Jasen
Wise
Final
Draft
Population
Genetics
Pteropsidia Polyploidy
"Under the microscope you can see
the strange and beautiful figures which the chromosomes execute to ensure
proper distribution of genes."
- Julian Huxley, 1953
Introduction
Despite
the absence of a universally accepted definition of a species, most would agree
that definable species exist within biological systems. Evolution, a key component to the origins of
species, is an ongoing and continuously changing force upon a population. Even though
this progression is continuous, it is still possible to define distinct units
where boundaries can be delineated and differentiated from one another. Around
2 million species have been identified through various comparisons such as
morphology, behavior, genetics, and ecology (Haufler and Hooper, 2000). Ferns
present prime examples of how speciation through the mechanisms of ecology and
genetics have lead to a successful, diverse, and genetically stable group of
plants collectively known as division Pteropsida.
The
division Pteropsida consists of the true ferns. There are anywhere between
10,000 to 15,000 species of ferns divided into 40 families. Two common examples of true ferns include
the genus Polystichum, which includes the Christmas Fern and the genus Asplenium,
which contains the Ebony Spleenwort (Cobb,1963). Ferns are among the oldest
extant land plants and appear in the fossil record for the past 360 million
years (Nicholls, 1998). Such long-term success can be partially attributed to
unique fern reproduction and genetic systems.
In order to understand the advantages of polyploidy used by ferns to be
successful and widely distributed throughout the world it is necessary to review the mechanisms by which polyploids
are formed, and types of
polyploids. It is also important to
evaluate the advantages pertaining to
inbreeding depression, buffering
effects, and colonization in reference to the challenges that polyploids must
face when establishing in new areas.
The
Unique Fern Life Cycle
Ferns
exist worldwide and all share an unusual form of reproduction through the
alternation of generations. The completion of each generation involves the
cycling of two very different morphologies and chromosome compliments. Unlike
angiosperms, organism that reproduce via seeds, ferns produce many tiny spores,
each of which forms a small haploid (n) plant called a gametophyte.
Gametophytes produce male and female gametes that form a sporophyte (2n). The
form of the fern familiar to most is called the sporophyte. The sporophyte forms and matures, starting
the cycle again (Cobb, 1963). Having a haploid gametophyte and a diploid
sporophyte allows for many variations in fern chromosome numbers. Multiple
ploidys (variations in chromosome number) sometimes occur within species, which
is termed a cytotype (Soltis and Soltis, 2000). The acquisition of another, or
more than one, extra genome is referred to as polyploidy.
Polyploidy
An organism may be defined as a polyploid
if it has more than two haploid (>2n) sets of chromosomes. In mammals,
polyploidy is devastating, however it occurs often in the plant kingdom. There
are two main types of polyploidy, autopolyploidy and allopolyploidy.
Autopolyploidy is polyploidy in which all the chromosomes originate from the same
diploid parent species. In the experiments of DeYoung et al., (1997) an
autotetraploid fern, Ceratopteris, was identified by the formation of
multivalents at metaphase.
Autopolyploids form multivalents in mitosis when the homologous
chromosomes pair up at metaphase making them easily distinguishable from their
diploid counterparts (DeYoung et al, 1997).
Allopolyploidy is a polyploidy in which the
sets of chromosomes are from different species. Usually hybrid plants (n + n')
are not fertile because proper pairing of chromosomes does not occur in
meiosis. Sometimes the chromosome number spontaneously doubles leaving tissues
with 2n + 2n'. If this tissue is germ
tissue, tissue than can give rise to haploid tissue via meioses, the result can
be gametes with the n + n' chromosome complement. The fusion of two of
these gametes results in an
allopolyploid plant with a viable chromosome complement (2n + 2n'). An example
of an allopolyploid fern is the Green Mountain Maidenhair fern, Adiantum
viridimontanum. This fern was formally described in 1991. The evidence for the allotetraploid cross
between common Woodland Maidenhair (Adiantum pedatum) and Aleutian
Maidenhair (A. aleuticum) is based on genetic evidence (bivalent
mitosis) (Ruesink, 2001).
G.
Ledyard Stebbins (1950) proposed an additional category of polyploidy called
segmental allopolyploidy. Segmental allopolyploids are formed when the parent
diploid is slightly different between its chromosome sets (a vs a'), but its
parents were similar enough to be identified as the same species. A chromosome doubling occurs and a new
segmental allopolyploid is formed. Some
multivalent pairings occur at meiosis but usually with the consequence of a
lower fertility rate than strict allopolyploids. They can also form some
fertile hybrids through backcrossing with autopolyploid derivatives of either
parental species.
There
are several mechanisms by which polyploids arise. Three examples are somatic
doubling, gametic nonreduction and triploid bridges. Somatic doubling occurs at the zygotic, embryonic, or
meristematic stages of a plant’s life cycle. Polyploid offspring can be
generated from the production of polyploid tissues. Although many examples of
polyploidy via somatic doubling have been reported, this mechanism now seems
less common than gametic nonreduction, or the production of unreduced gametes,
as a means of polyploid formation in natural populations (Harlan and deWet,
1975). Unreduced gametes have been
reported in a number of species, most notably those that also produce
polyploids (Ramsey and Schemske, 1998). Both auto- and allopolyploids can arise
in one step after unreduced gamete formation by the union of two unreduced
gametes from the same plant.
Alternatively,
the production of either an auto- or allotetraploid may involve a ‘triploid
bridges”. Tetraploids are formed by
triploid intermediates formed within a diploid population by backcrossing to
diploids or by self fertilization of the triploid. This two-step method has
been considered a significant pathway to polyploid formation (Harlan and deWet,
1975), but some (Bretagnolle and Thompson, 1995) suggest that the one-step
process involving the union of two unreduced gametes may be more common. Ramsey and Schemske (1998) concluded that
the triploid intermediates may be more significant in the formation of
tetraploids since triploids could be
more reproductively viable than originally thought.
The
Advantages of Polyploidy
The
main advantage of polyploidy is the production of heterozygotes. Typically the diploid Mendelian cross of AA
and A’A’ would produce a 1:2:1
genotypic ratio (1 homozygous AA, 2 heterozygous AA’ and, 1 homozygous
A’) of progeny. However, in a polyploid species the frequency of heterozygotes
are much greater. A tetraploid, for example, cross of AAAA and A’A’A’A’ would
result in a genotypic ratio of 1:32:1 (Stebbins, 1947). Heterozygotes offer
many advantages including buffering effects, protection from inbreeding
depression, and the unidirectional introgression phenomenon (Soltis and Soltis,
1995).
Buffering
Effects
Tetrasomic
inheritance has a buffering effect on intermediate genotypes, an effect of
great adaptive value to a population (Stebbins, 1950). This production of
nearly all heterozygous ferns is an advantage because it makes the appearance
of deleterious homozygous alleles rare because of the masking effect of
additional genomes (Soltis and Soltis, 2000).
Two
closely related tetraploid species, for example, that hybridize have five
possible genotypic progeny: (aaaa), (aaaa'), (aaa'a'), (aa'a'a'), and
(a'a'a'a'). Therefore, it can be expected that those with more
"a" alleles would be well suited for an area where that allele
thrived. Likewise it can be expected that a greater composition of the a'
allele would be best suited for areas where a' thrived. This combination
of recombination, natural selection, and genetic segregation is capable of
producing an entire spectrum of genotypic populations that would be compatible
with any region of intermediate environmental conditions (Stebbins, 1971).
Inbreeding
An isolated plant is forced to undergo self fertilization or selfing. In this situation the frequency of deleterious homozygous alleles increases leading to an overall reduction in the colony’s overall fitness. This inbreeding depression is defined as a reduction in fitness and vigor of individuals as a result of increased homozygosity through inbreeding in a normally outbreeding population. For example, an isolated colony of diploid plants would experience an increase in the number of deleterious homozygous alleles and have increased progression towards fixation or even loss of certain alleles. Studies have found that ferns actually have increased production of normal sporophytes when they are isolated and forced into self fertilization (Soltis and Soltis, 2000).
When considering a
single allele at a single locus, the effects of inbreeding depression do not
appear to a problem of great importance. The problem is escalated when all the
loci are taking into consideration (Lynch, 1995). For example, examinations of lower organisms and other plants
estimate about 100 deleterious alleles to be present in individuals when all
genetic loci are examined. Individually
these alleles produce only a small reduction in fitness ( 2%) when
homozygous. However, the
combination of all 100 homozygous loci
accumulated through inbreeding could potentially reduce the fitness of the
organism on the order of 200%! This is
enough to "kill" the individual two times over (Lynch, 1995)
Despite
the disadvantages of inbreeding,
polyploid ferns have grown to favor selfing as a form of reproduction
since polyploid protections against inbreeding depression. Two studies of
inbreeding depression in diploid and tetraploid ferns show this tendency. In Phegopteris
30-60% of all selfed gametophytes from the diploid race produced normal
sporophytes. However 100% of the selfed gametophytes of the tetraploid race
formed sporophytes. Another example of selfing preference is present in Lepiosorus.
Here, only 4% of the selfed diploid race produced normal sporophytes when
nearly 100% of the selfed tetraploid race produced normal sporophytes (Soltis
and Soltis, 1995).
Unidirectional
introgression
Unidirectional
introgression is an important advantage in that the tendency occurs to
assist chromosomal segregation in helping ferns colonize into new
areas. A combination of hybridization and natural selection on the
backcrossed and better suited progeny, produces a tendency for the diploids to
form tetraploids or other higher number systems. When triploids occur
from this diploid–tetraploid cross, many are incompatible as a triploid
hybrids. Therefore there is a tendency for these variants to form
tetraploids (Sebbins, 1971).
Colonization
of New Areas via Polyploidy
It
is estimated that as much as half of all angiosperms and nearly all (95%)
pteridophytes have multiple polyploid races, also called cytotypes (Soltis and
Soltis, 2000). One advantage of cytotypes is that they can exist in a region in
a broad range. The Appalachian Bristle Fern (Trichomanes boschianum),
for example, has two distinct cytotypes or ‘genetic races’ found at the eastern
and western ends of its range (Farrar, 1993). Polyploid fern populations are
scattered throughout the world. An examination of the Rockfern, Asplenium
ceterach, has shown several cytotypes spread throughout Europe. Tetraploid
populations were found throughout the continent , but diploid populations were
scarce and localized in the Pannonian-Balkan region.
Hexaploids found in southern
Mediterranean populations. A separate
polyploid complex in Greece had diploid, tetraploid and hexaploid populations
with two native haplotypes. These findings suggest that populations in the southern
Mediterranean have been persistent for a long time. Though examination of cpDNA (chloroplast DNA), three haplotypes
were found to be common among the tetraploids of Spain and Italy (Trewick and
Morgan-Richards, 2003). Another example of regional variants are the Adiantum
raddianum ferns of the Nilgris, in South India. A diploid (n=57), tetraploid (n=114), and even an octoploid
(n=228) were observed in that region (Bir and Irudayaraj, 2001).
Polyploid
Potential for Evolution and Success
Observations that new species arise
from the formation of polyploids, like the previously mentioned Green Mountain
Maidenhair fern, have not gone unnoticed. However, environmental factors play a roll in the success of these newly
formed polyploids. Some suggest that the evolutionary potential for polyploids
depends on a number of factors. Mainly, how the genes on the new chromosomes
are distributed (Soltis and Soltis, 2000).
The success of the polyploid may depend
partially on the particular parental DNA sequence, paternal or maternal, and
how it interacts with the organellear genomes.
The location of the sequences and their coding or non-coding function
are also have an effect. Sequences near
telomeric, centromeric, or heterochromatin will all behave differently than
other regions of the chromosome. The question remains to what extent the
differentiation between parents affects the genetic make-up of the organism
(Soltis and Soltis, 2000).
The effects of hybrid vigor do not
always create a super plant that will dominate the region. More often , polyploid plants must over come
barriers to establish populations such as the minority cytotype exclusion. Minority cytotype exclusion is at work when
newly-formed outcrossing polyploids have few potential mates when a polyploid
ends up among many diploids. This is detrimental because the tetraploid may
waste all of its gametes on sterile matings. The success that polyploids
demonstrate is biased because we observe the examples that have taken advantage
of the numerous benefits of polyploidy and have overcome polyploidy barriers to
establish themselves as species .
Ferns have
taken full advantage of their polyploid gifts and established themselves
throughout the world. They have been
successful in isolated populations by using the advantages of polyploidy to
quench inbreeding depression and also evolve new species. They have overcome
the hardships of minority cytotype exclusion and moved into new regions by
unidirectional introgression. They have
also taken advantage of their hybrid formation for the function of buffering
effects. The unique reproduction
abilities and genetic advantage of polyploid cytotypes in the Pteropsidia, have
enable the fern to evolutionarily adapt and maintain success for the past 400
million years.
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“We have the receipt of fern
seed – we walk invisible.”
William Shakespeare –Henry IV