary Biology Yale University New Haven Connecticut 06520‐8041
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Homayoun Bagheri‐Chaichian
Center for Computational Ecology Department of Ecology and Evolutionary Biology Yale University New Haven Connecticut 06520‐8041
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Accepted:
20 November 1996
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Abstract
Canalization is the suppression of phenotypic variation. Depending on the causes of phenotypic variation, one speaks either of genetic or environmental canalization. Genetic canalization describes insensitivity of a character to mutations, and the insensitivity to environmental factors is called environmental canalization. Genetic canalization is of interest because it influences the availability of heritable phenotypic variation to natural selection, and is thus potentially important in determining the pattern of phenotypic evolution. In this paper a number of population genetic models are considered of a quantitative character under stabilizing selection. The main purpose of this study is to define the population genetic conditions and constraints for the evolution of canalization. Environmental canalization is modeled as genotype specific environmental variance. It is shown that stabilizing selection favors genes that decrease environmental variance of quantitative characters. However, the theoretical limit of zero environmental variance has never been observed. Of the many ways to explain this fact, two are addressed by our model. It is shown that a “canalization limit” is reached if canalizing effects of mutations are correlated with direct effects on the same character. This canalization limit is predicted to be independent of the strength of stabilizing selection, which is inconsistent with recent experimental data (Sterns et al. 1995). The second model assumes that the canalizing genes have deleterious pleiotropic effects. If these deleterious effects are of the same magnitude as all the other mutations affecting fitness very strong stabilizing selection is required to allow the evolution of environmental canalization. Genetic canalization is modeled as an influence on the average effect of mutations at a locus of other genes. It is found that the selection for genetic canalization critically depends on the amount of genetic variation present in the population. The more genetic variation, the stronger the selection for canalizing effects. All factors that increase genetic variation favor the evolution of genetic canalization (large population size, high mutation rate, large number of genes). If genetic variation is maintained by mutation‐selection balance, strong stabilizing selection can inhibit the evolution of genetic canalization. Strong stabilizing selection eliminates genetic variation to a level where selection for canalization does not work anymore. It is predicted that the most important characters (in terms of fitness) are not necessarily the most canalized ones, if they are under very strong stabilizing selection (k > 0.2_Ve_). The rate of decrease of mutational variance Vm is found to be less than 10% of the initial Vm. From this result it is concluded that characters with typical mutational variances of about 10–3 Ve are in a metastable state where further evolution of genetic canalization is too slow to be of importance at a microevolutionary time scale. The implications for the explanation of macroevolutionary patterns are discussed.
Literature Cited
Altenberg
,
L.
1994
.
The evolution of evolvability in genetic programming
. Pp.
47
–
74
in
J. K. E.
Kinnear
, ed. Advances in genetic programming.
MIT Press
,
Cambridge, MA
.
Barton
,
N. H.
, and
M.
Turelli
.
1987
.
Adaptive landscapes, genetic distance and the evolution of quantitative characters
.
Genet. Res. Camb.
49
:
157
–
173
.
Barton
,
N. H.
, and
M.
Turelli
.
1989
.
Evolutionary quantitative genetics: How little do we know?
Annu. Rev. Genet.
23
:
337
–
370
.
Bulmer
,
M. G.
1980
. The mathematical theory of quantitative genetics.
Clarendon Press
,
Oxford
.
Bürger
,
R.
1988
.
Mutation‐selection balance and continuum‐of‐alleles models
.
Math. Biosci.
91
:
67
–
83
.
Bürger
,
R.
1989
.
Linkage and the maintenance of heritable variation by mutation‐selection balance
.
Genetics
121
:
175
–
184
.
Bürger
,
R.
1991
.
Moments, cumulants, and polygenic dynamics
.
J. Math. Biol.
30
:
199
–
213
.
Bürger
,
R.
, and
J.
Hofbauer
.
1994
.
Mutation load and mutation‐selection balance in quantitative genetic traits
.
J. Math. Biol.
32
:
193
–
218
.
Bürger
,
R.
,
G. P.
Wagner
, and
F.
Stettinger
.
1989
.
How much heritable variation can be maintained in finite populations by mutation‐selection balance?
Evolution
43
:
1748
–
1766
.
Cheverud
,
J.
, and
E.
Routman
.
1995
.
Epistasis and its contribution to genetic variance components
.
Genetics
139
:
1455
–
1461
.
Clayton
,
G. A.
, and
A.
Robertson
.
1955
.
Mutation and quantitative variation
.
Am. Nat.
89
:
151
–
159
.
Crow
,
J. F.
, and
M.
Kimura
.
1970
. An introduction to population genetics theory.
Harper & Row
,
New York
.
Davies
,
A. G.
,
A. Y.
Game
,
Z.
Chen
,
T. J.
Williams
,
S.
Goodall
,
J. L.
Yen
,
J. A.
McKenzie
, and
P.
Batterham
.
1996
.
Scalloped wings is the Lucilia cuprina Notch homologue and a candidate for the modifier of fitness and asymmetry of Diazinon resistance
.
Genetics
143
:
1321
–
1337
.
Endler
,
J. A.
1986
. Natural selection in the wild.
Princeton Univ. Press
,
Princeton, NJ
.
Ewens
,
W. J.
1979
. Mathematical population genetics.
Springer
,
Berlin
.
Falconer
,
D. S.
1981
. Introduction to quantitative genetics.
Longmans
,
London
.
Fleming
,
W. H.
1979
.
Equilibrium distribution of continuous polygenic traits
.
Siam. J. Appl. Math.
36
:
148
–
168
.
Gavrilets
,
S.
, and
A.
Hastings
.
1994
.
A quantitative‐genetic model for selection on developmental noise
.
Evolution
48
:
1478
–
1486
.
Gibson
,
G.
, and
D. S.
Hogness
.
1996
.
Effect of polymorphism in the Drosophila regulatory gene Ultrabithorax on homeotic stability
.
Science
271
:
200
–
203
.
Goodman
,
N.
1955
. Fact, fiction, forecast.
Hackett Publ. Co.
,
Indianapolis
.
Goodnight
,
C. J.
1987
.
On the effect of founder events on epistatic genetic variance
.
Evolution
41
:
80
–
91
.
Goodnight
,
C. J.
1988
.
Epistasis and the effect of founder events on the additive genetic variance
.
Evolution
42
:
441
–
454
.
Haken
,
H.
1978
. Synergetics.
Springer‐Verlag
,
New York
.
Houle
,
D.
,
K. K.
Hoffmaster
,
S.
Assimacopoulos
, and
B.
Charlesworth
.
1992
.
The genomic mutation rate for fitness in Drosophila
.
Nature
359
:
58
–
60
.
Kauffman
,
S. A.
1993
. The origins of order.
Oxford Univ. Press
,
New York
.
Kauffman
,
S. A.
, and
S.
Levin
.
1987
.
Towards a general theory of adaptive walks on rugged landscapes
.
J. Theor. Biol.
128
:
11
–
45
.
Keightley
,
P. D.
, and
W. G.
Hill
.
1988
.
Quantitative genetic variability maintained by mutation‐stabilizing selection balance in finite populations
.
Genet. Res., Camb.
52
:
33
–
43
.
Lande
,
R.
1975
.
The maintenance of genetic variability by mutation in a polygenic character with linked loci
.
Genet. Res.
26
:
221
–
235
.
Lande
,
R.
1980
.
The genetic covariance between characters maintained by pleiotropic mutations
.
Genetics
94
:
203
–
215
.
Layzer
,
D.
1980
.
Genetic variation and progressive evolution
.
Am. Nat.
115
:
809
–
826
.
Lynch
,
M.
1988
.
The rate of polygenic mutation
.
Genet. Res.
51
:
137
–
148
.
Mackay
,
T. F. C.
,
R. F.
Lyman
, and
M. S.
Jackson
.
1992a
.
Effects of P‐element insertions on quantitative traits in Drosophila melanogaster
.
Genetics
130
:
315
–
332
.
Mackay
,
T. F. C.
,
R. F.
Lyman
,
M. S.
Jackson
,
C.
Terzian
, and
W. G.
Hill
.
1992b
.
Polygenic mutation in Drosophila melanogaster. estimates from divergence among inbred strains
.
Evolution
46
:
300
–
316
.
Mackay
,
T. F. C.
,
R. F.
Lyman
, and
W. G.
Hill
.
1995
.
Polygenic mutation in Drosophila melanogaster: non‐linear divergence among unselected strains
.
Genetics
139
:
849
–
859
.
Mather
,
K.
1953
.
The genetical structure of populations
.
Symp. Soc. Exp. Biol.
7
:
66
–
95
.
Moreno
,
G.
1994
.
Genetic architecture, genetic behavior, and character evolution
.
Annu. Rev. Ecol. Syst.
25
:
31
–
44
.
Prout
,
T.
1962
.
The effects of stabilizing selection on the time of development in Drosophila melanogaster
.
Genet. Res. Camb.
3
:
364
–
382
.
Raff
,
R. A.
, and
T. C.
Kaufman
.
1983
. Embryos, genes and evolution.
MacMillan
,
New York
.
Rechenberg
,
I.
1973
. Evolutionsstrategie.
Friedrich Frommann
,
Stuttgart
.
Rechenberg
,
I.
1997
. Evolution strategy.
Yale Univ. Press
,
New Haven, CT
.
Rendel
,
J. M.
1967
. Canalization and gene control.
Academic Press
,
New York
.
Riedl
,
R.
1978
. Order in living organisms: a systems analysis of evolution.
Wiley
,
New York
.
Robertson
,
F. W.
1964
.
The ecological genetics of growth in Drosophila. 7. The role of canalization in the stability of growth relations
.
Genet. Res.
5
:
107
–
126
.
Routman
,
E.
, and
J. M.
Cheverud
.
1994
.
Individual genes underlying quantitative traits: molecular and analytical methods
. Pp.
593
–
606
in
B.
Schierwater
,
B.
Streit
,
G. P.
Wagner
and
R.
DeSalle
, eds. Molecular ecology and evolution: approaches and applications.
Birkhäuser Verlag
,
Berlin
.
Scharloo
,
W.
1991
.
Canalization: genetic and developmental aspects
.
Ann. Rev. Ecol. Syst.
22
:
65
–
93
.
Scheiner
,
S. M.
1993
.
Genetics and the evolution of phenotypic plasticity
.
Ann. Rev. Ecol. Syst.
24
:
35
–
68
.
Scheiner
,
S. M.
,
R. L.
Caplan
, and
R. F.
Lyman
.
1991
.
The genetics of phenotypic plasticity. III. Genetic correlations and fluctuating asymmetries
.
J. Evol. Biol.
4
:
51
–
68
.
Schlichting
,
C. D.
1986
.
The evolution of phenotypic plasticity in plants
.
Ann. Rev. Ecol. Syst.
17
:
667
–
693
.
Schmalhausen
,
I. I.
1986
. Factors of evolution: the theory of stabilizing selection.
Univ. of Chicago Press
,
Chicago and London
.
Stearns
,
S. C.
1992
. The evolution of life histories.
Oxford Univ. Press.
,
Oxford
.
Stearns
,
S. C.
1993
.
The evolutionary links between fixed and variable traits
.
Acta Paleont. Polonica
38
:
1
–
17
.
Stearns
,
S. C.
, and
T. J.
Kawecki
.
1994
.
Fitness sensitivity and the canalization of life history traits
.
Evolution
48
:
1438
–
1450
.
Stearns
,
S. C.
,
M.
Kaiser
, and
T. J.
Kawecki
.
1995
.
The differential canalization of fitness components against environmental perturbations in Drosophila melanogaster
.
J. Evol. Biol.
8
:
539
–
557
.
Tebb
,
G.
, and
J. M.
Thoday
.
1954
.
Stability in development and relational balance of X‐chromosomes in Drosophila melanogaster
.
Nature
174
:
1109
–
1110
.
Turelli
,
M.
1984
.
Heritable genetic variation via mutation‐selection balance: Lerch's Zeta meets abdominal bristle
.
Theor. Popul. Biol.
25
:
138
–
193
.
Vogl
,
C.
1996
.
Developmental buffering and selection
.
Evolution
50
:
1343
–
1346
.
Waddington
,
C. H.
1957
. The strategy of the genes.
MacMillan Co.
,
New York
.
Wagner
,
A.
1996
.
Does evolutionary plasticity evolve?
Evolution
50
:
1008
–
1023
.
Wagner
,
G. P.
1986
.
The systems approach: an interface between development and population genetic aspects of evolution
. Pp.
149
–
165
in
D. M.
Raup
and
D.
Jablonski
, eds. Patterns and processes in the history of life.
Springer
,
Berlin
.
Wagner
,
G. P.
1989
.
Multivariate mutation‐selection balance with constrained pleiotropic effects
.
Genetics
122
:
223
–
234
.
Wagner
,
G. P.
, and
L.
Altenberg
.
1996
.
Complex adaptations and the evolution of evolvability
.
Evolution
50
:
967
–
976
.
Whitlock
,
M. C.
,
P. C.
Phillips
,
F. G.‐G.
Moore
, and
S. J.
Tonsor
.
1995
.
Multiple fitness peaks and epistasis
.
Ann. Rev. Ecol. Syst.
26
:
601
–
629
.
Wimsatt
,
W. C.
, and
J. C.
Schank
.
1988
.
Two constraints on the evolution of complex adaptations and the means for their avoidance
. Pp.
231
–
273
in
M.
Nitecki
and
D.
Nitecki
, eds. Evolutionary progress.
Univ. of Chicago Press
,
Chicago, IL
.
Zhivotovsky
,
L. A.
, and
S.
Gavrilets
.
1992
.
Quantitaive variability and multilocus polymorphism under epistatic selection
.
Theor. Popul. Biol.
42
:
254
–
283
.
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