Apomixis and Sexuality in Three Species of Amelanchier, Shadbush (Rosaceae,
Maloideae)
Christopher S. Campbell; Craig W. Greene; Scott E. Bergquist
American Journal of Botany, Vol. 74, No. 3. (Mar., 1987), pp. 321-328.
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Amer. J. Bot. 74(3): 321-328.
1987.
APOMIXIS AND SEXUALITY IN THREE SPECIES OF AMELANCHIER, SHADBUSH (ROSACEAE, MALOIDEAE)' Department of Botany and Plant pathology, University of Maine, Orono, Maine 04469, and
*College of the Atlantic, Bar Harbor, Maine 04609
ABSTRACT
We used Nomarski differential interference contrast microscopy of cleared, whole ovules to
examine megasporogenesis and megagametogenesis in tetraploid (N = 34) individuals of three
species of Amelanchier in Maine. Amelanchier canadensis and A. stolonifera conform to the
general pattern of apomixis in the Maloideae by being aposporous and by frequently forming
more than one megagametophyte per megasporangium. These species are also pseudogamous;
both self and foreign pollen elicit fruit set. Amelanchier bartramiana follows a sexual pattern
by producing a triad of megaspores and almost always only one megagametophyte per megasporangium. This boreal shrub, strikingly distinct morphologically and in its habitat preference
from other North American species of the genus, is primitive in its sexuality and self-incompatibility relative to other species we have studied.
THE MALOIDEAE contain about 20 genera of
woody plants with centers of distribution in
Asia and North America. Polyploidy and hybridization within and between these genera
are common in the group (Robertson, 1974).
Asexual seed production or apomixis, which
is often associated with hybridization and
polyploidy (Marshall and Brown, 1981; Nogler, 1984), has been reported in five maloid
genera: Amelanchier Medic. (Campbell et al.,
1985), Cotoneaster Ehrh. (Hjelmqvist, 1962),
Crataegus L. (Muniyamma and Phipps, 1979,
1984a, b; Dickinson and Phipps, 1986), Malus
Mill. (Dermen, 1936; Oldtn, 1953; Hjelmqvist, 1957, 1959), and Sorbus L. (Liljefors,
1953; McAllister and Gillham, 1980). Four
features are generally common to the approx.
three dozen species of the subfamily in which
apomixis has been reported. First, most are
triploid or tetraploid; higher ploidy levels are
rare in the subfamily. Second, apospory-the
development of a somatic cell of the megasporangium into a megagametophyte-occurs
in all apomicts except one diplosporous species
of Crataegus(Muniyamma and Phipps, 1984a).
Third, apomicts frequently contain more than
one megagametophyte per megasporangium,
derived from multiple aposporous initial cells.
Fourth, as a rule, maloid apomicts are pseuI Received for ~ublication14 Januarv 1986: revision
accepted 24 July i986.
We acknolwedge the Faculty Research Fund of the University of Maine at Orono for financial support of this
research.
dogarnous: fruit and seed set occur only after
pollination.
We have undertaken this study to determine
whether other species of Amelanchier manifest
these four features of apomixis and to search
for sexual species in the genus. We examined
A. bartramiana (Tausch) Roemer, A. canadensis (L.) Medic., and A. stolonifera Wieg.,
which cover a broad range of taxonomic diversity in the genus. Robinson and Partanen
(1980) divided eastern North American shadbushes into two groups: the canadensis complex, including A. canadensis, and the sanguinea complex, ofwhich A. stolonifera is a member.
The only species they could not fit into this
scheme was A. bartramiana, morphologically
so distinct that Landry (1975) isolated it in one
of his two subgenera, Oligocarpon Landry.
This boreal shrub is unique among North
American species for the imbricate arrangement of leaves, cuneate leaf base, short petiole,
one- to four-flowered inflorescence, subconical
ovary summit, and elongate fruit. In spite of
this morphological distance from other species
of Amelanchier, A. bartramiana presumably
hybridizes with at least seven species (Fernald,
1950).
AND METHODS -Material for this
MATERIALS
study comes from three individuals of Amelanchier bartramiana (Bergquist 1-3, Dead
River Township, Franklin County, ME) and
two each oT A. canadensis (Greene 1310, 1360,
Bar Harbor, Hancock County, ME) and A. stoIonifera (Campbell 4351, Orono, Penobscot
322
AMERICAN JOURNAL OF BOTANY
[Vol. 74
County, ME and Greene 1361, Bar Harbor, TABLE1. Number of megasporangia with one, two or more
than two mature megagametophytes for samples of
Hancock County, ME). All collections are
100 ovules of three species of Amelanchier
vouchered at MAINE.
For our study of megasporogenesis and
Number of megagametophytes:
megagametogenesis, we examined about 600
I
2
More than 2
ovules of Amelanchier bartramiana and about
97
3
0
150 of both A. canadensis and A. stolonifera. A. bartramiana
canadensis
50
28
22
Following fixation in FPA,, (formalin, pro- A.
A. stolonifera
47
40
13
pionicacid, 50% ethanol; 5:5:90 by vol), ovulefs
were cleared in Herr's 4% fluid (Herr, 19711;
modifications of Herr's 4I/z, such as BB-4 I/z ingly different pattern of megasporogenesisand
fluid, benzyl benzoate, 9:l by vol., were also megagametogenesis. One megasporocyte apeffective. Cleared ovules were observed with pears as the integuments grow up around the
Nomarski differential interference contrast megasporangium (Fig. 5) and divides into a
(DIC) using a Zeiss standard microscope. Mi- triad (Fig. 6). We did not make a more detailed
crosporocytes were squashed and stained in study of meiosis. We observed triads of megaacetocarmine for meiotic studies. Pollen stain- spores in several ovules but no distinct tetrads.
ability by cotton blue in lactophenol was taken The chalaza1megaspore develops into a megaas a measure of pollen viability. Racemes with gametophyte as shown by the presence of deemasculated or intact flowers were enclosed in generating tissue representing megaspores mifabric bags for pollination studies. Additional cropylar to the young megagametophyte. After
details of our methods are described in Camp- two-nucleate (Fig. 7) and four-nucleate (Fig. 8)
bell et al. (1985).
stages, the megagametophyte reaches the eightnucleate stage, with an egg apparatus, inconRESULTS-Inall three species, the ovules are spicuous antipodals, and polar nuclei that usucrassinucellate and anatropous, and the mi- ally join to form a fusion nucleus at maturity
cropyle is formed by the inner integument alone. (Fig. 9-1 1). Megasporangia rarely contain more
Amelanchier canadensis and A. stolonifera than one megagametophyte (Table 1).
consistently bear 10 ovules per flower while A.
Microsporogenesis proceeds normally in all
bartramiana has from four to 10 (x = 7.8 1, individuals of the three species studied. They
SD = 1.61. N = 100).
are tetraploids and produce viable pollen (TaIn the dvules we'examined, Amelanchier ble 2). Pollination is required for fruit set. Selfcanadensis and A. stolonifera show the same pollination results in fruit set in Amelanchier
pattern of apospory. In the center of the young canadensis and A. stolonifera but not in A.
megasporangium, a mass of degenerating tis- bartramiana (Table 2).
sue becomes prominent (Fig. 1, 2) and is asDISCUSSION-Thisstudy brings to three the
sumed to represent the remnants of the megasporocyte or its derivatives. No sign of triads number of species in Amelanchier known to
or tetrads indicative of the completion of mei- have apomictic individuals: A. laevis (Camposis was observed. In the vicinity of this de- bell et al., 1985), A. canadensis, and A. stogenerated mass of tissue, one or more cells Ionifera. Our pollination studies show that all
enlarge and exhibit prominent nucleoli (Fig. 1, three species are self-compatible. The individ2). These cells, which we interpret as apos- uals of A. bartramiana we studied, in contrast,
porous initials, develop into unreduced, Po- are primitive in being sexual and self-incomlygonum-type, eight-nucleate megagameto- patible. While all our chromosome counts are
phytes similar in all respects to those of A. tetraploid, diploid counts have also been relaevis (Campbell et al., 1985). As the mega- ported for all four species (Table 2; Robinson
gametophyte matures, an egg apparatus de- and Partanen, 1980). Sexuality is likely in dipvelops, with an egg and two synergids (Fig. 3, loid individuals of the three species in which
4; see also Fig. 9-1 1); polar nuclei remain un- we have found apomixis. The complex reprofused; and the antipodals degenerate. Rarely a ductive biology of Amelanchier, including hythird polar nucleus is found in mature mega- bridization, apomixis, and variation in pollengametophytes.
style compatibility, must affect speciation,
At least one half of the ovules of these two evolutionary rates, and patterns of variation
species contain two or more megagameto- in populations. A more detailed knowledge of
phytes (Table 1). Each megagametophyte is the biology and occurrence of apomixis will
elongate, with an egg apparatus at the micro- allow a fuller understanding of evolutionary
relationships within this taxonomically intripylar end (Fig. 3, 4).
Amelanchier bartramiana displays a strik- cate genus. We lack, for example, estimates of
March, 19871
CAMPBELL ET AL. -APOMIXIS IN AMELANCHIA
323
Fig. 1-4. Nomarski DIC photomicrographs of cleared megasporangia (micropylar end up) of Amelanchier stolonifera
(Fig. 1, 3, 4) and A. canadensis (Fig. 2). 1. Expanding aposporous initials adjacent to degenerating tissue. x 780. 2.
Aposporous, two-nucleate megagametophyte adjacent to degenerating tissue. ~ 7 8 0 3
. , 4. Two planes of focus in
micropylar end of the same mature megasporangium with two megagametophytes, each showing an egg apparatus and
two polar nuclei; each polar nucleus has a single prominent nucleolus within a distinct nuclear membrane (arrow, Fig.
4); granular plastids are in central cytoplasm of righthand megagametopkyte. x 600.
KEY TO LABELING: a = aposporous initial; d = degenerating tissue; e = egg; fn = fusion nucleus; ii = inner integument;
m = megasporangium; mg = megagametophyte; o = ovary wall; oi = outer integument; pn = polar nuclei; s = synergid
cell.
324
AMERICAN JOURNAL OF BOTANY
[Vol. 74
March, 19871
CAMPBELL ET AL. -APOMIXIS
325
IN AMELANCHIA
TABLE
2. Pollen stainability, compatibility, and chromosome numbers for three species of Amelanchier
Chromosome number
Previous reports
Species
Pollen stainability'
Compatibilityb
This report
A. bartramiana A. canadensis
98% (96-99%
for 5 individuals)
98%, 87%
self-incompatible
(0 fruits from 9 1
self pollinations)
self-compatiblet
A. stolonifera
82%
self-compatible
Number
n
=
34
2n
2n
n
=
34
2n = 68
n = 17
n
=
34
2n
n
68
= 32
=
s
=
=
34
28
State
NH
PA
Reference
Love and Love (1966)
Robinson and Partanen
(1980)
NJ, PA
Cruise (1964)
MA, NJ, Robinson and Partanen
VA
(1980)
Sax (1931)
ME
Robinson and Partanen
(1980)
Based on 100 grains per individual.
Robinson (1982) reported the A. bartramiana is self-cc3mpatible and that A, canadensis and A , stolonifera set very
few or no fruits respectively after selfing.
a
the frequency of apomixis in natural populations. Also, except for some information on
Malus species (Sax, 1959; Schmidt, 1977),
nothing is known about the inheritance of apomixis in the Maloideae.
Additional knowledge may also shed light
on the adaptive significance of apomixis. An
early hypothesis postulated that apomixis confers an "escape from sterility" imposed by hybridization and polyploidy (Marshall and
Brown, 1981). The high pollen stainability of
the apomictic species of Amelanchier (Cruise
[1964]; and see Campbell et al., 1985; Table
2) does not indicate sterility. There may nevertheless be some unknown mechanism controlling female sterility (Nogler, 1984). A second hypothesis, the "Henry Ford" or "Model
T" hypothesis (Clausen, 1954) suggested that
facultative apomixis could be adaptive by allowing abundant and faithful reproduction of
successful genotypes asexually with occasional
generation of novelty by sex. The three known
apomictic species of Amelanchier frequently
colonize early successional sites produced by
clear-cutting of forests, fires, or other disturbance. Their mode of reproduction, including
apomixis and self-compatibility, may facilitate
colonization, as it apparently does for apomictic Crataegus crus-galli (Diclunson, 1985).
Amelanchier bartramiana, in contrast, grows
in openings in cool, upland forests or peatlands,
both relatively undisturbed habitats.
Our data on the geographical distribution of
apomixis in Amelanchier are too fragmentary
for us to interpret its ecological significance.
Bierzychudek's (1985) review of plant parthenogenesis does not reveal a strong relationship between ecological disturbance and apomixis in the few genera for which information
is available. However, she did find that significantly more apomicts reportedly grow at
higher elevations and at higher latitudes in
comparison with their sexual relatives. These
trends should not be taken to indicate that
apomixis is a specific adaptation to higher latitudes and elevations, for, as Bierzychudek
points out, apomixis is almost invariably associated with polyploidy; it may be polyploidy,
not apomixis per se, that adapts plants to environments at higher elevations and latitudes
(see Johnson and Packer, 1965). Both tetraploid and diploid chromosome counts have
been recorded for each species of Amelanchier
we have found to be apomictic in Maine. While
the diploid counts come from more southerly
regions in northeastern North America (Table
2), tetraploids are found in both southerly regions in Maine. Analysis is further complicated
Fig. 5-1 1. Nomarski DIC photomicrographs of cleared ovules and megasporangia (micropylar end up) of Amelanchier bartramiana. 5. Young ovule with single expanding megasporocyte. x 700. 6 . Ovule with triad of megaspores
(arrows). x 620. 7. Ovule with two-nucleate megagametophyte; arrows indicate what may be degenerating micropylar
megspores. x750. 8. Megasporangium with vacuolate four-nucleate megagametophyte; arrow indicates micropylar
degenerating tissue. x 700. 9. Eight-nucleate megagametophyte prior to fusion of polar nuclei; arrow indicates three
inconspicuous antipodal cells. x 700. 10, 11. Two views of same megasporangium containing a single mature megagametophyte. 10. Egg apparatus with nuclei of egg and synergids in focus. x 700.11. Fusion nucleus in megagametophyte;
note granular plastids in egg cell and central cytoplasm. x 700. See p. 323 for key to labeling.
326
AMERICAN JOURNAL OF BOTANY
because we cannot assume that all tetraploids
behave as apomicts. A case in point is the
tetraploid sexual species, Amelanchier bartramiana. This species, although sexual, grows at
higher elevations in Maine than the apomictic
species we studied and extends farther to the
north as well (Scoggan, 1978).
Finally, when considering the origin of apomixis, the evolutionary significance of asexu2
ality and sexuality may be important to understanding the conditions in which these two
modes of reproduction may be adaptive
(Uyenoyama, 1984).
Evidence for apomixis in the MaloideaeHjelmqvist (1962) reported that previous evidence for apomixis in Cotoneaster was based
on "breeding true." Similarly Sax's (1959)
rationale for apomixis in some Malus species
was "Since apple species and varieties are generally self-sterile, the production of uniform
progeny from trees surrounded by other species
or varieties would indicate that these trees are
apomictic." Inbreeding, dominance, and maternal inheritance may also generate progeny
of maternal phenotype. Offspring of apomicts
could actually deviate phenotypically from their
parent due to mutation or autosegregation in
diplosporous taxa. Hemigamy, the introduction of sperm cytoplasm into the egg without
nuclear fusion, which is common in apomicts
(Nogler, 1984), could also conceivably generate non-maternal-like offspring.
Demonstration of the unreduced chromosome number for nuclei of the developing
megagametophyte provides the best evidence
for apomixis. Unfortunately, such evidence is
difficult to obtain and rarely reported
(Hjelmqvist, 1957). Chromosome numbers
from endosperm tissue, while easier to determine, may be misleading in pseudogamous
apomicts since different ploidy levels may arise
from different combinations of sperm and polar nuclei (Nogler, 1984). For example, fusion
of one unreduced polar nucleus with a reduced
sperm nucleus produces triploid endosperm,
indistinguishable from endosperm of fully sexual species. Numbers higher than expected from
sexuality may be due to pollen of a high ploidy
level and not apomixis. Therefore endosperm
counts are conclusive only when pollen ploidy
level is known and ploidy of endosperm is
higher than expected for sexual reproduction.
Ploidy level in progeny of controlled crosses
was the basis for Oldkn's (1953) determination
of apomixis and sexuality in Malus.
The most frequent substantiation of apomixis in the Maloideae is the inference, from
[Vol. 74
morphological studies of megasporogenesis and
megagametogenesis, of whether the megagametophyte is reduced or not (Dermen, 1936;
Liljefors, 1953; Hjelmqvist, 1957, 1962; Muniyamma and Phipps, 1979, 1984a, b; Campbell et al., 1985; and the present study). The
critical stage is meiosis, the successful completion of which is usually marked by a tetrad
or a triad of megaspores. In aposporous species
the megasporocyte or the megaspores break
down and are replaced by one to several nearby
somatic cells, which grow into megagametophytes. Less often the concurrent development
of such aposporous initials with a megaspore
may also occur. That Amelanchier bartramiana is sexual is supported by the combination of the presence of triads, indicating
completion of meiosis and the absence of aposporous initials. Triads, such as those seen in
A. bartramiana (Fig. 7), characterize several
families (Bouman, 1984) and occur in the Maloideae in Malus (Hjelmqvist, 1957, 1959) and
Crataegus ( ~ u n i ~ a m mand
a Phipps, 1979,
1985).
Some workers (Krylova, 1970; Dickinson
and Phipps, 1986) have used the presence of
multiple megagametophytes in an ovule as indicative of apospory, but such an assumption
is not valid for Amelanchier and may not be
for other apomictic groups either. In apospory
generally, only one aposporous initial arises in
an ovule or, if there are more, then only one
matures into a megagametophyte (Davis, 1966;
but see also Nogler, 1984). In aposporous taxa
of the Maloideae, there are often multiple aposporous initials and more than one mature
megagametophyte per megasporangium. In related sexual taxa, only one megagametophyte
usually develops (Liljefors, 1953; Muniyamma and Phipps, 1985; table 1; but see Schneider, 1953). The frequency of multiple megagametophytes varies from one aposporous
species to another. For example, Liljefors
(1953) found 69 cases of multiple megagametophytes in 7 1 ovules of a triploid member
ofthe Sorbus arranensisgroup. In Amelanchier
canadensis, on the other hand, only one-half
of the ovules contain multiple megagametophytes (Table 1). Multiple megagametophytes
may also arise through exclusively sexual processes. Extra megasporocytes in the Rosaceae
(Nogler, 1984) could generate multiple, reduced megagametophytes, as in Malus
(Schneider, 1953), although this may occur infrequently because secondary megasporocytes
are rare or usually degenerate (Hjelmqvist,
1962).
No one has yet identified definitive, mor-
March, 19871
CAMPBELL ET AL. -AP(3MIXIS IN AMELANCHIA
phological differences between reduced and
unreduced megagametophytes (Nogler, 1984),
although the problem has not been studied at
the ultrastructural level. Extra polar nuclei
sometimes occur in apomictic taxa of Amelanchier, Cotoneaster (Hjelmqvist, 196 2), and
Crataegus (Muniyamma and Phipps, 1984b)
and generally in apomictic groups (Nogler,
1984). The polar nuclei of Amelanchier bartramiana usually fuse prior to pollination (Fig.
lo), but those of A. canadensis, A. stolonifwa,
and A. laevis (Campbell et al., 1985) do not
fuse at maturity. It is nevertheless possible that
fusion of polar nuclei is not directly associated
with sexuality vs. apomixis; both fusion and
nonfusion occur widely in angiosperms (Willemse and Van Went, 1984), and the polar
nuclei do not fuse prior to fertilization in sexual
Crataegus (Muniyamma and Phipps, 1985).
Robinson (1982) asserted that Amelanchier
humilis Wieg. is not aposporous and pseudogamous because it set no fruit following pollination by Tussilagofarfara L. Our experience
is that extrageneric pollen does not lead to seed
set in Amelanchier, but some of its species are
nonetheless aposporous and pseudogamous.
While A. laevis set 9% fruit from 32 flowers
following pollination by Malus species, seed
set was not significantly nonzero. Pollen from
distantly related taxa has stimulated fruit set
in other maloid apomicts. For example, OldCn
(1953) recorded fruit set in Malus sieboldii
Rehd. of 26-36% in flowers pollinated by pear
and 30% using Taraxacum pollen. However,
he found no seed set in any of these crosses.
Seedlessfruits have been reported in Crataegus
(Dickinson and Phipps, 1986), Sorbus (Liljefors, 1953), and Amelanchier (Campbell et al.,
1985).
Pseudogamy and autonomy in the Maloideae-Pseudogamy predominates in all apomictic maloid genera (Liljefors, 1953; OldCn,
1953; Hjelmqvist, 1957; Muniyamma and
Phipps, 1979; Campbell et al., 1985; Dickinson and Phipps, 1986). In determining whether or not a plant is pseudogamous, care must
be taken in distinguishing between fruit and
seed set. While OldCn (1953) reported fruit sets
up to 34%, out of a total of 177 emasculated,
unpollinated flowers, he found only one seed.
Liljefors (1953) reported occasional production of small fruits from emasculated, unpollinated flowers of Sorbus, but these were seed
sterile. In Amelanchier laevis six seeds from
52 emasculated, unpollinated flowers represents a seed set that is not significantly nonzero
and probably due to experimental error.
327
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