Progress and Prospects in Reconstructing Plant Phylogeny

14 Pages·1994·6.7 MB·

by  Michael J Donoghue

AND
PROGRESS PROSPECTS
Michael Donoghue
J.
RECONSTRUCTING
IN
PHYLOGENY
PLANT
1
Abstract
Phylogeny reconstruction has become respectable science over the last few decades, and trees are accumulating
rapidly in the literature. Botanists have been active in this effort and can already cite success stories (e.g., recognition
of streptophytes, stomatophytes, anthophytes, eudicots). Nevertheless, only a small number of problems have been
addressed and some of these have resisted solution. To solve the toughest problems, especially those involving ancient,
rapid radiations, various sources of data will need to be combined, including evidence from fossils. Furthermore, in
view of limitations in analyzing data sets with many taxa, more attention must be paid to the consequences of different
taxon sampling strategies and to how large, variable taxa can be represented in more inclusive studies.
Over the next few years we should continue to move toward a phylogenetic system (monophyletic groups defined
We
by ancestry, diagnosed by characters), which will entail the elimination of familiar paraphyletic taxa. can expect
increased use of phylogenies by ecologists, molecular biologists, and others, which will force us to attend to the issue
of the reliability of phylogenetic hypotheses, and will necessitate the development of a database of phylogenetic studies.
Interactions with population biologists promise to be especially productive, since there are obvious mutual concerns
centered on the analysis of gene trees and reticulation.
Over twenty-five years have elapsed since the (e.g., Hennig, 1966; Farris, 1983; see Sober, 1988;
&
publication of Willi Hennig's Phylogenetic Sys- Swofford Olsen, 1990), to the availability of
implement
tematics (Hennig, 966), and for well over a de- computers and algorithms to this logic
1
&
cade 1988; Maddison Maddison, 1992;
botanical systematists have been conducting (e.g., Farris,
numerical phylogenetic analyses. The focus of the Swofford, 1 993), and to new sources of evidence,
Fernholm
Missouri Botanical Garden's Annual Systematics especially molecular data (e.g., et al.,
&
Symposium on the "Origin and Relationships of 1989; Hillis Moritz, 1990). While it is obvious
the Major Plant Groups" suggests that progress that these developments have had a significant
has been made, and the meeting documented impact on plant systematics, it is not entirely clear
itself
how measure the progress that has been
significant advances in our understanding of several best to
°1 the most challenging phylogenetic questions. The made. There are, however, several indicators that
aim
of this paper is to take stock, in general terms, bear consideration.
where
°i
things stand. Has phylogenetic analysis
°ad
a LEVEL OF ACTIVITY
substantial impact on our understanding of
plant
phylogeny, and where do we go from here?
One measure of progress simply the rate of
is
hypotheses. Phyloge-
phylogenetic
of
publication
Progress
accumulating the
undoubtedly in
are
netic trees
Although many but the magnitude of the effort is difficult
of the ideas underlying phylo- literature,
no one has been keeping track
genetic because
analysis have a rather long history (see to assess
79
Craw, 1992; Donoghue & Kadereit, 1992), phy- of such information. In a survey of journals
we
°geny 1989, 1990, and 1991, recently
reconstruction has become respectable sci- published in
ence on 40 articles that contained
only over the few decades. This happy assembled data 1 1
last
This remarkable
circumstance can be traced to a series of devel- trees (Sanderson et al., 1993).
a day) surely
pments number of studies (nearly a tree is
in the logic of phylogeny reconstruction
Wayne
am Dav.d Madd.son,
'I Toby Kellogg
David
y grateful to Bruce Baldwin, Peter Crane, Jim Doyle, Hillis,
unpublished
Maddison, and/or access to
Dick Olmstead, Mike Sanderson, and Liz Zimmer for helpful discussion
*>*. My work has been suppor ed
symposium
as well as to Mick Richardson for inviting me to participate in the
Smithsonian
** NSF Foundation Fellowship from the
(BSR-8822658), and Mellon
J the University of Arizona, a
'^'tution.
02138,
Massachusetts
Cambridge,
'Department Harvard University,
of Organismic and Evolutionary Biology,
405-418. 1994.
Gaud. 81:
Bot.
Ann. MISSOURI
406 Annals
of the
Missouri Botanical Garden
over 471 (53%) of the phylogenetic
studies used
some form
of molecular evidence
(including
allo-
zyme
data), with the percentage of such
studies
51% 56%
from
increasing to over the three-year
GREEN PLANTS
(199)
period.
We
312
identified studies of green plant groups
27%
namely
(ca. of the total), organisms with chlo-
rophyll b and starch storage, including the various
882 PHYLOGENETIC STUDIES lines of "green algae" and the land plants (San-
(1989-91)
derson et 1993). However, 113 (36%) of these
al.,
employed
only phenetic techniques, a greater per-
we
centage of phenetic studies than found in any
A
other major group of eukaryotes. breakdown of
major
all lines (4)
99
the remaining numerical phylogenetic studies
1
other green plants
ANGIOSPERMS (10)
23%
of green plants (ca. of all phylogenetic studies)
(168) other land plants
(4)
shown The 84%)
other vascular plants (5) is in Figure 1 vast majority (168,
.
other seed plants
(8) of these were of angiosperm groups. Within an-
giosperms, Asteraceae (30 phylogenetic studies)
most
and Fabaceae (15 studies) received the at-
199 GREEN PLANT STUDIES
(1989-91)
tention, while other large families, such as Orchi-
The 49
daceae (4 studies) are underrepresented.
Asteraceae
(30)
29%
studies of monocots account for around of all
Fabaceae
(15) Poaceae angiosperm studies, with 4 of these within grasses.
(14) 1
number
To some numbers the
extent these reflect
Orchidaceae
(4)
are
of species per group, but historical factors
Asteraceae
evident as well. For example, studies of
and promising re-
other monocots were stimulated by the early
(31)
other dicots Palmer, and col-
(74) striction site studies of Jansen,
l"o
leagues (see references in Palmer et al., «
Jansen 1992).
et al.,
ANGIOSPERM
168 STUDIES
(1989-91)
have
some groups re-
Figure 1 also shows that
FIGURE
1. Pie charts showing aspects of the taxo-
consid-
especially
ceived relatively attention,
nomic little
distribution of numerical phylogenetic studies pub-
phyloge-
understanding
importance
lished between 1989 and 1991 (compiled from an updated ering their in
green plants.
version of a database assembled by Sanderson netic relationships among major lines of
et al.,
1993). Top: Studies of green plants (chlorophytes; with For example, we found only five phylogenetic anal-
chlorophyll b, starch storage) account for ca. 23% of the than seed plants dur-
yses of vascular plants other
882
phylogenetic analyses in the Sanderson et al. data- phy-
great
84% ing the three-year period, despite their
base. Middle: Approximately
of the green plant
o
interest
and the evident
studies are of angiosperm groups; the remainder are of logenetic significance
a
"other seed plants" (specifically conifers, cycads), "other pteridologists in phylogenetic questions (e.g., 8
groups
vascular plants" (ferns, lycopsids), "other embryophytes" Such including fossil
ner, 1980). studies,
(mosses,
liverworts), "other green plants" (various "green an
"Coenopteridales
"Cladoxylales,"
(e.g.,
algae"), or included representatives of "all major lines."
or-
needed in
"progymnosperms"), are desperately
Bottom: Of 168 angiosperm 49 29%)
studies, (ca. are of
eusporan-
monocot whether
groups; Asteraceae and Fabaceae account for der to establish, for example,
38% ep^
to
ca. of the "dicot" studies. giate fern groups are more closely related
progymnospern
perhaps to
tosporangiate ferns or
Fortunately,
groups (and hence seed plants). w
arc
an
underestimate inasmuch we fossils)
as did not survey and lycophytes (including
terophylls
i
every journal containing phylogenetic studies and receiving more attention (e.g., Bateman et al.,
we
were
unable
to include analyses published in Gensel, 1992). s^
d .
molecular
books.
Nevertheless, our study probably provides Although the absolute number of
e^
a reasonably accurate picture of what phylogeny increased slight y
exists in the ies of green plant
Of 882 over the
literature. the total, (77%) of the studies year, the percentage of such studies ^^
employed some "cladistic" method (including around 50%, the res
par- year period fluctuated
simony and some *>***£
distance methods, but not phe- based on morphology and/or secondary
studies
netic clustering methods such UPGMA), molecular
as and Overall, about half of the
Number 3 Donoghue 407
Volume 81
,
1994 Reconstructing Plant Phylogeny
&
based on restriction fragment variation, especially references in Kenrick Crane, 1991), provide
DNA. The number
chloroplast of plant studies excellent examples of the importance of fossils in
in
based on nucleotide sequences has risen dramati- understanding the early evolution of vascular plants.
cally since 1991 (e.g., studies of the chloroplast Again, these conclusions are consistent with recent
gene rbch), and will undoubtedly continue to in- molecular evidence (e.g., Palmer et al., 1988;
& &
crease in number, but rather few such studies (32, Manhart Palmer, 1990; Raubeson Jansen,
24% of the plant molecular studies) were published 1992).
in the 1989-1991 period. Over half of the se- Morphological phylogenetic analyses of seed
&
quence studies involved ribosomal genes (see Zim- plants (Crane, 1985, 1988; Doyle Donoghue,
& &
Hamby Wa-
mer 1989; Zimmer, 1992; 1986, 1992; Loconte Stevenson, 1990; Doyle
et
al.,
ters et al., 1992), and in the near future, especially et al., 1994, this issue; Nixon et al., 1994, this
have
at lower taxonomic levels, analyses of the internal issue), while not agreeing in detail, consis-
group
transcribed spacer (ITS) regions Baldwin, tently concluded that Gnetales are the living
(e.g.,
angiosperms This
1992; Wojciechowski et 1993) promise to be most closely related to (Fig. 2).
al.,
productive. Phylogenetic studies using "single- clade also supported (though not very strongly)
is
copy" nuclear genes are rare, but technical by chloroplast and ribosomal sequence data (Chase
still
&
difficulties in obtaining such sequences have been et al., 1993; Hamby Zimmer, 1992; but see
An
largely overcome, and expect that they will play Troitsky et al., 1991; Hasebe et al., 1992).
I
two
an increasingly important "anthophyte" clade, consisting of these living
role.
and Pentoxylon, a
Phylogenetic studies that include fossils are still groups plus Bennetittales is
have included
rare, despite their potential significance (Donoghue regular feature of the studies that
some
et al., 1989). While molecular studies of fossils are fossils. Furthermore, with the exception of
promising by Nixon (1994), of these studies
(e.g., Golenberg et al., 1990; Soltis et analyses et al. all
monophyletic,
al., 1992), their impact depend on developing have determined that Gnetales are
will
more
the ability to repeatably obtain significant segments with Gnetum and Welwitschia closely related
DNA
of from plant parts fossilized in standard ways. to one another than either is to Ephedra. In this
compelling
molecular data are especially
case, the
1994).
(Doyle et
al.,
SUCCESS
STORIES
monophyly
There has also been consensus on the
conclusion view of
While angiosperms, a significant in
it is obvious that botanists have actively of
they are
engaged more adherence to the belief that
in phylogenetic research, dif- lingering
it is
1991). Within angio-
Krassilov,
ficult to determine how have polyphyletic (e.g.,
successful these efforts
have been promising results.
been. However, sperms there also
progress
in several cases significant
"tricolpate" clade
does appear Some Perhaps most importantly, the
to have been made. of these
& Doyle
Donoghue Doyle (1989; "eudicots" of
successes
are accompanying of
highlighted in the
symposium & Hotton, 1991) has surfaced in recent rbcL stud-
papers, so only a few are noted here
Chase 1993),
(Fig. (Olmstead et al., 1992; et al.,
2). ies
The majority of "dicots" (the
studies by Mishler and colleagues (see Mish- implying that the vast
1988; Takhta-
,er et al., 1994, this issue) have confirmed earlier "higher" subclasses of Cronquist,
opposed having
mdications 1987) form a clade, as to
that green groups with phrag- jan,
algal
among "magnoliids," as
rooplasts, separate origins
especially charophytes such as Coleo- several
needed
rnaetr Further analyses are
are more suggested previously.
than
closely related to land plants
%
conclusion.
,h <7 are to other "green algae." They also solidify to check the robustness of this
"success"
lhe clear that
»iew that "bryophytes" are paraphyletic, with Even from this short list it is
any one type of
J^ses more These has not been tied to the use of
closely related to tracheophytes.
success
very impression of
ypotheses the
are being borne out by molecular evi- evidence. In fact,
dence "making sense" of of the data,
from all
(Mishler stems
et 1992, 1994).
al.,
& on and Recent organ-
Kenrick information fossil
Crane 99 have made great prog- including
( 1 1 )
ress m morphology and molecules. In stressing this
establishing among early lines isms,
relationships
provided a
Hennig (1966)
vascular major "criterion of veracity,"
plants, suggesting that several
have
which
analogy,
splitting convincing I
events and morphological innovations pre- characteristically
example, the pro-
* ed the radiation giving rise to extant groups. reproduced in Figure 3. In this
evidence likened
eir detailed coupled with cess of accounting for all of the is
studies of tracheids,
assemble the torn
geographer attempting to
remarkable Remy a
and colleagues to
discoveries of
°n map so as to bring together all of the
Sametophyte Remy, 1982; pieces of a
morphology
(e.g.,
408 Annals of the
Garden
Missouri Botanical
*»
<£
*
^
v
&&
tt#j&Jfa$
ffi
ANGIOSPERMS
(flowering plants)
ANTHOPHYTES
SPERMATOPHYTES
(seed plants)
LIGNOPHYTES
TRACHEOPHYTES
plants)
(vascular
POLYSPORANGIOPHYTES
STOMATOPHYTES
EMBRYOPHYTES
(land plants)
STREPTOPHYTES
CHLOROPHY
major
FIGURE An showing
2. overview of green plant phylogeny (based on analyses cited in the text),
afC
Many
seem polychotomies). 8
reasonably well supported and areas of continuing uncertainty (unresolved ^^
afe
Only three fossil
omitted, and resolution is simplified to highlight familiar clades (see O'Hara, 1992). J
^^^
supporte
included (marked by *), which are probably paraphyletic (quotation marks). Some of the best
been
have not
have long been recognized (e.g., land plants, seed plants, flowering plants), though these v
centl
on re
polysporangiophytes) y
accepted; others have been re-circumscribed (e.g., tracheophytes) or named (e.g.,
&
Charales+Choleochaetales+bmDry y ^
(Kenrick Crane, 1991); several others have not yet been named
(e.g.,
recent
outcome of ^^
Recognition of the monophyly of a number of terminal taxa (e.g., eudicots) is also an p
mo
not
Note some "gymnosperms") are
studies. that traditional groups (e.g., "green algae," "bryophytes,"
and are not shown.
Number
3 Donoghue
Volume 81 409
,
1994 Reconstructing Plant Phytogeny
roads, rivers, and other landmarks. The corre-
sponding operation in phylogenetic systematics
is
assessing, as Hennig (1966: 130) put "whether
it,
the differently determined views concerning the
phylogenetic relationships of different groups of
organisms are in agreement." Satisfaction
is
when
achieved the pieces are assembled so that
One
everything of the central points of the
fits.
example that a perfectly consistent explanation
is
for any one road, or bit of evidence, might turn
out to be highly unparsimonious when other fea-
may
tures, however minor they have seemed at
the outset, are taken into consideration.
OUTSTANDING PHYLOGENETIC PROBLEMS
For each success story there are, of course,
many
other problems that have not been addressed
or for which a satisfying result has not yet been
obtained. Thus, as also shown in Figure 2, rela-
among
tionships the major extant lines of seed
plants (cycads, ginkgos, conifers, anthophytes) have
&
not yet been convincingly resolved (Doyle Don-
oghue, 1992; Doyle 1994). Likewise, the
et
al.,
among
position of the root of angiosperms, whether
"magnoliids" or among "paleoherbs," has re-
37 panel) and 38 (bottom
FlGURE Figures (top
3.
mained
unsettled (but see Doyle et al., 1994). In from Hennig (1966), illustrating the "criterion of
panel)
both cases, particular data provide con- Hennig's original captions are as follows: "Fig-
sets to veracity."
fail
reconstruction of a
vincing support for one hypothesis over another ure 37. Criterion of veracity. In the
map from several fragments, a, a', and a"
topographic
and/or
there are among based
conflicts the results
stream
adjacent sections of a
could be interpreted as
on
different data Even however,
sets. in these cases, The remaining elements of the map, however,
course.
some map
hypotheses appear less likely to be true than remain isolated. The joining of the fragments is
others. For example, there evidence that wrong." "Figure 38. Criterion of veracity. If in the re-
is little
map from several fragments,
topographic
the construction of a
root of angiosperms among monocots, and
is
and a" are interpreted as adjacent sections of a
a, a',
I find it interesting that molecular data in particular map form
elements of the also join to
stream, the other
do
not support rooting the tree in the vicinity of The joining of the map fragments
a sensible illustration.
^hloranthaceae.
Furthermore, worth noting
correct."
it is is
mat
among
conflicts appear to be as significant
&
different Dowd,
molecular Martin
trees (contrast
19 Hamby & morphology, such as detailed studies
^1; Zimmer, 1992; Chase proaches to
et al.,
Endress,
1*93), and among development and function (e.g.,
different morphological results of flower
(contrast Dahlgren & Donoghue & 1987; Tucker, 1988; Erbar, 1991; Williams et
Bremer, 1985;
phyloge-
Doyle, 1989; Loconte & Stevenson, 1991; Taylor al., 1993), continue to provide valuable
make
Comparative analyses that
Hickey, characters.
1992; Nixon 1994), as they are netic
j* et al.,
mechanisms
etween on the molecular
molecular and morphological results. use of recent findings
&
Coen Mey-
What development
can underlying flower (e.g.,
be done to solve such problems? First,
we can New 1991) promise to be especially useful in
hope more erowitz,
to obtain decisive data.
homology of the structures that
Molecular elucidating the
evidence be forthcoming,
will certainly
morphological phy-
have been most heavily used in
" traditional from
sources of evidence are far
m
research.
exhausted. Much logenetic
6 of the information present
com-
can be
evidence also
,n standard compendia 1981) has Different sources of
Cronquist,
(e.g.,
1989;
(Kluge,
o simultaneously
yet been bined and analyzed
incorporated phylogenetic analyses.
in
&
1992;
Th Donoghue Sanderson,
can 1991;
,s and should be done, but require a Barrett et al.,
will
de
1993;
critical Swofford, 1991; Bull et al.,
reassessment of homology hypotheses (Don- but see
weak
ahue & Here the hope that signals
Sanderson, Furthermore, new ap- Queiroz, 1 993). is
994).
1
410 Annals of the
Missouri Botanical Garden
present in several separate data sets might com- uate alternative hypotheses critically or to explore
plement one another and provide a single stronger the robustness of the results using tests such
as
result. Obviously, this need not be the outcome, the bootstrap (Felsenstein, 1985; Sanderson, 1989)
but behooves us to explore such possibilities in or decay analysis (Bremer, 1988; Donoghue
it et
al.,
particular cases. In the case of the angiosperm 1992). Of course, the same limitations apply
to
root, the combined analysis of Doyle et al. (1994) large morphological studies (e.g., Hufford, 1992;
&
favors a placement among paleoherbs more con- Kellogg Watson, 1993).
vincingly than any single data set. This not simply In view of these problems, analyses involving
is
a matter of a larger number of molecular characters large numbers of taxa must employ carefully de-
swamping
out the morphological evidence, because signed (and explicit) search strategies to discover
some elements in the combined trees are more separate "islands" of parsimonious trees (Maddi-
consistent with morphology. The temptation to son, 1991; Maddison et 1992; Page, 1993b;
al.,
compete molecules against morphology simply Olmstead et 1993). Alternatively, there may
is al.,
—
counterproductive combining the evidence may be ways of reducing the number of taxa without
One
provide the best hope of success (Sytsma, 1990; sacrificing accuracy. possibility, the use of a
&
Donoghue Sanderson, 1992; Doyle et al., 1994). single "exemplar" species to represent a large clade,
Incorporation of fossils is likely to be critical in has the advantage of avoiding (at least partially)
cases of presumed rapid radiation in the distant the problem of inferring basal states for the group
own
past (Donoghue et al., 1989; Huelsenbeck, 1991b; in question. This strategy, however, entails its
Novacek, 1992). Fossils might represent more risks. Most importantly, the inadvertent choice of
faithfully those character combinations that were an exemplar that in reality, nested well within
is,
mistaken
present closer to the splitting events of interest. the clade in question, might result in a
Their addition could, in effect, "shorten" the lengths estimate of the true relationships of the group. This
of branches leading to extant taxa, thereby less- could happen, for example, if the exemplar be-
ening the chance of spurious connections owing to longed to one specialized line within the group,
chance convergences "long-branch which happened have converged on another
(the attrac- to
tion" problem; Felsenstein, 1978). Already there terminal taxon in the analysis.
are examples of this effect (e.g., "progymno- A second option is the use of a "placeholder'
sperms" relative to seed plants), and the addition for a number of terminal taxa, where there is
In
of recent paleobotanical discoveries (e.g., Crane et evidence at the outset that these form a clade.
al., 1989; Pedersen et al., 1991; Cornet, 1986) this case, some prior information on relationships
could have a similar effect as regards angiosperms within the group may make possible to establish
it
& most
the
(Doyle Donoghue, 1993). a set of ancestral conditions, by finding
node o
the basal
parsimonious character states at
by
described
are
the clade in question (algorithms
METHODOLOGICAL
ISSUES
& approach, ad-
Swofford Maddison, 1987). This
name *conv
Solving difficult phylogenetic problems will re- voca ted by Mishler 994) under the
1
(
morphology
quire additional evidence, but will also depend partmentalization," has been used in
it
very
on always
basic methodological advances. Thus, both the analyses for some time (though not
&
thought of combining data sets and the possibility explicitly). For example, Donoghue Doyle (19 _J
analyse
of long-branch phylogenetic
attractions highlight the need for performed a preliminary
es
more core-Laura
attention to taxon sampling for phylogenetic within a presumably monophyletic
& to
analysis Donoghue assign states
(e.g., Sanderson, 1992; clade and used the results to
& Doyle 4.
Wheeler, 1992; Kellogg Watson, 1993). This placeholder for that line. Similarly,
relatiM-
on
especially view hypotheses
is critical in of the significant lim- (1994) used preliminary
to
monocotyledons
itations of presently available computer algorithms ships within such groups as
ternim
&
in handling large numbers of taxa (Swofford down" information on a set of observed
Olsen, 1990; Maddison, 1991; Maddison et al., taxa to a set of ancestral state assignments,
par
a
1992; Penny have only
et al., 1992). Although there is some tunately, may be sufficient to ^
it
*
state
comfort the
in the extensive sampling of angiosperms prior hypothesis of relationships, as
in the Chase et al. (1993) analysis of 499 rbcL taxa nested well within the clade in question i
^
any
sequences, the results are correspondingly from having
"screened-off"
difficult be effectively
conditions
to interpret. It is unclear whether all (or even any) feet on the assessment of basal
of the most
parsimonious
trees actually have been dison et 1984).
al.,
more
mean that
recovered, and
it is practically impossible to eval- The use of placeholders will
Number
Volume 3 Donoghue
81
411
,
1994 Reconstructing Plant Phytogeny
than one character state will occur in some terminal be of lasting value only of the evidence un-
if all
An
taxa. alternative approach, advocated by Nixon derlying the results made available for scrutiny.
is
& Davis ( 1 99 1 ), is always to subdivide polymorphic Otherwise, it is impossible to make reasoned choices
monomorphic among
taxa into terminal units. This, of alternative hypotheses, or to learn anything
course, can only aggravate the real-world problems from experience.
at all
posed by large numbers of taxa. Furthermore, sub-
division based on the states of a character (one of Prospects
which presumably
ancestral within the group)
is
What
can we look forward to over the next few
will result in para- or polyphyletic terminal units
Here what
years? I will briefly highlight I believe
many
in cases. For example, angiosperms were
if
to be several important trends and their likely con-
subdivided into two terminal taxa based on the
sequences. At the base of each of these trends
is
presence and absence of vessels highly likely
it is
more fundamental what O'Hara (1988)
a shift to
that neither would be a clade. The same would be
has called "tree-thinking": understanding diversity
many
true of other characters, such as the presence
as the product of an underlying branching process,
and absence of an active cambium, or different
and observed differences as having resulted from
types of embryo sac development. Inclusion of
evolutionary changes along the branches of a tree.
nonmonophyletic
terminal taxa in an analysis can
That the away from a linear view of evolution
shift
result in erroneous conclusions about relationships
from complete evidenced by the language
far is
is
and
character
evolution, at least taxa are inter-
if
so often used to describe evolutionary history,
still
preted
in the standard way, namely as representing
such as "lower" and "higher" in reference to taxa
real (single) branches of a phylogenetic tree.
(O'Hara, 1992). Fortunately, however, tree-think-
In the end, the best method of coding large
more prominently the
ing likely to figure in
is
polymorphic
taxa will depend on the circumstanc-
MacClade (Mad-
curriculum, with software such as
es. Sometimes be and appropriate
it will feasible &
Maddison, 1992) making easy and fun
dison it
to split a polymorphic terminal unit into two or
explore the implications of evolutionary trees.
to
more
groups
(hopefully monophyletic), and
this
may
not number
significantly increase the overall
PHYLOGENETIC SYSTEM
A
°t taxa. In other cases some form of compart-
undoubtedly take
mentalization be on Although major changes will
will possible, leaning cautiously
move
the results of previous analyses. The latter requires time, I suspect that botanists will continue to
mean
By
that the assumptions used in one analysis be vig- toward a truly phylogenetic system. this I
conform our
orously be delimited so as to to
tested in other, independent analyses, but that taxa will
such phylogeny and be defined in
tests are certainly possible (e.g., Doyle et al., best estimates of will
*"4). Another option to simply code a terminal terms of ancestry rather than in terms of the char-
is
taxon as polymorphic, as can be done PAUP acters used to diagnose them (Hennig, 1966; de
in
&
& Donoghue Cantino, 1988;
(SwofFord, 993) and MacClade (Maddison Mad- Queiroz, 1988, 1992;
1
&
terms
dison, 1992). In the case of multistate characters de Queiroz Gauthier, 1992). In practical
some paraphy-
(such mean familiar
as eliminating
nucleotides at a particular site) this need this will
not be equivalent groups. An excellent example is provided by
to coding the taxon as completely letic
unknown," on Asteraceae, culminating
research
since particular subsets of states can phylogenetic
new names
1992) several
specified. Although coding a taxon as unknown recently (Bremer et al., in
can sometimes have & conclusions that are well supported by
undesirable (Doyle to reflect
effects
Donoghue, & Barnadesioideae
evidence
1986; Nixon Davis, 1991; Platnick different sources of (e.g.,
of the family).
al., 1991), may be necessary, especially to as the sister group of the rest
it
made
^corporate incomplete (Maddison & Mad- Many more changes of this sort will be as
fossils
dison, phylogeny improves. In par-
1992). our understanding of
angiosperm
kven some
traditional
in cases that continue to resist resolution, ticular, it is clear that
more mono-
one or
P ogress made when are paraphyletic, with
is relevant data and analyses families
are nested within them. For example,
published, because, if nothing else, this clarifies phyletic families
toe documented the or-
implications Cantino (1992) has carefully
of alternative hypotheses. This
is
/u^
Lamiaceae from within Ver-
of course, only to the extent that sources of igin of several lines of
documented
have
ormation (especially voucher specimens) are benaceae. Judd et al. (1994)
carefully phylogenetic analyses of other
documented, and assumptions similar situations in
only the
if
underlying presumably closely related families. In particular,
the delimitation of taxa and characters
are clearly Asclepiadaceae appear to be nested within a para-
can
spelled out. Phylogenetic research
-
412 Annals of the
Missouri Botanical Garden
phyletic Apocynaceae, Apiaceae within Araliaceae, servationists, and others will surely continue
to
&
Brassicaceae within Capparaceae, Valerianaceae increase (e.g., Brooks McLennan, 1991; Harvey
&
plus Dipsacaceae within Caprifoliaceae, Urticaceae Pagel, 1991). In the case of angiosperms,
for
within Moraceae, and Aceraceae and Hippocas- example, the availability of trees has already had
tanaceae within Sapindaceae. Many of these con- an impact on studies of a wide variety of characters,
&
clusions based on morphology are now also sup- including vessels (Young, 98 Donoghue Doyle,
1
1 ;
ported by molecular evidence (e.g., Chase et al., 1989), dioecy (Donoghue, 1989), double fertiliza-
1993). In most of these cases, we have proposed tion and endosperm (Donoghue, 1989; Freidman,
&
to eliminate paraphyly through recognition of a 1992; Donoghue Scheiner, 1992), pollen mor-
&
single more inclusive family (Judd et al., 1994). phology (Doyle Hotton, 1991), pollination (Pell
This, we hope, will help counteract a bias on the myr, 1992), and self-incompatibility (Weller et al.,
Many
part of temperate botanists to segregate and elevate 1994). other ideas on the direction of mor-
the rank of mainly temperate, mainly herbaceous phological evolution (discussed, for example, by
groups, leaving behind a residue of woody tropical Stebbins, 1974; Carlquist, 1975; Cronquist, 1988;
plants with which they are less familiar. Takhtajan, 1991) will soon be tested in a phylo-
Although the shift to monophyly may entail rath- genetic context. Similarly, phylogenies will have
er major changes in some cases, this should hardly an increasing impact on our understanding of mo-
be viewed with dismay. Instead, such changes are lecular evolution. For instance, we can look forward
a concrete sign that we are making progress in to a fruitful period of "reciprocal illumination"
understanding phylogeny. Furthermore, although between studies of plant phylogeny and molecular
mechanisms underlying
there will be resistance to changing traditional genetic analyses of the
&
names, such changes are very occur flower development (Coen Meyerowitz, 1991).
likely to in
the long run because a phylogenetic system most The use of phylogenies in other studies will force
is
of
useful in helping us understand evolutionary and phylogenetic systematists to attend to the issue
who
ecological processes, biogeography, and so on reliability. Quite naturally, those intend to rely
how
(Hennig, 1966). Moreover, recognition of mono- on phylogenies will want some indication as to
phyletic groups makes much easier to teach plant believable they are. A variety of methods have
it
1985; Bremer,
diversity and for students to learn about It also been developed (e.g., Felsenstein,
it.
helps from the standpoint of continued analysis of 1988; Sanderson, 1989; Archie, 1989; Hillis,
1991a;
phylogeny to have names for the clades we work 1991; Huelsenbeck, 1991a; Goloboff,
The name Donoghue 1992) and there is
with. "anthophyte," for example, has Faith, 1991; et al.,
on the logic
been useful in describing seed plant phylogeny. a growing (mostly critical) literature
Carpenter,
Likewise, we hope that the "stem-based" name and behavior of such methods (e.g.,
& 1992;
"angiophyte" (Doyle Donoghue, 1993) 1992; Goloboff, 1991b; Kallersjo et al.,
will fa-
&
to
how Here be critical
cilitate discussion of fossils such as Sanmi- Hillis Bull, 1993). it will
underlying
guelia (Cornet, 1986) relate to modern angio- develop a deeper understanding of the
emerges
sperms. philosophical and statistical issues. If it
then
it
In addition to better phylogenies, the develop- that particular methods are unsatisfactory,
why the
ment of a phylogenetic system requires attention behooves us to articulate exactly this is
methods.
to the logic of phylogenetic taxonomy and nomen- case and then to develop and test better
warned
be
clatural conventions. Here the analysis and rec- In the meantime, users of trees should
& ac-
ommendations of de Queiroz Gauthier (1992) of uncertainties and encouraged to take into
ny
pM°&*
provide an excellent starting point. Among other count ambiguities in estimates of the
199
things, I agree with them that we should seriously and of character change (e.g., Maddison, .
press).
reconsider the need to designate standard Linnean Maddison et al., 1992; Weller et al., in
a
require
ranks, especially in view of the evident temptation Progress in assessing confidence will
erro
of
to treat taxa assigned to the same taxonomic rank better understanding of possible sources ,
e
as though they are somehow Such Albert
equivalent. rank- such as long-branch attraction (e.g.,
more pre-
know
based approaches can lead, for instance, to sys- 994). In particular, we need to
1
spunou-
from
tematic
errors in studies of rates of extinction and cisely how to distinguish real signal
& I* h
]
diversification (Doyle Donoghue, (Hillis et al.,
1993). results. Despite their limitations
u>e
be a
continue to
computer simulations will
^
e
making ss
approach to such questions, it P<>
PHYLOGENIES
IN USE ame
a '
explore a very wide range of possible P
"
&
The
use of phylogenies by ecologists, paleon values Lanyon, 1988; Huelsenbeck
(e.g.,
sue
tologists, biogeographers, molecular Kim Of course,
biologists, con 1993; et al., 1993).
Number 3 Donoghue 413
Volume 81
,
Reconstructing Plant Phylogeny
1994
leave open the critical question of exactly where ent in particular areas of endemism (e.g., Nelson
&
parameter space any particular problem Platnick, 1981; Page, 1991).
in is sit-
uated, but it is nevertheless important to formalize
the universe of possibilities and the impact of crit-
PHYLOGENIES AND POPULATION BIOLOGY
variables.
ical
&
Work known Systematics sometimes portrayed as being
with phylogenies (e.g., Atchley is
1991; 1992) and experimen- neatly separated from population biology, and it is
Fitch, Hillis et al.,
tation with real data sets (e.g., Smith, 1989; Don- sometimes implied that this gap should be main-
&
&
Nixon Wheeler, 1990). This,
oghue 1989; Allard Miyamoto, 1992) tained (e.g., I
et al.,
On
also will be useful. An approach that deserves more believe, is a mistake. the contrary, interactions
promoted
random sequences with population biologists should be ac-
attention the use of nucleotide
is
as benchmarks to help determine whether real se- tively. Such contacts promise to be especially fruit-
quences have retained signal relative to a particular ful in view of obvious mutual concerns centered
phylogenetic problem Miyamoto and Boyle, on the analysis of gene trees and the recent emer-
(e.g.,
&
988;
1989; Wheeler, 1990; Maddison 1992). gence of coalescence theory (Pamilo Nei, 1
et al.,
Hudson, 1990;
1989; Takahata, 1989;
For example, David Maddison and (unpublished Avise,
I
&
Baum Shaw,
1992; Page, 1993a; in
analysis) are using this approach to evaluate the Doyle,
attachment of real outgroup sequences to the Cer- press; Maddison, in press).
alophyllum branch angiosperm based on The application of phylogenetic methods to what
in trees
problems
been population-level
rbcl data (Les 1991; Chase 1993). have traditionally
et al., et al.,
For example,
Is this the true position of the root, or are real is yielding promising results already.
&
Maddison 990) devised a phylogenetic
outgroup sequences so highly diverged that, in Slatkin ( 1
has
effect, they no longer retain phylogenetic infor- measure of gene flow, and Felsenstein (1992)
population
mation? Our show most approached the estimation of effective
preliminary studies that
perhaps
random" sequences (generated under several size from a phylogenetic standpoint. It is
how especially those of
models) also attach to the "long" Ceratophyllum less obvious systematists,
deeper branching
branch. concerned with
Nevertheless, there are some aspects of us primarily
from interacting with pop-
the behavior of real outgroup sequences that de- events, stand to benefit
fundamental
However, several
viate from any of the random sequences we have ulation biologists.
One such
investigated, implying sequences may questions require population-level input.
that the real
estimate of
not be More concern the possibility of a false
entirely devoid
of phylogenetic signal. is
organ-
experiments are needed, more phylogeny based on uniparentally inherited
as are sensitive sta-
&
DNA 1991; Doyle,
Rieseberg Soltis,
tistical
tests. ellar (e.g.,
example,
Increased demands 1992). Whether lineage sorting, for is
interest in phylogenies also
a par-
that we have been an important factor in
develop better ways of making information likely to
and the
about them We depends on population sizes
case
accessible need, ticular
to potential users.
We
m
rec-
events.
short, between splitting
to assemble a database of phylogenetic time intervals
parameters,
important
data and these are the
ognize that
trees (Sanderson 1993). At the
et
al.,
^me values,
time, we means and we know something about their critical
should establish standard for
by population geneti-
epositing based on models developed
phylogenetic data as a co-requisite of
&
1988; see Maddison, in
Pamilo Nei,
publication, now
just as nucleotide sequences are cists (e.g.,
may
be able
routinely Moreover, population biologists
transmitted press).
electronically to repositories
*h parameters in particular cases.
Sl as Genbank On estimate these
(Cinkosky 1991). a to
et
al.,
way
on the in
could bear directly
Practical Ultimately, this
level, such a database would allow sys-
other
with
ematists which organellar data are integrated
to respond phy-
rapidly to requests for
1992).
(Doyle,
genetic evidence phylogenetic analysis
information example, in
in connection, for
be
*'*h from population geneticists also will
conservation Input
Vane-Wright
efforts (e.g., et al.,
such as con-
9 processes
understanding
1 ). Moreover, accessibility of the full range of critical in
^
dynamics underlying the
and the
Phylogenetic certed evolution
studies surely would facilitate the
obvious
of
search paralogous genes, issues
for general patterns; for example, patterns establishment of
Zimmer
et
evels & molecular systematists (e.g.,
of homoplasy Sanderson Dono- interest to
(e.g.,
&
Doyle,
Sanderson
ghue, 1988;
1980; Patterson,
1989),
or in tree shape Savage, 1983; al.,
(e.g.,
phenomena
u & understanding of these
Xer Better
1992).
Slowinski, 1991, 1993). would also
It
and
comparisons,
rev mistaken
guard against
olutionize help
the search for general patterns in will
some
^graphic turn them to our advantage in
allow us to
distributions, by allowing (at least po- will
phylogenies
comparison of
ly) ready For example,
cases.
access to every tree with taxa pres-
414 Annals of the
Garden
Missouri Botanical
may make W. &
based on paralogous genes possible Allard, M. M. M. Miyamoto. 1992.
Perspec-
it
to establish the root of a tree. In fact, this approach tive: Testing phylogenetic approaches with empirical
data, as illustrated with the parsimony method. Mo-
allowed Iwabe et al. (1989) to root the tree of life,
778-786.
lec. Biol. Evol. 9:
despite the lack of obvious outgroups.
W. A
ARCHIE, 1989. randomization
test for phylo-
J.
The ability to compare trees based on both nu- genetic information in systematic data. Syst. Zool.
239-252.
clear and organellar genes obviously has expanded 38:
&
W. W.
ATCHLEY, R. M. Fitch. 1991. Gene trees
our ability to identify hybrids and specify their
& and the origin of inbred strains of mice. Science 254:
parentage 1989; Rieseberg
(e.g., Soltis et al.,
554-558.
Brunsfeld, 1992). Although hybrids have occa-
AviSE, C. 1989. Gene trees and organismal histories:
J.
sionally been discussed by phylogeneticists (papers A phylogenetic approach to population biology. Evo-
& 1192-1208.
in Platnick Funk, 1983; Funk, 1985), detailed lution 43:
BALDWIN, B. G. 1992. Phylogenetic utility of the in-
empirical studies of their impact on phylogeny re-
DNA
ternal transcribed spacers of nuclear ribosomal
construction have appeared only recently (Mc-
in plants: An example from the Compositae. Molec-
Dade, 1992). Nevertheless, botanists should soon 3-16.
Phylogenetics and Evolution
ular 1:
&
play a major role in developing methods for the Barrett, M., M. J. Donoghue E. Sober. 1991.
486-493.
Against consensus. Syst. Zool. 40:
and
recognition incorporation of reticulations in
&
Bateman, R. M., W. A. DiMichele D. A. Willard.
&
phylogenetic analysis (e.g., Rieseberg Morefield,
anatomi-
1992. Experimental cladistic analysis of
in press). Ultimately, what needed a general
is is preserved arborescent lycopsids from the Car-
cally
theory covering reticulations of all sorts (Page, boniferous of Euramerica: An essay on paleobotanical
500-
1993a), including recombination in the case of phylogenetics. Ann. Missouri Bot. Gard. 79:
DN 559.
A
genes (Hein, 990), lateral transfer of Val-
1
( &
Baum, D. A. K. L. Shaw. The genealogical species.
&
dez Pifiero, 1992), and even the fusion of entire &
Ex-
In P. C. Hoch A. G. Stephenson (editors),
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Gard.
velopment of such a theory depends on breaking systematics. Monogr. Syst. Bot. Missouri Bot.
down whatever barriers have tended to separate (in press).
sequence
BREMER, K. 1988. The limits of amino acid
population from
biologists systematists.
Evo-
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data in angiosperm phylogenetic
795-803.
lution 42:
Summary M. Kallersjo, b.
R. K. Jansen, P. 0. Karis,
,
Palmer
Keeley, Kim, H. Michaels, D.
C. K.-J. J. J.
It seems clear that headway has been made in & Wallace. 1992. A review of the phylog-
R. S.
Nordic
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141-148.
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is
& Phylogen>
McLennan. 1991.
Brooks, D. R. D. A. ;
tinued success. It is also clear, however, that many Chi-
Chicago Press,
Ecology, and Behavior. Univ.
basic phylogenetic questions be rather
will difficult
cago.
n
to answer. New morphological and molecular ev- Bull, P. Huelsenbeck, C. W. Cunningham, v.
J. J., J.
Swofford & Waddell. 1993. Partitioning
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5>>s
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384-397.
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