Assessing homology of morphological features in families that contain large
genera is often difficult for several reasons. Such families are frequently
comprised of one or two large genera and several smaller genera. In the larger
genera, rapid species radiation may have occurred, often resulting in diverse
morphologies that are difficult to interpret across the rest of the family.
The situation may be complicated when a well-supported familial phylogeny
is unavailable, possibly due to limited sampling in the smaller genera or from
a lack of phylogenetic signal in rapidly radiating lineages. A primary example
of this situation is the Passifloraceae. This family consists of approximately
17 pantropical genera, the largest of which are the primarily New World
Passiflora L. and Old World Adenia Forsk. Both of these
large genera have floral and vegetative morphologies that are difficult to relate
to the smaller, often monotypic genera in the rest of the family. Passifloraceae
has been traditionally divided into two tribes, Passifloreae and Paropsieae.
Passifloreae is comprised of approximately 12 genera that are primarily climbing
plants with tendrils (MacDougal, 1994). Paropsieae primarily consists of shrubs
and small trees and has been viewed as transitional between Malesherbiaceae,
Turneraceae, and Flacourtiaceae (De Wilde, 1971; MacDougal, 1994; Bernhard,
1999).
The taxonomic circumscription of Paropsieae has been difficult because many
of its characters suggest conflicting familial affinities. While stamen number
does not exceed 10 in the tribe Passifloreae, it may range from five to 20 or
more in Paropsieae, especially in the genera Viridivia and
Smeathmannia (De Wilde, 1971). Very little is known about the primitive
floral condition in Passifloraceae. Bernhard (1999) examined floral development
in members of both Passifloreae and Paropsieae to determine the primitive
androecial condition in the family and to address questions of homology among
the corona and disk structures observed across the genera. The rarity of many
of the smaller genera in Passifloraceae restricted sampling in that analysis,
thus limiting conclusions about ancestral floral character states. Recent
molecular phylogenetic analyses by Alford (2005) on the Flacourtiaceae sensu
lato suggest that the monophyletic tribe Paropsieae is sister to the
remainder of the Passifloraceae. However, a well-supported phylogeny at the
familial level is still unavailable, leaving many unanswered questions about
the evolution of this group.
Passiflora, the largest genus in the family, contains approximately
490 species of vines, lianas, and small trees native to Central and South America,
with approximately 22 additional species endemic to Southeast Asia and the
Austral Pacific. The genus is well-known for the complex and diverse morphologies
observed in both its vegetative and floral organs, but few of these features
have been studied in an evolutionary context. All species have axillary tendrils,
and many species are distinguished by the presence and type of laminar and
petiolar nectaries. Passiflora flowers are characterized by an
androgynophore, one to several series of coronal filaments, five stamens, and
three carpels (Ulmer and MacDougal, 2004). There is a high degree of variation
in floral morphology across the genus, even within small groups of closely
related species (MacDougal, 1994; Kay, 2003; Porter-Utley, 2003). The
morphological details of the hypanthium, coronal filaments, operculum, and
limen are extremely variable in Passiflora. For this reason, it has
been difficult to assess the homology of these organs within the genus and
even more difficult to compare these features to other genera in Passifloraceae
and allied families.
Relatively few studies have addressed the developmental patterns leading
to the complex floral morphology of Passiflora. Payer (1857) was the
first to examine the development of the flower in the hybrid Passiflora
×loudonii. Masters (1871) provided the most extensive treatment
of development and homology in the genus. This work was the first of its kind
to identify and define the morphological features unique to Passiflora.
There has since been little investigation into the nature of these features.
The ontogenetic sequence of floral development in the economically important
Passiflora edulis Sims. and P. quadrangularis L. was
characterized by Moncur (1988), but these are the only complete ontogenetic
sequences available for the genus to date. Bernhard (1994) investigated the
developmental pattern of the corona and operculum in several species of
Passiflora and Adenia. Most recently, Bernhard (1999)
examined the development of the androecium, corona, operculum, and floral disk
in P. racemosa to assess homologies of these structures among the
genera of Passifloraceae.
Within Passiflora, the number of reproductive structures is
generally uniform, with most of the ca. 520 species consistently exhibiting
five stamens and three carpels united on an androgynophore. However, three
Asian taxa, Passiflora tonkinensis W.J. De Wilde, P. moluccana
var. glaberrima (Gagnep.) W.J. De Wilde, and P. siamica
Craib have significant variability in these features. These taxa have between
five and eight stamens and three to five carpels. In P. siamica, the
number of stamens ranges between five and seven, and the number of carpels may
be either three or four. In P. moluccana var. glaberrima,
the number of stamens is either seven or eight, and the number of carpels either
four or five. Passiflora tonkinensis has been documented with seven
stamens and between three and four carpels (De Wilde, 1972a). All other
morphological features in these taxa are similar to the general conditions
observed across the rest of the genus.
In previous hypotheses of relationships in Passiflora,the 17 species
endemic to Asia were thought to be sister to the remainder of the genus
(Cusset, 1968; Tillett, 1988). This was supported by two characters observed
in some of the Asian taxa: the presence of branched inflorescences and the
insertion of additional stamens and carpels in certain species. Branched
inflorescences are common in Passifloraceae, but this feature has been greatly
reduced in Passiflora, suggesting that this might be a plesiomorphic
state in those species retaining this feature. The second hypothesized ancestral
feature, the presence of additional stamens and carpels, is similar to the
situation in the dioecious genus Adenia Forssk.and in the hermaphroditic
Mitostemma Mast., Dilkea Mast.,and Ancistrothyrsus Harms.
Based on these similarities, increased stamen number was thought to be a
plesiomorphic character state in the Asian species.
Krosnick and Freudenstein (2005) showed that the 22 species of Old World
Passiflora are a monophyletic group and supported their current
placement in subgenus Decaloba (DC.) Rchb.supersection Disemma
(Labill.) J.M. MacDougal & Feuillet. Disemma was shown to be
nested within subgenus Decaloba, refuting previous hypotheses that
placed Disemma as sister to the rest of the genus. Additionally, the
morphologically similar supersection Multiflora (Small) J.M. MacDougal
& Feuillet was shown to be sister to supersection Disemma. Within
supersection Disemma, two monophyletic groups were resolved: an Asian
clade spanning India, China, and Southeast Asia, and an Austral-Pacific clade.
While it is now clear that the Old World Passiflora are not sister to the
rest of the genus, their anomalous morphology raises several new issues. De Wilde
(1974) hypothesized that the ancestor of Passifloraceae was diplostemonous or
possibly even triplostemonous. According to his hypothesis, the five stamens
would represent the innermost whorl, while the outer whorls have been reduced
and transformed into the limen that protects the nectary at the base of the flower.
De Wilde proposed that the Asian species retained some members of these outer
whorls, resulting in six to eight functional stamens. Bernhard (1999) refuted
this hypothesis based on both morphological and histological differences between
the secretory cells characteristic of the limen and the true staminodial tissue
in the androgynophore. Moreover, the delayed initiation of the limen until long
after the differentiation of the stamens suggests that these structures are not
likely to be homologous. Thus, at present there is no convincing explanation
for the presence of additional stamens and carpels in these anomalous species. It
is possible that the condition observed in the Asian species is a synapomorphy
for the anomalous taxa, resulting from a unique ontogenetic pathway unrelated
to the polyandry characteristic of other genera in Passifloraceae. Alternatively,
the Asian species may represent a reversal to the plesiomorphic polyandrous
condition for the family.
Material from:
Krosnick SE (2006) Phylogenetic relationships and patterns of morphological
evolution in the Old World species of Passiflora (subgenus
Decaloba: supersection Disemma and subgenus
Tetrapathea). Ph.D. Dissertation, Columbus: The Ohio State
University.