BiologicalJoumal ofthe Linnean Sociib (1997), 61: 51-94. With 7 figures
Asynchronous expression of duplicate genes in
angiosperms may cause apomixis, bispory,
tetraspory, and polyembryony
JOHN G . CARMAK
Plants, Soils, and Biomebomlo&y Department, Utah State Universip, Logan, LJT
84322-4820, USA.
Receiued 4 M a d 1996; accepedfor publication 29 November 1996
Apomicts that produce unreduced parthenogenetic eggs are generally polyploid and occur
in at least 33 of 460 families of angiosperms. Embryo sacs of these apomicts form precociously
from ameiotic megaspore mother cells (diplospory) or adjacent somatic cells (apospory).
Polysporic species (bisporic and tetrasporic) are sexual and occur in at least 88 families.
Their embryo sacs also form precociously, but only non-critical portions of meiosis are
affected. It is hypothesized that (i) the partial to complete replacement of meiosis by embryo
sac formation in apomictic and polysporic species results from asynchronously-expressed
duplicate genes that control female development, (ii) duplicate genes result from polyploidy
or paleopolyploidy (diploidized polyploidy with chromatin from multiple genomes), (iii)
apomixis results from competition between nearly complete sets of asynchronously-expressed
duplicate genes, and (iv) polyspory and polyembryony result from competition between
incomplete sets of asynchronously-expressed duplicate genes. Phylogenetic and genomic
studies were conducted to evaluate this hypothesis. Apomictic, polysporic, and polyembryonic
species tended to occur together in cosmopolitan families in which temporal variation in
female development is expected, apomicts were generally polyploid with few chromosomes
per genome (it =9.6 0.4 SE), and polysporic and polyembryonic species were paleopolyploid
with many chromosomes per genome (a = 15.7 f0.6 and 13.2 f0.4, respectively). These
findings support the proposed duplicate-gene asynchrony hypothesis and further suggest
asexual reproduction in apomicts preserves primary genomes, sexual reproduction in polysporic and polyembryonic polyploids accelerates paleopolyploidization, and paleopolyploidization may sometimes eliminate gene duplications required for apomixis while
retaining duplications required for polyspory or polyembryony. Hence, apomixis, with its
long-term reproductive stability, may occasionally serve as an evolutionary springboard in
the evolution of normal and developmentally-novel paleopolyploid sexual species and genera.
0 1997 The Linnean Sorirty of Inndon
ADDITIONAL KEY WORDS:-apospory - diplospory
parthenogenesis phylogeny polyploidy - pseudogamy.
~
-
embryology
-
evolution
-
~
CONTENTS
Introduction . . . .
Material and methods
Data collection .
Data analyses . .
+
. . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . .
0024-4066/97/05005 1 44 $25.00/0/bj960 1 18
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52
55
55
56
0 1997 The Linnean Society of London
52
J. G . CARMAN
Results . . . . . . . . . . . . . . . . . . . . . . . .
Frequency of reproductively-anomalous species . . . . . . . . . .
Paleopolyploidy among reproductively-anomalous species . . . . . .
Phylogenetic associations among reproductively-anomalous species . . .
Discussion . . . . . . . . . . . . . . . . . . . . . . .
Duplicate genes and reproductively-anomalous species . . . . . . .
The duplicate-gene asynchrony hypothesis . . . . . . . . . . .
The transitional-phase hypothesis . . . . . . . . . . . . . .
Conclusions . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . .
Appendix. . . . . . . . . . . . . . . . . . . . . . . .
57
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66
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74
76
77
81
INTRODUCTION
Historically, the term apomixis, when applied to flowering plants (angiosperms),
has included various forms of vegetative propagation. In this treatment, the term
apomixis is limited to those processes routinely resulting in parthenogenesis from
unreduced eggs. These are frequently described as forms of gametophytic apomixis
(Asker &Jerling, 1992)and involve anomalies that disrupt normal ovule development.
Bispory and tetraspory (collectively referred to as polyspory herein) also disrupt
ovule development, but normal reduced eggs, which require fertilization, are formed
(Fig. 1). The recent identification of cytological similarities between apomixis and
polyspory (Carman, Crane & Riera-Lizarazu, 1991; Peel, Carman & Leblanc, 1997;
Peel et d.,1997b) suggests a common origin. This paper reviews these cytological
similarities and presents a new hypothesis to explain why they occur and how the
various anomalies evolved. It also examines phylogenetic and genomic evidence in
support of the new hypothesis.
Megasporogenesis (female meiosis) in angiosperms occurs in megaspore mother
cells (MMCs), and the female gametophyte (embryo sac) normally develops from
one of four meiotic products (megaspores). Most angiospermous embryo sacs are
eight-nucleate and contain an egg (fertilized to form the embryo), two synergid cells,
a central cell composed of two polar nuclei (fertilized to form the endosperm), and
three antipodal cells (Pobgonum-type embryo sac). Each nucleus is originally haploid
and is derived from the nucleus of the surviving megaspore through three sequential
Figure 1. Development of representative types of sexual (mixis) and apomictic embryo sacs (seeJohri
et al., 1992 and Asker and Jerling, 1992, for complete lists and descriptions of variant types). Pohgonurntype development is the norm and is expressed exclusively in >90% of all angiosperms. The horizontal
row(s) of numbers associated with each developmental type denote stage-specific gene expression: (1)
premeiotic interphase and early meiotic prophase (crossing-over and envelopment of MMCs in callose),
(2) meiotic divisions, (3) megaspore maturation (digestion of callose from and initial vacuolization of
the surviving megaspore), (4) embryo sac development, (5) double fertilization and early endosperm
formation, and (6) embryogenesis (usually initiated after early endosperm formation). Parallel rows of
numbers indicate hypothesized asynchronous expression of duplicate genes, the members of which
originate from different genomes in polyploids or segments of different ancestral genomes in paleopolyploids. Gaps in the numbers represent mutations (mostly null alleles) and deletions. Note that
gaps are most prevalent among the paleopolyploid polysporic types and least prevalent among the
polyploid apomictic types. Some null-allele formation probably enhances seed set in apomicts.
The arbitrary elimination of gene duplications in developmentally-asynchronous polyploids and
paleopolyploids may represent a major evolutionary process in which new reproductive types (apomixis,
polyspory and polyembryony) evolve.
EVOLUTION OF MOMIXIS AND RELATED ANOMALIES
53
54
J. G . CARMAN
endomitotic divisions (Fig. 1). Apomixis disrupts this process, resulting in diplospory
or apospory.
In diplospory, an unreduced embryo sac forms from a MMC in which meiosis
is disturbed and replaced by precocious embryo sac formation (Fig. 1). The
completion of embryo sac formation is also precocious, and the unreduced egg
divides parthenogenetically to form a proembryo, often prior to fertilization (Gustafsson, 1946; Leblanc & Savidan, 1994; Peel et al., 1997a,b). Apospory is similar to
diplospory except the unreduced embryo sac forms from a somatic cell of the ovule
wall near the MMC (Fig. 1). During apospory, either the meiotic MMC or the
young sexual embryo sac aborts and is replaced by one or more aposporic embryo
sacs (Asker &Jerling, 1992),which also tend to develop precociously (Savidan, 1982;
Nogler, 1984a; Lutts, Ndikumana & Louant, 1994; Peel et al., 1997a). Hence, both
of these anomalies result from the premature expression of genes required for
embryo sac formation, and both may have been influenced by mutation (Gustafsson,
1946; Nogler, 1984a; Mogie, 1992; Peacock, 1993; Koltunow, 1993). Most if not
all apomicts are facultative sexuals (Asker & Jerling, 1992), which means sexuality
has been retained during their evolution.
Tetraspory, in which meiotic karyokineses occur but cytokineses do no (Fig. 1;
Willemse & van Went, 1984;Johri, Ambegaokar, & Srivastra, 1992), has also been
attributed to a ‘precocious gametophytization’ of the MMC (Battaglia, 1989). Both
tetrasporic (Battaglia, 1989) and diplosporic (Crane & Carman, 1987; Leblanc &
Savidan, 1994; Leblanc et aL, 1995) MMCs undergo vacuolization, which normally
occurs later on, during the onset of embryo sac formation, i.e. in the surviving
sexual megaspore. Such vacuolization also occurs in aposporous initials (Naumova
& Willemse, 1995). In both diplospory and tetraspory, embryo sac formation
continues without interuption (Fig. 1; Peel et aL, 1997a,b). In normal species,
megasporogenesis and embryo sac development are temporary separated during
which time callose (p, 1-3 glucan)in the walls of the survivingmegaspore is catabolized
(Rodkiewicz, 1970).
The MMC walls of diplosporic (Carman et al., 1991; Naumova, Den Nijs &
Willemse, 1993; Leblanc et al, 1995; Peel et al., 1997a) and tetrasporic (Rodkiewicz,
1970; Johri et al., 1992) species lack callose, which normally envelops MMCs of
monosporic and bisporic species during early prophase (Fig. 1) and is deposited in
the cross walls during megasporogenesis (Rodkiewicz, 1970). These deposits are
catabolized following meiosis, which permits rapid megaspore expansion at the onset
of embryo sac formation. The absence of callose in diplosporic and tetrasporic
species permits precocious expansion of MMCs (Fig. 1) and is further evidence of
MMC gametophytization (Battaglia, 1989). Forms of polyspory, like forms of
apomixis, are derived anomalies of widespread polyphyletic origin (Schnarf, 1983;
Johri, 1963; Lakshmanan & Ambegaokar, 1984; Dahlgren, Clifford & Yeo, 1985;
Battaglia, 1989;Johri et al., 1992).
There are many forms of polyembryony, which is the formation of more than
one embryo per ovule (synergid and antipodal embryony, cleavage polyembryony,
adventitious embryony; see Maheshwari & Sachar, 1963; Lakshmanan & Ambegaokar, 1984; Johri et al., 1992; Naumova, 1993). Like apomixis and polyspory,
the various forms of polyembryony are polyphyletically derived and involve temporally and spatially-misplaced developmental programs.
I propose the “duplicate-gene asynchrony hypothesis” to explain the above
EVOLUTION OF APOMIXIS AND RELATED ANOMALIES
55
cytological and developmental similarities. The fundamental premise of this hypothesis states: apomixis, polyspory, polyembryony, and related anomalies result
from asynchronously-expressed duplicate genes in polyploids, mesopolyploids, or
paleopolyploids. Tenets of this hypothesis include (1) the responsible duplications
constitute intergenomic heterozygosity for the time and duration in which various
phases of female development occur, (ii) such heterozygosity is more prevalent in
cosmopolitan families, thus, reproductive anomalies occur more frequently among
such families, (iii)nearly complete sets of asynchronously-expressedduplicate genes (as
occur in polyploids and mesopolyploids)are required to competitivelyreplace meiosis
with embryo sac formation (apomixis),(iv)grossly incomplete sets of asynchronouslyexpressed duplicate genes (as occur in mesopolyploids and paleopolyploids) are required to allow portions of meiosis, embryo sac formation, and embryony to occur
simultaneously (polyspory and polyembryony),and (v) mutations, most of which produce null or “leaky”alleles, are ofsecondary importance in the evolution ofreproductive
anomalies and may be retained if fitness is improved (Fig. 1).
MATERIAL AND METHODS
Data collection
The CAB abstracts, Current Contents and Agricola data bases were searched to
identify species of angiosperms exhibiting apospory, diplospory, bispory, tetraspory,
and polyembryony. Anomalous species were also identified from Johri et al. (1992),
Davis (1966), Asker & Jerling (1992), Naumova (1993), and Nygren (1967). Genus
synonyms not recognized by the Kew Botanical Garden were replaced by recognized
synonyms (Brummitt, 1992). Genera containing one or more apomictic, polysporic,
and/or polyembryonic species were tabulated by superorder, order and family
according to the phylogenetically-based classificationsof Dahlgren (1980), as modified
by Dahlgren (1989b) and Judd, Sanders, & Donoghue (1994), and of Dahlgren et
al. (1 985), as modified by Dahlgren (1989a). The phylogeny of angiosperms is being
refined by molecular procedures, but only those ofJudd et al. (1 994) are incorporated
herein.
Genome base numbers ( x values)were tabulated for all species of genera containing
reproductive anomalies and for all species of the following 72 sexual monosporic
genera, which were selected at random from those recognized by the Kew Botanical
Garden (Brummitt, 1992): Actaea, Adenium, Andrachne, Anisothrix, Apios, Arrhenatherum,
Arum, Astragalus, Caloscordum, Centaurium, Cercocarpus, Chaptulia, Chloranthus, Chlomphytum,
Chorispora, Cirsium, Cnicothamnus, Conyza, Deinanthe, Dichmtophora,Dimorphotheca, Diosma,
Lhplorhynchus, D?ymophila, Dyschoriste, Qsolobium, Echium, Eriosema, E y g i u m , Ferula,
Guazuma, Henninium, Heteropappus, Joannesia, Kelhia, Lagophylla, Leptuctina, Leptospmum,
Leucojum, Melaleuca, Melanthera, Monnina, Myrrhis, Orychophragmus, Osmorhiza, Pachycymbium, Paracaym, Paranephlius, Phgzocheilus, Polanzsla, Portulacaria, finsepia,
Prunella, Pseudorlaya, Psophocarpus, Reichrdia, Rindera, Sapium, Scariola, Schizophragma,
Sesamum, Sonchus, Stapeliopsis, Sta’ractinia, Thesium, Tulbaghia, Uraria, Vella, V p a , Kkx,
Wumzbea, and Xanthirma. Chromosome numbers were obtained from the on-line
Missouri Botanical Garden data base of plant chromosome numbers (1 994 through
1996) and from the 1973 to 1991 indices of plant chromosome numbers (Moore,
56
J. G . CARMAN
1977; Goldblatt, 1981, 1984, 1985, 1988; Goldblatt &Johnson, 1990, 1991, 1994).
Numbers not reported after 1973 were not recorded. However, the most current
literature was searched first, and few x values were added by searching the earlier
literature (1973 to 1974 and 1975 to 1978 indices of plant chromosome numbers;
Moore, 1977; Goldblatt, 1981). Nevertheless, some x values have undoubtedly been
overlooked. Base numbers were determined by comparing common denominators
among sporophytes and gametophytes with recognized x values (Raven, 1975;
Goldblatt, 1980; Lewis, 1980; Jones, 1985). Values not previously reported but
which appear stable (multiple reports and/or both sporophyte and gametophyte
congruity) and derived through aneuploid increases and reductions were tabulated.
Data anabseJ
comparison tests: anomalies of reproduction and x values
Evidence for paleopolyploidy (high x values and multiple x values per genus; see
Lewis, 1980) was examined for each genus belonging to each of eight reproductive
categories (sexual vs apomictic x monosporic vs polysporic x monoembryonic vs
polyembryonic). All stable x values for each genus per category were identified, and
the number of stable x values for each genus was determined. These variables were
subjected to analysis of variance. Each unique x value of each genus in each category
was included once in each analysis, regardless of its frequency of occurrence.
&up
Phylogmetic associations among repmductiveb-anomalous species: cross chqfied analyses
Chi square (x') analyses were used to determine if apospory occurred independent
of diplospory, bispory of tetraspory, apomixis (apospory or diplospory) of polyembryony, apomixis of polyspory (bispory or tetraspory), and polyspory of polyembryony. Families were classified into four groups: families exhibiting only one
anomaly (first group, at least one species in the family exhibiting the anomaly) or
only the other anomaly (second group), families with both anomalies (third group),
and families with neither anomaly (fourth group). T o avoid over-representing the
fourth group, families lacking embryological data were excluded.
Three analyses were conducted for each comparison. The first analysis assumed
either anomaly could be expressed in all families (included all 348 families for which
some embryological data were available). The second analysis included all families
from orders in which at least one of the two anomalies was represented. This
categorization assumed (i) if one of the two anomalies is expressed in an order, then
the other anomaly could also be expressed among the families of that order, and
(ii) it was impossible for both anomalies to be expressed in some orders (those in
which neither anomaly is expressed). The third analysis included only families from
orders in which both anomalies were represented. This assumed (i)if both anomalies
are expressed in an order, then either anomaly could be expressed among the
families of that order, and (ii) it was impossible for both anomalies to be expressed
in some orders (those in which neither anomaly or only one anomaly is expressed).
Chi square analyses (2 x 2 x 2 cross classified data) determined if apomixis,
polyspory, and polyembryony were independently distributed among families. Eight
null hypotheses were tested: complete independence of all three forms of reproduction,
conditional independence between two forms of reproduction given the level of the
EVOLUTION OF WOMIXIS AND RELATED ANOMALIES
57
third form (three hypotheses tested), independence of one form from the two
remaining forms taken jointly (three hypotheses tested), and independence from
second order interactions (Fienberg, 1980).Pearson residuals ((Oi- Ei)+(E2i)}standardize the deviations of the observed (0)from the expected (E) values and were
calculated for the three null hypotheses that tested for independence of one form
of reproduction from the two remaining forms taken jointly and for the three null
hypotheses that tested for conditional independence between two forms at each of
the two levels of the third form (expressed or not expressed). Pearson residuals were
averaged across the least, more, and most restrictive groupings of families (grouped
as in the 2 x 2 analyses) and means and ranges (n = 3 for each category) were plotted.
RESULTS
Frequenc_y
of reproductiveb-anomalous speck
Reproductive data were not available for 112 of the 460 families considered in
this study, and were not available for most species of most families. Hence, the
number of genera known to contain reproductive anomalies (currently 506) is
expected to increase. Genera expressing apospory, diplospory, bispory, tetraspory,
adventitious embryony (nucellar or integumentary embryony), or apogamety (synergid or antipodal embryony) are listed (Appendix). Pseudomonospory (Johri et al.,
1992) is listed as tetraspory. Genome x values were found for 1 18 of 126 apomictic
genera, 170 of 220 polysporic genera, and 227 of 255 polyembryonic genera
(Appendix). There is evidence of apomixis or polyembryony in at least 16 additional
genera, but the mode of development is uncertain. Genera in this category include
Calostmma (Amaryllidaceae), Amsonia (Apocynaceae), E y i m u m and Draba (Brassicaceae), Adenophora (Campanulaceae), Isomeris (Capparidaceae), Cotylanthera (Gentianaceae), Dianella (Liliaceae), Ardisisa (Myrsinaceae), Andmpogon, Coix, Melinis, and
Schmidtia (Poaceae), Rumex (Polygonaceae), &lea (Rutaceae), and Pr0cri.s (Urticaceae)
(Asker & Jerling, 1992).
Polyembryony was the most common anomaly studied and occurred in 63 of 109
orders and 115 of 348 families. Adventitious embryony occurred in 52 families.
Polyspory occurred in 53 orders and 88 families (bispory in 68 families, tetraspory
in 40 families). Apomixis occurred in 28 orders and 33 families. Diplospory and
apospory each occurred in 21 families.
Monospory and eight nucleate Polygonurn-type embryo sac development are ancestral traits (Johri, 1963; Dahlgren et al., 1985; Battaglia, 1989; Johri et al., 1992)
and occurred exclusively in 53% of the families studied. This percentage increased
to 54% when families displaying apomixis were added. Adding families exhibiting
polyembryony increased the percentage to 75% (260 of 348). This percentage has
fluctuated little over the past 50 years (Palser, 1975). Polyspory occurred in the
remaining 88 families (25Yo). Nevertheless, monospory followed by Pobgonum-type
embryo sac development generally predominates in these families (Johri et al., 1992).
Paleopolyploidy among wpmductiveb-anomalous species
Most genomes with x 2 11 are paleopolyploid, many with x = 9 or 10 are paleopolyploid, and, as a result of descending aneuploidy, some with x<9 are also
J. G . CARMAN
58
9
3.2
g
2.8
-
f
c 14
161
r
'1
T
-b
iI
I
AM
AMPS AWPE
NM AMIPWE PE
Reproductive category
PQPE
PS
Figure 2. Bar graphs depicting, by reproductive category, (i) the mean (+SE) number of different
chromosome base numbers per genus (bases per genus) and (ii) the mean (kSE) chromosome base
number (mean base number). Three variables were used to circumscribe reproductive categories: (i)
the form of megasporogenesis, which included sexual or apomictic (AM) spore development, (ii) the
form of embryo sac development, which included monosporic or polysporic (PS) development, and
(iii) the form of embryogenesis, which included monoembryonic and polyembryonic (PE) development.
Anomalies not listed with a bar do not characterize that bar. Bars not represented by the same letter
are significantly different according to Tukey's Multiple Comparison Test. See text for significant
differences involving bases per genus.
paleopolyploid (Goldblatt, 1980; Lewis, 1980). Thus, most polysporic and polyembryonic species contain paleopolyploid genomes (X= 15.7 and 13.2, respectively)
while most apomicts, nearly all of which are polyploid (Asker & Jerling, 1992),
contain primary genomes (X=9.6) (Fig. 2). The mean number of x values per genus
(low for primary genomes and high for paleopolyploid genomes) also supports this
conclusion. Genera containing polysporic but not apomictic species had significantly
(B0.05) more x values per genus (2.7 k 0.4 SE) than genera containing apomictic
but not polysporic species (1.7 f0.1) (Fig. 2). Genera containing polysporic and
apomictic species had highly variable x values (Fig. 2, note large standard errors).
Phylogenetic associations among n$mductive~-anomalous speak
Phylogenetic unrelatedness is suggested by significant differences in base number
variables observed between apomicts and species exhibiting other anomalies (Fig.
2). Indeed, of 506 genera containing variant species, 83% contained only one of
the three forms of anomalous reproduction: polyembryony (34%),polyspory (33%),
EVOLUTION OF APOMIXIS AND RELATED ANOMALIES
59
Figure 3. Pie charts depicting the proportion of angiospermous genera, families and orders expressing
gametophytic apornixis (AM),polyspory (PS), polyembryony (PE), or various combinations of AM,PS
and PE. Only genera (506), families (1 63) and orders (75) expressing one or more of these anomalies
are represented.
TABLE
I. Three chi square analyses, including observed (OBS) and expected
(EXP) values, relating the occurrence of apospory (A) to that of diplospory (D)
among families of angiosperms. The three analyses differed in the characteristics
of the families included (see Material and Methods)
Families included in the
x2 analyses'
Those from orders that contain
Presence of
apomixis
A
AU families
A and/or D
D
OBS
EXP
Y
Y
Y
N
N
N
Y
N
9
12
12
314
Chi square2
Power of test'
A and D
OBS
EXP
OBS
Exp
1
9
20
20
306
12
12
128
3
18
18
122
9
0
1
2
7
8
24
46.6***
1 .oo
16.0***
0.99
31
30.7***
1 .oo
' Excludes families for which embryological data were not found.
significant at P ~ O . 0 0 1 .
'Power of test based on a =0.05.
'***
and apomixis (15%). Only 1 7 % contained two or three anomalies (Fig. 3). In
contrast, strong associations were observed at the familial level, e.g. 30 of 33
families containing apomicts also contained polysporic or polyembryonic species.
The expected value was 17 (Fig. 4).Likewise, apospory was associated with diplospory,
bispory with tetraspory (Tables 1, 2), apomixis with polyspory and polyembryony,
and polyspory with polyembryony (Tables 3, 4, 5; Fig. 4).Furthermore, 65% of
orders contained two or more of the three categories of variants, while 22% contained
all three categories (Fig. 3).
Polyspory and polyembryony were associated with apomixis (Model A, Table 6),
regardless of the grouping strategy (Fig. 5 , top graphs) and were distributed
independently of each other in families containing apomicts. Note the top four
observed values for model B (Table 6) differed little from the expected. In contrast,
polyspory and polyembryony occurred less frequently than expected (compare the
bottom four observed and expected values for model B, Table 6) in sexual families
but were associated with each other in these families. The x2 of model B (Table 6)
J. G. CARMAN
60
TABLE
2. Three chi square analyses, including observed (OBS) and expected
(EXP) values, relating the occurrence of biopory (B) to that of tetraspory (T)
among families of angiosperms. The three analyses differed in the characteristics
of the families included (see Material and Methods)
Families included in the
xz analyses'
Those from orders that contain
Presence of
POlYSPOry
B
Y
Y
N
N
AU families
B and/or T
B and T
T
OBS
EXP
OBS
EXP
OBS
EXP
Y
N
20
48
20
256
8
60
32
244
20
48
20
159
11
57
29
I50
20
14
6
83
6
27
19
70
Y
N
Chi square'
Power of test3
24.0***
1 .oo
10.8***
0.93
37.0***
I .oo
' Excludes families for which embryological data were not found.
'*** significant at P50.001.
Power of test based on a =0.05.
TABLE
3. Three chi square analyses, including observed (OBS) and expected
(EXP) values, relating the occurrence of apomixis (AM) to that of polyspory
(PS) among families of angiosperms. The three analyses differed in the characteristics of the families included (see Material and Methods)
Families included in the
x* analyses'
Those from orders that contain
AU families
AM and/or PS
AM and PS
Presence of
anomaly
AM
PS
OBS
Exp
OBS
EXP
OBS
EXP
Y
Y
N
N
Y
N
Y
N
17
16
71
243
8
25
80
234
17
16
71
155
11
22
17
I49
17
7
I1
Chi square'
Power of test'
I1.7***
0.95
4.33*
0.54
I
16
51
26
41
26.8***
1.oo
' Excludes families for which embryological data were not found.
significant at P50.05 and 0.001, respectively.
Based on u = 0.05.
2*,***
is the sum of the two x2 defined by the two groupings, apomictic and sexual. While
the x* from apomictic families was negligible, the x2 from sexual families was
significant (P<O.OZ). This interaction also occurred in the more and most restrictive
groupings of families (Fig. 6, top graphs).
Apomixis and polyembryony where associated with polyspory (model C, Table
6; Fig. 5, middle graphs) and were associated with each other in both polysporic
and monosporic families (compare top four and bottom four observed and expected
EVOLUTION OF APOMlXlS AND RELATED ANOMALIES
61
TABLIC
4. Three chi square analyses, including observed (OBS) and expected
(EXP)values, relating the occurrence of apomixis (AM)to that of polyembryony
(PE) among families of angiosperms. The three analyses differed in the characteristics of the families included (see Material and Methods)
Families included in the
x2 analyses'
Those from orders that contain
AU families
AM and/or PE
AM and PE
Presence of
anomaly
AM
PE
OBS
EXP
OBS
EXP
OBS
EXP
Y
Y
Y
N
N
N
Y
N
28
5
87
227
11
22
I04
210
28
5
a7
I63
13
20
102
148
28
0
23
77
17
40
60
Chi square'
Power of test"
41.5***
1 .oo
2a.2***
I1
50.9***
1.oo
1 .oo
' Excludes families for which embryologiral data were not found
* *** significant at P<O.OOI.
'Based on a=0.05.
TABLE
5 . Three chi square analyses, including observed (OBS) and expected
(EXP) values, relating the occurrence of polyspory (PS) to that of polyernbryony
(PE) among families of angiosperms. The three analyses differed in the characteristics of the families (see Material and Methods)
Families included in the
x2 analyses'
Those from orders that contain
Presrnre of
anomaly
PS
Y
Y
N
N
AU families
PS and/or PE
PS and PE
PE
OBS
EXP
OBS
EXP
OBS
EXP
Y
43
45
72
187
29
59
86
, I73
43
45
72
I44
33
55
82
134
43
20
29
85
26
37
46
68
N
Y
N
Chi square'
Power of test'
12.2***
0.95
5.77*
0.67
29.1 ***
I .oo
' Excludes families for which embryological data were not found.
' *,*** significant at P I 0 . 0 5 and 0.001, respectively.
I
Based on a = 0.05.
values for model D, Table 6; Fig. 6, middle graphs). Apomixis and either polyspory
or monospory were associated with polyembryonic families. Likewise, sexuality and
monospory were associated with monoembryonic families (model E, Table 6; Fig.
5, bottom graphs). While apomixis was associated with polyspory among families in
general (highly significant association, Table 3), this association was not evident
when families were grouped according to polyembryony (top four observed and
expected values in model F, Table 6: single x2 was significant at PC0.07) or
J. G . CARMAN
62
AM-PS-P E
PS-PE
.8
AM-PE
PE
2
AM-P s
PS
AM
None
-
5
-
m
Observed
Expected
7
20 40 60 80
160 180
Families
Figure 4. Observed numbers of angiospermous families belonging to each of eight categories defined
by the presence or absence of apomictic (AM), polysporic (PS), and/or polyembryonic (PE) species.
Also presented are the expected numbers of families for these categories assuming apomixis, polyspory
and polyembryony are distributed independently of each other among families. Families were delimited
according to the least-restrictive-analysis criteria (see Material and Methods). The chi square, 88.2 (4
d.f.), was highly significant (RO.00 1).
monoembryony (bottom four observed and expected values in model F, Table 6;
Fig. 6, bottom graphs). However, these non-significant analyses involved small
sample sizes with high probabilities of falsely concluding associations do not exist
(b=O.57 and 0.91, respectively).
The no-second-order interaction model best fit the 2 x 2 x 2 data (model G , Table
6). In this model, pairwise interactions among the three forms of reproduction may
be significant, but collectively they do not interact with values of the remaining
form (Fienberg, 1980).
DISCUSSION
The results of this study indicate apomictic, polysporic and polyembryonic species
are polyploid or paleopolyploid and probably possess duplicate genes for female
development. They also indicate that such species are associated at the familial level
and are evolutionarily linked.
Duplkati? genes and reproductiveb-anomalous species
Pobploidy and the evolution of angiosperms
Polyploidy is a major mechanism of speciation among angiosperms. Stebbins
(1985) believes successful polyploids are almost always derived from interracial
(heterozygous) or interspecific hybrids. He attributes their tolerance of diverse
habitats to increased heterozygosity conferred by hybridity and their widespread
occurrence in some groups of angiosperms (grasses in particular) to secondary
contacts between previously isolated populations. In contrast, Levin (1 983) cites
EVOLUTION OF APOMIXIS AND RELATED ANOMALIES
Sexual
Apomictic
-3
3
PE
ME
AM
sx
Polyembryonic
4
0
-2
-4
63
PE
ME
AM
sx
Monoembryonic
sru',
PS
I S
PS
MS
Figure 5. Mean Pearson residuals for the following three models: (i) independence of the levels of
apomixis (apomictic or sexual) from the levels of polyspory and polyembryony taken jointly (top
graphs), (ii) independence of the levels of polyspory (polysporic or monosporic) from the levels of
apomixis and polyembryony taken jointly (middle graphs), and (iii) independence of the levels of
polyembryony (polyembryonic or monoembryonic) from the levels of apomixis and polyspory taken
jointly (bottom graphs). Pearson residuals were averaged across the least, more and most restrictive
groupings of families (see Material and Methods). The ranges of the three values averaged together
are indicated by vertical lines. Each of the eight points in each set of graphs (top, middle and bottom)
represents one of the eight combinations of the three binary variables. The degree of deviation from
the expected for each point, in either a positive or negative direction, is represented by the deviation
from zero. PS =polysporic, MS = monosporic, PE =polyembryonic, ME =monoembryonic, AM =
apomictic, SX = sexual.
cytological, biochemical, genetic, physiological, and developmental findings to support his view that even homozygous autopolyploids can express punctuated phenotypes adapted to diverse habitats.
Auto and allopolyploidy provide raw materials for duplicate-gene evolution and
are often followed by ascending or descending aneuploidy, diploidization, and the
stabilization of new x values. This process fragments genomes and produces meso
and paleopolyploids (Ehrendorfer, 1980; Lewis, 1980; Goldblatt, 1980). The shift
from polyploidy to paleopolyploidy may, because of rapid aneuploid formation and
stabilization, be abrupt. Alternatively, it may occur gradually, by mutation and
selection, with a distinct mesopolyploid phase (Fig. 7). Thus, both polyploids and
paleopolyploids may form rapidly, and the resulting phenotypes can be adapted to
diverse habitats. Species containing meso or paleopolyploid genomes may be diploid
or polyploid. This cyclic mechanism of polyploidization and paleopolyploidization
(Fig. 7) may be central to the evolution of apomixis, polyspory, polyembryony, and
related .anomalies.
Y
Y
N
N
Y
Y
N
N
Y
Y
Y
Y
N
N
N
N
Y
N
Y
N
Y
N
Y
N
PE
6.72
2
0.05
53.4
3
0.001
X2
P<
df
1
3
1
2
2
5
6
177
B
EXP
4
4
7
18
39
41
65
170
A
EXF'
15
2
13
3
28
43
59
185
OBS
0
1
7
4
4
N
Y
Y
Y
Y
Y
Y
N
N
Y
Y
N
N
AM
Category
N
N
N
PS
Y
N
Y
N
Y
N
Y
N
PE
P<
X2
df
2
28
43
13
3
59
185
15
OBS
19.6
3
0.001
65
170
4
22
58
21
1
7
C
EXP
37.5
2
0.001
8
9
3
3
4
1
6
176
D
EXF'
Model'
Model'
2
8
5
6
N
N
Y
Y
N
N
Y
Y
N
N
Y
Y
N
N
AM
Category
Y
Y
PE
Y
N
Y
N
Y
N
Y
N
PS
df
P<
x'
28
59
2
3
43
185
13
15
OBS
50.2
3
0.001
44
48
163
5.54
2
NS
184
I
4
10
18
33
54
F
EXF'
11
11
81
6
5
23
E
EXF'
Model'
Number of families
0.03
I
NS
28
59
2
3
43
185
13
15
G
EXP
I Models A, C m d E test whether the counts in each of the four categories specified by the second and third variables are proportional acros the two levels of the first variable
( A ? PS
, and PE, respectively). Models B, D and F test for independence of the second and third variables at each level of the first variable (AM, PS and PE, respectively).
Model G is the no second order interaction model and indicates that while painvise interactions among the three variables may exist, they are not, when taken collectively,
affected by the third variable pienberg, 1980).
PS
Category
AM
Number of families
Number of families
according to the least-restrictive-analysis criteria (see Material and Methods)
TABLE
6. Assignment of 348 families of angiosperms to eight categories (OBS)defined by the presence M or absence (N) of apomixis (AM), polyspory (PS),
and polyembryony (PE) and the expected (Em)counts for seven models that reflect possible relationships among the variables. Families were delimited
0
i-
4
m
EVOLUTION OF APOMIXIS AND RELATED ANOMALIES
3.0
1
Apomictic
PE
ME
-1.5
-3.0
1
Sexual
PE
ME
AM
sx
-1.5
-3.0
AM
3.0
3.0
65
sx
1 Polyembryonic
PS
MS
3.0
1Monoembryonic
PS
YS
Figure 6. Mean Pearson residuals for the following three models: (i) conditional independence of the
lcvels of polyspory from the levels of polyembryony given the level of apomixis (apornictic or sexual)
(top graphs), (ii) conditional independence of the levels of apomixis from the levels of polyembryony
given the level of polyspory (polysporic or monosporic) (middle graphs), (iii) conditional independence
of the levels of apomixis from the levels of polyspory given the level of polyembryony (polyembryonic
or monoembryonic) (bottom graphs). Pearson residuals were averaged across the least, more and most
restrictive groupings of families (see Material and Methods). The ranges of the three values averaged
together are indicated by the vertical lines. Each of the eight points in each set of graphs (top, middle
and bottom) represents one of the eight combinations of the three binary variables. The degree of
deviation from the expected for each point, in either a positive or negative direction, is represented
by the deviation from zero (symbols as in Figure 5).
Genomes of apomictic, pobsporic and polyemblyonic species
Most angiosperms are in some sense polyploid (Goldblatt, 1980; Lewis, 1980)
and contain duplicate loci. Apomicts are generally polyploid and contain primary
genomes that have not been subjected to recent paleopolyploid processes (most
apomicts, low x values and few x values per genus, Fig. 2) or mesopolyploid genomes
that have undergone moderate aneuploid-induced base number shifts (few apomicts,
high x values and many x values per genus, Fig. 2, Appendix). Thus, apomicts
contain complete or nearly complete (genetically balanced) duplicate sets of genes.
The existence of diploid apomicts with primary genomes would not be consistent
with the duplicate-gene hypothesis. The few existing ‘diploid’ apomicts (reviewed
by Asker & Jerling, 1992) with their x values include: Hieracium umbellatum, x= 9
(apomixis uncertain), and Parthenium argentatum, x = 17,18 (Asteraceae);Arabis holboellii,
x = 4,6,7 (Brassicaceae);Sorbus exima, x= 17, and Potentilla argentea, x= 7 (Rosaceae);
Anthoxanthum australicum, x = 5,7 (Anthoxanthum and Hierochliie combined by Schouten
& Veldkamp, 1985), and Nardus stricta, x = 13 (Poaceae). Sexual diploids that become
apomictic upon autopolyploidy or apomictic tetraploids that become sexual upon
J. G . CARMAN
66
Evolution8y
Primary diploid
1
Reproductive
&!.waw&
Sexual
Genome dynrmiu
liuumlh
LOW
FCW
Low
Few
Monosporic
Monoembryonic
Sexual or apomictic
Monosporic
Mono or polyunbryonic
Mesopolyploid
Sexual or apomictic
Mono or polysporic
Mono or polyunbryonic
Low to high
Few to many
Paleopolyploid
Sexual, seldom apomictic
Low to high
Many
Low to high
Few to many
Mono or polysporic
Mono or polyembryonic
SCXUd
diploid
Mono or polysporic
Mono or polyembryonic
Figure 7. Schematic representation of general relationships observed in this study among the following
variables: the evolutionary status of genomes, reproductive characteristics, chromosome base numbers,
and base numbers per genus. Macroevolution often follows polyploidy, mesopolyploidy and palepolyploidy (see text). Paleopolyploidy may occur gradually (after long periods of mesopolyploidy)or
rapidly (by Skipping the mesopolyploid phase). The genomes of many angiosperms were probably
derived by cycling through the polyploidy-paleopolyploidyloop followed by microevolution (mutation
and natural selection).
dihaploidy (reviewed by Asker & Jerling, 1992) include: Ranunculus auricomus, x = 7,8
(Ranunculaceae); Pmpalum hexastachyum, x = 6,lO; Panicum maximum, x = 9,lO; and
members of the Bothnochloa-Dichunthium complex, x = 10 (Poaceae). That these
apomicts are paleopolyploid is suggested by high base numbers (>9) or multiple
bases per genus, either in the apomicts themselves or among related genera.
Many polyembryonic (Gustafsson, 1946, 194713; Asker & Jerling, 1992) and
polysporic (Bharathan, 1996)species are considered diploid. However, polyembryonic
species generally have high x values (Fig. 2), and, as suggested by Naumova (1993),
true diploidy may be rare among them. Likewise, the average nuclear DNA content
of selected polysporic diploids was 5-fold higher than selected monosporic diploids
(Bharathan, 1996). High x values and multiple x values per genus (Fig. 2) indicate
most if not all polyembryonic and polysporic species are paleopolyploid and contain
grossly imbalanced sets of genes. This genomic promiscuity contrasts sharply with
the genomic integrity of apomicts, and this contrast may partially explain the
evolution of these anomalies.
l'he duplicate-gene asynchrony hypothesis
Asynchronous duplicate-gene-induced development
The genomes of hybrids often inhabit separate nuclear domains (Leitch et al.,
1990), and they often respond to their own genomic signals. For example, the
EVO1,UTION OF APOMIXIS AND RELATED ANOMALIES
67
chromosomes of aposporous Schizachyrium segregated asynchronously as genomes
during anaphase I and I1 as if they were responding to their own signals (Carman
& Hatch, 1982). It is hypothesized herein that genome-specific signals are expressed
asynchronously for whole developmental programs.
Apomixis, polyspory and polyembryony involve developmental programs that are
ectopically and/or prematurely expressed. The duplicate-gene asynchrony hypothesis
claims (i) asynchronously-expressed duplicate genes cause these anomalies and (ii)
the duplicate genes originate from different genomes in polyploids or different
fragments of genomes in meso or paleopolyploids. Genetic balance (completeness)
appears important to apomixis. Genetic imbalance (competition between superimposed and genetically-incomplete meiotic and embryo sac development programs)
appears important to polyspory, in which embryo sac development only partially
replaces meiosis (Fig. 1).
Heterokaryon studies with yeast shed light on the types of developmental mechanisms that might cause apomixis, polyspory and polyembryony. Entire cell cycle
stages are skipped when yeast cells in G1 are fused with cells in S-phase, i.e. G1
chromosomes replicate precociously. The rate of initiation of replication depends
on the S:G1 nucleus ratio in the heterokaryon. In mitotic yeast cells fused with
interphase cells, the interphase nuclei (all stages) prematurely enter mitosis (Lewin,
1994).
Apomixis may occur in an analogous manner. If embryo sac development signals
from one genome are superimposed on megasporogenesis signals from another
genome, meiosis may be skipped (diplospory) or embryo sac development may be
ectopic (apospory). Accordingly, apomictic-like tendencies would occur in polyploids
only if major differences in timing of megasporogenesis and embryo sac development
(relative to ovule maturation) existed among the ancestral ecotypes or species. Such
natural variation might only be found in highly cosmopolitan angiosperms.
According to this hypothesis, many secondary contacts between previously isolated
populations must have occurred to produce the large number of currently extant
apomicts. The distribution patterns of most apomicts suggest a Pleistocene origin
(Stebbins, 1971; Asker & Jerling, 1992). Eight major glaciations, which covered up
to 20% of the earth’s surface, occurred during the Pleistocene. These were separated
by warm interglacial periods lasting for several thousand to a hundred thousand
years. Likewise, most of the major glacial events consisted of glacial advances
interrupted by minor interglacial periods lasting for a few thousand years (Frakes,
Francis & Syktus, 1992). Hence, during the Pleistocene, the northern latitudes
of North America and Eurasia were repeatedly deglaciated and revegetated by
cosmopolitan taxa capable of adapting to cool climates and short growing seasons.
A precocious meiosis and embryo sac development in young ovules may have
been one of many adaptations to short summers in high latitudes. Glacial advances,
which followed the numerous interglacial periods, cooled the lower latitudes permitting high latitude taxa to invade low latitude flora. Hence, throughout the
Pleistocene, numerous opportunities existed for ecotypes with a putatively-precocious
embryo sac development to form polyploids with ecotypes (or different species) with
a putatively-delayed embryo sac development. These polyploids would have exhibited
asynchronous female development from which efficient apomixis systems may have
evolved.
The type of anomaly expressed in angiosperms may be a function of (i) the degree
of asynchrony among competing developmental programs and (ii) the degree of
68
J. G . CARMAN
genetic completeness in such programs. Meiosis during diplospory of the Taraxacum
and Ixeris types (Fig. 1) is initiated, and some chromosome pairing and recombination
may occur (Gustafsson, 1946; Kindiger & Dewald, 1996) prior to disruption by
precocious embryo sac formation. In contrast, embryo sac formation completely
replaces meiosis in the Antennaria and Eragrostis types of diplospory, perhaps because
of earlier or stronger embryo-sac-formingsignals. In tetraspory, the meiocyte reflects
characteristics of both developmental programs. Meiotic reduction occurs, but the
meiocyte lacks callosic walls and cross walls (Rodkiewicz, 1970) and precociously
expands by vacuolization, which is typical of diplosporic MMCs and young monosporic embryo sacs (Fig. 1; Battaglia, 1989). Signals from fragmented genomes with
grossly imbalanced sets of duplicate genes (typical of paleopolyploids) may induce
such asynchronous disturbances (Fig. 1, note theoretical gaps in developmental
programs). Polyembryony also represents asynchronous development, and may be
induced by a prolonged exposure (caused by asynchronously-expressed duplicate
genes) to signals that confer embryogenic competence to floral tissues (Carman,
1990).Nucellar cells might be similarly ‘conditioned’ to produce aposporous embryo
sacs.
Three other anomalies are consistent with the proposed existence of competing,
asynchronously-expressed, and genetically-incomplete female developmental programs. The first, preleptotene chromosome condensation, involves a superpositioning
of a mitotic prophase, possibly induced by duplicate signals from a second genome,
between premeiotic S and leptonema. The affected chromosomes condense to a
mitotic metaphase state, decondense, and then resume a normal meiotic prophase
(Bennett& Stern, 1975).This anomaly occurs in Lilium, Tradescantia, Trillium, Fitillaria,
ficotiana, Ecia, and Psilotum, and appears evolutionarily linked with polyspory, i.e.
the first five genera also contain species that express bispory or tetraspory (Appendix).
In the second anomaly, Allium odorum-type diplospory (Asker & Jerling, 1992), a
mitotic S phase is duplicated, possibly encoded by a second genome, prior to meiosis,
and a 4n GI-phaseMMC is produced. Chromosome pairing during meiotic prophase
occurs only between homologous sister chromosome pairs, resulting in twice the
number of bivalents at metaphase I as in a monosporic plant. No effective recombination occurs. As in bispory (Fig. l), which occurs in many other Allium, the
second meiotic division in one cell of the dyad fails and the failed cell degenerates.
Cytokinesis fails in the surviving cell, and the two nuclei, resulting from a successful
karyokinesis, undergo two further mitoses to produce an unreduced eight nucleate
Pobgonum-type embryo sac. This process is referred to as automixis in parthenogenetic
animals (Suomalainen et al., 1987).
In the third anomaly, a precociously-formed MMC, possibly encoded by one
genome, degenerates and is replaced by one or more functional MMCs, possibly
encoded by another genome. This anomaly occurs in Alchemilla, Cotoneaster, Sorbus
and Rubus (Davis, 1966),which also contain aposporic, diplosporic or bisporic species
(Appendix),and in Aphanes, which may contain apomictic species (Sven Asker, pers.
comm. 1996).All species expressing apomixis, polyspory, polyembryony or the three
additional anomalies just described appear to contain chromatin from multiple
genomes (they are polyploid or paleopolyploid) and asynchronously express various
female developmental pathways. Furthermore, these species are phylogeneticallyrelated, i.e. they are mostly derived from cosmopolitan families that probably contain
extensive temporal intergenomic heterozygosity for female development.
EVOLUTION OF APOMIXIS AND RELATED ANOMALIES
69
?he role of mutation
The degree of gene duplication, high for apomicts and moderate for polysporic
and polyembryonic species, appears inversely related with the number of cytological
irregularities observed in the respective anomalies. For example, development during
apomixis is generally normal, though precocious or ectopic (Fig. 1). Thus, a ‘nearly
complete set’ of embryo-sac-forming genes may be required to completely replace
meiosis. In contrast, polyspory is characterized by numerous cytologicalabnormalities
(Fig. I), probably because ‘complete sets’ of asynchronously-expressedgenes are not
present, e.g. Adoxa and h a - t y p e tetraspory involve only one or two embryo sac
mitoses (Fig. 1). Alternatively, polyspory may simply represent a less extreme form
of duplicate-gene asynchrony. If so, Poaceae which has numerous sexual and
apomictic polyploids, should contain numerous polysporic species, but it does not.
In contrast, polyspory is strongly associated with the frequent (and recent?) occurrence
of aneuploid series formation and stabilization, which has not recently occurred in
Poaceae.
Mutations have probably played a secondary role in the evolution of most female
anomalies. For example, the first genotypes of many apomicts probably exhibited
low fertility and only tendencies for apomixis. Today’s highly fertile apomicts may
be the result of few mutations (probably null alleles) that greatly improved seed set
(fitness) in the primal genotypes by eliminating deleterious competition between
asynchronous signals. Hair (1966), commenting “the stages in the evolution of
apomixis are complete” in Agmpyron scabrum (now Ebmus rectisetus) identified four
groups of genotypes: (i) completely sexual, (ii) facultatively diplosporous (frequent
formation of haploids, triploids and unbalanced forms following the failure of meiosis
or fertilization), (iii)predominantly apomictic with meiosis largely suppressed on the
female side, and (iv) near-obligately apomictic with suppression of both female and
male meiosis. However, the completely sexual genotypes (Wellington I and Tawera)
were recently reclassified as Ebmus solandn (Connor, 1994),which suggests the “stages
in the evolution of apomixis” begin with weak facultative expression. Variable
fertility exists in many other apomicts, and “tendencies towards apomixis” are
common in natural and synthetic polyploids (Asker & Jerling, 1992).
Null-alleles that enhance fertility in polyploid apomicts, and which have functional
homoeologous but asynchronously-expressedcounterparts, may be lethal to gametes
at the diploid level (monoploid gametes) if they originally encoded essential steps of
gamete production. Gamete lethality would occur when the functional allele(s)from
the other genome are not present, i.e. in 50% of gametes produced by a polyhaploid
of a polyploid apomict. Gamete-lethal gene(s)appear to prevent passage of apomixis
in polyhaploid Ranunculus auricomus (Nogler, 1982) and may be prevalent among
other meso and paleopolyploid apomicts.
Male meiocytes in apomicts often escape nonreduction (Asker & Jerling, 1992;
Mogie, 1992). It is likely the precocious expression of embryo-sac-forming signals
has no direct developmental analogue on the male side. Furthermore, differing
durations of male and female meioses, as is observed in many species, coupled
with reduced meiotic durations caused by polyploidy (Bennett, 1977) could force
reproductive plasticity towards apomixis but have little or no effect on the male
side.
Female developmental asynchrony may be caused by differences among genomes
in stages of ovule development in which signals for megasporogenesis and embryo
sac development occur. Such variation is high in some families, e.g. female meiosis
70
J. G. CARMAN
in Liliaceae and Orchidaceae may occur before, during or after male meiosis,
depending on the species (Bennett, 1977). Asynchrony could also result from
polyploidy-induced differences in the durations of different female developmental
phases and from cryptic interactions among duplicate genes. I believe deletions and
mutations (mostly null alleles) have chiselled at initially-complete sets of duplicate
asynchronously-expressed genes and, through natural selection, inadvertently sculptured numerous and diverse anomalies of reproduction.
?he squelching of EmstS hybridization hypothesis
Ernst (1 9 18) amassed much evidence to support his hypothesis that apomixis
results from hybridity and that genes specific to apomixis are not required. His
evidence included the fact that apomicts have high chromosome numbers, are highly
polymorphic, and their sex cells often degenerate in a manner observed in interspecific
hybrids. He suggested that such hybrids form a continuum from fully-functional
sexual reproduction, to apomixis, and finally to vegetative reproduction. Where a
hybrid fit on the continuum depended on how closely related the parental species
are. Ernst disagreed with Strasburger’s earlier hypothesis that some unknown latent
propensity for apomixis, which according to Strasburger resides only in certain
sexual species, is required for apomixis (Gustafsson, 1946; Asker & Jerling, 1992).
Ernst’s hypothesis may be largely incorrect, but it may be more correct than the
mutant-gene hypotheses that replaced it. Clearly, apomixis is not part of a reproductive continuum dictated by parental relatedness. However, it may belong to
a continuum dictated by intergenomic asynchrony in the expression of female
developmental genes. Such asynchrony may be rare in many families, regardless of
phylogenetic unrelatedness. This would account for the rarity of apomixis in nature
and in artificial hybrids and amphiploids.
Hybrids obtained between sexual amphiploids of certain genotypes of Raphanus
sativus and Brassica oleraceae are aposporic, i.e. they appear to fit in the ‘tendencies
for apomixis’ realm of a developmental asynchrony continuum. From 36 to 70%
of ovules in six hybrids contained from 1.6 to 2.9 aposporic embryo sacs (Ellerstrom
& Zagorcheva, 1977). The authors noted that these data support a heterozygosity
hypothesis for the origin of apomixis. It should also be noted that apospory is not
expressed elsewhere in the parental species, genera, family, or entire Brassicales
order (Appendix).This strongly suggests that apospory did not in this case surface
as a result of a gradual accumulation of developmentally-suppressedapomixis genes.
Maternal progeny of aposporic Raphanobrassica were also obtained (Ellerstrom, 1983).
Likewise, apospory and diplospory occur together in diploid (2n = 34) and tetraploid
(2n = 68) cytotypes of Sorbus eximia, which are putative hybrids and amphiploids,
respectively, of two sexual but paleopolyploid diploids (x = 17), Sorbus aria x Sorbus
torminalis (Jankun & Kovanda, 1988; Jankun, 1993). Apomixis or tendencies for
apomixis have also been reported in interspecific hybrids or amphiploids of sexuals
in Asteraceae (Stebbins, 1932), Poaceae (Mujeeb-Kazi, 1981; Bothmer et aL, 1988),
and other families (reviewed by Asker & Jerling, 1992).
Ernst’s hypothesis was rejected for three reasons. First, apomixis had not occurred
in artificial hybrids (Gustafsson, 194713). As just noted, this is no longer the case.
Second, Mendelian analyses of apomixis pointed to relatively simple genetic control,
which suggested to many that apomixis genes must exist (Gustafsson, 1946, 1947a,
b). According to the duplicate-gene asynchrony hypothesis, which may be viewed
as a revision of Ernst’s hypothesis, normal regulatory gene(s)from one genome are
EVOLUTION OF APOMIXIS AND RELATED ANOMALIES
71
expressed out-of-synchronywith other normal regulatory genes from another genome
and are responsible for initiating precocious or ectopic embryo sac formation. These
regulatory genes have been mistaken for dominant mutation-produced apomhis
genes.
Third, it was determined that some apomicts arose from sexual diploids through
autopolyploidy. This observation decisively squelched Ernst’s hypothesis and any
perceived requirement for interspecific heterozygosity (Gustafsson, 1946). Indeed,
hybridization and heterozygosity are now believed by many to be a consequence of
apomixis, not a cause (Nogler, 1994).However, sexual diploids that become apomictic
upon autopolyploidization may do so because interracial autopolyploidy is involved,
or they contain paleopolyploid genomes. The potential role of paleopolyploidy in
the evolution of apomixis has not been previously considered.
Polyploidization often increases the frequency of haploid parthenogenesis (Bierzychudek, 1985), which suggests specific parthenogenesis genes are not required for
apomixis (Gustafsson, 1947a,b). Asker & Jerling (1992) attributed this increase to a
shortening of meiosis accompanying polyploidization (Bennett, 1977), which may
also force reproductive plasticity (duplicate-gene asynchrony) towards apomixis.
Such an acceleration occurs in paleopolyploid ( x = 18) irripsacurn. Megasporogenesis
in sexual diploids and embryo sac formation in diplosporous polyploids begin at the
same stage of ovule development. Likewise, the end of megasporogenesis (tetrad
stage) in diploids coincides with the two-nucleate unreduced embryo sac stage in
tetraploids (Leblanc & Savidan, 1994; Peel et al., 1997a). Development is similarly
accelerated by polyploidy in other aposporous and diplosporous species (Gustafsson,
1946; Peel et al., 1997a,b).
Gustafsson ( 1947a,b) believed apomixis might result from genetic interactions
following polyploidy in taxa previously containing a propensity for apomixis. Thus,
apomixis is under genetic control, but in not necessarily the direct result of mutation.
This view, also expressed by Asker andJerling (1992), is consistent with the duplicategene asynchrony hypothesis, i.e. substantial intergenomic heterozygosity for timing
and rates of female development exists in highly cosmopolitan families and constitutes
a “propensity for apomixis”.
Others suggest apomixis genes evolved through mutation (Nogler, 1984a, 1994).
Mogie (1992)believes haploid parthenogenesis is a preadaptation that allows a single
dominant meiotic mutation at one of many loci to induce apomixis. Two or more
mutations would be required in the absence of the parthenogenesis preadaptation.
Hence, apomixis occurs in some families more than others.
Mogie (1992) argues that apospory results from factors exuded from degenerating
MMCs. However, such sacs generally form prior to degeneration of the MMC or
its sexual products (Asker & Jerling, 1992; Nogler, 1995; Peel et al., 1997a).
Mogie further suggests that the mutant locus, which supposedly causes apomixis in
preadapted species, permits facultative sexuality because it is heterozygous and the
mutant apomixis allele is only mostly dominant. He believes heterozygosity is
maintained because the wild type allele is required in somatic cells. Mogie speculates
that the apomixis allele is dominant only in generative cells, and then only because
of polyploid dosage effects. The wild-type allele is only dominant in vegetative cells,
regardless of polyploidy, supposedly because of a different cellular “environment”
from generative cells.
Variations in preadaptations, cellular environments, loci mutated, genetic backgrounds, incomplete dominance relationships, etc., must be differentially invoked to
72
J. G . CARMAN
explain, using simple inheritance models, the frequent inconsistencies in reproductive
mode observed in progeny obtained when apomicts are crossed to apomicts, sexuals,
or different sexual or apomictic ecotypes (Gustafsson, 1946, 1947a,b;Asker &Jerling,
1992).Apomixis-gene hypotheses have failed to explain the many ambiguities found
in the apomixis literature without resorting to such elaborate and speculative
annotations. In contrast, the duplicate-gene asynchrony hypothesis predicts ambiguity, i.e. the mode of reproduction expressed in wide hybrids depends on how
dissimilarities in timing of developmental gene expression are affected by adding or
removing genomes.
lh transitional-phase hypothesis
Polyspory and polyembryony are evolutionarily-linked with apomixis, i.e. one or
both occurred in 30 of the 33 families that contained apomicts. The expected value
was 17 (Fig. 4). Apomixis may serve as a reproductively-stable transitional phase
during which paleopolyploid processes infrequently eliminate gene duplications that
cause apomixis but retain genes for monospory, or duplications for polyspory,
polyembryony, or other anomalies. This mechanism could foster the evolution of
new species, genera, and even families, a concept that contrasts sharply with the
views of Darlington (1939), who concluded that apomixis is an evolutionary blind
alley, and Stebbins (197l), who concluded that apomicts only produce new variations
upon old themes.
The phylogenetic data analysed herein support the transitional-phase hypothesis.
If related polysporic and polyembryonic species evolved from related but now extinct
apomicts, they should still be found in the same family. Accordingly, when polysporic
and polyembryonic species are found in sexual families (families that may have once
contained apomicts), they should tend to occur together. Such a skewed distribution
was observed (Table 6, lower four values of model B; Fig. 6, upper right graph).
Moreover, if polysporic and polyembryonic species tend to evolve from apomicts,
then their occurrence in families that currently express apomixis should be greater
than expected. This was also observed (Table 6, Model A). Furthermore, polyspory
and polyembryony involve different stages of development and are probably controlled by different genome modifications. Thus, they should be independently
distributed among families in which they are currently evolving, i.e. in apomictic
families. This too was observed (Table 6, upper four values of model B; Fig.
6, upper left graph). Finally, if apomicts occasionally produce polysporic and
polyembryonic progeny, then apomixis and polyembryony as well as apomixis and
polyspory should be associated among all families. These associations were also
clearly observed (Tables 3 and 4). The transitional-phase hypothesis may be the
simplest explanation for these associations. All four associations expected to occur
if polysporic and polyembryonic species occasionally evolve from apomicts were
observed and were generally highly significant.
Case study: macroevolution in Poaceae,Astt-raceae and Orchidaceae
If the transitional-phase hypothesis is correct, additional evidence should be found
among families that differ in their ‘current rates’ of paleopolyploid genome formation.
Poaceae, Asteraceae and Orchidaceae each contain more anomalous genera (1 13
EVOLUTION OF APOMIXIS AND RELATED ANOMALIES
73
TABLE 7. Mean number of chromosome base numbers in reproductively-anomalous genera and mean
basc number (anomalous genera only) for three families that collectively contain 22.4% of apomictic,
polysporic or polyembryonic angiospermous genera. Also presented are distributions of anomalous
genera by family and anomaly
Distribution of anomalous genera’
Family
Poaceae
Asteraceae
Orchidaceae
Mcan no. of bases
per genus‘
Mean
base no.’
k SD”
I .2r k 0.6
2 . l b k 1.5
4. la 2.6
9.5b f 2.6
9.2b f 3.6
I9.5a f 4.4
+
~
k SD’
~
Genera
Apomictic
Polysporic
%
YO
Yo
93
73
4
0
38
52
20
21
72
no.
40
48
25
~
~~
Polyembryonic
~
~
’ Percentages summed arross anomalies do not add to 100% because some anomalous genera express more than
one anomaly.
*Means within columns followed by the same letter are not significantly different according to Tukey’s multiple
comparison procedure (R0.05).
SD = standard deviation.
’
total) than any other family (506 genera express anomalies of reproduction, see
Appendix) and each represents a distinct stage in the evolution of paleopolyploid
genomes: mostly polyploid, mostly mesopolyploid, and mostly paleopolyploid, respectively (Fig. 7). Note that the percentages of genera that are apomictic versus
polysporic versus polyembryonic distinctly differ in these families (compare Table 7
with Fig. 7).
The anomalous Poaceae genera are mostly polyploid apomicts, though some
contain paleopolyploid genomes that have become diploidized near ancestral polyploid levels (Goldblatt, 1980; Stebbins, 1985). Because of low x values and few
stabilized x values per genus, the transitional-phase hypothesis predicts a low
frequency of polyspory and polyembryony, which was observed (Table 7; Fig.
7). In contrast, Asteraceae contains mesopolyploid genomes undergoing extensive
aneuploid series formation (Table 7, note high coefficients of variation for mean
number of x values per genus and mean x value). The transitional-phase hypothesis
predicts the high frequency of apomictic, polysporic and polyembryonic species in
this family (Fig. 7, Table 7). Most Orchidaceae are highly paleopolyploid with high
x values and multiple x values per genus (Table 7). Apomixis is nearly lacking in
this family (possibly eliminated by aneuploidy) while polyspory and polyembryony
predominate (Table 7; Fig. 7). Apparently, apomicts seldom become extensively
aneuploid without reverting to sexuality (monosporic or polysporic) or becoming
sterile. Thus, they remain euploid (or nearly so) and viable if enough recombination
occurs to retain fitness.
Many polysporic species belong to ancient, highly-paleopolyploid families and
may no longer be closely related to extant apomicts. It is not possible to find further
phylogenetic evidence for the transitional-phase hypothesis in such families. However,
in Asteraceae, many apomicts and polysporic species have evolved recently (see
Huber & Leuchtmann, 1992, for examples). As expected, some apomicts in this
family also express polyspory, including Tiidax trilobata (Johri et al., 1992), numerous
species of Erigmn (Harling, 1951; Nesom, 1989; Huber & Leuchtmann, 1992;Johri
et al., 1992; Noyes, Soltis & Soltis, 1995), several species of Rudbeckia (Johri et al.,
1992), and individual species in Anhnaria, Euvbiopsb and Leontodon. Species from a
few other families exhibit both anomalies, including Sambucus racemosa and various
74
J. G. CARMAN
species of Limonium, Cordia, and Cynoglossum(Carman, 1995).Furthermore, monospory,
bispory and tetraspory are expressed in different ovules of the same plant in some
polysporic species and all combinations of these forms of reproduction are expressed
in many species (Hjelmqvist, 1964;Johri et al., 1992). Such species may represent
early stages of polysporic evolution wherein the silencing of asynchronous signals
by aneuploidy and mutation is incomplete, allowing greater plasticity in reproductive
expression. Apomicts ancestral to some of these species may still exist.
Case study: macroevolution in Hyacinthaceae
According to the transitional-phase hypothesis, apomixis occasionally provides
long-term reproductive stability for the evolution of species with novel genome
modifications and reproductive behaviors (Fig. 7). Evidence for this is found among
the following genera of the Hyacinthaceae: Omithogalum (sexual and apomictic; x =
3-5, 7, 11, 13, 17, 19, 23), Hyacinthoides (polysporic, x=8), Scilla (polysporic; x =
6-1 1, 13, 17, 19),and Camassia (polysporic, x = 15). Ornithogalum is the most primitive
member of this clade (Svoma & Greilhuber, 1989; Dahlgren et al., 1985), and the
other genera are derived therefrom or from common but extinct ancestors. Support
for the transitional-phase hypothesis includes (i) the presence of apomixis in the
most primitive member and polyspory in the most derived members, (ii) extensive
aneuploid series formation and base number stabilization involving sexual, apomictic,
and polysporic species, and (iii) new paleopolyploid genera with solitary x values
(derived from earlier aneuploid series) that contain polysporic species.
Speciation by recombination and natural selection may proceed rapidly when
sexuality is restored (Fig. 7). This may have occurred in Orchidaceae (Table
7), Amaranthaceae, Amaryllidaceae, Boraginaceae, Brassicaceae, Burmanniaceae,
Casuarinaceae, Cucurbitaceae, Hyacinthaceae, Hypericaceae, Limoniaceae, Malpighiaceae, Moraceae, Myrtaceae, Ranunculaceae, Rhamnaceae, Rosaceae, Rutaceae, Thymelaeaceae, and Urticaceae. Genome base numbers in each of these
families were derived from one or more aneuploid series, and apomixis as well as
polyspory or polyembryony occur in each (Appendix).Apomixis may be facilitating
speciation in the following 47 genera: A l c h i l l a , Amlanchier, Atraphaxis, Bothriochloa,
Carthamus, Cenchrus, Eugenia (Syggium), Helianthus, Hiptage, Hypericum, Malus, Marah,
Melampodium, Omithogalum, Pennketum, &us and agopetulum, which express apospory
and polyembryony, Cordia, Cynoglossum and Leontodon, which express apospory and
polyspory; Euvbiopsk (Minuria), Sambucus and Tridax, which express apospory, polyspory and polyembryony; Alnus, Arabis, Balanophora, Casuarina, Garcinia, Momordica,
Taraxacum and Wzkstroemia, which express diplospory and polyembryony; Limonium
and Rudbeckia, which express diplospory and polyspory; Allium and Bumzannia, which
express diplospory, polyspory and polyembryony; Beta, Cucumis, E l a t o s h a , Hieracium,
Ochna, Poa, Potatilla, Sorbus and Sotghum, which express apospory, diplospory and
polyembryony; Rubus, which expresses apospory, diplospory and polyspory; and
Erigmn and Antennaria, which express apospory, diplospory, polyspory and polyembryony.
CONCLUSIONS
Phylogenetic relationships and genome characteristics of apomictic, polysporic
and polyembryonic species support (i) the duplicate-gene asynchrony hypothesis, for
EVOLU’I’ION OF APOMIXIS AND RELATED ANOMALIES
75
the evolution and genetic regulation of female anomalies, and (ii) the transitionalphase hypothesis, for the role of apomixis in the evolution of at least some novel
monosporic, polysporic and polyembryonic taxa. Evidence to date suggests species
expressing one or more of the female anomalies studied herein are polyploid or
paleopolyploid. Hence, they probably contain duplicate genes for female development. Furthermore, these species often occur in cosmopolitan families and
were characterized by cytological abnormalities readily explained by asynchronous
and ectopic expressions of multiple developmental pathways encoded by multiple
genomes.
The duplicate pathways causing some female anomalies appear at the cytological
level to be co-expressed but with major segments of each pathway being greatly
suppressed or absent. Examples of these putative conglomerations of incompletelyexpressed asynchronous signals include all types of polyspory and polyembryony,
preleptotene chromosome condensations, Allium odorum-type diplospory, and the
sequential formation of duplicate MMCs. Species expressing these anomalies contain
paleopolyploid genomes. In contrast, apomicts generally contain primary to mesopolyploid genomes, and their asynchronously-expressed developmental pathways
appear more complete. These interpretations suggest that complete or nearly
complete developmental pathways are required to replace one stage of development
with another stage, as generally occurs in diplospory and apospory. In contrast,
competition between asynchronously-expressed but genetically deficient pathways
permits segments of each pathway to be co-expressed (polyspory, polyembryony,
etc.).
The phylogenetic and genomic associations identified herein suggest that apomixis
is not always an evolutionary dead end, i.e. the polyspory and polyembryony found
in some species may be remnant expressions of apomixis. Hence, apomixis may be a
reproductively-stable evolutionary springboard, which occasionally radiates, through
paleopolyploid processes, reproductively-normal and novel species and genera.
Extreme paleopolyploidy (numerous deletions and mutations) may make it impossible for some forms of polyspory to revert to monospory and some potentiallyobligate apomicts to revert to sexuality. This appears to be the case with apomictic
animals, which are believed to have evolved at the diploid level (Suomalainen et al.,
1987).Yet, apomixis in animals may have evolved at the polyploid level in a manner
similar to that proposed herein for angiosperms. If so, some of the unusual sexual
and asexual reproductive systems found in animals (insects, amphibians, reptiles,
etc.) may, as in angiosperms, be remnant expressions of apomixis.
The allure of fixing hybrid vigor in crops through apomixis has been fueled by
reports of simple inheritance and has generated worldwide interest (Elgin & Miksche,
1992; Wilson, 1993).However, regulatory genes controlling duplicate developmental
pathways may mimic simple inheritance. Dominance or recessiveness for ‘apomixis
gene(s)’has been assumed when crosses between apomicts and sexuals have produced
apomictic or sexual progeny, respectively. Such experiments generally produce
inconsistant results. Indeed, sexual progeny obtained from crossing one facultative
apomict with another are not uncommon (Asker & Jerling, 1992). These findings
argue that other forms of genetic control may be at play. The duplicate-gene
asynchrony hypothesis predicts such ambiguities, i.e. the causal balance between
precocious and delayed developmental signals may be easily upset upon adding,
removing, or unequally-reinforcing genome-specific signals.
If apomixis is simply inherited, it could probably be induced in sexual crops
J. G. CARMAN
76
through mutation or readily transferred by breeding and genetic engineering.
However, if apomixis results from competition between duplicate genes, induction
by mutation may be impossible and transfer by breeding or genetic engineering
extremely complicated. If regulatory genes of one genome can control subordinate
genes of a companion genome, apomixis might be transferred by transferring one
or a few regulatory genes. However, this seems unlikely because apomixis appears to
result from competition between genetically-balanced genomes, i.e. nearly complete
cassettes of genes.
The transfer of apomixis to sexual crops will be further complicated if polyploidy
(multiple copies of asynchronously-expressed genes) is required. Nogler (1 984b, 1995)
crossed sexual Ranunculus cassubicfolius (2n = 2%= 16) with aposporous R. megacarpus
(2n = 4x= 32) and obtained aposporous triploids (2n = 3%= 24). One triploid (CM,)
was only infrequently parthenogenetic, which suggests precociously-expressed sets
of asynchronous signals were strong enough to induce embryo sac formation (from
nucellar cells) but too weak to induce embryogenesis (parthenogenesis). CM, was
backcrossed to the sexual diploid and many BC, diploids (272 = 16) were produced.
All were sexual. However, an aposporous and infrequently parthenogenetic BC,
trisomic (2n = 17) was produced. The trisomic chromosome may have encoded
signals that delayed MMC formation (allowing for apospory) and overly-delayed
embryo initiation such that parthenogenesis occurred infrequently. The trisomic
plant was backcrossed again to the sexual diploid. Interestingly, the BC2BIIIhybrids
(2n = 25) were aposporous and the frequency of parthenogenesis more than doubled.
The genome of the recurrent parent (sexual diploid) may have provided additional
copies of genes that more adequately reinforced the encoding of temporally-advanced
embryogenesis-inducing signals.
Many questions remain unanswered concerning subtle interactions that cause
anomalies, e.g. we know little concerning how signals of one genome supplant those
of another, or how somatic tissues gradually gain competence for embryogenesis or
embryo sac formation. We plan to hybridize molecular probes specific for meiosis,
embryo sac development, and embryogenesis to sectioned ovules of apomictic and
tetrasporic species. Detection of mRNAs specific to meiosis and embryo sac formation
in young MMCs would largely prove the duplicate-gene asynchrony hypothesis,
especially if the asynchronous signals are traced to separate genomes. Knowledge
gained from these and other molecular and developmental studies of female
development may be required to create efficient systems of transferring apomixis to
sexual crops.
'
ACKNOWLEDGEMENTS
I thank the stafF of the Intermountain Herbarium, Logan, Utah, for providing
taxonomic references, Landon Farmer, Becky Kowallis, Chester Ogborn, and
Gordon Reese for assistance in gathering data, Richard Cutler for assistance with
statistical analyses, and Christopher Campbell, Daniel Grimanelli, Kurt Gutknecht,
Wayne Hanna, and Frank Messina for reviewing earlier versions of the manuscript
and providing valuable suggestions. This study was supported in part by USDAARS Specific Cooperative Agreement No. 58-5428-1-130, the Center for Valueadded Seed Technology (Utah State University and the State of Utah), and by the
EVOLUI'ION OF APOMIXIS AND REIATED ANOMALIES
77
Utah Agricultural Experiment Station, Logan, UT 843224845 (approved as journal
paper no. 4884).
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EVOLUTION OF AF'OMIXIS AND RELATED ANOMALIES
81
APPENDIX
Angiospermous genera containing apomictic (AM)species (apospory (A) or diplospory (D)),polysporic
(PS) species (bispory (B) or tetraspory (T)),and polyembryonic (PE) species (nucellar embryony (N),
integumentary embryony (I), apogamety (AG), adventitious embryony (AE, nucellar or integumentary
embryony)). Chromosome base numbers (x) of genera are also listed.
I axonomic unit'
r l
Liliidae
Nismatanae
Alismatales
Nismataceae
Alisma
Damasonium
Echinodom
hmnophyton
Marhaemcarpus
Sngiliaria
Aponogetonaceae
Aponogelon
Hydrocharitareae
Ntchamandra
Limnorharitacear
Butomopsb
Hydmclqs
Iamnocha&
Najadales
Junraginareae
Tilochin
Najadareae
NhjanJ.
Zaniiirhelliarear
Zannichellia
Arecanae
Arerales
Arecareae
Borassus
Hyphme
coc0.c
Aranar
Araks
Araceae
Aglaonema
Spathiphyllum
Lemnareae
Lemna
Wo@a
Bromelianae
Bromeliales
Bromeliaceae
i'illandsia
Commelinanae
Commelinalrs
Commelinaceae
Qmmlina
Traahcantia (Rhoeo)
Erioraulareae
Eriocaulon
Xyridacear
Xyrk
AM
PS
PE
X
7,12, I3
7
11
I1,12
PE
9,ll
PE
8.13
PE
8
B
B
7,8
B
10,13
PE
PE
6
PE
18
18
16
N
7,20
15
B
B
B
10,18,21
10
B
B
PE
18-20,22,25
8,9,11-15,23
6,7,I1,20,25
PE
B
12.16
9,13,17
conld
J. G . CARMAN
82
Taxonomic unit'
Cyperales
Cyperaceae
Carex
Poales
FlageUariaceae
Flagellaria
Poaceae
Anthephora
Anthoxanihum ( H h c h h )
Bothriochloa
Boutelma
Brachiaria
B7WUU
Buchloc
Calamapstis
Capill$edium
Cmhm
Chlmis
Cmtodnia
Duhthium
Echinochloa
EhUS
Eragmsh
Eremopogon
Eriochloa
EUStaChyS
Fingerhuthia
Harpochlod
Hetmpogon
Hypanhenia
Lamprthyrd
Nanius
%ra'
Panicum
Paspalum
Pmnisetum
Poa
Rendlia?
Sacchamm5
Schkachyriurn
.!&cab
setaria
Solghum
numeah
Trichoha
Tnpsacum
Umchlon
Lilianae
Asparagales
Agavaceae
Aha
Alliaceae
Allaum
AM
PE
PE
B
A
A
A
A
A
N
N
A
A
A
A
D
D
A
A
A
A
A
A
A
A
D
AE,AG
A
N
A,D
A
D
N,AG
PE
A
A,D
A
A
D
A
N
T
Tulbaghia
9
5,7
10
10
7-9
7
10
7
10
9
10
12
10
9
7
10
10
9
10
10
10
10
12
13
12
9,lO
6,lO
7-9
7
10
10
A
Nothosconium
5,6,8,11,13,14,17,19,23
10
A
A,D
D
X
19
N
A
D
A
A
Lnrcocolyw
Amaryllidaceae
Calos&mma
CliIlWn
Habranthur
PS
B
B
B
B
7
9
5
10
18
18
12
30
I,AG
7-9,l 1
I
4,5
6
AE
PE
D
10,ll
6,7
contd
EVOLUTION OF AF'OMIXIS
Taxonomic unit'
Pancratium
/Sphyranthes (Cooperk)
Convallariaceae
Convallaria
Maianhum
Medeola
Po!vgonatum
Streptopus
Funkiaceae
Funkia (Hosta)
Hemerocallidaceae
Hememcallis
Hyacinthaceae
Gmacsia
Hymnthoides
Omithogalum
Scilla
Hypoxidaceae
Hypoxis
Ruscaceae
Ruscus
Tecophilaeaceae
Cyanella
Burmanniales
Burmanniaceae
Bumannia
Diosroreales
Dioscoreareae
hoscorea
Smilacaceae
Smilacina
Taccaceae
Tmca (Schizocapsa)
Trichopodaceae
Trichopus
Trilliaceae
Paris
Trillium
Liliales
Colchiraceae
Colchicum
Iphigenia
Ldiaceae
&aphis
Cardiocrinum
Evthmnium
Fritillaria
Cqea
Lilium
Tulipa (Amana)
Uvulariaceae
Clintonia
Tirhi
Melanthiales
Melanthiaceae
Vmatmm
Orchidales
Cypripediaceae
CyPripedium
AM
AND RELATED ANOMALIES
PS
PE
83
X
B
I1
6,lO
B
T
T
19
6
7
8-15,19
8,12,13
D
B,T
B
N
N
T
B
N
A
I1,18
15
8
3-5,7,11,13,17,19,23
6-1 1,13,17,19
B
7
B
20
N
D
B
PE
6-8
PE
7,8,10,11,18
N
14,18
14,18
A
PE
B
B
AE
N
N
PE
T
T
T
T
T
T
PE
B,T
N
N
5
5
6,7,9,19,22,23
I1,13
I1,12
10,12
7,9, I 1,12
9,12
12
12
T
T
12,14
12.13
B
8
B
10
J. G. CARMAN
84
Taxonomic unit'
Orchidaceae
Bhtia
Bhhlla
Calanthe
Cephahf/Ura
Cymbidium
Cymhis
Cynosorchis
Epidendrum
Epipaccis
Eria (Forbesina)
Eulophia
Gadmdia
@nnaahia
Lislera
M a h (Acmanthes)
Neottia
Ni'&lla
W i u m
Orchic
Oreonhic
Paphwpedilum
Phalamopsrr
Spiranthes
&.rim
i&opetalum
AM
Ps
T
T
B
B,T
T
B
PE
PE
PE
AE
PE
N
N
N
AE
PE
N
N
AE
N
AE
PE
I
N
1,AG
AM
A
Pandananae
Pandanales
Pandanaceae
Pandanw
Triuridanae
Triuridales
Triuridaceae
Triurir
Zingiberanae
Zingiberales
Costaceae
16
16,19
14, I9-24,26
16-19,22
19-22,26
19,20,31
17-20,30
12, 17-20,23
17,19,21,22,24,27,28,30
11,15,18,20
15,18,20,21
17-23,28
15,18,21
18,20,21,23
16,20
13-15,18-22
10,16,18-2 I
2 1,24
12-2 I ,29,3 1
19
15,22
10
20
cosh*r
Zingiberaceae
Hedychium
Magnolidae
Apianae
Apiales
Apiaceae
Ammi
Azorella
Bowhsia
Bupleunim
h a
Heha
Pimpinella
Po~s&
Tractyspmum
Pittosporales
Pittosporaceae
Bursaria
Pittospomm
Asteranae
Asterales
Asteraceae
X
9
PE
17
I
10-1 1
8
T
T
B
T
B
6-1 I
PE
12
8-1 1
PE
9,lO
PE
PE
12
B
contd
EVOLUTION OF APOMIXIS AND RELATED ANOMALIES
Taxonomic unit'
Ammobium
Ana&us
AndTala
Antmnaria
Anthemir
Amica
Artemisia
Aster
Bellis
Biden,
Blumea
Bractyscome
Calotis
Carthamus
Cmtaurea
Chondrilla
Chysanllremum
Cichorium
Coreopsis
Crepis
ETigmn
Eupatorium
Euybiopsis (Minuria)
Gaillardia
Gerbera
Grindelk
Gutierrezia
Haplopappus
Helianthus
Helichtysum
Hieracium
AM
PS
PE
PE
PE
I
PE
PE
PE
I
IX&
Leontodon
Leontopodium
Leucanthemum
Matricaria
Melampodium
AE,AG
85
X
9
9
14
9
19
8-1 1
4,5,7-10
9
10,12
8-1 1
4,599
4,5,7,8
10,12
8-12
5
9,15
8,9
10,12- 14
3-5,7
9
10,17
9
10,17
12
6
4
z4-6
17
7,12
9
7,8
4-7
7,12
9
9
s12
O&
Parthium
Acris
Ratibida
Rudbeckia
Sanvitalia
Solidngo
lanacetum (Balramita)
Taraxacum
Tiridax
Vmonia
Campanulales
Campanulaceae
Jasione
Wahhbergia
Lobeliaceae
Laurentia (Isotoma)
Labelia
Balanophoranae
Balanophorales
Balanophoraceae
Balanophora
PE
PE
17,18
5
14
9
8
9
9
8
9
9-1 2,17
PE
PE
6
9
PE
PE
7
6,7
PE
J. G. CARMAN
86
Taxonomic unit'
Ditepalanthus
Helosis
Caryophyllanae
Cqophyllales
Aizoaceae
Aptmia
Delospmna
Mesemb~anthrmum
Tithema
Amaranthaceae
A m
Celosia
Comphm
Cactaceae
hcantha
Mammillaria
Opuntia
Pereskia
Rqfinesquii
Caryophyllaceae
Pobcarpon
C henopodiaceae
Be&
AM
PS
PE
B
B
PE
Suocda
Nyctaginaceae
Bonhavia
Mirabdis
Portulacaceae
Portuha
Cornanae
Caprifoliales
Caprifoliaceae
Cephalaria
Lonuera
Scabwsa
9
9
9
AE
N
N
N
AE
9,ll
11
11
PE
7-9
N,AG
PE
9
9
PE
12,13
20,29,33
PE
8-10
PE
5,7,9
9,11
7-9
7-9,11
N
T
A
COl?lUr
Ganyaceae
Ganya
Menyanthaceae
N+mphoi&s ( L i m n a n h u m )
Symplocaceae
Symplocos
Ericanae
Ericales
Actinidiaceae
Actinidia
Cyrillaceae
Cltfbnia
Empetraceae
Empetrum
Ericaceae
PE
PE
B
VoleIiaM
Cornales
Adoxaceae
Adoxa
Sambucus
Kbumum
Aucubaceae
Aucuba
Cornaceae
PE
9
9
9
8,13,14
D
B
T
T
B,T
X
PE
PE
18
18
8.9
B
8
T
9-1 1
PE
11
PE
9
N
11
PE
29
PE
13
A
conhi
EVOLUTION OF APOMDaS AND RELATED ANOMALIES
Taxonomic unit'
Carsiope
F'yrolaceae
plerospora
Gentiananae
Gentianales
Apocynaceae
gnanchum
Kopsi
Plum'a
Kncetoxicum
Gentianaceae
Swmtia
Rubiaceae
Coffea
Crucianelh
Rubia
Scyphhiphora
Oleales
Oleaceae
Frm'nrcr
Jminum
OIea
Lamianae
Lamiales
Acanthaceae
Acanthus
Andmgraphis (Haphnthus)
Bar&
Ruellia
Stmbilantlles (hicocabx)
Globulariaceae
Globularia
Lttntibulariaceae
utriculotia
Plantaginaceae
Plantago
Scrophulariaceae
AIectra
Anticharis
Linatia
Mehmpyrum
Scmphuhtia
Verbenaceae
Avicmnia
Nyctanthes
Magnolianae
Aristolochiales
Aristolochiaceae
Arirtalochia
Illiciales
Schisandraceae
Schisandra
Laurales
Calycanthaceae
Cabcanthus
Chimonanthw
Moniminceae
Peumus
Rafflesiales
Hydnoraceae
AM
PS
PE
87
X
B
13
B
24
I
PE
PE
PE
11
9
9
11
PE
7,8,10,13
PE
I1
11
11
PE
PE
23
13
23
PE
PE
PE
PE
PE
20,22,28
T
T
B
B
15,24,25
20,22
16,17,22
10
8
A
PE
PE
18,20,22
4-7
PE
6-8
9
12-1 5,2&23,29,34
18,24
18.22
PE
4-7.13
B
I
I
B
13
contd
J. G . CARMAN
88
Taxonomic unit'
Hydnora
Pmsopanche
Nymphaeanae
Nymphaeales
Nymphaeaceae
Euryale
JYPPhO
Piperales
Piperaceae
Heekeria
Pepmmia
Pipm
Saururaceae
Anttll0pSi.S
Houttynia
Malvanae
Euphorbiales
Euphorbiaceae
Acabpha
Alchomea (Coelebogu
ChmZophora
Euphorbia
Mallow
Malvales
Bombacaceae
Bombac0pSi.S
Bombax
Pachira
Dipterocarpaceac
Diphcarpus
Shorea
Hopea
Malvaceae
Gosvpium
Sterculiaceae
77uobma
Tiliaceae
Cmhonrs
Rhamnales
Rhamnaceae
Pomadmir
&z$hus
Thymelaeales
Thymelaeaceae
Daphne
Whhormia
Urticales
Uhaceae
Ulmus
Urticaceae
Boehmnia
DMJtmia
Elahstma
AM
PS
T
B
X
8
PE
PE
T
T
T
29
14
1&13,19
13,18,2&22,24,30,32
B
11
11.12
D
10
N
9
N
N
11
5-9, I 1,13,15,17,19
11
N
N
N
46
46,48
44
N
N
N
B
PE
13
PE
10
PE
7
PE
12
12
AE
T
N,AG
9
699
PE
14
N
N
AE
N
10,14
12
7-10,13
13
14
12.14
D
D
A,D
FUUS
Moms
Stnblus
Myrtanae
Myrtales
Alzateaceae
Alzaba
PE
B
contd
EVOLUTION OF APOMIXIS AND RELATED ANOMALIES
Taxonomic unit'
Combretaceae
Conibrptum (Poima)
Getonia (Ca4ropk-i;)
Guiera
Lumnitzera
Tminalia
Heteropixidaceae
Heternpyxit
Melastomareae
Melaxtoma
Osbeckia
Sonerila
Myrtaceae
Callistemon
Eugenia (&gum)
Onagareae
Camirsonia (Taraxia)
Clarkia
Cnidoscolus uussima)
Epilobium (xauchnma)
Oenothera
Penaeareae
Brachysphon
Penma
Saltera (Sarcocolla)
Plumbaginanae
Plumbaginales
Limoniaceae
Limonium
Plumbaginaceae
Armeria
Ceratoshgma
Plumbagella
Plumbago
Mgelia
Polygonanae
Polygonales
Polygonaceae
Atraphank
Prirnulanae
Ebenales
Ebenaceae
DioJpymJ
Primulales
Myrsinaceae
Ardisia
Primulaceae
Airnula
Ranunculanae
Papaverales
Papaveraceae
Atgnnone
Dicentra
Ranunrulales
Berberidacear
Berberii
Caulophyllum
Ranunculareae
Aconitum
Adonis
AM
89
PS
PE
X
T
N
PE
PE
PE
PE
13
PE
AE
PE
8
9,10, I2
9,11,17
N
1.N
11
11
PE
N
7.9
12
B
A
AE
N
N
T
T
T
18
7
10
10
D
6-9,17
8.9
N
A
PE
15
N
23
PE
8-13
PE
PE
14
8
PE
14
T
8
PE
B,T
8-10, I3
8
contd
90
J. G . CARMAN
Taxonomic unit'
Anemone
Cerhcephdn
CIemarir
De4hinium
Ngelhl
Ranwlus
ntalictnrm
Rosanae
Buxales
Buxaceae
Sanococca
Casuarinales
Casuarinaceae
CasUarina
Droserales
Droseraceae
Dmsophyllum
Fagales
Betulaceae
AlnW
&tuhl
Ah4
PS
PE
B,T
B
T
5,7,8
7
PE
PE
A
N
12,14
PE
9,lO
NAG
N,AG
N,AG
14
14
11,14
PE
8
PE
12
B
D
hChhi4l
Corylaceae
Carpinw
Fagaceae
Q....(
Gunnerales
Gunneraceae
Gunwa
17
Hamamelidales
Myrothamnaceae
MyOthilm7IU
Juglandales
Juglandaceae
10
3uglmrr
Rosales
Rosaceae
Alchemilh
Amclunchin
CotnnuCFtcr
@
awrc
A
A
A
A,D
Geum
16
N,AG
PE
16
17
PE
N
N,AG
N,AG
p4m
Grossulariaceae
Ribcs
PE
17
Malw
Phoriniu
Pountdhl
Rubus
Sanguisorba
Sibbabaldia'
sOrbopym8
Sorbur
Saxifragales
Crassulaceae
Adromirchus
Aeonium
EchcvRin
Scdum
8,9,11,13
8,9,10,13
5-7
7,8
.7,8
T
D
X
17
7
17
17
7
17
7
7
PE
7
AE,AG
17
T
T
T
B
18
12,14-20,22-25,27,29
5-24,2638,4&43,45-52,
54,56-58
N
8
contd
EVOLUTION OF APOMIXIS AND RELATED ANOMALIES
Taxonomic unit'
Podosternaceae
Sphaemrhyh (Anmtmphea)
Apinagia (Omone)
CladoplIJ
Dalzellia (Lawia, Tmiola)
Dicraeia
Fameria
GRllh
Hydmhyum (Hydmhyopsis,
{qhnidium)
Indotristicha
Inversodicrnea
Lophogyne
Mourera
Oserya
Podostemum
PoIypleurum
Rhyncholacis
Tristicha
Mllisia
Saxifragaceae
BtTgE?lia
Penthorum
Rodgersia
Smtaga
Xllima
%lmka
Rutanae
Balsaminales
Balsaminaceae
Hydmcera
Impatimc
Celastrales
Celastraceae
Celashus
Euonymus
Fabales
Fabaceae
Bauhinia
AM
PS
B
B
B
B
B
B
B
B
10
PE
PE
B
B
B
B
X
10
B
B
B
B
B
B
B
B
B
B
PE
B
B
Cmsia
Cmkzlaria
Laburnum
Millctria
Pongamia
Tnilium
Geraniales
Peganaceae
Peganum
Zygophyllaceae
,?ogophyllum
Linales
Linaceae
Linum
Oxalidaceae
Biophytum
Oxalis
Polygalales
Malpighiaceae
Aspicarpa
Banirteriopsis
PE
91
17
15
5-1 7,19,20,23,25,31
7
7
8
3-10,12-18,20
I
I
23
8
PE
N,AG
PE
PE
I 2-1 4,16
7,8,12,13
73
7
8,11,12
10,ll
5-8
PE
11,12
N
8,11,14
PE
7-10,13,15,17
B
N
B
B
B
9,lO
5-8, I 1
N
N
10
contd
J. G . CARMAN
92
'raxonomic unit'
Bunchosia
Galphimia ('Thyallis)
HeWW
Hiprcrgc
Malpighia
Srignaphylhn
Polygalaceae
Pobgala
Rutales
Buneraceae
Cmmiphorag
Ganrgn
Meliaceae
Aphanamixis
Azadirachh
Lanrium
Melia
Rutaceae
A&
Cihus
Fmniella
AM
PS
PE
T
B
A
B,T
T
N
N
N
N
N
T
N
N
N
PE
N
PE
13
14,18
14
14
9
9,lO
9
9,lO
9
9
7
8,9
15
AM
Fdunc[ln
&lia
Ruh
A
AM
AM
Lannea
MlVgttfla
Santalanae
Santalales
Loranthaceae
Dendmphthoe
Olacaceae
O h
Santalaceae
Bucklqw
Exocarpos
Iodina
Mida
@inchdium
Sunkalum
Vicaceae
Aneuthobium
cinalloa
KorthaheNa
Vucum
Solananae
Boraginales
Boraginaceae
Anchusa (Lycopsir)
Cali0
9,lO
10
10
8,9,11-14,17,19
Munaya
Poncim
skimmia
T l k
<antho.ylum
Simaroubaceae
Bnuea
Sapindales
Sapindaceae
Acer
Anacardiaceae
6
10
N
N
9
PE
12
PE
13
PE
N
15
20
9
12
B
B
B
B
A
B
B
PE
10
PE
PE
PE
10
PE
698
8,9,14,15
conid
EVOLUTION OF APOMIXIS AND RELATED ANOMALIES
Taxonomic unit'
Cortesia
Cynoglossum
Trichodesma
Ehretareae
Ehrztia
Solanales
Convolvulaceae
Conuoluulrcr
Cuscutareae
Cuscuta
Solanaceae
Capsicum
Cestrum
Datura
Lycoperhon
Ncotiana
Petunia
Scopolia
Solanurn
Mthania
Theanae
Paeoniales
Paeoniareae
Paeonia
Theales
Hypericaceae
Clusia
Garcinia
Hypericum
Ochnaceae
Ochna
Stachyuraceae
Slnchyum
Theaceae
Camellia (%a)
Violanae
Brassicales
Brassicaceae
Arabis
Raphanobrrusica"'
Capparir
Cucurbitales
Cucurbitaceae
Benincrua
Cucumirl'
Hoksonia
hffi
Marah
Momordica
Siyos
Datiscaceae
Datkca
Salicales
Salirareae
Populrcr
Salix
Tamaricales
Tamaricaceae
Myricaria
Ta77Uri.7
AM
PS
A
B
B
PE
X
AE
12
11,12
B
8,9
PE
9-15
PE
7-9
PE
N
11-13
8,11
12
12
7-12
7-9
7,12
8,12
12
N.AG
5
N
PE
N
I
AE,AG
D
A
B
1)
93
N
N
8
PE
7-10
1,AG
12,14
PE
11.12
PE
15
PE
4,697
I
10-12.2 1
A
B
N
N
12
7,12
9
9,12,13
15
7,8,11
12
PE
N
14,18-20,22-24
9,17,19-2 I
PE
PE
12
12
A,D
AE
PE
D
A
D
PE
B
T
T
contd
J. G. CAFWAN
94
Taxonomic unit'
AM
PS
PE
X
~
Tropaeolales
Limnanthaceae
Floerlua
Limnanthes
Tropaeolaceae
liimlum
Violales
Caricaceae
Caka
T
T
5
N
T
12-14
9
'Unless otherwise indicated, references to the definitive studies may be found in the reports of Asker & Jerling
(1992), Davis (1966), Hjelmqvist (1964),Johri et al. (1992), Maheshwari (1947, 1950), Maheshwari (1955),Nygren
(1967), and Naumova (1993). 'Strydom & Spies (1994). 'Conner & Dawson (1993). 'Zhi-Ping, Rui-Juan & XiHua (1990). 'Kellogg (1990). 6Campbell, Greene & Dickinson (1991). 'Czapik (1990). 'Jankun (1993). 'Gupta,
Shivanna, & Mohan Ram (1996) (added in proof, not used in statistical analyses), EUerstrom & Zagorcheva
(1977). " Zagorcheva (1989).