PLANT EVOLUTION IN MAN-MADE HABITATS
Proc. Vlti'Symp. lOPE, Amsterdam 1998. L. W,D. van Raamsdonk & J.C.M dell Nijs. editors
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Species concepts in agamic complexes
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Timothy A. Dickinson
Vascular Plant Herbarium (TRT), Center/or Biodiversity & Conservation Biology
Royal Ontario Museum, 100 Queen's Park, Toronto Canada M5S 2C6
Botany Department, University o/Toronto, 25 Willcocks Street, Toronto, Canada M5S 3B2
tel: (416) 586 8032,jax: 5865527, e-mail: [email protected]
Abstract
\
\
A range of species concepts is available for use with the components of agamic complexes in plants. The
apparent tension between pattern- and process-based species concepts is probably less important than
consideration of (1) the relative frequencies of asexual and sexual reproduction; (2) the consequences of
life history features (e.g., growth habit, pollination, seed dispersal, seedling establishment, etc.), and (3)
the hierarchical level at which species concepts are applied. Support for these assertions will be drawn
from experience with members of Rosaceae subfamily Maloideae, as well as from the literature on agamic
complexes in the Asteraceae and Poaceae.
Keywords: Species concepts, agamic complexes, apomixis, taxonomy, conservation
Introduction
Species are fundamental to systematics since, of all the taxonomic categories, these can
be the one that is most readily and unequivocally observable in nature, categories at
higher or lower levels usually being much more obviously intellectual constructs (ef
Rieseberg & Brouillet, 1994). MayI' (1992) describes an example of the commonplace
experience that in a particular locality, "...virtually all species of flowering plants...
[seem] to be remarkably well defined and sharply set off from other sympatric
species." Equally commonplace is the experience that where instead it is the family or
genus that is most readily recognised, it may be because species identificallion depends
© Hugo de )fries Laboratory, Amsterdam, 1999. ISBN 90-804431~6-6
(~
319
Dickinson
on characters not readily observed with the naked eye (e.g., sedges, grasses), or because the taxonomy of the 'group in question is complicated by apomixis (e.g., brambles, dandelions, hawthorns). To understand why species can be so readily recognised
in so many cases, but not in others, requires careful thought about species concepts,
and hence about what it is that species 'do', what it is that species 'are', and what it is
they 'are not'. The earliest principles underlying definitions of species are (1) the constant morphological distinctness of the entities recognised as species, and (2) the realisation that this distinctness was the result of common descent. Implicit in the incorporation of these principles into taxonomic thinking was the assumption that, by analogy
with more familiar humans and other vertebrates, descent is fundamentally biparental.
Thinking about what it is that species of angiosperms with uniparental reproduction
'are' has progressed considerably since Gustafsson's (1947) comprehensive review of
apomixis, partly as a result of technical advances in the collection of data on genetic
variation and partly as a result of methodological advances in how data are to be transformed into classifications. The impact of the latter was reviewed in the symposium,
'Species and evolution in clonal organisms' (Budd & Mishler, 1990; Mishler & Budd,
1990). The overview of species concepts provided by Mishler & Budd (1990) was subsequently incorporated, with further discussion, into the chapter on taxonomic considerations in Asker and Jerling's 1992 review of apomixis (Asker & Jerling, 1992). However, it is only since these two reviews that most of the data on genetic variation in
apomicts have become available. Likewise, thinking about the implications of these
data for species concepts has also progressed, to the point that conceptual divides that
earlier appeared to be unbridgeable now seem to reflect merely alternative aspects of
the same underlying phenomenon. Accordingly it seems worthwhile to look once more
at the species concepts and the data available with which to employ them, in order to
see if any new recommendations can be made for the taxonomy of groups where
apomixis occurs.
Species Concepts
The first of the principles enumerated above corresponds to what has come to be
known as the morphological, typological (Mayr, 1957), or taxonomic (Davis & Heywood, 1965) species concept. As the synonyms suggest, taxonomic species are distinguished by correlated discontinuities in morphological variation understood in a variety of ways (Davis & Heywood, 1965; Gornall, 1997). This species concept can be
seen to underlie the way in which Linnaeus recognised species, i.e., by means of constant morphological differences (Linnaeus, 1737, quoted by Steai'n, 1957). More recently this species concept has formed the basis for the phenetic concept, in which
320
Species concepts in agamic complexes
Table 1. A classification ojspecies concepts (sc's), based on comments in Mishler (1990),
Davis (1995), and Maddison (1997), but emphasising different criteria. 'Pattern' sc's
emphasise the relative distribution oj variation or oj synapomorphies within and between
groups recognised as species. 'Process' sc's emphasise phenomena seen as explanations
(or observed patterns oj variation. The distinction between 'Non-historical' and 'Historical'
relates to thee extent to which species are recognised on the basis ojpotential or achieved
divergence.
Pattern
Process
Non-historical
Taxonomic sc
Davis & Heywood, 1965
Phenetic sc
Sakal & ClVvello,1970
Sneath & Sakal, 1973
Biological sc
MayI', 1957
MayI', 1970
Ghiselin, 1997
Cohesion sc
Templeton, 1989
Recognition sc
Paterson, 1985
Historical
Phylogenetic sc
Cracraft, 1989
Nixon & Wheeler, 1990
Evolutionary sc
Simpson, 1961
Ecological sc
Van Valen, 1976
Monophyletic sc
Mishler & Donoghue, 1982
Genealogical sc
Bawll & Donoghue, 1995
Baum & Shaw, 1995
..\:kL...
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quantitative, similarity-based methods are used to evaluate morphologirarol'~ther cor- ~ to-l.:" related discontinuities (Sokal & Crovello, 1970; Sneath & Sokal, 1973) between popu- ~~~',<­
lations or groups of populations (Davis & Heywood, 1965), Arguably (see below), ;"s~d.M~
many of the taxonomic problems associated with groups in which apomixis occurs can w.~. t. sc ,
be attributed to uncritical applications of a m?rphologically-based species concept to
these groups, More careful usage has adapted the taxonomic concept to use with apomicts, Gustafsson (1947, p. 269) writing of his preference for "the harmless expression
microspecies"." and noting that these "".are no species in the sexual implication of the
word."
The second underlying principle, that of genealogical relatedness, also goes back to
the eighteenth century and John Ray's observation that "plants which differ as species
preserve their species for all time, the members of each species having al1 descended
from seed of the same original plant" (Ray, 1704, quoted by Stearn, 1957, pp. 156157), In modern times, as Davis & Heywood (1965) suggest, this inferred biological
321
Dickinson
relationship between members of a species was seen as an explanation for the success
of the taxonomic species concept (implicitly, Stebbins, 1993). The fact that many species recognised morphologically proved to represent groups of interbreeding individuals thus led, in an attempt to base species on their more fundamental properties, to
various formulations of what has come to be known as the biological species concept
(Mayr, 1957). Thus, according to Mayr (1970, p. 12) species "... are groups of interbreeding natural populations that are reproductively isolated from other such groups."
As indicated above, Gustafsson (1947) employed the biological concept and clearly
distinguished apomictic microspecies as being outside its application. Turesson also
distinguished the species concepts applicable to apomicts and amphimicts as agamospecies and coenospecies respectively, the latter corresponding to the biological species concept (Turesson, cited in Asker & Jerling, 1992). Although his cladistic methodology is vital to some of the historical SCs described below (Table I), Willi Hennig
also espoused a biological concept (Ghiselin, 1997; Mayden, 1997) and distinguished
between the reticulate relationships that exist within species from the hierarchical ones
among species (Davis & Nixon, 1992).
Other formulations emphasise the positive processes by which conspecific organisms share a common fertilisation system, rather than the negative process of isolation, as in Paterson's recognition species concept (the " ...most inclusive population of
individual biparental organisms which share a common fertilisation system." Paterson,
1985, p. 25). Another concept that emphasises the processes by which members of a
species remain related is Templeton's cohesion species concept (Templeton, 1989).
This concept defines species as "...the most inclusive population of individuals having
the potential for phenotypic cohesion through intrinsic cohesion mechanisms..." such
as (I) those that promote gene flow within, or constrain gene flow between, species,
and (2) those that contribute to defining the species' fundamental niche (Templeton,
1989, p. 12). Note the use of the word 'population' in the preceding definitions, and in
the following one. Ghiselin (1997, p. 99) has restated the definition of the biological
species concept in the context of his thesis that species are individuals rather than classes as "...populations within which there is, but between which there is not, sufficient
cohesive capacity to preclude indefinite divergence." Reference to populations is important, as it requires the multiplicity of the individual organisms (genotypes) making
up a species.
.
The biological species concept has been severely criticised for its inapplicability to
situations in which well-defined morphological species are present even though one or
the other criterion of the biological species concept may not be met (Mishler & Donoghue, 1982). In particular, it has been suggested that if a biological species concept
is used then apomicts cannot be species if within-species gene flow does not occur
&
(Gustafsson, 1947; Van Valen, 1976). Emphasis, instead, on relationships that are
322
Species concepts in agamic complexes
primarily historical and due to common descent rather than contemporary, reproductive, and hence non-historical has led to definitions of groups, at all taxonomic
levels, on the basis of inferred evolutionary history (Table 1). Depending on the nature
of the inference, these concepts may be seen as emphasising either the pattern of variation from which evolutionary history is inferred, or the processes or special properties
by which individuals within a species are related to one another (Table 1).
The evolutionary species concept was put forward by Simpson (1961, p. 153) so as
to define an evolutionary species as "...a lineage (an ancestor-descendent sequence of
populations) evolving separately from others and with its own unitary evolutionary
role and tendencies." Using the same definition of lineage (expanded to include clones
as well as ancestor-descendent sequences of populations), this definition was recast by
Van Valen (1976, p. 233) as the ecological species concept, to argue that a species is
"...a lineage (or a closely related set of lineages) which occupies an adaptive zone
minimally different from that of any other lineage in its range and which evolves separately from all lineages outside its range."
Alternatively, historical species concepts may emphasise the imputed special properties of species, such as monophyly (Mishler & Donoghue, 1982 and other references given in Mishler & Budd (1990) or exclusivity (Baum, 1992; Baum & Donoghue,
1995; Baum & Shaw, 1995). Motivation for the monophyletic species concept and the
genealogical species concept seems to have come from the ease with which conflicts
between species trees and trees based on single characters can be modeled (Baum &
Donoghue, 1995) and the desire for a criterion against which to evaluate taxonomic
hypotheses (Baum & Shaw, 1995).
1n contrast to the foregoing concepts are the historical species concepts that emphasise the diagnosis of irreducible clusters of organisms on the basis of at least one
character-state that is shared by members of the cluster and absent from other, closely
related organisms (Cracraft, 1989; Nixon & Wheeler, 1990). The phylogenetic concept
emphasises operability, especially in situations in which it appears that concepts like
the biological species concept break down (Cracraft, 1989). Although these concepts
have been attacked as sacrificing historicity for operability (Baum & Donoghue, 1995),
they are clearly based in methods for inferring evolutionary histories (Davis & Nixon,
1992; Davis, 1997).
.
With the increasing availability of methods for collecting molecular data with
which to infer gene trees, non-equivalence of individual gene trees and species trees
(Doyle, 1992; Doyle, 1995) and of trees inferred from different genes (Maddison,
1997) has become critical. These conflicts are due to "...the fact that species lineages
are not simple, indivisible lines but rather that each has a fine structure consisting of
many [sexually reproducing] organisms and their genes" (Maddison, 1997, p. 532).
Nevertheless, Maddison suggests that there may be complementary 'Views of phylo323
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Dickinson
genies (as realised genetic histories, and as reflections of potentials for interbreeding)
that parallel the complementarity of the biological species concept and the historical
species concepts.
In summary, the biological species concept describes what species are, to the best
of our knowledge, in terms of the biological process they manifest with whatever frequency. This process, sexual reproduction, interacts through natural selection with
historical contingency to produce a realised history of ancestor-descendant relationships. This interaction likewise results in the extent to which lineages can be distinguished by whatever means, phenetic or cladistic. Phenetic and diagnostic species
concepts may use alternative data types and analytical methods to operationally recognise what is a species (Luckow, 1995); biological and genealogical species concepts
emphasise how those units got to be what they are (Table 1).
Species concepts and agamic complexes
As noted briefly above, species concepts vary in the extent to which they apply to
organisms in which (biparental) sexual reproduction is infrequent or absent ("Too little
sex," Templeton, 1989, p. 8). As described below, the taxonomic species concept has
been applied to apomicts with success that varies according to the taxonomic philosophy of the person making the assessment. Alternatively, the biological concept can
be interpreted as not applying to asexually reproducing organisms (Van Valen, 1976).
Related concepts, however, have been formulated so as to apply equally to these cases,
as in the cohesion species concept (Templeton, 1989). Mishler & Budd (1990) point
out that species as breeding groups that are held together by gene flow is implicit in the
evolutionary and ecological species concepts. On the other hand, the emphasis with
historical species concepts on either diagnosis or monophyly is apparently no bar to
applying them in agamic complexes. How then should taxonomists and others dealing
with apomicts choose a species concept? Before discussing my answer to this question,
I would like to review data now available concerning the application of species concepts to some ofthe apomicts considered by Gustafsson (1947).
Poaceae
The genera considered below span a range of variation patterns that appear to be linked
to the ecology of establishment and perennation. At one extreme are the apomictic species complexes in the genus Poa. As Gustafsson (1946) noted about this group, these
very large complexes bear no obvious relationship to diploid species and cannot readily be dissected into microspecies. Results from recent work on the PaN secunda Presl
324
s
Species concepts in agamic complexes
complex (Kellogg, 1990) parallel those of earlier studies of other complexes in the
genus (Gustafsson, 1947; Ishimitsu & Tateoka, 1983), in that detailed morphometric
analyses failed to substantiate the existence of distinct microspecies even in obligately
apomictic lines. Kellogg points out the life history and ecological contrasts between
these agmllospermous grasses and both the Rosaceous genera and the dandelions that
are discussed below. While the grasses considered are all long-lived perennials occupying stable habitats, formation of microspecies in the other genera is associated with
rapid, long distance dispersal into disturbed, often evanescent, habitats. In the case of
the Poa secunda complex, Kellogg concludes that rational application of phenetic,
diagnostic, or biological species concepts leads to the same result, namely that "...the
entire 'agamic complex' must be considered as a species even if it contains some malesterile lines" (Kellogg, 1990, p. 121).
Rosaceae subfamily Rosoideae
In contrast to Poa, the genus Rubus probably provides the quintessential problematic
apomict. Nevertheless, the historical introduction to a modern account of British Rubus
(Newton, 1988) makes no mention of Gustafsson's (1946) review of the genus and his
earlier cytological work, although apomixis, hybridisation, and polyploidy are certainly
mentioned subsequently in the characterisation of the genus. Another recent and more
complete account of the taxonomic treatment of apomicts in Rubus subgenus Rubus
(Weber, 1996, p. 379) suggests that while "...modern methods like DNA fingerprinting
may give some interesting results, ...they cannot substitute for morphological studies."
The results in question (reviewed by Nybom, 1996) suggest that some named biotypes
(microspecies) may be identical and that these and others may be virtually invariant
over great distances. Such results, as well as those obtained by Alice and co-workers
(Campbell, this volume), would seem to call into question reliance exclusively on morphology and distributional area in characterising species (Weber, 1996). Gustafsson's
(1946) application of the circle-species concept to Rubus would seem to be equally
valid, encouraging reciprocal illumination from studies on genera like Crepis (Stebbins, 1950) and Antennaria (Bayer, 1997). Finally, work by Matzke Hajek (1997)
suggests that ecological and historical factors have played a role in Rubus diversification in Europe comparable to that inferred for"North American Crataegus.
Rosaceae subfamily Maloideae
Despite the fact that several other genera in Rosaceae subfamily Maloideae such as
Cotoneaster, Malus, Sorbus, and Crataegus (see below) present substantial taxonomic
problems only Amelanchier has so far received the combination of cytological, morphological, and molecular study needed to begin putting its classification "onto a sound
325
Dickinson
basis, informed by data about both the patterns of variation present and their probable
origin. Early work on the genus employed a taxonomic species concept (e.g., Landry,
1975) and demonstrated the OCCurrence of hybridisation and polyploidy (Cruise, 1964;
Favarger & Stearn, 1983), but data concerning the occurrence of apomixis and patterns
of variation have become available only recently (see Campbell, this symposium, for
review). These studies have demonstrated a lack of differentiation between local population samples in the agamospennous polyploid, A. laevis Wieg. (Campbell et aI.,
1997), hybridisation between an informally named microspecies A. 'erecta' and A.
laevis (Campbell & Wright, 1996; cf Campbell, this volume), and the presence of a
multiplicity of entities (some of them named informally) at a single, heavily disturbed
site (Dibble et al., 1998).
In contrast to Ameianchier, Sorb us has a well-developed infrageneric classification.
This has helped to organise data on the occurrence of apomixis, hybridisation, and
polyploidy (Gustafsson, 1947; Liljefors, 1953; McAllister, 1986; Aldasoro et al.,
1998). Starch gel electrophoresis of peroxidase isozymes contrasted the variability of
sexual diploids with the uniformity of individual microspecies (Proctor et al., 1989;
Proctor & Groenhof, 1992). Aldasoro et al. (1998) rejected use of the biological species concept and recognised 12 taxonomic species in European Sorbus based on morphological comparisons. These included both typically diploid taxa corresponding to
each of five subgenera, and taxa known (or believed) to be hybrids. Many of the microspecies of supposedly hybrid origin that they compared were found to be morphologically indistinguishable.
Crataegus
The genus Crataegus L. illustrates some of the difficulties that taxonomists have
encountered with agamic complexes, especially as they appear to have evolved in manmade habitats. In the century following the 1753 publication of nine species and two
varieties by Linnaeus (Linnaeus, 1753, facsimile 1957) the number of species (not
taking into account in either case taxa later transferred to other genera) increased to 70
(with over 300 entries for synonyms; Steudel, 1840). Brown (1910) noted how, during
the period 1857-1897, numbers of Crataegus species recognised in eastern North
America had hovered around 10 to 20. However, between 1897 and 1903, just in the
southeastern United States, the number of species recognised jumped from 15 to 185.
Summarising the situation as of 1910, Brown observed how about 100 species had
been described from North America prior to 1896, while since 1896 866 species and 18
varieties had been described. Of these new taxa, 843 species and nine varieties were
described by three workers: C.D. Beadle (144), W.W. Ashe (165), and C.S. Sargent
(524/6).
•
326
Species concepts in agamic complexes
Brown surveyed these three and three others (E. Brainerd, J. Dunbar, W.W. Eggleston) in order to discover what might explain the tremendous increase in the number of
species recognised that had taken place in such a short time. The five questions he asked each worker were (Brown, 1910, p. 253): (I) "Why did not the systematic botanists discover the large number of species of Crataegus years ago?" Referring to A.
Jordan's recognition of inbreeding lines in various Brassicaceae as "true" or "elementary" species (Davis & Heywood, 1965), Brown asked (2) "Do you consider the species now being described elementary species?" Concerned whether seed families when
grown out exhibited evidence of segregation, and hence hybridisation, he asked (3)
"Do the species breed true or come true to seed?" and (4) "Will different species hybridize?" Brown's final question was (5) "Do you consider the numerous species to
have arisen as mutations?" The answers he received are broadly comparable, although
those from Sargent reflected a degree of testiness at having his judgement questioned,
especially in connection with subjects he lacked the time or inclination to follow in
detail (species concepts, mutation).
All of the workers interviewed agreed that the work of earlier taxonomists had suffered from the lack of observations on living plants, especially ones marked so that
both flowering and fruiting material from the same individual could be studied. It was
only a few years earlier that the North American workers had begun to take note of
features such as stamen number and the colour of the undehisced anthers (Beadle,
1902; Sargent, 1902; cf Schneider, 1906, fn. p. 767). With one exception (Dunbar),
those who answered the question about elementary species indicated that at least some
Crataegus taxa represented elementary species. Both Sargent and Beadle had the
opportunity to grow out seed families from type trees and had not observed any
segregation of morphological features among the seedlings. All six workers thus
referred to the ability of Crataegus species to breed true, but only Sargent and Dunbar
replied categorically that hybridisation did not occur in Crataegus. Sargent and Dunbar
also demurred concerning the role of mutation in the origin of Crataegus species. None
of the workers mentioned above made any reference to the then still slowly developing
European literature on apomixis (Gustafsson, 1946). Only Brainerd and Brown referred to the impact of European land-clearing (much as that of earlier aboriginal swidden ~J.. K \ C.
agriculture was referred to subsequently by Marie-Victorin, 1938), pointing out that (1'1"> iD)
cleared and then abandoned agricultural land vastly increased the area of suitable
habitat in which Crataegus species could establish and come into reproductive contact
\
with each other.
&Iso ·Kw.~kd<e.J (,q,,;)!i~l),,,,,h)
It soon became apparent that the simplistic view of Crataegus held by workers like
Sargent and Dunbar could not be maintained. l.'vidence of hybridisation (Standish,
1916) and polyploidy (Longley, 1924) were soon obtained, so that everl'though embryological data were not obtained until much later (Muniyamma & Phipps, 1979; Muni327
i)
Dickinson
yamma & Phipps, 1984; Dickinson & Phipps, 1986; Ptak, 1986; Smith & Phipps,
1988a; Ptak, 1989), reference was soon being made to apomixis, together with hybridisation and polyploidy, as an explanation for 'the Crataegus problem' (cf Eggleston,
1910; Palmer, 1932; Camp, 1942).
Throughout all of the work on North American Crataegus the species concept
employed has been an essentially morphological one. In recent work it has varied in
breadth with the complexity of the entities involved (Phipps & Muniyamma, 1980;
Brunsfeld & Johnson, 1990). As in Sorbus, the taxonomic species concept has been
applied in the context of a well-established and apparently robust subgeneric classification (Phipps & Muniyamma, 1980; Phipps, 1983; Phipps et aI., 1990), so that any
uncertainty at the species level may be compensated for by confidence in serial or
sectional assignments. Revisionary work on the genus by Phipps has taken a "moderate" approach, recognising that "... many of the 'microspecies' of earlier authors do
appear to represent real entities and cannot automatically and cavalierly be disregarded" (Phipps, 1988, p. 402). Phipps and Muniyamma (1980) found that few of the
specimens they examined could not be referred to named taxa, so that the challenge
they faced with the genus in Ontario, Canada, was to select the best available name
(often the earliest one applied to Ontario material). The objective is to catalogue the
variation present, as a basis for more detailed work in the future.
Studies of samples from local populations (Rickett, 1936; Rickett, 1937; Dickinson
& Phipps, 1985; Dickinson, 1986; Smith & Phipps, 1988b) make it clear that variation
between local populations of the same species can be substantial, while at the same
time variation within these populations may be minimal (Dickinson & Campbell,
1991). Studies of Cratciegus sectionCrus-galli Loudon in Ontario, Canada, documented the breeding system and quantified morphological variability of local population
samples (referred to as topodeme samples, in order to avoid assumptions about the
reproductive relationships implied by the word 'population'; cf Rieger et aI., 1976)
using ordinations, cluster analyses, and one-way ANOVAs of multivariate Levene
statistics (Table 2; Van Valen, 1978; Schultz, 1983; Dickinson & Phipps, 1985; Dickinson, 1986; Dickinson & Phipps, 1986). Topodemes were found to be well differentiated from each other for the most part; samples of the sexual diploid C. punctata
Jacq. showed generally greater variability than did those of facultatively apomictic,
polyploid C. crus-galli s.l. (Dickinson & Phipps, 1985; Dickinson, 1986).
The uniformity of the Ontario Crus-galli topodemes is highlighted, for example, by
the contrast made by two long-fruited individuals in one of the topodeme random samples (T2 in Fig. 8.7, Dickinson, 1983; Fig 6, Dickinson & Phipps, 1985). Fruits of all
the remaining 15 10-stamen individuals studied at this site are nearly isodiametric by
comparison. Most of the individuals in these topodemes can be ascribed to either of
two typically tetraploid, pollen-fertile, and facultatively apomictic IO>-stamen mor328
SPI
Ta
sIc
fr<
19
tei
pe
in
(L
w
(L
VI
fI
s
4
5
9
Species concepts in agamic complexes
Table 2. Ontario variants of Crataegus crus-galli L. s.L, contrasted with respect to modal numbers of
stamens (range, mean in parentheses) and styles, color of undehisced anthers, fruit size and shape, and
frequency of occurrence and compared with C. punctata Jacq. (Dickinson, 1983; Dickinson & Phipps,
1985; Dickinson, 1986). Crataegus crus-galli val'. crus-galli and val'. pyracanthifolia are predominantly
tetraploid, with occasional triploid individuals (Dickinson & Phipps, 1986). Frequency: COM, common,
more than one topodeme known; ace, occasional, only one topodeme known (a single individualofC.
persimilis is known from a second site); ISO, isolated, only single individuals noted. 1) Believed to be an
intersectional hybrid, Crus-galli x Macracanthae (Wells, 1985); calyx lobes densely toothed; tetraploid
(Dickinson & Phipps, 1986).2) Believed to be an intersectional hybrid, Crus-galli x Punctatae, or a
variant ofC. crus-galli; triploid (Wells, 1985 and personal communication). 3) Triploid and tetraploid
(Dickinson & Phipps, 1986). 4) Believed to be an intersectional hybrid, Crus-galli x Punctatae; anthers
very small, male-sterile; triploid (Dickinson & Phipps, 1986). 5) Diploid (Dickinson & Phipps, 1986;
Wells & Phipps, 1989).
Stamens
Anthers
4-13 (8.6)
pale yellow
pale yellow
Styles
Fruit
(1-) 2-3 (-4)
(1-) 2-3 (-4)
5-13 (9.4)
pink
(0-) 1-2 (-3)
1-3
9-19 (11.6) pink
1-2
(9.8)
red
12-21 (17.8) pale yellow
1-3 (-4)
15-21 (19.4) red
2-4
13-23 (19.1) pale yellow, pink
2-5
Name
Frequency
isodiametric C. crus-galli var.crus-galli
COM
C. crus-galli var. crus-galli
elongate
ISO
C. crus-galli var. pyracanthifolia Aiton occ
C. persimi!isl Ashe
occ
C. ?dispermi Ashe
occ
C. tenax' Ashe
COM
C. ?grandis4 Ashe
occ
C. punctata5Jacq.
COM
photypes, C. crus-galli L. VaL crus-galli and vaL pyracanthifolia Aiton (Dickinson &
Phipps, 1986, Table 2). In addition to these taxa there are also more or less isolated
occurrences of entities that are morphologically intermediate to some degree between
C. crus-galli and C. punctata. These are mostly triploid, pollen-infertile apomicts
(Wells, 1985; Dickinson & Phipps, 1986) with either 10 stamens (c. ?disperma Ashe;
Table 2) or 20 stamens per flower (c. tenax Ashe, C. ?grandis Ashe). Wells (1985)
collected flavonoid data from Ontario individuals of these taxa that have been re-analysed here (Fig. 1). Figure 1 emphasises an intermediacy of the latter three taxa relative
to C. crus-galli and C. punctata that was less apparent in morphological comparisons
(Dickinson & Phipps, 1985; Wells, 1985). They support the hypothesis (rejected by
Wells, 1985 for C. ?disperma but not for the other two taxa) that these entities represent hybrids arising from crosses involving reduced gametes from tetraploid, facultatively apomictic C. crus-galli and diploid C. punctata.
These results, like earlier, preliminary ones of Rickett (1936; Rickett, 1937; cf Fig.
3, Dickinson & Campbell, 1991), suggest that the specimens (herbarium material,
seedling families from type trees) upon which Sargent, Ashe, and Beadle based their
(taxonomic) species too often were, at best, samples from topodemeg dominated by
only one or a few different genotypes, in some cases of hybrid origin (Ashe stated to
329
=======,------------------ .
-j
Dickinson
N
0
tenax
?disperma
FL1
FL3
~p nctata
?grandis
FL4
~
crus-galli
0
0>
~
~
()
N
9-
pyracanthifolia
FL2
"''i'
-0.4
-0.2
0.0
0.2
CV1 (73%)
Figure 1. Ontario variants of Crataegus crus-galli L. s.l. (Table 2) compared with C. punctata
lacg. with respect to flavonoid profiles (Wells, 1985 and personal communication) in a biplot
of a contingency table canonical analysis (Gittins, 1985, chapters 5, l2). Data are occurrences
of 27 flavonoid spots (visualised using paper chromatography and sorted into four groups,
FLl-FL4, using Euclidean distances and complete linkage sorting) in 28 Crataeglls individuals (three C. crus-galli var. pyracanthifolia, six var. crus-galli, four C. lenox, four C. ?disperlI1a, four C. ?grandis, and seven C. punclala).
Brown, "Many species hybridise and some of those which have been proposed are
undoubtedly hybrids."). This conclusion is based not only on the morphometric and
flavonoid results, but also on the ecology of the genus. Crataegus individuals typically
establish on disturbed sites, the frequency of which in eastern North America appears
to have varied over the past 500 or more years (Brown, 1910; Marie-Victorin, 1938;
Vlf-Hansen, 1985; Dickinson, 1986; Dickinson & Phipps, 1986; Dickinson, 1998). The
relative uniformity of individual topodeme samples, and the variation observed
between these samples, could be explained by the interception, at anyone site, of seed
crops from only one or a few agamospermous individuals. In Table 2, taxa like C.
?grandis and C. persimitis that are found at only one or two even-agecbstands in Ontario in fact are likely to represent individuals of single, probably hybrid, clones that
330
Species concepts in agamic complexes
should probably have status only as informally named microspecies. Even the topodeme of C. crus-gall! var. pyracanthifolia (Table 2) is so uniform that it too likely
represents a single clone - of an entity that occurs more widely than do the two
preceding ones.
Asteraceae
In their review of 'The nature of dandelion species' Dudman & Richards (1997)
distinguish between the wide- and narrow-scope taxa comprised by Taraxacum in
Britain. The former are the sections into which the genus has been divided, as described by Kirschner and Stepanek (1994; 1996), while the latter are the microspecies
(equivalently, agamospecies) to which Dudman and Richards provide a guide for Great
Britain and Ireland. Virtually all of the fonner include at least some sexually reproducing entities; many, however, also include at least some microspecies. These are entities that are either facultatively or obligately diplosporous apomicts (Kirschner &
Stepanek, 1996). Some have been shown to be of hybrid origin (King, 1993). Because
of their vast numbers, the sometimes cryptic differences between them, and their considerable phenotypic plasticity (Dudman & Richards, 1997; Vavrek, 1998), these
microspecies give the genus its reputation for taxonomic difficulty. Comparisons of
sexual and agamospermous dandelions using isozymes and other molecular markers
have demonstrated contrasting patterns of genetic variation (cf references in Dickinson, 1998). Extensive gene flow via pollen between sexuals and asexuals has been
documented by Menken et 01. (1995). DNA fingerprinting has demonstrated the wide
geographic range of individual genotypes in section Polustria Dahlst., and the common
origin ofthree other microspecies (Van Heusden et 01., 1991).
Discussion
It has been suggested that " ... taxonomic philosophies which rely on panmixis fail
spectacularly when they attempt to treat non-panmictic plants" (Richards et 01., 1996,
p. 281). I would like to suggest that th~ failure referred to comes not from the misapplication of species concepts, but rather from the hierarchical level at which the
attempt is made to apply those species concepts (compare Stebbins, 1950, Fig. 38;
Kellogg, 1990). Likewise, patterns of molecular and morphological variation associated with apomixis have yet to be compared with those associated with panmixis on a
sufficiently wide and comparable basis to permit generalisation. Predictions certainly
exist about the patterns of variation to be expected in apomictic groups, but testing
these predictions requires control of potentially confounding fattors like habitat
331
Dickinson
s,
availability, seed dispersal, the relative frequencies (and outcomes) of apomixis,
selfing, and outcrossing.
Diagrams like those of Heslop-Harrison (1967, Fig. 3; similar ones now appear with
increasing frequency in the literature) remind us that at any given point in time species
are made up of populations of individuals (genotypes), cross-linked by more or less
frequent sexual reproduction. Over the course of time, these individuals are nodes on
strat;tds (ancestor-descendant lineages) that make up, more or less tightly, the rope-like
diachronic history of a species as a whole (the rope, in synchronic cross-section might
have the appearance of jigsaw puzzle pieces, as suggested by Gornall, 1997). The
analogy is more forceful as a picture than it is recast in words, but the point is that the
analogy represents the fundamental reality, some or all aspects of which are captured
by the species concepts discussed here. Pattern-based species concepts are useful as
tools with which to distinguish the ropes (or strands) from each other (also, to erect
hierarchical classifications of the rope-ends); process-based species concepts capture
the more or less frequent cross-linking of strands by sexual reproduction, but the data
needed to use them may be difficult to obtain.
For taxonomists of agamic complexes the implication of this analogy, and the biological phenomena it represents, is that they need to find the ropes (or perhaps nets) to
which the strands they study belong. A nominalist syllogism to the effect that since
taxonomists study species, and A is a taxonomist, then what A studies must be species,
needs to be eschewed. In its place is the opportunity to understand asexual reproduction in a group as one means by which populations of related genotypes may persist
from one generation to the next, particularly well, and in particular kinds of circumstances.
In several of the genera mentioned above there are fairly clear indications where
some ropes are. Apomicts, especially if they are facultatively sexual, link diploid
sexual species with each other or with other facultatively sexual (groups of) lineages.
In Crataegus isolation breaks down (cohesion is maintained), or not, as a function of
the timing of flowering in relation to vernal accumulated heat, local co-occurrence (cf
Campbell et aI., 1991, Fig. I; Dickinson & Campbell, 1991), the vagaries of the advance of spring and micrometeorological factors, pseudogamy, and the frequency with
which embryos are formed parthenogenetically or by selfing. Something similar
appears to be going on in Sorbus. In Amelanchier, although more information is
needed about the structure of the genus as a whole, the data available so far are
suggestive. In Taraxacum combinations of obligate and facultative apomixis, as well
as diplospory rather than apospory, apparently are responsible for the much greater
numbers of microspecies that workers with these genera have felt called upon to
recognise formally.
•
In Rubus, however, morphological variation and (or) phenotypic plasticity, combin-
e
a
332
~
r
(
t
Species concepts in agamic complexes
ed with the apparent capacity for long-distance dispersal and (or) the polytopic hybrid
origin of apomictic genotypes may make it exceedingly difficult to establish what the
populations of related genotypes are that may be persisting from one generation to the
next. It may be that the situation in Rubus is actually intermediate between that in the
other Rosaceae mentioned, and that in Poa where the argument can be made that distinguishable microspecies are absent.
What then is to be done? It seems clear that in many agamic complexes there are
real, recognisable entities present that persist for many generations by means of agamospermy and that have been derived from one or more known or unknown (or now
extinct) sexual ancestors. Where a robust subgeneric classification is available, it may
be that the sections or other such entities may be the evolutionary units comparable to
(one or more) species in genera that reproduce exclusively by sexual means (Kirschner
& Stepanek, 1996; Dickinson, 1998). Recognition of apomictic nothotaxa may help to
draw attention to the hybrid origins of particular entities (ef Christensen, 1992). In
order to have comparable taxa regardless of reproductive mode (i.e. ropes), apomictic
microspecies (strands) should be recognised informally, using parenthetical (Burtt,
1970) or quoted (Campbell & Wright, 1996; Dibble et al., 1998) informal infraspecific
names. In conservation issues, especially ones where legal protection may revolve
around recognition of a single genotype as a species, these informal names may be less
subject to challenges that would otherwise divert attention from concerns to protect habitat rather than individual species. Similarly, in agronomic applications these informal
names can be used to recognise economically important genotypes (Kellogg, 1990).
A species concept that is appropriate for agamic complexes thus is one, the use of
which results in comparable units regardless of predominant mode of reproduction.
Regardless of mode of reproduction, species comprise multiple lineages (see Dickinson, 1998 for a discussion of exceptions) sharing a common ancestor. In agamic complexes genotypes may be repeated over space and time because of predominant selfing
and (or) agamospermy. These genotypes may appear to be represented by homogeneous local populations because their genetic uniformity is not recognised. Variation
between individual genotypes that is commonplace in biparentally reproducing species
may become the basis for recognition of microspecies when the variants are represented by what can be mistaken for local, p~nmictic populations. Alternatively, depending
on mode of dispersal, local populations may comprise many different apomictic genotypes, in which case their recognition as microspecies may be a function of their occurrence at numerous sites (e.g., dandelions; Richards, 1986).
With such a concept of what species 'are', the issues involved in the choice of a
species concept to use with agamic complexes become more clear. Counting differences (e.g., Landry, 1975; Phipps & Muniyamma, 1980) or autapomorphies (Nixon &
.
Wheeler, 1990) can be highly operational but ultimately might produce a taxonomy m
.
333
Dickinson
which the entItles recognised as taxonomic or phylogenetic species in seifers and
apomicts are no more meaningful than are individuals of a panmictic species: such
elementary species, agamospecies, or microspecies are present in a particular place, or
they're not; so what? Arguably, it's more useful to recognise that' Crataegus ?grandis'
is important less for itself and its single occun'ence in Ontario, Canada, than for what it
may say about hybridisation between diploid and tetraploid Crataegus. On the other
hand, it may be out of the question to obtain the data needed to arrive at the limits of
biological or genealogical species. Moreover, evidence about species interfertility certainly suggests that biologically or ecologically meaningful entities might be lost from
sight if subsumed in a single unit. The self-incompatibility of diploid Crataegus punctata sets it apart from self-compatible, typically tetraploid C. crus-galli in a way that
probably is compounded of not only the morphological differences on the basis of
which these species have been ascribed to different sections but also of their pollinator
relationships and colonising ability. What a potential loss of biological information, if
C. crus-galli and C. punctata were subsumed in a single species because evidence (Fig.
I) suggests that they hybridise to produce entities like those recognized as C. tenax, C.
?grandis, and C. ?disperma.
\'Acknowledgements
I am' grateful to Deb Metsger and M. Jafar for bibliographical assistance at the outset
of this writing project. Christopher Campbell, Nadia Talent, and an anonymous reviewer provided helpful comments on the original draft of this paper. Dr Tom Wells
generously shared his dissertation data on flavonoid and morphological variation in
Ontario C. section Crus-galli with me; re-analysed, the former appear here as Fig. 1.
Wells' work on hybridisation in Ontario Crataegus and mine on section Crus-galli
were supported by Grant AI726 from the Natural Sciences and Engineering Research
Council of Canada (NSERCC) to J.B. Phipps. My research on consequences of apomixis and systematics in Crataegus is supported by NSERCC Grant A3430. This paper
is Contribution 155 from the Center for Biodiversity & Conservation Biology of the
Royal Ontario Museum.
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