Table Of ContentVolume 81 Number 2 HaTcour et al. 301
,
Phyllanthus odontadenius
1994
several genera of Compositae [Madia, Layia erale pantropicale, Phyllanthus urinaria L. (Eu-
in
phorbiaceae). Etude du polymorphisme de l'entite
(Clausen, 1951), Microseris (Chambers, 1955), 1 .
P. urinaria et premier essai de classification. Bull.
and Helianthus (Heiser et al., 1962)], in the genus
Mus. Nat. Hist. Nat. Paris, IV. 6 (sect. B, Adansonia
Gilia (Polemoniaceae) (Grant, 1954), and in Clark- 63-74.
1):
&
(Onagraceae) (Lewis Lewis, 1955). 1984b. Elements d'analyse de structure
la — la
— — — — — — —
r *^" m
f^
we des populations de revolution d'une espece rud-
In the Cruciferae find the pattern exemplified et
erale pantropicale Phyllanthus urinaria L. (Eu-
by Hrassica (Yarnell, 1956), in the Scrophulari-
phorbiaceae). 2. Etude de la variation genetique et
aceae by Collinsia (Garber, 1960), in the Sola-
de traduction phenotypique. Bull. Mus. Nat. Hist.
la
naceae by several annual sections of Nicotiana 6 Adansonia 157-191.
Nat. Paris, IV. (sect. B, 2):
(Goodspeed, 1954), and in the Graminaceae HALL, B. M. 1955. Genetic analysis of interspecific
it is
Bromus hybrids in the genus Bromus, section Ceratochloa.
displayed inter alia by sect. Ceratochloa
175-192.
Genetics 40:
Hall, 1955).
&
Heiser, C. B., C. Martin D. M. Smith. 1962. Spe-
cies crosses in Helianthus I. Diploid species. Brittonia
In mature Cited 137-147.
14:
&
Lewis, H. M. Lewis. 1955. The genus Clarkw
&
Buliakd,
J. J. Besse. 1 980. Etude du role des feuilles 241-392.
Univ. Calif. Publ. Bot. 20:
dans un phenomene deux
d'incompatibilite entre tax-
MONNIER, M. 1973. Croissance et developpernent del
ons de Phyllanthus odontadenius Muell. Arg. Bull.
embryons globulaires de Capsella Hursa-pastoris
Soc. Bot. France, 127, Lettres Bot. 5-21.
(1):
cultives in vitro dans un milieu a base d'une nouvelle
&
ItoUNEL, J. F. J. Roux. 1981. Phyllanthus subsect. Mem.,
solution minerale. Bull. Soc. Bot. France, Coll.
Odontadenii
(Euphorbiaceae) au nord du fleuve Con-
179-194.
Morphologique,
go (Afrique de l'Ouest). Willdenowia 11: 69-89. & A
Rossignol, M. Rossicnol R. Haicour. 1987.
L.,
I hambers, K. L. 1955. A biosystematic study of the
Phyllanthus subsection
systematic revision of liri-
annual
species of Microseris. Contrib. Dudley Her- 1853-
naria (Euphorbiaceae). Amer. J. Bot. 74:
barium
(Stanford) 207-312.
4:
1862.
•UUSEN,
1 J. 1951. Stages in the Evolution of Plant Tran Ha, N. M. & L. Bancilhon-Rossignol. 1976.
Species. New
Cornell Univ. Press, Ithaca, York.
mode de reproduction des
Premieres donnees sur Ie
\Rber,
E. D. I960. The genus Collinsia IX. Speci-
Phyllanthus (Euphorbiacees) decoulant d'une etude
ation and chromosome
repVatterninc&. Cytoloeia 25: cytogenetique comparee de six taxons de /'. odon-
233-243.
chromosomiques
tadenius Muell. Arg. a garnitures
I'Oodspeed,
T. H. 1954. The genus Nicotiana. Chroni- =
(2n 12, 24, 28, 56). Rev. Cyt. Biol.
differentes
ca
Botanica, Waltham,
Massachusetts.
201-234.
Veget. 39:
^
A
1954. Genetic and taxonomic studies in & 1976. Analyse mor-
BELLIARD.
J.
Ufca. VI
t
Interspecific relationships in the leafy- comparee de taxons de
biometrique six
phologique et
stemmed
Gilias. Aliso 3: 35-49. odontadenius Muell. Arg. a garnitures
Phyllanthus
97
• 1 1 Plant Speciation. Columbia Univ. Press, (2n = 24, 28, 56)
. chromosomiques differentes 1 2,
New
York. 269-
Rev. Gen. Bot. 83:
descendance.
H et de leur
*icour,R.
1983 La variabilis de compatibility entre
310.
a'vers
taxons de Phyllanthus urinaria L. (Euphor- The genera of Euphorbiaceae
WEBSTER, G. L. 1967.
lacees): Mise
en evidence perspectives ouvertes Arnold Arbor.
et the southeastern United States. J.
in
pour
son
analyse. Bull. Soc. Bot. France 130, Lettres
304-430.
48:
Bot- 207-226.
(3): Cytogenetic the vegetable
Yarnell, H. 1956. <»f
S.
^ 1984a. Elements d'analyse de structure 81-166.
la Rev. 22:
Crucifers. Bot.
crops.
II.
populations
et de revolution d'une espece rud-
EARLY EVOLUTION OF
W. Armbruster 2
Scott
DALECHAMPIA
(EUPHORBIACEAE):
FROM
PHYLOGENY,
INSIGHTS
AND
BIOGEOGRAPHY,
COMPARATIVE ECOLOGY
1
Abstract
Ihilechampia contains over 120 species and occurs throughout the lowland tropics of Asia, Africa, and the Ne*
World. Most species in both the Old and the New World secrete terpenoid resin from large glandlike aggregations
DM
use
of bractlets in the pseudanthial inflorescences (blossoms) and are pollinated by bees that collect resin for in
construction. Using comparative chemical, morphological, and ecological data and phylogenetic analyses, I attempt
character
to ascertain the early evolutionary and biogeographic events that led to the present distribution of species,
states, and pollination systems throughout the tropics. Available evidence suggests the genus originated in western
Condwana or South America in the mid Cretaceous or early Tertiary, respectively, and spread throughout the tropio
by the rafting of land masses, or by migration across higher latitudes when they had subtropical climates, or both.
There is some evidence for two migrational events between the Old and New Worlds. The original pollination system
may The origin
have involved pollination by pollen-collecting insects or by fragrance-collecting male euglossine bees.
the earlie>
of pollination by resin-collecting bees appears to have been a consequence of a preadaptation (exaptation):
Dalechampia apparently used triterpene resins to defend flower parts against attack by herbivores and/or m,cry*^'
bees
and resin secondarily assumed the role of pollinator reward. The mutualistic relationship with resin-collecting
may
have originated independently in the Old and New Worlds.
computer
Trans-oceanic disjunctions of similar plant spe- record. The development of powerful
ho*
cies have intrigued plant biologists since the earliest assisted methods of phylogeny reconstruction,
We retrospective
botanical explorers began to report them. have ever, now makes realistic to attempt
it
evolutionary
long wondered how such disjunctions arose, when analysis of ancient biogeographic and
(see
and how dispersal occurred, and how absence of a fossil record
populations processes in the
b.oge
vicariate
evolved in isolation from each other. Disjunctions Donoghue, 1989). The field of
:»c
• at*
approach in
create natural evolutionary experiments which ography represents one such
in
relations^
two or more populations of similar genetic stock tempt use analyses of phylogenetic
to
ascerta
evolve independently in response to local environ- of several independent taxa as an aid to
distnbuUon^^
An
5ntal conditions. interesting challenge to ing the processes that affected the
is
&
Humphries
unravel the history of disjunctions and reconstruct those taxa (see review in
the evolutionary events that have occurred since 1986).
que^
itiofli
four
the isolation of plant populations. in the present paper I consider ^
c0gr* ru-
P
Research on and b,°6
this topic has rarely proceeded about the early evolutionary
ifJ
|
beyond the phase of description of the distributions events that affected the members of the P*111^^
Where an
of disjunct sister taxa and their taxonomic euphorb genus Dalechampia: (I)
rela-
e>
What ol
tionships. This is because research on historical did the genus originate? (2) series
•'
phenomena, distribution
especially those as ancient as the events led to the present geographical
system*-
creating trans-oceanic and pollination ^
disjunctions, is extremely cies, character states,
system
and
difficult, until recently required a detailed What was the original pollination
fossil
^
L*» ^
.VD..
1 I thank M. Huft and G. L. Webster for organizing the symposium that elicited this contribution,
M
D. Otero for generously providing me with unpublished and M. Edwards, G. Levin, P.
data, E. ' ' B>*
<
aIlt ^
by
an anonymous supported g
reviewer for comments on earlier versions of manuscript. Research was
this
gran
8509031, BSR-9006607, and BSR-9020265 (USA) and a
from Foundation
the National Science
National
(Geographic Society. **
Fairb*1
Fairbanks,
2 Department of Biology and and Alaska-
Wildlife Institute of Arctic Biology, University of
Alaska 99775-0180,
U.S.A.
Ann. Missouri Bot. Gard. 302-316.
81: 1994.
Number
Volume 81 2 Armbruster
303
,
1994 Early Evolution of Dalechampia
how
and
genus, did the early diversification of grance-collecting male euglossine bees (Apidae:
&
pollination systems occur? (4) How, when, and Euglossini) (Armbruster Webster, 1979; Arm-
where did the novel mutualism with resin-collecting bruster et al., 1989; Armbruster et al., 1992).
bees arise? Using the cladistic method of phylogeny These bees apparently use fragrances as precursors
reconstruction, I develop explicit hypotheses ad- in the biosynthesis of sex pheromones (Dressier,
dressing the four historical questions. I evaluate 1982; Whitten et al., 1989). Several species in
the hypotheses by considering independent data on the Neotropics and in Madagascar appear to pro-
the relationships between the plants and their her- duce no reward for pollinators other than pollen;
and
bivores pollinators. these species are pollinated by pollen-collecting bees
and beetles (Armbruster et 1993).
al.,
Dalechampia
Species of are found throughout
Natural History and
Distribution of
New
the lowland tropics of Asia, Africa, and the
Dalechampia
World, although the greatest diversity expressed
is
Dalechampia
is distinctive within the Euphor- in South America (Fig. 1). Species bearing resin
biaceae: the ca. 120 species have pseudanthial glands (and pollinated by resin-collecting bees) are
inflorescences (blossoms) in which usually 3 pistil- by far the most widespread; they occur in every
late flowers and usually 4-16 staminate flowers major region where Dalechampia is found, except
are united into subterminal and terminal cymules, Madagascar. Those species pollinated by male eu-
respectively. Close examination of the Dalecham- glossine bees are necessarily restricted to the Neo-
pia inflorescence, however, indicates that ar- tropics, because euglossines are endemic to the
its
rangement probably homologous New World. Species lacking the resin gland and
is to that of the
inflorescences of Tragia and Plukenetia (although pollinated by pollen-seeking insects are most di-
in these taxa the inflorescences are not pseudan- verse in Madagascar, but are also found in northern
thial, i.e., do not function as single pollination units South America and southern Central America.
&
as in Dalechampia) (Webster Webster, 1972). Several authors have concluded that the gland-
These Madagascar form most
three taxa are also similar in habit. Unlike less species found in the
most other euphorbs, Tragia and Plukenetia com- basal species group in the genus (Michaelis, 1924;
&
prise viny Webster Armbruster (1991)
species and Dalechampia comprises Magin, 1987), while
mostly viny species. Tragia and Dalechampia are considered the glandless species of northern South
also similar in having urticating, crystaliferous America (sect. Rhopalostylis) to form probably
tri-
chomes Mad-
of virtually identical morphology (Webster the most basal group. It is possible that the
&
Webster, 1972). For these reasons, Webster agascan and South American glandless species,
form
(1994) has recently proposed Dalechampia which share numerous characteristics, a sin-
that
be included monophyletic or paraphyletic duster of
in tribe Plukenetieae (with Tragia and gle basal
Dalecham-
Plukenetia) rather than own as species. This raises the possibility that
isolated in its tribe
n
earlier treatments Webster, 1975). The pia has a complex biogeographic history, with
(e.g.,
striking similarities among these three genera and multiple migrations among the continents and in-
their inferred make dependent evolution of the mutualism with resin-
close relationship possible to
it
New World
use, with considerable confidence, Tragia and Plu- collecting bees in the Old and tropics
&
*enetia as candidate outgroups the phylogenetic (Armbruster Mziray, 1987). Alternatively, if the
in
analyses between Madagasenn species and
described resemblance
below.
Rhopalostylis the result of
Respite the relatively uniform blossom mor- members of section is
ology convergence and/or rever-
p n Dalechampia, homoplasy (character
there considerable
i
is
very simple
variation may be no reason to reject a
in the reproductive biology. Most species sals), there
,n involving an origin in the
tn tne biogeographic history
Paleotropics and Neotropics offer resin
as a New World, followed by dispersal to the
P°Ninator reward and are pollinated by female or the Old
° Work
T
er bees that collect resin from a variety of other hemisphere.
ant & Mziray (1987) proposed four al-
P sources and use (Cam- Armbruster
in nest construction
it
roerloher, & hypotheses that could explain
1931; Armbruster Webster, 1979; ternative dispersal
Dalechampia speoes:
Armbruster, & of
present distribution
1984; Armbruster Mziray, 1987). the
»nionp
ne dispersal of l|WCi<
resin long-distance
is secreted by a cluster of modified bract- ) recent
( 1
ffs the migration across mu\- to high-lati-
"resin gland") associated with the sta- continents, (2)
<
when these
gnate & during the Tertiary,
flowers (Webster Webster, 1972). About tude land bridge-
con-
nearly
* dozen species in the New World offer fragrances latitudes had subtropical climates (3) a
mid
18 a western Gondwanan distribution in the
pollinator reward and are pollinated by fra- tinuous
CO
3
Spp.
4
spp.^S
^
/
EQUATOR
o
=•
CD
O
CD
0)
AMI
o
Q
0)
3.
Fu;i)RE Approximate distribution and number of species of Dalevhampia in the Paleo- and Neotropics.
1
.
Number
Volume 81, 2 Armbruster 305
1994 Early Evolution of Dalechampia
to late Cretaceous disrupted by subsequent conti- polarize characters and specify ancestral character
nental drift, and (4) distribution of primitive Dal- states, and the outgroups were eliminated. These
echampia in South America, Africa, and Mada- procedures left unaltered the relative positions of
New
gascar by continental drift, followed by extinction Old and World taxa.
of primitive species in Africa and a second migra- Iterative cladistic runs were conducted to de-
by
tion (either long-distance dispersal or migration termine the sensitivity of cladistic results to initial
more
via higher latitudes) of derived species be- assumptions about character reversibility (Table
2).
tween South America, Africa, and Asia. Circum- varied the assumption of character reversibility
I
stantial evidence they provided supported the sec- (reversible vs. irreversible between plesiomorphic
ond, third, and fourth hypotheses, but not the [primitive] and apomorphic [derived] states) for
first.
They did not attempt to identify the site of origin each of three selected characters, and in all possible
of the genus nor the direction dispersal events. The combinations of the three characters.
purpose of the present study to use phylogenetic then examined each of the numerous maxi-
is I
New
analyses of the and Old World species to mally parsimonious trees to determine the simplest
refine these biogeographic hypotheses and specify biogeographic and evolutionary scenarios that could
possible sites of origin of the genus, directions of explain the distribution of taxa, character states,
dispersal, pollination ecology of the earliest species, and pollination systems and were consistent with
and the site(s) of origin of the novel mutualism the tree. This was accomplished by manually map-
with and ecology data onto
resin-collecting bees. ping distribution pollination
each tree using the parsimony assumption (see
&
Phylogenetic
Inference Maddison Maddison, 992).
1
METHODS
RESULTS
o
reconstruct among
I phylogenetic relationships
Old and New World Dalechampia, When characters were assumed reversible,
species of all
I
436
conducted cladistic analyses on a data set of 46 cladistic analysis of the set of 34 taxa yielded
morphological characters (Table from 25 neo- equally parsimonious trees (120 steps, consistency
1)
=
number
tropical, 4 African, and 3 Madagascan species of index [CI] 0.47). The large oi equally
Dalechampia
the place-
and representatives of two sister parsimonious trees reflects instability in
The
genera, Tragia and Plukenetia, to serve as possible ment of a few similar taxa (Fig. 2). gland
°utgroups (Appendix). The species of Dalecham- characteristics, pollination ecology, and geograph-
pia. were chosen of the various ancestral taxa (nodes
to represent the major species ical distribution
groups in the genus. used the heuristics algorithm of the tree) were inferred by parsimony from the
I
PAUP
of across the ex-
3.0 (see Swofford, 1993) on a Macintosh distribution of these characteristics
&
"Map-
microcomputer Maddison, 1992).
(Maddison
to find the shortest trees. In this tant taxa
analysis onto the consensus tree
ancestral states were not specified ping" of characteristics
(i.e.,
characters were not polarized). Instead, PAUP de- allowed inference of the history of these ecological
abundance
termined Despite the
the ancestral states through global par- and biogeographic features.
simony (Maddison more parsimonious trees, the evolutionary and
of equally
et al., 984), selecting the
1
analysis
Parsimonious of the two sister taxa to be the out- biogeographic implications of this cladistic
g foup. I used MacClade 3.0 (see Maddison & Mad- generally supported Hypothesis 1 (Tabic 3): Dal-
m western
,son, 1992) echampia originated the Neotropics or
to explore alternate tree topologies,
were
a, yze character Gondwana, and the earliest species initially
evolution, assess tree congru-
male eu-
ce fragrance-collecting
with alternative biogeographic hypotheses, and pollinated by either
Produce pollen-collecting insects (Figs. 2, 3).
graphics. glossines or
(pollination)
After an Dalechampia evolved a mutualistic
run taxa
initial with the full set of
Neo-
deluding bees the
the sister genera), eliminated but relationship with resin-collecting in
all
I
°ne member and recently in the genus's evo-
relatively
of each stable, well defined clade of tropics,
species colonized
^tropical resin-reward
species and but two of the very lutionary history a
all
m occurred a migration
ar More there
taxa recently,
1 the paraphyletic section Rhopalo- Africa.
Mad-
The colonic of
Madagascar.
**yti*. This reduced number New World from Africa to
the of
by pollen-
,a * a to and Old World The decreased agascar apparently evolved pollination
1 1 taxa to 4.
nUmber of taxa greatly reduced PAUP run time collecting bees and/or beetles just after they col-
1,11 the Madagascar.
computer. To onized
further educe run times the
i
results o( the reduced set of taxa
of analysis
the Cladistic
initial cladistic analysis were used to
306 Annals
of the
Missouri Botanical Garden
Table 1. Characters and character states used in Table Continued.
1.
"0"
phylogenetic analyses. The character state the
is
ancestral condition, as determined by global-parsimony = =
33. Pollen shape:
prolate; subspherical.
1
outgroup analysis. * indicates character was not used = =
in 34. Seed surface: smooth; =
rugulose; 2
1
the phylogenetic
analysis.
tuberculate.
= =
=
35. Seed shape: round; 3-angled; 2
1 lentic-
=
=
1. Nature of proximal involucral bract: ular; 3 slightly flattened.
stipuli-
= =
form; involucral. 36. Petiole of proximal involucral bract: present;
1
=
=
2. Nature of distal involucral bract: stipuliform; 1 absent.
= = =
1 involucral. 37. Pollen exine: reticulate; 1 psilate.
3. Position of proximal involucral bract: = separated 38. Relative size of pistillate sepals in fruit: = < XA
=
=
from pistillate cymule; 1 adjacent to pistillate capsule length; 1 approximately capsule length;
=
cymule. 2 fully enveloping capsule.
= = =
4. Stipels on proximal involucral bract: present; 39. Stinging crystalliferous trichomes: absent;
1
=
absent. present.
1
Number = Number = 1=4.
5. of basal veins of involucral bracts: 40. of carpels: 3;
3;
=
Number
1 5 or more. 41. of sterile arms in staminate pleiochasium:
= = = =
6. Color of involucral bracts: white to pale green; 0; 1 1; 2 2.
= = = = =
pink; 2 yellow; 3 brown; 4 deep 42. Pollination: pollen-collecting bees (Trigonn
1 green.
= =
Shape
7. of base of involucral bracts: cuneate; workers) or cetoniine beetles; 1 resin-collecting
1
=
cordate. bees (Hypanthidium females, Trigona worker-.
=
=
Shape
8. of tip of involucral bracts: entire, acute; Euglossa, Eulaema, and Eufriesea females); 2
=
lobed. fragrance-collecting male euglossine bees {Euglos-
1
=
9. Persistence of involucral bracts: deciduous sa, Eulaema, Eufriesea).
= = =
shortly after anthesis; 1 persistent into fruiting. 43. Fusion of distal pistillate bractlets: free; 1
Number = =
10. of pistillate sepals: 5-6; 1 >7; 2 connate.
=
= =
4. 44. Presence of leaf stipels: absent; 1 present.
= = = =
11. Margins of pistillate sepals: 45. Leaf nectary: absent; present.
entire; 1 lobed. 1
=
12. Presence of distal pistillate involucellar bractlets: 46. Inflorescence condensation: not condensed; 1
= = =
present; 1 absent. highly condensed.
= =
13. Size of distal pistillate involucellar bractlets: 47. Expression of leaf stipules: well developed: 1
=
=
small, stipuliform; 1 large, enveloping. reduced to absent.
14. Shape of =
pistillate sepals (excluding
lobes):
=
ovate;
linear.
1
=
15. Style shape:
cylindrical
to slightly dilated at
= = =
tip; 1 clavate; 2 strongly dilated at tip; 3 yielded 50 equally parsimonious trees (70 steps,
=
umbraculiform; 4 deeply lobed. = with the
CI 0.61). All of these were consistent
Number = =
16. of stamens: 5-10; >11.
1 drawn
biogeographical and evolutionary conclusions
17. Fusion of staminate =
involucellar
bracts:
free;
(Table 2.
= from of taxa
connate. the analysis of the full set
1
18. Symmetry =
of staminate
pleiochasial arms: Fig. 4).
de-
=
cussate; How char-
1 bilateral. assume that all
reasonable to
is it
Number
19. of staminate =
pleiochasial arms: 4; and backward repeat-
1 acters can evolve forward
D.
an-
structures
edly? expect that
20. Arrangement of staminate = Is it realistic to
bractlets: symmet-
rically distributed; = regained as easily (frequently) as they are 0«
clustered into "gland."
1
may
21. Tip of staminate = = answer
bractlets: acute; 1 truncate. For certain characters at least, the
22. Margins = =
of staminate wit
bractlets: uncomfortable
entire; 1 "no." Upon became
reflection
I
laciniate.
male involuce ).
allowing characters 7 (fusion of
23. Resin secretion by staminate = 1
bractlets: absent;
rese
= 20 and 41 "^
present. (presence of a "resin gland"), (P
1
24. Resin = = revert to the p
color: clear, whitish; 1 yellow, orange; of sterile pleiochasial arms) to
=
=
2 maroon; 3 blue. 436 analys'
siomorphic state as they do in all (first
25. Staminate = =
sepal
color: green parsimony
to whitish; 1 and 50 maximally
(second analysis)
pink.
P°^
im
not
seemed (although
26. Stigma color: = pale to deep green; 1 = pink to trees. It unlikely r
these
maroon. from developmental perspective for
a
= = omorp
27.
Habit: a
vine; 1 shrub. acters to revert from the derived ( P
28. Relative • = Jn
petiole length: >Va (plesiomorphicK^
limb length;
1 condition back to the primitive
<
V limb length. *
U)
character 1 7:
For example, consider
= dition.
29. Leaf shape: =
simple, entire; 1 compound; 2 ^
*
= stam a
simple, 3-5-lobed. er the involucellar bracts of the ^
ding
_^
30. Leaf = = each su
venation: palmate; florescence (pleiochasium) are free,
pinnate.
1
31. Leaf = =
stipules: stipuliform; connate (fused),
1 foliose. a pleiochasial arm, or are
32. Involucral = =
bract
stipules: stipuliform; 1 fo- on outgroup comparisons, the former sta Y
^
liose.
deriv
to be plesiomorphic and the latter
Number
Volume 81, 2 Armbruster 307
1994 Early Evolution of Dalechampia
Table 2. Consequences of varying initial assumptions of reversibility of characters upon the biogeographic/
evolutionary conclusions drawn from the most parsimonious trees obtained by cladistic analysis of the reduced of
list
Numbers
Dalechampia taxa. indicate biogeographic/evolutionary hypothesis(es) with which the most parsimonious
Numbers
trees were consistent (see Table 3). in parentheses indicate the proportion of maximally parsimonious trees
consistent with each hypothesis.
In combination with character
Character assumed irreversible Alone 20 41 17,20
oo%y
17. Fusion of staminate bracts 2 (96%)' 3 (60%)2 3
1
(
4 (3%) 3 (33%)
2,
3,4(1%) 5 (4%)
5 (4%)
2,
20. Presence of resin gland or vestige 3 {607oY 3 00%)>
its 1
(
5 (33%)
3,
5 (4%)
5 (4%)
2,
3(100%>'
41. Presence of sterile arms in staminate 3 (100%)'
pleiochasium
Non<
(100%)4
1
N
252
equally parsimonious
trees
N
114
equally parsimonious
trees
42
equally parsimonious
trees.
•N
50
equally parsimonious
trees.
96%
though the shift to the connate condition may not 252 maximally parsimonious trees, of which
be expected to occur frequently, seems even less supported H, (Table 2). In this hypothesis, Dale-
it
ikely that the connate involucre would up into champia originated in the Neotropics or western
split
the "correct" number Gondwana, a glandless stock colonized the Paleo-
of bractlets, in the arrange-
ment that recreates the original relationship be- tropics (by the breakup of Gondwana or migration
tween bracts and pleiochasial arms. Thus there via higher latitudes), the mutualism with resin-
if
uom
,S oplasy in this character, seems more likely collecting bees originated in the Neotropics, fol-
it
to reflect convergence than lowed by one or more additional colonizations of
reversal.
New
he assumption of irreversibility was applied to the Old World from the by gland-bearing
each
of these characters turn and possible (resin-producing) species (Fig. 6).
in in all
combinations. The cladograms from the seven dif- All other assumptions and combinations of as-
ferent runs of characters yielded
generated hypotheses and 4 sumptions of irreversibility
3, 2, 5,
* order supported H cither or most
of frequency (Tables 2, 3). By far the shortest trees that all
t
most commonly H„ Thus appears that the
supported hypothesis was with of the time (Table 2). it
hypotheses
a biogeographic/evolutionary
distant second. For example, the assumption most likely
2
a a H„ and H Which of these one favors
sterile pleiochasial arm cannot readily be- are H,,
.
2
come on whether one assumes char-
fertile again 42 depends not only
resulted equally parsi-
in
monious trees that support H Dalechampia acters in general are reversible or irreversible, but
all
3 :
combination
gmated character or
in the Neotropics or western Gondwana, also on which particular
Assump-
* glandless lineage colonized the Paleotropics (by of characters are assumed irreversible.
characters
e reakup of certain
of Gondwana about the irreversibility
or migration via higher tions
conclusion
on biogeographic
t|todes), mutualisms have stronger effects
with resin-collecting polli-
^tors assumptions of irreversibility
evolved New That
separately Old and than others. is,
in the
()r|c, >. followed by recolonization of the Neotrop- of certain characters appear to be dominant, in
,
The "pecking order"
Old World over others.
y gland-bearing (resin-producing) their effects,
>
Character
species, Character 41
Table 2
extinction of the glandless species from apparent in is
of Africa, and Madagascar 20 > Character 17.
their persistence in
from
dens.
hypotheses
phylogenetic m
of the I
All
Tr two bas.e conclusions.
analyses lead to
,e assumption
staminate the cladistic
that the fusion of
or
aC,s the .tropics
Dalechampia originated in IS
ls lrreversible, when taken alone, produced (1)
308
Annals of the
Missouri Botanical Garden
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I
I
DISTRIBUTION
NEOTROPICS
HS
AFRICA
TreeLength: 117
PANTROPICAL
equivocal
Figure
2. Consensus tree for set of 32 Dalechampia species and two candidate outgroups (Tragia and Plukenetia)
based on assumption that all characters are reversible. Taxa with unstable arrangements in the 436 maximally
parsimonious
trees are indicated by polytomies
(points of branching of more than two taxa).
western Gondwana. The
(2) earliest species were specialist herbivores on dalechampia
pollinated by
pollen-collecting
insects or fragrance-
nymphalid butter-
There are several genera of
collecting male
euglossine
bees. Uncertainty
re-
fohvores
mains as to when and which flies whose larvae appear to be specialist
in direction
dispersal
The phr
on New and Old World Dalechampia.
between New
the Old and Worlds
occurred.
New an
among
the
logenetic relationships
abou
World may give us some clues
Tests of Hypotheses butterflies
migration-
the history of their and their host plants'
There
are several sources of independent data among and Paleotropics.
the Neotropics
that could be used folivor*
to evaluate the biogeographic/ Assuming Dalechampia
that specialist
evolutionary hypotheses make ^ e
generated by phylogenetic feed only on Dalechampia, one can bt
re£
analyses. These
include information on phylogenetic
the rela- specific predictions about the
Wor *
among
tionships specialist insect herbivores on Old tionships between those of the New and Old
New
and World us
Dalechampia,
scenario
the chemical de- depending on biogeographic
the
fense systems Dalechampia (U
that
uses against her- account present distribution.
for their
bivores, details of from the
pollination biology of Old and Dalechampia
initial dispersal of
New
World
Dalechampia, distanCe
and
morphological de- World to the Old occurred by long" ^-
r
tails of the resin gland of Old and New World achieved close to
persal after the continents
m
species.
herbivores
present positions, the butterfly
Number
Volume 81 2 Armbruster 309
,
1994 Early Evolution of Dalechampia
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BBBBBBBBBDBBBH
BEE
D G D D D
TreeLength: 117
POLLINATION
POLLEN-COLLECTING INSECTS
BEES
RESIN-COLLECTING
BEES
FRAGRANCE-COLLECTING
equivocal
Figure Same mapped onto the branches.
3. cladogram as is in Figure 2, with pollination systems
Old and New Worlds tinuous population of the herbivores to also disperse
should be completely unre-
from
ated. This is because extremely unlikely that into the Old World. (3) If the initial dispersal
it is
tn host plant and herbivore would have become the New World to the Old occurred by a continuous
established in the Paleotropics by long-distance dis- population being split into two or more populations
breakup
persal from New apart of the continents (the
the World, and Old World by the rafting
the
New
Old and
herbivore fauna would more likely be the result of of Gondwana) in the Cretaceous, the
members of the local butterfly fauna evolving to World herbivores should again be sister taxa, but
eed second scenario.
f on Dalechampia. not as closely related as in the
the dispersal
(2) If initial
from the New World There some ecological information available
to the Old occurred by mi- is
Dalechampia
on
gration of a semi-continuous population stretching on butterfly herbivores that feed
&
Armbruster
across Armbruster, 1983;
North America and Europe or Asia in the (Table 4; see
early to mid 1987; DeVries, 1987). Unfortunately there
Tertiary, when these continents had Mziray,
on
available their
subtropical information
not yet detailed
climates, the butterfly herbivores in the is
The systematic (Table
Id World phylogenetic relationships.
should be taxa of
closely related sister
New available
e World and phylogenetic information that is
species. This because a semi- 4)
is
between
e°ntinuous phylogenetic relationship
indicates a close
population across the
of host plants
two
forming
New World possibly
'fcner latitudes should have allowed a semi-con- Old and taxa,
310
Annals
of the
Missouri Botanical Garden
Table 3. Five most parsimonious biogeographic hy- World could be derived from Tragia
-feeding
an-
potheses derived from the cladistic analyses under varying
cestors. In this case phylogenetic
relationships
assumptions about character
reversibility. among may
lepidopteran herbivores
yield insights
into the biogeographic history of Tragia,
but not
H, The genus and the resin-collection mutualism
Dalechampia.
of
New
originated in the World, with a subse-
quent migration to the Old World from the
EVOLUTION OF THE RESIN REWARD SYSTEM
New
and the loss of the resin-collection mu-
Madagascan
tualism in taxa. How
likely that an unusual pollination
is it sys-
H
The genus originated in the New World or tem such as pollination by resin-collecting bees
western Gondwana; an
migration
initial (or
could have originated more than once within Dal-
rafting) to the Old World from the New
echampia? Elsewhere kingdom
the plant has
in
it
was followed by the evolution of the resin-
apparently originated only one other time, in Clusia
New
collection mutualism in the World, and
(Guttiferae) (Armbruster, 984). Therefore, seems
1 it
then by a second migration to the Old
World by gland-bearing at first highly unlikely that pollination by resin-
species.
collecting bees would have arisen multiple times in
H, The genus originated in the New World or
Any
the genus. biogeographic scenario invoking
western Gondwana; an
migration
initial (or
rafting) to the Old World was followed by this would also seem improbable. Consideration of
how makes
the independent evolution of the resin-col- the system arose, however, multiple
lection mutualism in Old and New Worlds, origins of the relationship seem more probable.
followed by a migration of gland-bearing
New
species to the World from the Old.
Table and
4. Provisional phylogenetic classification
H, The
genus and the resin-collection mutualism
host-plant associations of lepidopteran herbivores feeding
New
originated in the World, followed by a
on Dalechampia and related genera. Systematic rela-
migration
of gland-bearing species to the
tionships and host plant information from Jenkins (un-
Old World,
loss of the mutualism Mada-
in
&
published manuscript), Armbruster Mziray (198.).
gascar, and
finally recolonization of the
Ackery (1988), Otero (1990), and D. Lees (unpublished
New
World
by
gland-bearing
species.
data).
H, The genus and
the resin-collection mutualism
New
originated in the World, followed by
Neotropics Paleotropics
two or more migrations
of gland-bearing
Nymphalidae
species to the Old World and subsequent
recolonization of the New World by Subfamily Eurytelinae
gland-
bearing species. Tribe Neptini
Neptis{T, A, others)
Tribe Eurytelini
groups Biblis (T) Byblia (D, T, P)
with vicariant genera
in both areas (Jenkins,
Mestra D) Mesoxantha (T)
(T,
unpublished &
manuscript; Armbruster
Mziray,
T)
Neptidopsis (D,
1987; Otero, 1990; Ackery,
1988). This
obser-
Ariadne (T, R, D,
vation generally supports
the predictions of the
Te, Ac)
hypotheses of early Dalechampia
"migration" by D, Te)
Eurytela (T, R,
continental and
drift migration
in the Tertiary via
Tribe
Epicaliini
higher
latitudes. It does not support the hypothesis Hamadryas Sallya (D, T, others)
of recent
long-distance
dispersal (see Armbruster (D,T)
&
Mziray, 1987,
for additional discussion). Thus Ectima (D)
the evidence from
the relationship among Panacea (D??)
the
lep-
idopteran
herbivores of the Old and New Worlds Batesia (D??)
supports Catonephele
the hypotheses show
that a fairly early
colonization of the Old World from New. (A, D, V)
the
Myscelia Ad)
The (D,
observation many
that of the lepidopterans
Nessaea A)
(P,
that feed on Dalechampia may
sometimes
also
Tribe Dynamini
feed on Tragia
(Table however,
4), raises another
Dynamine
(D, T)
possibility.
It is possible that Tragia and
her-
its
= Mchornia.^'
A
bivores achieved a pantropical 1 Abbreviations for host plants:
distribution prior to
= Y
=
D Dalechampia.
Acalypha, Ad
Dalechampia. Adelia,
were
If this true, then the lepidop- = Telracarp^-
=
R T Te
-Tragia,
kenetia, Ricinus,
now
terans
specializing on Dalechampia
=
in the Old V
Veconcibea,
