New Species of North American Cystopteris and Polypodium, with Comments on Their Reticulate Relationships

17 Pages·1991·10.6 MB·English

by  Christopher H Haufler

American Fern 7-23
Journal 81(1): (1991)
New
American
North
Species of Cystopteris
and Polypodium^ with Comments on
Their Reticulate Relationships
Windham*
Christopher Haufler and Michael
H. D.
Department of Botany, Haworth Hall, University of Kansas, Lawrence. Kansas 66045-2106
complexes and
Biosystematic studies of temperate species in Cystopteris
Poiypodium have helped answer some of the seemingly intractable questions
to
among members These
about patterns of variability the diploid of these genera.
many By
have polyploid combining
studies also resolved the origins of species.
chromosome
field observations, analyses of cultivated plants, studies of meiotic
isozyme well surveys
behavior, electrophoretic investigations of variants, as as
of macro- and micro-morphological features using living and preserved speci-
mens, we have found new species and worked out the reticulate patterns of
hybridization and polyploidy. In developing contemporary treatments for the
we
Flora North America project, decided to assemble a separate report that
some
would recapitulate past systematic work in the two genera, introduce
2)
1)
of the taxonomic complexities encountered in these groups, 3) discuss the
new
characters analyzed, describe species, and provide an overview of the
4) 5)
studying
remaining problems and challenges facing systematists
future
and Poiypodium.
Cystopteris
Hybridization, allopolyploid speciation, and the resulting reticulate patterns
of evolution have been the primary impediments to developing a clear picture
and Poiypodium.
of species origins and interrelationships in Cystopteris
when and only the remaining
However, even polyploids are identified
all
can elude
discriminating species
diploids are compared, obvious features for
the casual observer. The morphological similarity of diploid species in these
among
diploids in the
genera in sharp contrast to the great differences
is
Adiantum
Ongoing A.
Appalachian Asplenium complex. studies of (C. Paris],
Botrychium & Wagner), Cryptogramma R. Alverson], Drj^opteris
(W. H. (E.
F. S.
Werth], and Gymnocarpium Pryer) are showing that the Cystopteris/
(C. R. (K.
may
be
species
Poiypodium morphological differentiation of
pattern of subtle
becoming our goal
clear that
the rule rather than the exception in ferns. It is if
and understand
recognize natural units their
as systematic pteridologists to
is
we must be increasingly tolerant of treatments that
evolutionary
histories,
we
the following
emphasize cryptic characteristics. In this spirit, offer
taxonomic
revisions.
Background
named systematic treatment
Once reevesiana,
Cystopteris,— Lellinger (1981) C.
Lake Utah
•Current Address: Utah Museum of Natural Histor>% University of Utah, Salt City,
84112.
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8 1 (1991)
of diploid taxa in North American Cystopteris seemed to reflect well the natural
situation Thus, three North American diploids have been named:
(Fig. C.
1). 1]
with
buJbi/era Bernh.. a primarily cliff-dwelling species elongate-triangular
[L.)
leaf blades that bear prominent laminar bulblets and unicellular glandular
trichomes; C. protrusa (Weath.) Blasdell, a species inhabiting forest floors in
2)
North America and having rhizome pubescence and
east-central distinctive a
prominent rhizome apex beyond and
that protrudes the current year's leaves;
3)
C. reevesiana, confined to mountains of the southwestern U.S. and having a
creeping rhizome that lacks the peculiar pubescence and protruding apex of C.
and commonly more
protrusa has finely dissected leaves than either of the other
During no were
diploids. the present study, additional diploids encountered.
Over
parts of their ranges, C. hulhifera sympatric with the other diploids, but
is
populations of C. protrusa and C. reevesiana are separated by over a thousand
miles.
North American
In Cystopteris, the remaining systematic problems are the
at
new
polyploid Although one from
level. tetraploid originating extant diploids
will be proposed, by far the most troublesome group centers on
C. fragilis (L.)
Bernh. This cosmopolitan polyploid contains considerable morphological
variability, and in North America occurs and hexaploid The
tetraploid
at levels.
may
origin of these polyploids obscure and involved an
is (Fig. extinct diploid
1)
The
(Haufler, 1985]. cosmopolitan range
of C. suggests a
fragilis that
it is
we may
relatively old species. Given morphological
its variability, infer that
evolution (and perhaps
speciation) actively taking place the polyploid
is at
These
level. complications confound attempts developing
at a stable systematic
treatment and
argue for a conservative approach. Thus, except the
for
[Michx.) Desv., variants
of C.
/]
formally
dium.—
Members com
of the vul^are
P. L.
more
group. This
extraordinary attention can be and
attributed biogeographical
to
morphological Members
features. group
of this are largely north temperate in
and many
distribution thus are in the "backyards"
of pteridologists. In addition,
Polypodium
an
exhibits array of ploidy accompanied by
levels that are subtle
but discrete variations in morphology. Our proposed
systematic revisions in
North American
Polypodium
are the same time more complex and more
at
We
htforward than
those
in Cystopteris. more
are suggesting changes in
Polypodium
taxonomy,
but the discovery between
of correlations isozymic
markers and
stable, qualitative morphological somewhat
characters
(albeit
made
have
cryptic) us quite confident about
these systematic
modifications.
Manton
demonstrated
(1950) that there were three ploidy among
levels
representatives of the P. vulgare complex in eastern North America. now,
Until
R
three have been
all called cytotypes virginianum &
of Kott Britton
L. (1982)
developed
a careful analysis of the morphological
characteristics that
discriminate
the three ploidy showing
levels, between
discrete differences
and
diploids and
tetraploids the intermediacy of There has been
triploids.
HAUFLER WINDHAM: CYSTOPTERIS AND POLYPODIUM RELATIONSHIPS
&
9
C. hulhifera C. utahensis C. reevesiana
(4x)
(2x) (2x)
C
laurentiana
(6x)
C
C. tennesseensis fragilis
(4x)
(4x)
C. protrusa C. tenuis C. "hemifragilis"
(2x)
(2x) (4x)
North
complex.
the Cystopferis
fragilis
showed
Shivas
(1961)
the tetraploid.
considerable debate over the origin of
and suggested that the
abundant formation during meiosis in triploids
bivalent
Evans (quoted in
diploid cytotype was one of the progenitors of the tetraploid.
Northwest
from
the Pacific
Lloyd & Lang, 1964) suggested that a diploid species
Suksdorf)
virginianum
enome
Love & Love argued
Although (1977)
gendered nomenclatural debate.
„
&
was CranfiU Britton's (1983)
virginianum diploid,
that the type of P.
name virginianum
convincing evidence that the P.
reexamination provided
named.
had not been
The therefore,
belonged the tetraploid cytotype. diploid,
to
more Polypodium species than in the
In western North America, there are
Northwest
work helped the species in the Pacific
Lang's to clarify
east. (1971)
Maxon from two
hesperium originated
and demonstrated that tetraploid P.
P H UOrthem
„„4. iJ:„1„:J„ r» „, T,,,.., or^rl nhrr^^rrrhi7nn Fflton fFis. 2l. IH
and
glycyrrhiza P.
diploids P.
involving the
allopolyploidy
California,
ali/i
Whitmore
Ifornicum."
name
backcross
comolex, triploid
sterile
hybrids has
The presence of these sterile
and sympatric.
diploids tetraploids are
and
has
sexual species
the
morphological distinctness of
blurred the
AMERICAN FERN VOLUME NUMBER
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1 (1991)
(2x) (4x)
P. californicum
P. calirhiza
P. glycyrrhiza
hesperium
P.
hum
amorp
P.
saximontanum
P.
P. sibiricum
P. virginianum
appalachianum
P.
Fig. 2. Diagrammatic representation of reticulate relationships among North American members
of
um
the Polypodi vuJgare complex.
contributed
to the systematic
controversies. Slight morphological
differences
between
northern and
southern
California populations
of the diploid
P.
californicum
(Harrington have
et al., 1986) also tended to confound the
situation.
Windham
has
(1991] clarified relationships in Polypodium from the
southwestern He
U.S. described an
additional
tetraploid
species, P.
Rocky
the Mountains
more
demonstrated two
that the tetraploids each contain a genome derived from
P.
amorphum.
However,
two
the species
are quite
distinct genetically because the
second genome was
contributed by
different species belonging
(Fig. to
2]
lineages that probably diverged
millions The
of years ago. these
fact that
distantly
related tetraploids could be confused
for so long emphasizes the
complexities group and how
of this
illustrates reliance exclusively on aspects
of gross leaf morphology can
lead
to inaccurate and
interpretations of species
their phylogenetic
history.
—
New
and
Revised Names
CysraPTEms
/ America, most
the
collected
yet confusing
tetraploid element
still Long
is C. tenuis. considered a
ma
jragilis
(C. fragilis var.
Moran
showed
(19831
discriminatin
HAUFLER & WINDHAM: CYSTOPTERIS AND POLYPODIUM RELATIONSHIPS
11
recommended
[1983] recognizing C. tenuis as a separate species. Subsequent
confirmed
electrophoretic analyses (Haufler, 1985) the genetic distinctness of C.
tenuis and provided clues to ancestry. In contrast to past hypotheses
its
(summarized in Moran, 1983), isozyme data indicated that C. tenuis was an
combining marker bands from diploid protrusa and an
allotetraploid, C.
component
unidentified diploid related to tetraploid C. /ragilis (Fig.
1).
Three aspects of Cystopteris biology are responsible for the difficulty
when
encountered trying to develop a clear understanding of the morphological
between and Cystopteris species are
differences C. tenuis C. /ragilis. First,
remarkably "plastic" and leaf morphologies can vary greatly depending on
tendency
habitat conditions. Especially problematic the of tetraploid
is
when
become
Cystopteris species mature (produce spores) their leaves are
to
very This most occur under adverse conditions
small. situation likely to
still is
and, because C. /ragilis tolerates environmental extremes of cold and exposure
better than other ferns found higher latitudes than any other species),
all is at
(it
we
grows suboptimal Second, have seen a
this species frequently in habitats.
definite "ploidy effect" in Cystopteris. At higher ploidy levels, Cystopteris
become and some than can be
leaves reduced in complexity lose of the features
when
used in distinguishing species. Third, Cystopteris species are sympatric,
This
they forming morphological intermediates.
are likely to hybridize, sterile
made
combination of features has the systematics of Cystopteris especially
and
techniques characters
challenging and has necessitated the application of
employed
not generally in recognizing fern species.
There some geographical and ecological features differentiating C. tenuis
are
common and lower
lower
from While latitudes
tenuis at
C. /ragilis. C. is
elevations in the northeastern U.S. and southeastern Canada, C. /ragilis is
commonly found north Canada) and west (in the U.S. and Canada).
further
(in
mountain
common, confined tops.
In regions where C. tenuis C. /ragilis is to
is
may found on but tenuis also inhabits
Ecologically, both species be cliff faces, C.
Mor-
perhaps owing protrusa parentage [Fig.
forest to C. 1).
floors, its
may
be
from
phologically, C. tenuis difficult to distinguish C. /ragilis. It
is
we
intermediate between putative progenitors, but do not have the C. /ragilis
its
two
diploid make comparisons. Further, likely that the tetraploids,
to direct it is
"polyploidy"
C. tenuis and C. /ragilis tend to resemble each other because the
effect leads to reduction in plant size and the complexity of leaf blade dissection
can be
combination morphological features
in Cystopteris. In most cases, a of
Moran
by
As
pointed out
used two [Table
tetraploids
to separate reliably the 1).
proximal pinna in
pinnule the C.
proximal basiscopic of
the base the
(1983), of
and has truncate base.
tenuis cuneate while that in C. /ragilis is nearly sessile a
is
between
intermediate C. fragilis
This also provides evidence that C. tenuis is
pinnule Other features
and whose proximal basiscopic stalked.
protrusa is
C.
more
acute
include a
from
found and distinguishing C. frngilis 1)
in tenuis
C. it
pinnae curve
tendency
for to
angle pinna departure from the rachis, a
of 2)
having crenulate
towards and narrower pinnae often (vs.
blade apex,
the
3)
considerable variability in these
Admittedly there
sharply toothed] margins. is
VOLUME NUMBER
AMERICAN FERN JOURNAL:
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1 (1991]
Table Comparison and
1. of Cystopferis fragilis C. tenuis. Features represent those of "ideal"
Most
specimens. individuals fail to exemplify all of the characteristics.
C. fragilis C. tenuis
Base of proximal basiscopic pinnule Obtuse truncate Cuneate obtuse
to to
of proximal pinna
Leaf margin Sharply toothed Crenulate or with
rounded
teeth
Pinna axis of median pinnae Straight Curved apically
Angle median
of pinnae axes Perpendicular Acute
with
rachis
Shape
of pinnae along distal V3 of blade Deltate to ovate Ovate to narrowly
elliptic
and
features, there vtrill be difficulty consistently separating these two closely
related tetraploid Cystopteris species.
Cystopteris reevesiana and C. utahensis.—Tetraploid plants from Arizona and
western Texas having and
glandular trichomes mis-shapened have
bulblets
been
called tennesseensis (Windham,
C. 1983; Lellinger, 1985). However, these
southwestern
U.S. tetraploids are over 1,000 miles west
of the nearest C.
tennesseensis With
collection. the report that a distinct diploid, C. reevesiana,
New
occurs
in the southwestern
U.S. (Arizona, Mexico, western Texas, Utah,
Colorado),
the identity the western
of tetraploids referred tennesseensis
to C.
was
called into question. Isozyme evidence
established
clearly that C.
buJbi/i
from
markers
Because
common
C. buJbi/era occurs both
in
regions, involvement
the
its as
second
progenitor
diploid of both tetraploids was not surprising. This new
information, however,
requires
a reconsideration of the identity of specimens
from
the southwestern
U.S. Given our knowledge
of differing parentage,
is
it
logically inconsistent and
biologically meaningless apply same name
to the
both
eastern U.S. and southwestern
U.S.
tetraploids.
As
usual
in Cystopteris, problems
arise in developing morphological
criteria
for distinguishing two
these
evolutionarily
separate This not
entities.
is
surprising because
they share one
diploid
progenitor
(C. bulhifera; Fig.
1).
Although
their other diploid maybe
progenitors
clearly distinguished from each
many
other, they share morphological
features (Table Both and
protrusa
C.
2).
reevesiana have
C. long-creeping rhizomes and
ovate blades can be
leaf that
characters provide means
the best
o
pubescence on
rhizome
the
the rhizome
the other hand,
lacks golden pub
AND
HAUFLER WINDHAM: CYSTOPTERIS POLYPODIUM RELATIONSHIPS
&
13
Table Comparing and
morphologically similar diploids tetraploids in the Cystopteris utahensis/
2.
Many
tennesseensis complex. Features represent those of "ideal" specimens. specimens fail to
exemplify of the characteristics.
all
C. reevesiana C. utahensis C. tennesseenis C. protrusa
Blade shape Ovate Elongate deltate Elongate deltate Ovate
Long
Rhizome Long Short Short
internodes
Rhizome apex Flush with Flush with Flush with Protruding
beyond
leaf bases leaf bases leaf bases leaf
bases
Rhizome Absent Absent Absent Present
trichomes
brown brown
Rhizome brown Dark brown, Light Light
scales Light
subclathrate
Common Often abundant Rare in pinna Absent
Multicellular in
pinna
gland-tipped pinna axils in axils axils
trichomes
38-42 |im 28-34 fim
Spore 33-41 39-41
size |jim
iJim
averaging
Chromosome 4211
84II
42II 84II
number
(2n]
US
Eastern
Southwestern Eastern
Southwestern
Distribution
US North America
US, Mexico
AUhough
has current bases flush with the rhizome apex. neither
leaf
its
rhizome
rhizome apex, the scales of C.
has an obviously protruding
tetraploid
are
brown
with
more uniform in color tan to light
scales in tennesseensis are
C.
trichomes frequent in
gland-tipped are
muUicellular,
lateral walls. In addition.
whereas such trichomes are rare in C.
the pinnae utahensis
axils of in C.
isozyme
may but
be considered cryptic,
These
tennesseensis. features
from
markers
demonstrate only reevesiana
that C.
consid
although frequently
Further,
iploid.
their
Thus, utahensis
appears be absolute. C.
two to
separation of the tetraploids
confined to the
and tennesseensis
occurs only southwestern U.S. C. is
in the
eastern U.S.
United
3).—Type:
Windham & nov.
Cystopteris utahensis Haufler, sp. (Fig.
tributary
km
Canyon SE
3.93 of
Bill
i
Windham
2 1990,
July
(9(
KANU, MO, UTCl
UC, US,
VOLUME NUMBER
AMERICAN FERN
JOURNAL:
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A
= =
Fig. 3. Illustration of Cystoptens utahemis. WTiole B
plant. pinna
Detail of axil (located at
showing
ght}
Detail of abaxial
blade
surface (located open on whole
at circle leaf to leffTshowing sori with fugacious, hood-shaped
indusium, numerous
=
unicellular glandular trichomes, and an D
abortive rhizome
bulblet, Single
E =
scale. Detail of cellular structure of rhizome scale (from area enclosed by on whole
circle scale
showing
to right] subclathrale nature of cells.
HAUFLER WINDHAM: CYSTOPTERIS AND POLYPODIUM RELATIONSHIPS
& 15
Cystopteri tennesseensi Shaver similis, a qua differt paleis rhizomatis
trichomatibus numerosioribus multicellularibus
atrobrunneis subclathratis,
et
pinnarum.
gladulosis in axillis
crowded
Rhizome creeping, internodes short with leaves near the apex,
cm
up
Leaves 45
rhizome dark brown, lanceolate, subclathrate. to long.
scales
brown
Petioles shorter than blade, variable in color but mostly dark at base,
becoming stramineous toward blade. Blade tripinnatifid, deltate to
gradually
with without
usually widest or near the base; rachis or
deltate-lanceolate, at
pinna with
with gland-tipped trichomes, axils often
unicellular
bulblets,
abundant gland-tipped trichomes. Pinnae with short stalks
multicellular,
toward ovate oblong,
toward blade broadly attached apex, pinnatifid, to
base,
and
with margins. Veins with veins directed into teeth
serrate free,
indusium cup-shaped with truncate
emarginations. Sori round, discrete, the
gland-tipped
under bearing unicellular,
apex, broadly attached receptacle,
41 pim long.
monolete
mes. Snores
=
Chromosome number 2n (Windham. 1983 as Cystopteris cf.
84II
tennesseensis).
on
on
summer Cracks and ledges rarely terrestrial,
Sporulating cliffs,
to
fall.
1700-2700 m. Arizona, Colorado, Texas, Utah.
calcareous
substrates,
Canyon de Chelly National
Canyon Muerto,
Pamtypes: Arizona: Apache Co., upper del
W
Windham
Elden Mountain, 93
Monument, Coconino on slope of
R. HaJse 329 (ARIZ); Co., cliffs
N
Munds
ASU, Windham Windham 319 (ASC, UNM); small canyon on face of
(AC, UT),
S-
NW
Harding Hole,
Mountain, Windham Harbsfer 150 (ARIZ, UTj; Colorado: Moffat Co., cliffs of
6-
South
COLO]; Texas: Culberson Co.,
Monument, O'Kane 3170 (BRY.
Dinosaur National
S.
Guadalupe
Hudspeth
Warnock 23174 (SRSC); Co.,
McKittrick Canyon, Guadalupe Mountains, B.
Grand
8534 (ASU, BRY, UTC); Utah: Co..
Mountains National Park, Pine Canyon. L. Higgins
Moore 2320 (BRY); Utah Co.,
Monument, Welsh, Harrison, 6-
Freshwater Canyon, Arches National
Windham
Windham & (UT).
S American Fork Canyon, (89-07)
wall
of
puzzle tenuis
the of C.
reconsidered.—In addition to
Cystopteris
/ragih's
poses addition
bove, C./ragilis
from
quite different
fragilis is
those
most geographically
the
presumed Cystopteris fragilis is
diploid parents.
known
widespread member genus extending well beyond the ranges of all
the
of
many enzyme
chromosomally a tetraploid, at
Although species
diploids. this is
gene silencing
Such extensive
diploids.
loci the population samples act like
some
Windham,
& In
[Werth 1991).
may
be hallmark an ancient tetraploid
the of
identify
possible to
polymorphic
species, is
parts of the range of this it
given the
which, especially
mornholoeical v
employed discriminatin
in
have
However, these variants
additional species.
could be used describing
in
The
final
using isoz^Tnic data.
proven be indistinguishable
to genetically
spore surface
such distinctive
some characters as
problem
cases,
in
is that,
while
morphological
and traits
other
geography
with
features appear correlate
to
m
most
Thus, cases.
polymorphisms.
mere populational
in other cases they are
mor
species
variable
highly
AMERICAN FERN VOLUME NUMBER
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we
fragilis is one of the best examples have of a species that diversifying
is at
the tetraploid level. seems likely that reciprocal gene silencing has played
It a
role in isolation of these different variants. Available techniques, however,
are
what
insufficient to elucidate fully has occurred nor consistently possible
is it
ematic
be
entities will discussed below.
—
We
became
fragilis.
first
through
fragil
(Weath.) an
Blasdell, allopolyploid involving
tetraploid
C. fragil
ploid
C. hulhifera as the othe
limestone on Manitoul
cliffs
them
from
small
me
these
am
Thus,
fragilis. there appeared be
to
new
for describing
a taxon.
However,
further exploration added
complications. Hexaploids were
obtained from
other
parts of the range of Montana, and
C. fragilis (Alaska,
Arizona} had
that similar morphological and
ecological features but did not
from same
the
from
com
fragilis
in the hexaploids
another example
is of ploidy-related
not only
effects, in
reduction
of
leaf cutting complexity,
but
also in the production
of rugose spores
and
the preference
for basic
(limestone)
substrates. Similar
characteristics
(rugose
spores, calciphily) seen some
are
in hexaploid
individuals reported
from Europe
(e.g., C. regia Desv. [Tutin
(L.) et al., 1964]). Thus, although
distinctive members
(especially
for
of Cystopteris], these have been
variants not
formally They
recognized.
do, however, provide
a dramatic demonstration
of
elements
fragil
Cystopteris dickieana.—
There
a long
is history involving presumed
the
Sim
morphological
variant no more
is systematically meaningful
than
the
hexaploids
discussed
above.
Cystopteris dickieana was
a
is tetraploid that
originally segregated from
C. fragilis primarily on
the
basis of rugose spores as
opposed
to the echinate
spores
of other Cystopteris As
species. described above
for the hexaploids and by
others Jermy &
(e.g., Harper, seems be
1971), there
to
a variety of mechanisms by which
rugose
spores
are generated. Furthermore,
when
surveying the morphology
of plants bearing
rugose
spores, not
it is
possible
to find
a consistent
set of sporophytic
characteristics
that correlates
ith
/i