Botanical Journal of lhe Linnean Sociely (1985), 91: 367-394. With 5 figures
Rusts (Uredinales) of Triticeae: evolution and
extent of coevolution, a cladistic analysis
B. R. BAUM F.L.S. AND D. B. 0. SAVILE
Biosystematics Research Institute, William Saunders Building,
Central Experimental Farm, Ottawa, Ontario, Canada K I A OC6
Received March 1984, accepted f o r publication
Jub 1984
BAUM, B. R. & SAVILE, D. B. O., 1985. Rusts (Uredindes) of Triticeaer evolution and
extent of coevolution, a cladistic analysis. Established evolutionary trends in Uredinales as a
whole are reviewed, and primitive and advanced character? are presented. The rusts of all Poaceae
are presented in a table that strongly indicates Bambusoideae to be the oldest and Pooideae
the youngest subfamily The rusts of Triticeae and their ecogeography are outlined; the rusts of
Cyperaceae, selected as an out-group, are beiefly summarized; and the available characters and
character states for rusts of Triticeae are given. Host alternation complicates the analysis. The
aerial host (never a grass) is ecologically associated with the unrelated telial (grass) host. There are
no appropriate methods to permit analysis of the combined components: aecial host evolution, telial
host e\olution, rust evolution, and their coevolution. Also, several aecial hosts are unknown.
Consequently it was necessary to omit aecial hosts from the analysis. Cladistic analysis of the rusts of
Triticeae was performed using five methods and consisted of cycles of tree analysis and modification
of character state trees. A cladogram put together from a Dollo and a Wagner cladogram was used
as a basis for the classification of rusts given. Subsequently a cladistic analysis of genera of Triticeae,
using presencelabsence of rusts as characters (Brooks’ approach) was performed. T h e Triticeae
dadogram of Baum (1983) was also analysed. Distances between the cladogram generated by
various methods and that of Baum were computed for each possible pair, using the method of
Robinson & Foulds, and then the resulting distance matrix was reduced in dimensionality by
principal components and non-metric multidimensional scaling. The results are discussed in light of
the limitation of the analyses and the data. It is concluded that coevolution is limited and that
frequent jumps to ecologically associated hosts explain the parallelism in evolution of rusts on
Triticeae.
ADDITIONAL KEY WORDS:-Ecology
-
phylogeny
-
Puccinla - Uromyces.
CONTENTS
Contents are numbered to aid cross-references in the text
( 1 ) Introduction .
. . . . . . . . . .
(2) Biology and parasitism of the rust fungi . . . .
(3) Material and methods
. . . . . . . .
(3.1) Rusts of Triticeae: hosts and ecogeography . .
(3.2) Selection of the out-group: the rusts of Cyperaceae
(3.3) Primitive and advanced characters in rust fungi .
(3.4) Rust characters and states . . . . . .
(3.5) Methods of cladistic and other numerical analyses
( 4 ) Results of numerical analyses .
. . . . . .
. . . . .
(5) Natural groups of rusts of Poaceae
(6) Comparative chronology of grass subfamilies . . .
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0 1985 The Linnean Society of London
B. R. BAUM AND D . B. 0. SAVILE
368
(7)
(8)
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(10)
Discussion . .
Conclusions . .
Acknowledgements
References . .
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( I ) INTRODUCTION
Although data from rust fungi (Uredinales) have been variously used to
indicate host plant relationships, as summarized by Savile ( 1979a), there seems
to have been no attempt to compare detailed phylogenetic trees of rust groups
with those of their host plants. After Baum (1983a) had completed a tree for
Triticeae and Savile (1984) had been engaged in a taxonomic revision of the
cereal rusts, such a study became possible. The main aim of this paper is to
document our attempts at elucidating the extent of coevolution between
Triticeae and their rust fungi, by examining the degree of agreement between
phylogenetic trees of hosts and parasites. As a second aim we wished to use data
from the rusts to indicate the relative ages of grass subfamilies. The main aim
was accomplished by using various methods of cladistic analysis, first in our
investigation of parasite evolution and secondly in telial evolution. The second
aim was achieved through using evolutionary sequences in rust fungi to place
the grass rusts in groups of increasing advancement and to tabulate the recorded
grass hosts in these groups.
Following Hennig (Davis & Zangerl, 1966), zoologists have tended to shun
parasite data in taxonomic studies. The frequency of jumps by animal
ectoparasites seems to have been important in rendering parasite data suspect
(Ernst Mayr, personal communication). However, it is certainly true that at
higher taxonomic levels (e.g. host subfamily or above) host plants and
permanent parasites approximately reflect each others’ ages and phylogenetic
relationships. At lower taxonomic levels (e.g. host genus), at least in plantparasitic fungi, jumps to ecogeographically associated plants do tend to confuse
the evolutionary picture, although they may help to establish a comparative,
but not an absolute chronology (Savile, 1971b, 1979a): the groups can be put in
a chronological, but not necessarily evolutionary, sequence.
Before developing a tree for rusts of Triticeae, to aid readers we must: give an
account of the biology of the rusts; discuss primitive rust characters, to establish
polarization of transformation series for cladistic analysis; summarize the rusts of
all Poaceae; and select an appropriate rust out-group.
(2) BIOLOGY AND PARASITISM OF THE RUST FUNGI
The rusts arose from ancestors that have been parasitic approximately as f u
back as there have been land plants (Savile, 1955, 1968a, 1976, 1979a, b). Apart
from their obligate parasitism the rusts are notable for the widespread
occurrence of heteroecism (host alternation): pycnial and aecial spore states
occur on plants ecogeographically but not genetically related to those that bear
uredinia and telia. For example, stem rust of grasses, Pucciniu gruminis Pers.,
forms its pycnia and aecia on Berberis. Nearly all primitive rusts are heteroecious,
but autoecism is increasingly prevalent in advanced genera and clearly derived
from heteroecism (Savile, 1976, 197913).
EVOLUTION OF UREDINALES
369
Rusts normally have closely restricted host ranges, but discordances do occur,
with results that may be merely exasperating but are often informative. It has
long been realized that rusts and their host plants approximately reflect each
others' ages of origin; but this link could not be rationalized until Savile (196813,
1971b) documented a jump by Puccinia palmeri Diet. & Holw. on Penstemon to
Pedicularis, giving rise to Puccinia rufescens Diet. & Holw. Given ample
information on both host genera in the Pacific Northwest it was simplest to
assume that jumps demand evolutionary young parasites and prospective hosts
together with strong ecogeographic overlap. That study showed an evolutionary
sequence of rusts on Cheloneae, a jump from Penstemon to Pedicularis that
indicated the comparative chronology of these genera, and a short progression
on Pedicularis. These conditions maximize the chance of compatible genomes
meeting. Being later in the sequence, the new host will ordinarily be slightly
younger than the original one. At the species level a jump may obscure our
coevolutionary picture, but it also reflects the ecogeography of the hosts. If there
has been no detectable morphological divergence between the rusts on the two
hosts we could infer that the jump was relatively recent; b u t an exact
chronology is usually impossible because rust clans do not evolve at uniform
rates. If speciation by jumps seems surprising, we should remember that
heteroecious rusts change hosts twice per annum. A limitation of the use of rust,
or other parasite, data is that we seldom find parasites on much more than half
the genera of a host group, and this is conspicuously true in this study.
(3) MATERIAL A N D ME'I'HODS
(3.1) Rusts of Triticeae: hosts and ecogeography
As noted in section 6, the relatively recent evolution of the Triticeae and their
rusts means that we are concerned with sea-level fluctuations and climatic
changes rather than continental movements. In our context sea-level has been
critical for the Bering Strait and perhaps the Japan Sea. A conspicuous sea-level
drop in the late Miocene (Hallam, 1981) was probably the first one to open the
Bering Bridge to Triticeae and their parasites. Climatic deterioration in late
Pliocene and repeatedly in Pleistocene times opened the bridge b u t also drove
populations far southward, making a break between those of eastern Asia and
western North America. These climatic fluctuations also must have fragmented
plant, and rust, populations within the continents, notably in mountainous
regions. Most of the Japan Sea is deep, but during the Pleistocene glaciations
the sea gap between Korea and Kyushu was somewhat narrower and the
intervening islands larger, facilitating the passage of plants and their rusts.
Some grass rusts are limited by the ranges of their aecial hosts. Puccinia
montanensis Ellis is restricted in western North America by the occurrence of
Berberis and Mahonia; and P. pattersoniana Arth. is even more narrowly restricted
by the range of Brodiaea douglasii Watson, but some of the grass hosts of these
rusts have a much wider range. Often, the rust is eliminated by climatic
conditions. Rusts tend to be sensitive to climatic change, for they are affected
both directly by the physical changes and indirectly by reduced vigour and
abundance of the hosts. T h e sparser the host density, the smaller is the chance of
the parasite persisting.
We include 16 rusts in this study. These are almost all the rusts known to us
B. R. BAUM AND D. B. 0.SAVILE
370
Table 1. States assigned for all characters of rusts of Triticeae and out-group.
See text section 3.4 for details of characters
Characters
I
2
3
4
5
6
7
8
9
10
Puccinia graminis subsp.
graminicola
Puccinia graminis subsp.
graminis var. stakmanii
Puccinia graminis subsp.
graminis var. graminis
Puccinia striformis
Puccinia triticina
Puccinia hordei
Puccinia recondila
Puccinia coronata
Uromycesfragilipcs
Uromyces turcomanicus
Puccinia montanensis
Puccinia pattersoniana
Puccinia ehmi
Puccinia procera
Puccinia kiusiana
Puccinia asperellae-japonicae
3
1
2
1
2
3
1
1
3
2
3
1
3
1
2
3
1
1
3
2
3
1
4
2
2
3
1
1
3
2
2
3
3
3
2
3
2
1
3
3
3
1
3
2
2
2
2
2
2
2
2
2
2
2
1
2
6
5
6
5
6
6
6
6
5
6
6
1
5
2
2
2
2
1
3
2
3
3
3
3
2
1
1
1
1
1
1
2
1
2
3
3
2
1
1
2
2
2
1
3
3
3
2
3
1
2
3
3
1
1
1
1
1
2
2
1
3
1
1
1
1
1
1
1
1
1
2
2
1
2
1
1
1
1
1
2
1
2
1
4
4
4
4
2
2
1
1
3
3
3
3
4
5
5
5
5
3
3
1
1
Out-group (species of Puccinia
on Cyperaceae)
3
1
2
2
2
1
1
1
1
2
Rusts
I
2
3
4
5
6
7
8
9
10
I1
12
13
14
15
16
to have species of Triticeae as their normal hosts. A few elements of the Puccinia
recondita Rob. complex are omitted because only abundant cross-inoculations
and very detailed morphological study would indicate the valid taxa, published
information being wholly inadequate. There are a few other doubtful reports,
probably based either on ephemeral infection of a triticoid grass adjacent to a
heavily infected non-triticoid, or on misdetermined rusts or grasses (Savile,
1981 ; and section 5). Atypical infections, often resulting from man-made
ecological changes, can have little evolutionary significance.
The rusts are arbitrarily numbered 1 to 16 for ease of reference and named in
Table 1. Their presumptive pre-Columbian geographic ranges are shown in
Fig. 3, and their host ranges and habitats are listed below. Because some of the
grass hosts are important as cereals or forage crops, or are aggressive weeds
(Elytrigia repens ( L . ) Nerski), and some aecial hosts (Berberis, Rhamnus) have been
injudiciously planted for ornamental purposes, several of the Eurasian rusts are
now widespread in North America or elsewhere. Some of the rusts overwinter in
the uredinial state on perennial or winter-annual grasses, and are thus
independent of their aecial hosts.
1. Puccinia graminis Pers. subsp. graminicola Urban: This rust, with urediniospores
more typical of grass rusts than P. graminis subsp. graminis, evidently includes
several biotypes that collectively attack many pooid grasses in several tribes.
One biotype occurs mainly on Ebtrigia, but also attacks Agropyron, Hordeum,
Leymus and Roegneria. This subspecies cannot attack cereals, but the cereal rusts,
P. graminis subsp. graminis, can attack hosts of P . graminis subsp. graminicola,
permitting the occasional formation of somatic hybrids (Savile, 1984).
EVOLUTION OF UREDINALES
37 I
2. Puccinia graminis Pers. subsp. graminis var. stakmanii Guyot, Massenot & Saccas
ex Urban: This rust has spores larger than P. graminis subsp. graminicola but
slightly smaller than P. graminis subsp. graminis var. graminis. Morphologically
identical biotypes attack Avena, and Hordeum and Secale. This rust may have
arisen by hybridization on hexaploid Avena and jumped to adjoining cultivated
Hordeum or Secale. Confirmed triticoid hosts are Anthosachne, Elymus sensu stricto,
Elytrigia, Hordeum, Roegneria and Secale.
3. Puccinia graminis Pers. subsp. graminis var. graminis: This is the largest-spored
and morphologically most advanced member of the stem-rust complex, for
which the classification of Urban (1967) is followed. It is believed (Savile &
Urban, 1982) to have resulted from hybridization on hexaploid Triticum of rust
biotypes adapted to at least two of the diploids that gave rise to the hexaploid.
The main hosts are Aegilops, Elymus and Triticum; but when Triticum is heavily
rusted some infection is found on Elytrigia, Hordeum, Ltymus, Roegneria and Secale.
The interpretation of the origins of the varieties of P. graminis subsp. graminis
infers that they date from incipient grain cultivation, less than 10000 years bp,
for the polyploids were probably scarce prior to their selection by man. Natural
host ranges indicate that these varieties were confined to Eurasia, within the
range of Berberis vulgaris, in pre-Columbian times, but P. graminis subsp.
graminicola possibly reached extreme northwestern North America, using
Mahonia, the only other potential aecial host. All three rusts, with their aecial
and telial hosts, reached eastern North America after European settlement.
When cereals were grown widely in the Great Plains an annual cycle of
urediniospore movements was established. Spores from winter crops in the
extreme south blew northward in spring, later generations finally passing
southward near the Rockies to infect the fall-sown southern crops. Here, and in
Australia and Kenya, P. graminis is thus independent of Berberis. In Europe,
where east-west mountain systems prevent such a circulation, occurrence is
dependent on proximity to Berberis. Rusts 2-3 are adapted to mesic or seasonally
arid grasslands.
4 . Puccinia strizformis Westend.: No aecial host known; overwinters on winter
cereals and perennial grasses. Probably naturally circumboreal; known on
native species of five genera in North America. Recorded on Aegilops, Elymus,
Elytrigia, Hordeum, Roegneria, Taeniatherum and Triticum. Shown, in Canada and
U.S.S.R., to spread from wild grasses to Triticum (Savile, 1984). Adapted to cool
grasslands, and found in low latitudes only at high elevations.
5. Puccinia triticina Eriks.: Basically Eurasian, with occurrence proven on Triticum,
and aecia on old-world (but not new-world) Thalictrum. Now common in
western North America on Triticum with spore circulation as in 2,3. Often placed
in synonymy with 7, but morphologically distinct and genetically isolated
(Savile, 1984). Mesic grasslands.
6. Puccinia hordei Otth.: Basically Eurasian, on species of Hordeum with aecia on
Ornithogalum. Secondarily in North America and elsewhere, surviving by
uredinia on winter barley and perennial species of Hordeum. Mesic grasslands.
7. Puccinia recondita Rob.: Basically Eurasian, confined apparently to Secale,
with aecia on Anchusa, Lithospermum and Lycopsis. Persists on winter Secale cereale
372
B. R . BAUM A N D D. B. 0. SAVILE
in North America and elsewhere. Confusingly, several other rusts have been
grouped with P. recondita. Mesic grasslands.
8. Puccinia coronata Corda f. sp. agropyri.: Basically Eurasian, probably east to
Mongolia. Described from Elytrigia repens, the main host, but occurs under very
favourable conditions (including inoculation) on Agropyron, Hordeum, Roegneria,
Secale and Triticum. It is strongly dependent on the aecial host Rhamnus cathartica
L. Now firmly established in eastern Canada where E. repens and R. cathartica are
abundant. Mesic grassland or parkland.
9. Uromyces fragilipes Tranz.: Widely disjunct: Mediterranean to southern
U.S.S.R., Iran, Iraq, on Eremopyrum buonopartis (Spreng.) Nerski, Hordeum
bulbosum L., H. spontaneum L., Secale cereale L.; and intermontane Idaho to New
Mexico on Hordeum brachyantherum Philippi and H. jubatum DC. Aecial hosts
unknown. A morphologically advanced rust with diasporic teliospores, adapted
to seasonally arid grasslands. The geographic pattern is probably due to
Pleistocene climatic fluctuations. Aecia may be on Allium, which bears several
somewhat similar rusts in both regions, and which apparently reached western
North America in late Tertiary via the Bering Bridge (Savile, 1971a). Uromyces
fragilipes reached North America at the same time on H. brachyantherum or
H. jubaturn. Arid grasslands.
10. Uromyces turcomanicus Katajev.: Southern U.S.S.R. to Israel, Iran, Iraq, range
nearly that of old-world populations of 9, to which it is closely related. O n
species of Hordeurn, Secale montanurn Guss.; aecia on Bellevalia, Muscari (tr.
Scilleae, not native in North America). Arid grasslands.
11. Puccinia montanensis Ellis: North American Cordillera, Pacific Coast to east
flank of Rockies, almost exactly range of aecial hosts Berberis and Mahonia. Some
reports from further east are erroneous, but a few may be from wind-borne
urediniospores. Hosts include Agropyron, Aneurolepidium, Asperella, Elymus,
Elytrigia, Hordeum, Roegneria. Dry to mesic grassland. Presumably evolved in the
region.
12. Puccinia pattersoniana Arth.: North American Cordillera, east flank of Cascades
to west flank of Rockies, s B.C. to N.M. Telia on Aneurolepidium, Elytrigia, Leymus,
Sitanion. Aecia on Brodiaea douglasii only. Range is that of aecial host, some grass
hosts being more extensive. Mesic grassland.
13. Puccinia elymi Westend.: Apparently disjunct: western Europe to beyond
Urals on Leymus arenarius (L.) Hochst., L. giganteus (Vahl) Pilger; and a longerspored variety, Kamtchatka to Japan on L. mollis (Trin.) Pilger. Aecia on
Thalictrum in Europe. The Leymus hosts are mainly on beach sands, which may
partly account for the discontinuity. Leymus mollis and its northern subsp.
villosissimus occur from coast to coast in Canada but have not been found
infected. Both climate and lack of associated aecial hosts may be responsible.
14. Puccinia procera Diet. & Holw.: Widely disjunct: (a) California coastal sand,
on Aneurolepidiurn condensatum (Presl.) Nerski and Leymus mollis, and aecia on
Phacelia and Eucrypta (Hydrophyllaceae); (b) coastal sand of Black, Caspian and
Aral Seas on Leyrnus giganteus, aecia unknown (Hydrophyllaceae absent). The
geographic pattern is very like that of 9, but the coastal sand habitat is
EVOLUTION OF UREDINALES
373
distinctive. The old-world population obviously has an aecial host not closely
related to the California one, which suggests that the separation is not very
recent. The original descriptions suggest some difference between the two
populations; but spore sizes in an isotype of the California rust and a topotype of
the Black Sea rust are not reliably separable. Arenicolous Leymus are
approximately circumboreal.
15. Puccinia kiusiana Hirats. fil.: Endemic in Japan on Asperella japonica Hack.
Aecia unknown. Widespread but rare. Woodlands.
16. Puccinia asperellae-japonicae Hara: Endemic in Japan on Asperella japonica.
Aecia unknown. Known only from type collection. Woodlands. Both 15 and 16
seem to be endemic to Japan, and both are taxonomically isolated. Perhaps
related rusts on other species of Asperella await discovery on the adjoining
mainland. It may be noted that at least one other grass rust, Puccinia rangiferina
Ito, is endemic to Japan, being qualitatively distinct from the population of
P. coronata Cda., on Calamagrostis in China, that has been confused with it.
(3.2) Selection of the out-group: the rusts of Cyperaceae
In order subsequently to determine character polarity by the method of outgroup comparison (Watrous & Wheeler, 1981), the most appropriate candidate
must be chosen from various possible groups. The rusts of other Pooideae have
too many species or species groups in common with those of Triticeae to supply
a meaningful taxonomic out-group. T o choose all the rusts of non-pooid grasses
would involve a very large sample, with many species not personally familiar to
us. We considered taking those of a single subfamily; but the other subfamilies
are predominantly tropical, and the morphological characters of their rusts must
be ecologically induced to a considerable extent. Poaceae and Cyperaceae are
the two main sources of Puccinia sensu lato. (The families of Restionales
commonly considered close to the ancestors of Poaceae are all devoid of rusts.)
Although their parasites are largely different (Savile, 1979a: 462-464) the two
families probably originated nearly contemporaneously (Savile, 1979a). The
rusts of Cyperaceae (including Juncaceae with three shared rust clans), being
much fewer than those of Poaceae, are known in considerable detail, and their
main evolutionary trends are understood (Savile, 1972, 1979a: 479-486); also,
although apparently tropical in origin, they have radiated freely in north
temperate regions. They can thus profitably be compared with those of
Triticeae as a taxonomic out-group (Watrous & Wheeler, 1981).
(3.3) Primitive and advanced characters in rust f u n g i
One trend is seen throughout the rusts, from those on ferns and early evolved
woody dicotyledons, through those on more recently evolved but still mainly
woody dicotyledons and on Poaceae and Cyperaceae, to those on herbaceous
dicotyledons and Liliales: first increased exposure of the teliospores, from
enclosure in host tissues to erumpent crusts or columns; then separation of
individual spores, followed by repeated evolution of spore pedicels, facilitating
liberation of basidiospores formed when the teliospore germinates; and finally
teliospores becoming deciduous (and diasporic) through weakening of the
pedicel. Adding a new diaspore to a non-motile organism is adaptive under any
374
B. R . BAUM AND D. B. 0. SAVILE
conceivable circumstances. This last change is usually followed by nearly even
(rather than apical) wall thickening, development of wall decorations that give
the spores added buoyancy in air, and shifting of germ pores from the ancestral
apical position. The change has been traced in clans of 15 genera in three rust
families, often by two or more release mechanisms in one genus (Savile, 1976:
159- 167). Deciduous teliospores definitely constitute an evolutionary grade, not
a clade (genetic relationship). Only some seven grass rusts out of c. 372 species
have fully deciduous teliospores (Savile, 1979a: 461), and the fact that three of
them attack Triticeae supports the advanced position of the tribe, inferred by
Stebbins (1956: 243).
Other changes that increase exposure of the teliospores, including loss of fused
paraphyses and increased pedicel length, may be regarded as forerunning
teliospore separation. Well-developed fused paraphyses with melanized walls
may enclose groups of teliospores in locules within the host tissue. They seem to
be a reaction to hot and seasonally arid conditions, for melanized walls are
highly impervious to water and other fluids. They are known in both
cypericolous and graminicolous rusts. The cypericolous species occur freely in
tropical and subtropical areas, probably in response mainly to arid savanna
conditions. Early stages in locule evolution are seen in Uromyces
americanus Speg. and U . lineolatus Schroet. on the primitive sections of Scirpus
(sections Actaeogeton and Bulboschoenus) and U . bermudianus Cumm. on Cyperus. In
other rusts of Scirpus, Eleocharis and Cyperus at low to middle latitudes the locules
are fully developed; but in rusts of Eriophorum, Scirpus (sections Scirpus,
Trichophorum, etc.) at middle to high latitudes the paraphyses become few and
scattered or nil; and in the rusts of Carex, Lueula and Juncus, morphologically
advanced in other respects, there are no paraphyses (Savile, 1979a: 479-486). A
few rusts on non-pooid grasses are incipiently loculate without fused paraphyses,
for example Puccinia polysora Underw. on Tripsacum and Zea; but most typically
loculate species are on pooids, and they perhaps evolved in Mediterranean
regimes with arid summers. These 50 or more species, with other correlated
characters, are the P. recondita clan. By evolution on aecial hosts of the complex,
notably Allium and Ranunculaceae, they also gave rise to many autoecious
species. Within Triticeae, and other Pooideae, the current trend is definitely
toward loss of telial paraphyses (and to increased mobility) even in arid
climates.
Urediniospore germ pores are primitively few (usually c. 2-5) and
approximately equatorial in both graminicolous and cypericolous rusts. They
have repeatedly become more numerous (c. 6-10 or more) and scattered in
graminicolous rusts; but they usually remain few and equatorial (or
superequatorial in one group) in cypericolous species, only Uromyces americanus
on Scirpus (Savile, 1972) and Puccinia karelica Tranz. subsp. laurentina Savile
(Savile, 1965) having some spores with six or rarely more pores which tend to be
scattered.
One other uredinial character is significant: the occurrence of clavate to
capitate, apically thick-walled and essentially hyaline, more or less marginal
paraphyses. These unpalatable structures apparently served to protect the
young spores and sporogenous cells from small mycophagous animals (perhaps
mites or Collembola); but as larger mycophages evolved they gave little
protection and were often eliminated (Savile, 1976: 167-1 74). They occur with
EVOLUTION OF UKEDINALES
375
modifications in various genera of Melampsoraceae, and are sparingly carried
over in a few genera of the advanced families Phragmidiaeae, Pucciniaceae and
Raveneliaceae; but they are almost always lacking in autoecious rusts derived
from paraphysate heteroecious ones and in genera with complex morphological
changes that indicate advancement. Paraphyses may be present or absent in
different members of a grass rust clan, in which their presence must be regarded
as primitive because they are nearly always lacking in species with
morphologically advanced telia. However, a few grass rust groups that are
otherwise primitive lack uredinial paraphyses, and these groups probably arose
from aparaphysate ancestors. Significantly all cypericolous rusts lack them.
Only in clans possessing taxa with uredinal paraphyses can we say that their
presence is primitive and absence is advanced.
Some morphological characters that are useful for distinguishing rust species
are of limited value in evolutionary studies because they reflect potentially
reversible ecological conditions. Thus, seasonal aridity favours increased spore
size, increased spore wall thickness and increased melanin deposition in the
walls. These changes govern the passage of water through the spore walls. In
rusts that reinvade tropical rain forest or other humid habitats these trends are
often reversed (Savile, 1976: 174- 176). Increased spore size and wall thickness
are often seen in grass rusts, but the apparent frequence of convergence makes
these characters difficult to use in evolutionary studies.
(3.4) Rust characters and states
Microfungi inevitably have fewer (and often mainly quantitative) characters
than most flowering plants. Aeciospores occasionally yield usable characters, but
the aecia are unknown for four of our species and not available for two others.
There are also interpopulation differences in a few species. It has thus been
impossible to use aeciospore characters in this study.
The arrangement of states for each character in the character state trees
whose descriptions follow was done initially by arranging the various states in
each character tree in the untuitively most plausible and parsimonious sequence
These were then modified after several iterative cycles (see step 2, section 3.5).
Their final configuration is implicit from the cladogram (Fig. 2).
The available characters (1-10) for the rusts of Triticeae and Cyperaceae
are given below with apparent directions of evolution (polarized morphoclines).
Characters 1, 2, 3, 6, 7 and 8 are further discussed in section 3.3, and Table 1
shows assigned states for all rusts.
Available characters
1. Uredinial paraphyses are definitely primitive in many grass rusts notably
on bambusoids) and are progressively lost: common ( 1 ) +occasional
(2)+absent (3). They are always absent in cypericolous rusts and possibly
some grass rust groups never possessed them (see end of section 3.3).
2. Urediniospore germ pore position: equatorial in most cypericolous
rusts; equatorial in many grass rusts, but tending to become scattered.
Equatorial (I)+scattered (2) in both groups.
3. Urediniospore pore numbers. Recognized states, with pore numbers in
parenthesis, are: 1(2), 2(3), 3(4), 4(5), 5(6-8), 6(9 or more). Maximum
376
9. R . BAUM AND D. 9. 0. SAVILE
pore numbers are lower in sedge rusts than grass rusts. Mode state for
primitive sedge rusts is 2(3 pores). The trend in states is 1 t 2 + 3 + 4 + 5 + 6 .
4. Urediniospore size. Medium size (state 2) is predominant, apparently
reflecting average climatic conditions, with small ( 1 ) and large (3) derived
in grass and sedge rusts, l t 2 - 3 .
5. Urediniospore wall. Intermediate thickness and pigmentation (state 2) are
predominant; and thin (1) and thick (3) probably usually derived in grass
and sedge rusts, l t 2 + 3 . As noted in section 3.3, characters 4 and 5 are
subject to change under altered climatic conditions; and they thus have low
value in evolutionary studies.
6. Fused telial paraphyses, forming locules that enclose groups of teliospores.
This character is discussed in section 3.3. It developed independently in
sedge and grass rusts but is dropped in advance species. In our context,
abundant paraphyses (l)+scarce (2)+lacking (3) in grass and sedge rusts.
7. Teliospore wall. Smooth (state 1 ) +sparsely ridged (2)+closely ridged (3)
in grass rusts. Always smooth in sedge rusts.
8. Teliospore predicel. Firm ( 1 ) +deciduous (2). Characters 7 and 8 denote
the achievement of dispersal by teliospores which is strongly adaptive. See
discussion in section 3.3. Pedicels always firm in sedge rusts.
9. Teliospore shape. Clavate shape (state 1 ) predominates in sedge rusts and is
evidently also basic in grass rusts. It may change either to cylindric (2) or
to clavate and ellipsoid, a space-filling combination (3), and finally to
ellipsoid-ovoid (4). 24- 1 +3+4.
10. Teliospore apex. States are: acute-conic ( 1 ), conic-rounded (2), rounded
or subtrunctate (3), digitate (4), rounded unthickened ( 5 ) . Conic-rounded
predominates in sedge rusts. It also seems to be basic in rusts of pooid
grasses, including Triticeae. Acute-conic is common, but not universal, in
rusts of bambusoids; and its occurrence in both rusts of Asperella may be
significant. Possibly it is adaptive in some circumstances, as in piercing the
epidermis over the sorus or in protecting from small mycophagous animals,
the latter being the evident function of digitate apical appendages. The
sequence of states seems to be 1t 2 + 3 + 4 or 5.
(3.5) Methods of cladistic and other numerical analyses
Details of the rust materials found above in sections 3.1 and 3.4. The grass
data are taken from the complete phylogenetic tree of Baum (1983a) simplified
to exclude genera for which we have no rust records.
Two necessary and complementary approaches were used for phylogenetic
inference: (1) out-group comparison (Watrous & Wheeler, 1981); (2) inference
of evolutionary trees by numerical methods (Felsenstein, 1982). The two in
combination are often known as cladistic analysis, the latter as numerical
cladis tics.
The general approach undertaken for the entire study was first to infer
phylogenetic relationships among the rusts of Triticeae themselves. This, we
thought, would be necessary for comparing evolutionary relationships drawn
from the rust character data with the phylogenetic relationships of the rusts
deduced from their paths on the phylogenetic tree of the Triticeae. Thus the
second approach used was to analyse the Triticeae cladogram in terms of the
rusts.
EVOLU'I'ION OF UREDINALES
377
The data matrix of rusts on Triticeae was established by scoring genera for
the presence/absence of each of the 16 rusts studied. Absence was scored as 0,
presence as 1. Thus, in this investigation the rusts are regarded as characters,
following one of the methods of Brooks (1981), since a single monophyletic
group of parasite-terminal taxa is compared with their host group. T h e rusts of
Triticeae are here considered a single monophyletic group, an aspect that
renders the analyses simpler than if they contained several monophyletic groups.
The basis for monophyly is that group 4-14 is essentially confined to Triticeae
(but biotypes of number 8 occur on other pooids), and the species are linked by
unique character states (Table 1 ) . Numbers 1-3 also have biotypes on other
pooids; but they are linked by teliospore morphology to 15 and IS, which are
DATA MATRIXRUST CHARACTERS
I
CHARACTER
STATETREES
I 1-1
,
1
DATA MATRIXRUSTS' PRESENCE
I
OUT-GROUP
ANALYSIS
BINARY
GENERATETREESBY
VARIOUS METHODS
ANALYSE
TREES
I
GENERATETREESBY
VARIOUS METHODS
ANALYSE
TREES
4
I
1
MODIFY
CHARACTER
STATE TREES
COMPUTE
DISTANCES
BETWEEN TREES
CHOOSE BEST
TREES
ORDINATION
OF DISTANCE
MATRIX
ELABORATE
FINAL TREE
ANALYSE
Figure I . Flowchart of operations.
SIMPLIFIED
TRlTlCEAE
CLADOGRAM
\
\/
3
Figure 2: Phylogenetic tree of rusts Triticeae. Numbers in squares: I = Purrinia graminis subsp. graminirofa. 2 = P . graminis subsp. graminis var. sfakmanii. 3 = P . graminis subsp.
graminis var. graminis. 4 = P . sttiifownis. 5 = P. triticina. 6 = P . hordci. 7 = P . recondita. 8 = P . coronalo f. sp. agropyn'. 9 = Uromycesfragilipes. I0 = U. turcomanicus. I 1 = Puccinia monlanensis.
12 = P . pattcrsoniana. 13 = P . elm?.. I4 = P . proccra. 15 = P . kiusiana. 16 = P . aspcrellae-japonicae. Numbers on branch segments: (a) number before colon indicates character number;
(b) numbers after colon indicate state changes with arrow indicating direction; (c) number below bar indicates number of steps on branch segment. Note: number of steps does not
necessarily match straight addition of (b) due to branching of some character state trees.
91-3
12-3
-
/
EVOLUTION OF UREDINALES
379
confined to Asperella. This interpretation is certainly true in the sense that the
Puccinia species on Poaceae are monophyletic.
Analysis I : rust phylogeny
Specifically the following steps were undertaken, outlined in the flowchart
(Fig. 1 ) .
Step I : Summary of characters and character states for the 16 EUs
(evolutionary units) (Table 1) into a data matrix (Table 2). T h e sources of
information for this data matrix cannot be fully or concisely presented.
They derive from cytological, taxonomic, ecogeographic, evolutionary and
coevolutionary studies by Savile since 1936. Much of the background for
the conclusions is given in sections 2, 3.2, 3.3 and 3.4 with pertinent
references.
Step 2: Determination of character state trees. This was done for each
character by placing the various states in the hypothetical evolutionary
sequence. No particular knowledge of transition of one state to another is
assumed. The evolutionary sequence is interpreted as the most plausible
arrangement resulting in minimum transitions from one state to another.
This arrangement was modified a number of times in the course of cladistic
analsyis; see step 7 and initial disposition in section 3.4.
Step 3: Determination of out-group and out-group analysis. For determination
of out-group see sections 3.2 and 3.4. For out-group analysis the method of
Watrous & Wheeler (1981) was followed.
Step 4: Additive binary coding was performed by the method of Kluge &
Farris (1969). Successive coding of the data matrix was necessary after step
7 was performed.
Step 5: The programs used were SOKAL, WAGNER, DOLLO, POLYM, CLIQUE and
MIX, which form part of a package for inferring phylogenies: PHYLIP version
Table 2. Occurrence of rust species in various genera of the Triticeae
Rust species by number
Genera of
7rifrceae
Aegilops
Jgropyron
ilneurolepidium
An fhosachne
Asperella
E!ymus
E!v/rigia
Eremopyrum
Hnrdeum
L<ymus
Rueperia
Serale
Sifanion
7aenialherum
Trificum
I
2
3
4
5
6
7
8
9
I 0 1 1 1 2 1 3 1 4 1 5 1 6
l
0
0
0
0
1
1
0
1
1
1
1
0
0
0
0
1
0
1
0
0
1
0
0
0
l
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
0
0
0
1
1
0
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
1
0
0
0
0
1
1
0
0
0
0
0
0
0
1
0
0
0
0
0
1
0
1
0
1
1
0
0
0
1
0
1
1
0
0
0
0
1
l
1
0
0
0
1
1
0
1
0
1
0
0
1
1
0
0
0
0
0
1
0
0
1
0
0
1
0
0
0
0
1
0
0
0
0
0
0
1
0
0
0
1
0
1
0
1
1
0
0
0
0
1
1
0
0
1
0
0
0
0
0
1
0
0
1
0
0
0
1
0
1
0
1
0
1
0
0
0
0
0
1
0
0
1
0
0
0
0
0
1
0
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
I = present, 0 = ahsrnt.
For hiiiomials of numhered rust species see pp. 370-373.
380
B. R . BAUM AND D . B. 0. SAVILE
2.3 (Felsenstein, Seattle, WA, U.S.A.); CLINCH version 3.0 (Estabrook &
Fiala, Ann Arbor, MI, U.S.A.); and WAGNER 78 (Farris, Stony Brook, NY,
U.S.A.); all on computer tape. Each data matrix was run 10 times in
different sequence of the rows with SOKAL, WAGNER, DOLLO, POLYM and MIX
to increase the possibility of finding the most parsimonious trees, as
recommended by Felsenstein (1982) and knowing that they may well not
yield the minimum length tree.
Step 6: The shortest trees obtained in the preceding step from SOKAL, WAGNER,
DOLLO, POLYM and MIX, and the trees obtained from CLIQUE and C L I N C H
were analysed for synapomorphies and other related details using WAGNER
78. The WAGNER 78 program has an option of analysing any given tree
topology. For this, the following are needed as input: an ancestor function
that describes the tree topology to the program and the data matrix. ‘ l h e
output optionally produces the following: a list of character changes for
every stem, synapomorphies, character lengths, total homoplasy and
detailed homoplasies, total length of tree and stem lengths. The output is
necessary for building the cladogram in detail. The results of these analyses
were especially useful for insight into each of the character state trees,
leading us to the next step.
Step 7: A modification of a character state tree was performed when the
sequence of the states could be changed in such a way as to make it more
compatible with the trees obtained and analysed in the preceding step. This
modification of course resulted in a change of the initial hypothesis from
step 2. The sums of these modifications were tested by repeating steps 4-7
until a number of so-called ‘best trees’ were obtained. Besides modifications
of character state trees, trials with different combinations of threshold
values and weights (Felsenstein, 1979, 1981) were carried out.
Step 8: The choice of ‘best trees’ was based on the following subjective criteria:
(a) Rusts 1-3 are a strongly natural group of which 1, Puccinia graminis
subsp. graminicola, is simplest in morphology and the most typical grass rust,
whereas both varieties of Puccinia graminis subsp. graminis are suspected to
have arisen through hybridization on polyploid early cereals (see section
3.1, and Savile & Urban, 1982).
(b) The rusts of Asperellajaponica, 1.5 and 16, although not very similar, are
closer to each other than to any other rusts of Triticeae; both have
primitive teliospore shapes slightly reminiscent of several rusts of
bambusoids.
(c) The remaining rusts, 4-14, are all members of the P. recondita clan that
is also well represented in other pooid tribes. These rusts are linked in
having numerous scattered urediniospore pores, teliospores with no germ
pores and usually only modest apical thickening, very short teliospore
pedicels (except in a few advanced species), and abundant fused telial
paraphyses (except in the most advanced species).
(d) Puccinia montanensis (11)is linked to U.fragilipes (9),U. turcomanicus (10)
and P. pattersoniana (12) by its advanced teliospore shape and teliospore
apex, but is primitive in possessing abundant uredinial paraphyses and
scanty telial paraphyses. Uromyces turcomanicus, possessing sparse uredinial
paraphyses, is considered slightly more primitive than U .fragilipes and
P. pattersoniana.
EVOLUTION OF UREDINALES
38 I
(e) Species 5-8, 13 and 14 are more typical members of the P. recondila clan
and all relatively closely related.
(0 Puccinia lrilicina (5) and P. recondila (7) differ in abundance of telial
paraphyses, as shown in the tree, have small quantitative differences in all
spore states and have different aecial and telial hosts; they are genetically
isolated but so closely related that pathologists often treat them as formae
speciales of P. recondila.
(9) Puccinia coronala f. sp. agropyri is a population of the P. coronala species
complex whose taxonomy has not been fully unravelled, most of the numerous
host genera being in Agrostideae, Aveneae and Poeae. It is clearly
distinguished by digitate appendages on the teliospores. O u r rust occurs
mainly on Elyfrigia repens, but under favorable conditions (including
inoculation) can attack other genera (section 3.1).
(h) Puccinia elymi (13) and P. procera (14) are a species pair with respectively
no and sparse telial paraphyses and small quantitative differences; both are
mainly on coastal Ltymus and both have strongly disjunct ranges (section
3.1, Fig. 3).
(i) Puccinia hordei (6) is separated from P. striifrmis ( 4 ) by its lack of
uredinial paraphyses and quantitative spore differences; i t seems to be
confined to Hordeum, whereas P. slrizformis attacks several genera (section
3.1).
If no tree is found that fully meets these criteria, select two that together
maximally fulfil the criteria, and are complementary.
Slep 9: The elaboration of the final tree is done from a combination of two
best trees that together meet all the criteria mentioned in step 8. This was
performed by interchanging major branching clades of the two cladograms,
that is combining those major branching clades of two trees at a time to
meet the nine criteria above (step 8) in the combined tree.
Step 10: The final tree thus obtained is then submitted to tree analysis, using
WAGNER 78 as in step 6. T h e final tree is then drawn, with synapomorphies
and character changes as well as binary step numbers per internode.
Analysis 2: lelial hosl phylogeny
Step 11: Elaborate data matrix of presence/absence of rusts on Triticeae as
mentioned above at the beginning of this section.
Step 12: Compute trees as in step 5 above, but without using MIX as there are
no grounds here for employing a combination of Wagner and Camin-Sokal
assumptions. All rusts should equally be considered here in the sense of
knowledge of whether presence is a derived state or that both presence and
absence are unknown to be derived.
Step 13: Analysis of the simplified Triticeae cladogram with the rusts as
characters by using WAGNER 78 as in step 6. This analysis yielded the
evolutionary tree of the rusts parasitic on the various genera of Triticeae.
When the parasite data could not resolve the branching pattern of the
simplified cladogram, the latter was modified further accordingly by
incorporating multifurcations.
Slep 14: The shortest trees from the parsimony methods obtained in step 12,
namely WAGNER, SOKAL, POLYM, DOLLO, and the various CLIQUE trees
obtained in the same step were arranged in all possible pairwise
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EVOLUTION OF UREDINALES
383
combinations. This process included sometimes competing topologies
obtained from using the same method when both trees were of identical
and shortest length. T h e simplified Triticeae tree was of course included in
these pairwise combinations.
Step 15: Compute distances between trees according to the method of
Robinson & Foulds (1981).
Step 16: The matrix of Robinson and Foulds distances was subjected to
ordination by non-metric multidimensional scaling (Kruskal, 1964), by
principal coordinate analysis, PCA (Gower, 1966); and by a combination
of both, that is by using the results of PCA as the starting configuration of
the former. The results that yielded best optimization were chosen to
represent the relationship between the trees in lower dimensions.
Computations were executed on VAX/VMS computer for steps 5 and 12 and
on an IBM 3033 computer for steps 6, 10, 13 and 16 as well as for
compatibility trees obtained using CLINCH running MVS and submitted to the
Systems and Consulting Directorate, Agriculture Canada, Ottawa.
(4) RESUL'I'S OF NUMERICAL ANALYSES
Dctails on the elaboration of the matrix of characters for the 16 EUs
(Table 1 ) were given in section 3.5.
Cladistic analysis was performed according to the methods described. No
single tree with all nine criteria for the best tree was found. It is to be noted that
these criteria are additional to the parsimony criterion mentioned in step 5 in
section 3.5, which was used only in step 8. Two best trees were found that are
complementary in the sense that they had together the desired criteria (see
above): the unweighted WAGNER tree, and the unweighted DOLLO tree. Similar
trccs were found with combination of weights and threshold with the same
methods as well as other methods, but preference was given to the two above as
they are trees with the simplest criteria, that is no weights and no particular
thresholds. Simplicity in this instance is being equated to parsimony.
The combined tree, the final tree after being analysed (Fig. 2), stipulates that
Puccinia graminis is a sister-group to all the other rusts of Triticeae, and has
retained a number of primitive characters in common with cypericolous rusts
(the out-group). These are: urediniospore pores equatorial (character 2, state 1);
urediniospore pores 3 (3,2) in Puccinia graminis subsp. graminicola; teliospore
shape clavate and ellipsoid (9,3); teliospore apex conic-rounded (10,2) (see
Table 4 ) . In both varieties of Puccinia graminis subsp. graminis the urediniospores
are more numerous but still equatorial.
The length of the final tree is 47 steps, little different from the best WAGNER
tree with 45 steps. Homoplasy is rampant in this tree (25) but is little different
from that in the best WAGNER tree (23). However, the sum of pairwise
homoplastic distances in the final tree is 462, substantially lower than the 606 in
the best WAGNER tree.
Character consistencies of the final tree are: 1, 0.35; 2, 1.00; 3, 0.58; 4, 0.29;
5, 0.37; 6, 0.37; 7, 1.0; 8, 1.0; 9, 0.65; 10, 0.83. Consistencies, also known as
(,'-ratios, express the amount of reversal and parallelism. They are obtained by
dividing the range of each character by its total length on the tree. They thus
give an indication of the amount of homoplasy.
384
B. R. BAUM AND D. B. 0. SAVILE
That is characters 2, 7 and 8 are perfectly consistent with the tree and best
reflect this hypothesis; and character 10 is only slightly inconsistent. Character 9
does not reflect the trees as well and causes some homoplasy. The other
characters cause much homoplasy (see the final tree, Fig. 2, and Table 3).
Characters 4 and 5 are readily affected genetically, although not
phenotypically, by climatic change (section 3.3), and thus have little
phylogenetic value although they are useful in distinguishing species. In rust
groups that possess them, characters 1 and 6 reliably indicate the direction of
evolution. Uredinial paraphyses ( 1 ) are, among group A rusts (Table 4),
predominant in species on bambusoids and andropogonoids, and must have
occurred in some of the earliest grass rusts; but perhaps not in all of them for
they do not occur in sedge rusts. Fused telial paraphyses ( 6 ) , although
widespread in rusts of the more primitive Cyperaceae, are in grass rusts
essentially a feature of the large Puccinia recondita clan. Thus, both these
characters arose within the grass rusts rather than being universally present in
the earliest species; and their absence may denote either loss or initial absence.
On the basis of the cladogram (Fig. 2) and analysis of the characters on it, we
wish to propose here a phylogenetic classification of the Triticeae rusts. This
classification is presented in Table 3 together with the characteristics to each of
the nested groups, that is the differential characters and their states.
The data matrix of the presence of rusts on Triticeae (Table 2 ) , when
subjected to various algorithms for inferring trees according to the methods
described, yielded two competing SOKAL trees and three equally likely
compatibility trees.
Pairwise comparisons of the trees, including the simplified host cladogram
(Fig. 4) were done, according to the methods described, and yielded a matrix of
Robinson and Foulds distances (Robinson & Foulds, 1981 ) . Gower ordination
Table 3. Phylogenetic classification of rusts of Triticeae: characteristic of the
groupings (for the characters see text pp. 375-376
Supergroup 1 Puccinia graminis
Urediniospore pore numbers (states 2, 3, 4); teliospore shape (state 3); teliospore apex
(state 2)
Supergroup 2
Urediniospore pore numbers (states I , 5, 6); teliospore shape (states I , 2); teliospore apex
(states I , 3, 4, 5)
Group I Puccinia kiusiana
Urediniospore pore position (state I ) ; urediniospore pore numbers (state I )
Group 2
Urediniospore pore position (state 2); urediniospore pore numbers (states 5, 6)
Subgroup I Puccinia asprrellae-japonicar
Teliospore apex (state 1)
Subgroup 2
'I'eliospore apex (states 3, 4,5)
Grouping 1 Puccinia montanensis, Uromyccs turcomanicur, Uromyccs fragilipcs, Puccinia paftersoniana
Teliospore shape (state 4); Teliospore apex (state 5)
Grouping 2
Puccinia triticina, Puccinia recondita, Puccinia @mi, Puccinia procera, Puccinia
striifrmis, Puccinia hordei, Puccinia coronata
Teliospore shape (states I , 2); Teliospore apex (states 3, 4)
EVOLCTION OF UREDINALES
385
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B. R. BAUM A N D D. B. 0. SAVILE
386
(Gower, 1966) of the latter yielded unsatisfactory results, the first two
dimensions explaining 50% of the variation only. When this was taken as a
starting configuration for input into non-metric multidimensional scaling, the
results in two dimensions were quite unsatisfactory since the stress obtained was
27% and correlation with the original distance matrix was 0.855. In another
attempt the first three dimensions of Gower ordination were taken as starting
configuration, but these did not yield better results in two-dimensional space by
non-metric multidimensional scaling. Therefore, the three-dimensional
representation of Gower ordination was selected as a means of representing the
comparison of trees in three dimensions. In this representation the variation
explained is about 67% and the correlation with the original distance matrix is
0.884. Visual comparison of trees can then be made by means of those results
(Fig. 5). Clearly one of the three possible compatibility trees (9) is closest to the
Triticeae tree (6) which is the simplified tree of Baum (1983a). The next closest
is one of the two SOKAL trees ( 1 ) . This could mean that, if Baum's tree is correct,
then coevolution proceeded in a manner between the evolutionary assumptions
of the two. That is: each character evolved independently; different lineages
evolved independently; the ancestral state may or may not be known for each
character; the true tree has branches which at most are not greatly unequal, so
that two changes in a long segment are more probable than one change in a
short one; it is intermediate in rates of evolution over time so that a 0- 1 change
is not so improbable as in the Camin-Sokal model, but is not as rapid as in the
compatibility model; the reversion 1-0 or retention of polymorphism for both 0
I
(
P
I
+5
+2
Figure 5. Three-dimensional chart comparing trees according to Gower ( 1966) ordination.
1 = SOKAL I; 2 = SOKAL 2; 3 = W A G N E R ; 4 = POLYM; 5 = DOLLO; 6 = BAUM; 7 = CLIQUE I ;
8 = CLIQUE 2; 9 = CLIQUE 3.
EVOLUTION OF UREDINALES
387
and 1 states have low probability but the probability of a single change in a
character is not as low an an incompatible character; and finally the probability
of two changes in a character evolving at a low rate is much smaller than the
probability if it is a high-rate character (Felsenstein, 1979). Most remote from
the Triticeae tree is WAGNER (3), then POLYM (4) and DOLLO (5).
The evolution of the rusts on the tree (Fig. 4) was obtained from the tree
analysis according to the methods described, which included presence/absence
of the rusts as characters in the data matrix. This analysis yielded a total tree
length of 46. The WAGNER tree obtained from the data matrix without tree input
requires a total of 29 steps; both CAMIN -SOKAL trees are 33 steps long; but the
compatibility trees are 39, 35 and 34 steps long.
From the character consistencies i t appears that P. hordei, P. recondita, P. elymi,
P. kiusiana and P. asperellae-japonicae are true to the tree. Other species exemplify
homoplasy at various degrees. In addition, the data are inadequate to resolve
the tree as there are multifurcations (Fig. 4).
(5) NATURAL GROUPS OF RUSTS OF POACEAE
Table 4 shows the distribution of the graminicolous rusts by subfamilies and
tribes, with the grasses arranged horizontally and the rusts vertically, each in
something approaching evolutionary advancement as indicated by comparative
morphology. Figures under each tribe are the species of that rust genus or
group. Figures in parentheses are totals for the grass subfamily or the percentage
of the rust genus or group, as indicated in the headings. The grass outline is
simplified by omission of tribes for which we have no rust records. Rusts omitted
include one each on Centotheca and Phaenosperma, whose subfamial dispositions
are obscure; and several known only by uredinia or telia, whose assignments to
groups are doubtful. A few dubious reports of rusts on improbable hosts are
omitted, as such records are usually based either on misidentification or on
ephemeral infection adjacent to heavily infected normal hosts (Savile, 1979b,
1981).
Although most rusts have a very limited host range, within one tribe or even
one genus, a few rusts of pooid grasses are very wide ranging (Savile, 1979a:
469-470). It is probable that most of these morphological species contain several
populations that do not have wide ranges in nature, although they may infect
members of several tribes in cultivation or by inoculation. For these wideranging species we have arbitrarily allotted one record (i.e. population) per host
tribe. This treatment seems best to reflect what happens in nature, and allows
all host tribes to be shown in the table. O n average this method gives us a close
approach to the numbers of biological species, rather than only broadly defined
morphological ones. The numbers of rust units thus do not correspond exactly
with those of Cummins (1971) whose compilation is the source of much of our
information. In a few instances we have used a narrower species concept than
did Cummins, when host isolation and consistent morphological distinctions
warrant it.
Two of our tribal placements may be questioned. Stipeae, once Milium is
removed, is surely not in Pooideae (Savile, 1979a: 472); it seems best assigned to
Arundinoideae. Olyreae has sometimes been assigned to Bambusoideae or
Oryzoideae. Savile (1979a: 472-474) showed that the species of Puccinia on Olyra
Total per subfamily
Grand total
Puainia
Purcinia
( l'romym)
A. Eq. Par.
B. Eq. Apar.
C. Scat. Par.
D. Scat. Apar.
E. Eq. Ver.
F.-F. (intermed.)
F. S<·at. Ver.
St~uoJtratum
DaJturrlla
Phakop.wra
Phy.roptlla
Rusts
7
2
2
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6
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(I I (0.6)
(4) (6.8)
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(12) 3
(1.9)
(100)
(100)
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Bambusoideae Oryzoideae
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2 2
85
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Arundinoideae
2 I
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6
3 2
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2 4 5
I
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66
5 (12)
19 (24)
(5)
I
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Chloridoideae
(17
(100)
(10)
( 15.5)
(18.6)
(10.6)
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64
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(37)
(4.5)
(4.5)
I 10.31
(60)
(70)
(38)
(3)
(7)
(3)
(II)
(3)
(9)
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34 4
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Panicoideae
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67
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22 28
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(76)
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(49) 155
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I (I) (1.7) 59
2 (12) 11.5) 104
6 (44) (62) 71
"..."'
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5 12
2
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Pooideae
II 5 2 II 34
221 (23) (39)
13 5 (18) (17)
I 2
8 6 4
(10)
(7)
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16) (3.9) 13 20 6
6
3
< . -.:.
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0
Andropogonoideae
Table 4. Numbers of rust species in subfamilies and tribes of Poaceae (see text for details)
""~
EVOLUTION OF UREDINALES
389
are utterly unlike any rusts of bambusoids but very similar to some of Paniceae.
Table 4 also shows that Olyra takes a species of Physopella, of which seven of the
thirteen graminicolous species are on members of Paniceae, but none occurs on
Bambusoideae or Oryzoideae. In view of the resemblance of mature Olyra florets
to large Panicum ones our assignment seems reasonable.
The first four rust genera in the table are in the Melampsoraceae, with telia
much more primitive than in Pucciniaceae, frequently with woody telial hosts,
and with aecia frequently on conifers. Unquestionably the average age of origin
of melampsoraceous genera is substantially greater than that of any Puccinia
species. We see that two small genera are confined to bambusoids; and the
others are on chloridoids, arundinoids and especially panicoids and
andropogonoids. None is on pooids.
Although there is a distinct genus Uromyces (with one-celled teliospores)
attacking Euphorbiaceae and Fabaceae, it and Puccinia (with two-celled
teliospores) in tergrade freely on Poaceae and Cyperaceae; for example
specimens of P. hordei vary from c. 95", two-celled to 95"/, one-celled. Thus, we
group them together for this study. Six informal groups of Puccinia sensu lato are
recognized here. They are nearly the same as the groups with roman numerals
in Cummins (1971); but, because of several small changes, notably in species
limits, we havc lettered them. They have no formal taxonomic status. Groups
A D have typical, sparsely echinulate urediniospores, whereas E and F have
closely verrucose spores. In A and B the urediniospores have equatorial pores
and the sori are with and without paraphyses, respectively. In C and D the
pores are scattered and the sori with and without paraphyses. E and F are
aparaphysate and evidently a natural group. Species in E have equatorial pores,
those in F have scattered pores, and two on Aristideae have pores tending to be
scattered and are clearly close to rusts of Aristideae in group E.
We see that the rusts of Bambusoideae are confined to groups A and B,
especially A. Rusts of Pooideae have one species (1.7%) in the presumptively
most primitive group A, and 12 out of 104 (1 lo/,) in B. I n C and D the rusts of
pooids number 49 and 76 (62 and 49Oh of group totals), the percentage in D
being brought down by a marked radiation in Eragrosteae and Chlorideae. T h e
Puccinia figures thus complement those for melampsoraceous rusts to indicate the
basal position of Bambusoideae and the advanced position of Pooideae. T h e
percentage of rusts attacking Chloridoideae goes up from A to B, C to D and E
to F, suggesting that this subfamily is also relatively modern. T h e figures for
Arundinoideae and Panicoideae are irregular, suggesting intermediate age; and
Andropogonoideae, with a marked percentage drop in all pairs of groups,
probably is second to Bambusoideae in age. Oryzoideae, largely aquatic except
f'or LeerJia, supports too few rusts to be informative.
(6) COMPARATIVE CHRONOLOGY OF GRASS SUBFAMILIES
Plate tectonics supports an early origin of Bambusoideae. Willis (1973)
records Ochlandra from Madagascar, India and Ceylon, and Cephalostachyum from
Madagascar and Indomalaya. Thus, these genera probably originated before
the Indian plate separated from Madagascar some 80 Myr ago (Raven &
Axelrod, 1974; Hallam, 1981). Munro (1868) actually listed four genera with
this pattern, but changed generic concepts since his work and lack of a modern
390
B. R. BAUM AND D. B. 0. SAVILE
world treatment of the bamboos makes a check of his claims difficult. Africa,
apparently due to climatic changes, today has few bamboos, and is weaker in
many other plant groups (Brenan, 1978) than other tropical regions, including
Madagascar (Leroy, 1978). But the ancestors of the South American bamboo
genera presumably reached there via Africa at least 90 Myr ago, before the
South Atlantic became wide, and probably before the origin of the other grass
subfamilies.
Pooideae probably originated in the Tertiary, when the continents were
already in nearly their present positions; and their distributions were governed
more by climatic fluctuations than by plate movements. Triticeae probably did
not arise before the mid-Tertiary. Being predominantly north temperate, as are
most pooids, distribution of Triticeae must have been governed largely by sealevel depressions that opened the Bering Bridge periodically from Oligocene
through Pleistocene times. Cool climates, notably those of the Pleistocene
glaciations, simplified crossing of the equator along the Andes system, for at low
latitudes cooler is equated with drier, and much montane forest must have been
replaced by temperate grassland. Also, sea-level depressions and drier climate
may have allowed limited crossing of the Palaeotropics in southeast Asia.
Marked disjunctions in ranges of some grasses and their rusts must be largely
due to strong climatic fluctuations at high and middle latitudes during the
Pleistocene.
(7) DISCUSSION
Although our study yielded new insights into evolutionary relationships of
rusts and genera of Triticeae by the combination of analytical methods used, the
application of the method of Brooks (1981) is inadequate for such studies. The
rusts studied occur not only on genera of Triticeae (telial hosts) but also on
unrelated aecial hosts (see sections 2 and 3). Coevolution is therefore more
complicated and more difficult to unravel because the ecology and distribution
of the telial hosts are seldom identical with those of the aecial hosts despite
strong overlap. There are thus three interacting factors: telial host evolution,
aecial host evolution, and parasite evolution. In our case telial host evolution
has been estimated by Baum (1983a) independently of the third factor. The
third factor has been considered independently of the first two factors and is
estimated in section 4. Aecial hosts become such through ecogeographic
association with telial hosts; they may be changed as a result of geographic or
climatic shifts, and defy precise evolutionary study; and the aecial hosts of some
rusts are still unknown and perhaps inactive. Only general inferences on
biogeography and ecology of these hosts can be offered (section 3.1). Despite
this attempt, the fact remains that we do not possess adequate analytical tools to
investigate coevolution of rusts and Triticeae completely. The first approach
that we have taken consists simply of attempting to estimate the phylogeny of
the Triticeae by employing rust presence/absence data in cladistic analysis by
different methods. The second approach is to analyse the cladogram for the
Triticeae (Baum, 1983a) with the same data. In the third approach we
compare, by numerical analysis, the relative similarities between the cladogram
for the Triticeae and the other cladograms obtained in the first approach. This
allows us to make inferences on the kind of coevolution that might have taken
EVOLUTION OF UREDINALES
39 1
place, in other words whether the evolutionary assumptions of one or the other
method are most likely. The sort of inferences we wish to make are in the forms
of the following questions: Did coevolution behave with the requirement of
fewest 1+0 changes and at most 0+1 change per character, that is the Do110
model? Did it follow the polymorphism model? Are there other possible models
or assumptions? (See also Felsenstein, 1979.) T h e answers to these questions fulfill
one aspect of the study. As noted above we cannot cope adequately with the
evolution and ecogeography of the aecial hosts, for which tentative conclusions
depend partly on field experience and conjecture.
Rusts, and at least some other plant parasitic fungi, evolve by radiating with
their diverging hosts, by jumping to ecogeographically associated plants, or
occasionally at least (Savile & Urban, 1982) by hybridization, for instance on
polyploids capable of supporting two or more rust biotypes. Almost all grass
rusts are heteroecious, although substantial numbers can overwinter in the
uredinial state on winter-green foliage. Ecogeography of grass rusts is clearly
extremely important. Winter-green foliage is often unavailable in continental
regimes in which winter precipitation is light or unreliable; whereas in moist
mesic regimes, either with mild winters or with reliable snow cover, green tissues
may persist until the new season’s growth has started. In section 3.1 we
summarized the ecogeography of the rusts of the Triticeae, and their
presumptive pre-Columbian ranges are shown in Fig. 3. We showed in section
3.1 that Puccinia montanensis and P. pattersoniana are closely restricted to the
ranges of their aecial hosts; but often climatic restrictions seem to be more
critical.
Many mesic range grasses have wide ecological scope, and can persist
indefinitely in mixed stands. Such grasslands may induce two contrasting trends
in their rusts (Savile & Urban, 1982):
A rust may jump to an ecologically associated grass either closely or
moderately distantly related to the parental host, and after isolation, finally
speciate on it.
If the grassland remains strongly heterogeneous, broadly adapted rust
biotypes may be prevented, by genetic swamping, from becoming closely
specialized.
Thus we may have not only morphologically defined species but individual
biotypes with wide host ranges; Savile (1984) recorded a morphologically
peculiar local biotype of P . strigormis on Elytrigia, Hordeum, Roegneria and
Triticum. Rusts I , 2, 4, I I and I2 are known (section 3.1) regularly to attack
between four and seven genera of Triticeae. Wide host ranges are clearly
commoner, although not universal, in typical grassland than in more specialized
habitats such as sand beaches (rusts 13, 14) and woodland (rusts 15, I6),where
the grass flora is less diverse.
There can be little doubt that jumps between ecologically associated grasses
have been important in the evolution of the rusts of the Triticeae. It is safe to
assume that genetic swamping, through a series of small jumps, is maintaining
the morphological and genetic unity of some of the rusts with wide host ranges.
Where closely related species have diverged, such as Puccinia recondila and
P. Iriticina, the process was presumably initiated in a period of separation of the
hosts. In an ecological context we may regard host extension by jumps as a form
of colonization. Population fragmentation is often slow, and due to climatic
392
B. R . BAUM AND D. B. 0. SAVILE
changes, in regions with low relief; but in regions such as the North Pacific rim,
with high relief and marked tectonic and volcanic activity, breakup may be
rapid and even catastrophic. It is clearly impossible to generalize on speciation
rates.
Ecological changes must affect the evolutionary rates of the grass rusts. In
stable mixed stands of grasses genetic swamping between rust populations must
minimize diversification. But if changed conditions break up the grass
associations a rust population on a newly isolated grass may diverge to the point
of speciation; and, if the climatic conditions are distinctly different either
through actual climatic change or through host migration, morphological and
physiological change may be rapid.
If the host later enters a new stable grassland association, the new rust may
then spread to related grasses with minimal genetic change.
The computation methods for phylogenetic inference used in this study are all
based on the assumption that evolutionary rates in different lineages are equal
and small, and that characters are independent. Felsenstein (1982) has stated
this and made the point that parsimony and compatibility methods would yield
inconsistent estimates of the true phylogeny when these assumptions do not
hold. In fact, in sections 3.1 and 4,we deduce that evolution in the rusts of the
Triticeae has been recent and consequently evolutionary rates have been large.
Furthermore, weights differ among characters; but we do not know the different
weights. We tried various weights, but there is nothing to check against except
for the criteria we set up ourselves in order to justify some of our preconceived
expectations of the rusts’ phylogeny. Baum (1983b) has recently addressed the
problem of weights and the impossibility of finding them with existing methods.
In spite of these and other shortcomings, the existing methods enable us to
make an educated guess at the various issues we have raised. Thus, on the basis
of the phylogenetic tree of the rusts we have proposed a new classification of the
rusts of the Triticeae. Moreover, with all the data available, even though we are
aware of their incompleteness, we were able to deduce that evolution of rusts on
genera of Triticiae might have been following the pattern partly of
compatibility and partly of Camin-Sokal types of evolutionary course. As we
have seen in the computations leading to Fig. 5 , evolution of the rusts on the
tree for the Triticeae (6) is closest to the compatibility (9) and Sokal ( 1 ) trees.
Now, if there has been coevolution it is most likely to have occurred close to
both courses of evolution based on those premises.
The only rust species that are consistent with the tree for the Triticeae are 6,
7,13, 15, 16,judging from the consistencies and as can be seen on the cladogram
(Fig. 4). Of these 7 and 13 are apomorphies. This means that if there was
coevolution at all, as opposed to host colonization (jumping), 6, 15 and 16 are
good coevolutionary candidates. Species 5 , l O and 14 have a consistency index of
0.5. Species 5 might have coevolved on Aegilops, Triticum and Secale, and 10 on
the latter and on Hordeum. The rest of the species either coevolved with an
incipient genus and subsequently jumped to colonize the others or just jumped.
This is difficult to speculate upon. All things being equal, the phylogeny of the
rusts (Fig. 2) is not reflected in their evolution on the tree for the Triticeae
(Fig. 4),probably meaning that colonization was the course of evolution for the
greater part. If strongly mixed north temperate grasslands predominated during
the evolution of Triticeae such colonization was almost certainly important.
EVOLUTION OF C'REDINALES
393
(8) CONCLUSIONS
Coevolution is limited in the rusts of the Triticeae, since a relatively large
amount of parallelism was found in the phylogeny. Jumps by parasites to
ecologically associated hosts is clearly important in temperate steppe grasslands
where various grasses persist indefinitely in association. Such associations allow
broadly adapted rust biotypes to persist indefinitely without speciating,
although speciation may occur if the association becomes broken.
Cladistic analysis is useful for making inferences, including the Brooks
approach to parasites, but it is insufficient because of limitations of the method,
incompleteness of data, and the small number of qualitative characters available
in rusts and other microfungi. Also, there is no method available to analyse
multiple (aecial compared with telial) hosts.
Although this study could not fully achieve its prime objectives, the need for a
thorough analysis of all the grass rusts, summarized in Table 4, provided a
welcome insight into the comparative chronology of origin of the grass
subfamilies.
(9) ACKNOWLEDGEMENTS
We are very grateful for useful comments made by Drs F. J. Rohlf, Stony
Brook, New York, and A. Stahevitch, this institute.
(10) REFERENCES
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