This file was created by scanning the printed publication.
Errors identified by the software have been corrected;
however, some errors may remain.
EVOLUTION OF WEEDY ANNUALS
Howard C. Stutz
of life. Organisms with brief lifespans usually experience
fewer environmental modifications than those with long
lifespans. Consequently, since natural selection always
tends to reduce plasticity, and hence lifespan, annual
plants are the result of exposure of populations to long
or intense directional selection. In many cases natural
selection is so effective in reducing plasticity that the species produced are so genetically and phenotypically uniform that they are incapable of accommodating new challenges when they arise and therefore become extinct.
ABSTRACT
In the evolution of annual plants. natural selection
always reduces both phenotypic plasticity and genetic flex·
ibility. All annuals derived by natural selection are there·
fore phenotypically uniform and self-fertilized. Some annuals have become weedy because they were fortuitously
preadapted for successful occupation of new "weedy» habi·
tats created by humans. Others became weedy because of
novel adaptive plasticity displayed when introduced into
new habitats. A few weedy annuals are genetically flexible
and also phenotypically plastic. These are not the products of natural selection, but owe their plasticity and flexibility to their recent origin from an ancestry that included
hybridization between a genetically uniform, phenotypi·
cally constant, annual species and a genetically flexible.
phenotypically plastic, perennial species. Because of the
resulting rich genetic heritage. these are sometimes phe·
nomenally aggressive.
Genetic Flexibility
Reduction of lifespan by natural selection is always
accompanied by, and accomplished by, a reduction in
genetic flexibility. As a result, most annual plants are
genetically uniform. During the long history of selection
that results in annual growth habit, many genotypes are
discarded. In contrast to many perennial species, each
plant in populations of most annual species is almost
identical to each of the others. Also, because annuals are
low in both flexibility and plasticity, even plants in separate populations of annual species are nearly identical.
Such high levels of integrity usually make annuals easy
to describe taxonomically. High integrity also makes them
highly susceptible to extinction.
The reduction in flexibility that results from intense
selection can be accomplished in several ways, the most
conspicuous of which is a reduction in effective sexuality.
Many, and probably the vast majority, of annuals have
"given up sex" in that most have perfect flowers and are
therefore capable of self-fertilization. Some are monoecious, which also permits self-fertilization. Rarely are
annual species dioecious. As shown in table 1, all annuals
INTRODUCTION
Survival on planet Earth is an awesome challenge.
Considering that no two spots on Earth are identical
and that no spot on Earth remains unchanged, even for
a moment, it is a marvel that living organisms can survive here at all. In a broad sense they do so because of
two principal attributes: (1) phenotypic plasticity and
(2) genetic flexibility.
Phenotypic Plasticity
Plasticity refers to the range of phenotypic expressions
that may be expressed by one specific genotype. Since
there is perpetual inconstancy everywhere on Earth, considerable plasticity is required of every living organism.
As the environment changes, so must each organism.
Death occurs when plasticity is insufficient to accommodate new conditions.
As pointed out by Waddington (1953), Stutz (1962), and
others, plasticity is under genetic control and is thereby
affected by natural selection. Where environmental
changes are rampant and natural selection is consequently minimal, plasticity is high. Where environmental
conditions are more constant and natural selection is
therefore more intensive and effective, plasticity is low.
Consequently natural selection always tends to reduce
plasticity.
One of the most conspicuous avenues by which plasticity may be altered is by extending or reducing the length
Table 1-8exuality of the annual species in the family Chenopod·
iaceae in North America (from Standley 1916)
Genus
Aphanlsma
Atriplex
8/itum
Chenopodium
Corispermum
Cyco/oma
Endolepis
Maiomarla
Mono/apis
Salicomia
Suaeda
Suckleya
Paper presented at the Symposium on Ecology, Management, and Restoration of Intermountain Annual Rangelands, Boise, ID, May 18-22, 1992.
Howard C. Stutz is Professor, Department of Botany and Range Sci·
ence, Brigham Young University, Provo, UT 84602.
Total
9
Bisexual
Number of s~ecles
Dloeclous
Moneclous
1
0
1
32
2
1
0
1
3
3
10
0
0
25
0
0
0
0
2
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
54
28
0
in the family Chenopodiaceae are hermaphroditic or
monoecious and therefore capable of self-fertilization.
Also among 101 species of grasses catalogued by Stebbins
(1950), 27 of the 30 annual species were self-fertile, three
were facultatively cross-fertilized, and none were obligately
cross-fertilized.
The inbreeding that results from self-fertilization in
annuals results in high levels of homozygosity. The principal source of variation to annuals is therefore from new
mutations. Because of their short lifespan, new mutations can be more readily incorporated in annual species
than in perennials, which is probably why the extinction
rate in annuals is less than would otherwise be expected.
Table 3-Lifespan and sexuality of Australian chenopods (from
Wilso~ 1984)
In contrast to annuals, perennial species are less subject to strong selection for phenotypic plasticity. During
the long lifespan of perennials, selection vacillates from
moment to moment, day to day, year to year, and therefore ~ermits the perpetuation of high levels of plasticity.
The unpact on genetic flexibility that accompanies intense
selection for low plasticity in annuals is therefore reduced
in perennials. Genetic flexibility in perennials may therefore be altered by natural selection independently of alterations in plasticity. Consequently, although selection for
low plasticity is always accompanied by a concomitant reduction in genetic flexibility, strong selection for reduced
genetic flexibility does not necessarily carry with it a corresponding reduction in phenotypic plasticity.
This is conspicuous in the modes of sexuality expressed
in perennials as compared with those in annuals. As
shown in tables 2 and 3, although all annual species of
chenopods in both North America and Australia are either
hermaphroditic or monoecious (and therefore have low
genetic flexibility), perennials may be hermaphroditic
monoecious, or dioecious. The higher frequency ofhe;maphroditic perennials in Australia, compared to North
America, reflects the much longer history of chenopod
evolution in Australia. During the millions of years of
com.P~atively more stable geology in Australia, genetic
fleXIbihty has been reduced in perennial chenopods by
natural selection resulting in a high incidence of perfect
1
0
0
0
31
0
0
1
0
1
0
0
1
2
Total
3
0
1
0
0
0
0
0
6
31
0
2
0
16
85
13
10
0
8
Total
29
103
Weedy annuals are usually subject to novel environments not experienced by nonweedy annuals and therefore have some unique attributes. Because they usually
occupy habitats that have been only recently disturbed by
humans, their uniqueness is new. In some cases, annuals
have become weedy because their genetic uniformity and
low plasticity fortuitously favor some particular uniform,
extant habitat created by human activity. Such appears
to be the case with weeds such as "lambsquarter" (Chenopodium album) and "purslane" (Portulaca oleracea) that
have found a favorable habitat in our gardens. They both
show little genetic flexibility and low phenotypic plasticity. Their success as weedy annuals appears, therefore,
to result mostly from a fortuitous abundance of a uniform
habitat to which they happened to be suitably adapted.
Some weedy annuals appear to have become successful because of residual phenotypic plasticity that became
Number of species
Moneclous
Dloeclous
Allenrolfia
Atripfex
Cerato/des
Grayia
Kochis
Sarcobatus
Suaeda
Zuckia
Annual
Perennial
Number of species
Moneclous Dloeclous
WEEDYVS. NONWEEDY ANNUALS
Table 2-5exuality of the perennial species of the family Chenopodiaceae in North America (from Standley 1916)
Bisexual
Bisexual
flowers. In contrast, because of the younger, less stable,
geology of North America, genetic uniformity bas been
less severely selected, and most perennials are consequently dioecious and therefore rich in genetic flexibility.
Phenotypic plasticity and genetic flexibility of plants
are thus reflections of the stability or instability of the
landscapes they occupy. Tumultuous environmental
changes translate to low predictability, and hence relaxed
selection, the consequence of which is high plasticity and
high flexibility. Repeated, predictable conditions such as
those that occur diurnally, seasonally, or after a summer
rainstorm, or in a plowed field, equate to effective selection, which always reduces both plasticity and flexibility.
As shown in table 4, high flexibility and high plasticity
~acterize perennials that occupy fluctuating, unpredictable sites. They are typically dioecious. Monoecious
or bisexual perennials that occupy rythmically predictable, but restricted, sites have sufficient plasticity to permit their long lifespan but, because of inbreeding, are low
in genetic flexibility. Highly predictable, narrow ecological sites are occupied by self-fertilized annuals that are
low in both flexibility and plasticity. There are no dioecious annuals, because they would require low plasticity
and high flexibility, an impossible situation because selection for low plasticity is always accompanied by selection
for low flexibility. Exceptions are in cases like cereal rye
that have a cross-fertilized perennial in their recent ancestry from which they attained both high flexibility and
high plasticity.
ANNUALS VS. PERENNIALS
Genus
Lifespan
10
Tabla 4-lntaractions of genetic flexibility and phenotypic plasticity in relation to lifespans and sexual strategies in chenopods
Flexibility
Sexual
strategy
Plasticity
LHespan
High
Dioecious
High
Perennial
High
Dioecious
Low
Annual
Low
Monoecious
or bisexual
High
Low
Monoceclous
or bisexual
Low
Ecological
niche
Examples
(genera)
Wide,
unpredictable
Atriplex
Perennial
Restricted.
rhythmically
predictable
Cerato/des
Sarcobatus
Maireana
Sclero/aena
Annual
Narrow, highly
predictable
Chenopodium
Atriplex
species, one of which is cereal rye (Secale cereale). The
annual habit, rich genetic flexibility, and extensive phenotypic plasticity of cereal rye preadapted it for its rapid
invasion of disturbed habitats both in the Middle East
and in western North America.
released in their new environments, without significant
increase in genetic flexibility. This appears to be true of
Bromus tectorum, 8alsola australis, Halogeton glomerata,
and several other species that became weedy upon introduction into new environments.
Other weedy annuals owe their success to t:Jleir evolutionary ancestry. This is true of the annual species Secale
cereale (cultivated rye), which only recently became weedy
in the Western United States. In contrast to most annuals, 8ecale cereale is cross-fertilized and is therefore rich
in genetic flexibility. It also differs from most annuals in
being phenotypically highly plastic. S. cereale obtained
these striking attributes from its ancestors, not from relaxed selection. One ancestor of 8ecale cereale (Secale
silvestre) is a highly uniform, self-fertilized annual species. As with most annuals, it is extremely site specific,
growing only in the sandy steppes of southwestern Russia
and southeastern Europe. It is low in both genetic flexibility and phenotypic plasticity. The other ancestor of
cultivated rye, 8. montanum, is a cross-fertilized, highly
variable, perennial species. It has a widespread distribution throughout the Mediterranean and Middle East countries from Spain and Morocco to Iran and Iraq. It is rich
in both genetic flexibility and phenotypic plasticity. Hybrids are common between S. montanum and S. silvestre
(and 8. vavilovii, a derivative of 8. silvestre) in northeastem Turkey and northwestern Iran. Hybrid swarms resulting from these hybrids have produced several new
ACKNOWLEDGMENTS
Gratitude is expressed to BHP-Utah International Inc.
for extensive support and encouragement of research from
which many of these concepts were generated.
REFERENCES
Standley, P. C. 1916. Chenopodiaceae. North American
Flora. 2: 1-93.
Stebbins, G. L. 1950. Variation and evolution in plants.
New York: Columbia University Press. 643 p.
Stutz, H. C. 1962. Within penetrance, between penetrance
and expressivity of the elymoides mutant in rye. Journal of Heredity. 53: 66-71.
Stutz, H. C. 1972. On the origin of cultivated rye. AmericanJournal ofBotany. 59:59-70.
Waddington, C. H. 1953. Genetic assimilation of an acquired character. Evolution. 7: 118-126.
Wilson, P. G. 1984. Chenopodiaceae. In: Flora of Australia.
vol. 4: 81-854.
11