Re-shaping spurge pioneers : circumscription,
taxonomy and phylogeny of Mallotus (Euphorbiaceae
s.s.)
Sierra Daza, S.E.C.
Citation
Sierra Daza, S. E. C. (2007, September 11). Re-shaping spurge pioneers : circumscription, taxonomy and phylogeny of Mallotus (Euphorbiaceae s.s.). Retrieved from https://hdl.handle.net/1887/12308
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This thesis focuses on the tropical genus Mallotus. This genus belongs to the Euphorbiaceae s.s. (spurge family), and comprises c. 110 species. These species are mainly found in (sub)tropical Asia and the West Pacific, with only two species in Africa and Madagascar. Mallotus and its sister genus Macaranga are important components of the forest vegetation of Southeast Asia and show a large variety of life-history strategies (both pioneer and climax species).
Most Mallotus species are shrubs or trees, and seldom climbers. The variable morphology of these species has resulted in three main subgeneric classifications, of which the latest by Airy Shaw (1968) recognizes eight sections.
The study presented here was part of a large project involving ecological, revisional and phylogenetic work on Mallotus. Five of the eight sections of the genus Mallotus were revised in the framework of the Flora Malesiana project (sections Mallotus, Philippinenses, Oliganthae, Axenfeldia and Rottleropsis), hereby provisionally accepting the sectional division of Airy Shaw (1968). The remaining three sections were already revised in a previous study. The monophyly of all eight sections and their evolutionary relationships were analyzed using morphological and molecular data (the chloropast gene matK and the nuclear gene gpd). Finally, the phylogenetic significance of the morphological characters used in the classification by Airy Shaw was evaluated.
What is the circumscription of Mallotus section Rottlera and which species occur in Malesia and Thailand?
During the revisional work on this section, the sectional name Rottlera had to be changed to Philippinenses, because the name Rottlera was found to be an illegitimate, later homonym (Chapter 2). The section is circumscribed based on the presence of alternate leaves with a triplinerved venation and unarmed fruits. The species occur from Pakistan, Southeast Asia to New Caledonia. In Malesia and Thailand five species (out of a total of c. eleven spp.) were recognized: M. leptostachyus, M. pallidus, M. philippensis, M. repandus and M. kongkandae. The New Guinean species M. chromocarpus was excluded from sect. Philippinenses because of its morphological dissimilarity with the other species of the section (stipules absent, extrafloral nectaries prominent with raised margins, anther connectives conspicuously broadened - umbrella-like, and fruits indehiscent). Instead, it was concluded that M. chromocarpus more resembles Octospermum pleiogynum, which also occurs in New Guinea. After finalizing the revisional work of sect. Philippinenses, the type and additional collections of a doubtful taxon, M. philippinensis var. mengliangensis, became available and its taxonomic status was clarified (Chapter 3). This variety from China, was reduced to M. kongkandae, which was thought to be endemic to Thailand.
Re-shaping spurge pioneers246 Summary and Conclusions 247
What is the circumscription of Mallotus sect. Mallotus and which species occur in Malesia?
Section Mallotus is circumscribed based on the presence of alternate leaves with tripli- or palminerved venation, spiny fruits and only one type of hair: stellate hairs. The latter feature is a new diagnostic charcater for the section discovered during this revision.
The section is found from India to Australia and New Guinea. In Malesia four species (out of a total of c. eleven spp.), M. barbatus, M. macrostachyus, M. mollissimus, M. paniculatus, and one variety, M. paniculatus var. formosanus, were recognized (Chapter 4). Mallotus paniculatus var. formosanus is in all its features smaller than var. paniculatus. The Thai species of sect. Mallotus were not included, because they have been treated separately elsewhere (in van Welzen et al., in press).
What is the circumscription of the monotypic Mallotus sect. Oliganthae in Malesia?
Based on a highly supported molecular phylogeny, the monotypic section Oliganthae was transferred to the monotypic genus Cordemoya from the Mascarene Islands (Chapter 5). Additional taxa transferred to Cordemoya were Mallotus section Hancea from Asia and three Mallotus species (M. baillonianus, M. capuronii and M. spinulosus) from Madagascar. In the new circumscription, the genus Cordemoya comprises a total of 17 species and two subgenera (Cordemoya from Madagascar and Mascarenes, and Diplochamys from Asia). Additionally, the subgenus Diplochamys is divided into two sections (Diplochamys and Oliganthae). Palynological and leaf anatomical studies revealed that the genus Cordemoya can be distinguished from Mallotus s.s.
by the presence of pollen with an areolate ornamentation with scabrae (perforate/
microreticulate ornamentation with scabrae in Mallotus s.s.) and capitate glandular hairs with multicellular stalks and sessile peltate-stellate hairs with a central cell (spherical to disc-shaped multicellular glandular hairs in Mallotus).
What is the circumscription of Mallotus sections Axenfeldia and Rottleropsis and which species occur in Malesia, Thailand and Africa?
Sections Axenfeldia and Rottleropsis were proposed by Airy Shaw based on the presence of opposite leaves. The main difference between the sections is in the leaf venation:
pinnate in Axenfeldia and tripli- or palminerved in Rottleropsis. Two phylogenetic analyses based on morphological and molecular data suggested that both sections are polyphyletic (with species from both sections intermixed), and that the venation character is homoplastic. However, both phylogenies suffered from insufficient taxon sampling for the Mallotus clade and from low support for the resulting clades.
In the absence of suitable morphological characters to distinguish between both sections, sect. Axenfeldia was reduced to sect. Rottleropsis s.l. (Chapter 6). However, this section might need further subdivision once a phylogeny with well supported clades is found. In Malesia, Thailand and Africa 44 species (out of a total of c. 68 spp.) were revised and six new species were described: M. connatus, M. longinervis, M. minimifructus M. mirus, and M. spinifructus.
Are the sections as recognized by Airy Shaw monophyletic and what are the relationships among them?
The traditional classification by Airy Shaw subdivided Mallotus into eight sections, Axenfeldia, Hancea, Mallotus, Oliganthae, Philippinenses, Polyadenii, Rottleropsis, and Stylanthus. In its new circumscription (Chapter 5) Mallotus s.s. was formed by excluding sections Hancea (except five species removed from it) and Oliganthae.
Additionally, due to the absence of characters to differentiate the sections Axenfeldia and Rottleropsis, sect. Rottleropsis s.l. was proposed (Chapter 6). The new circumscription of Mallotus was taken as the basis for a study focusing on the phylogeny of the genus in the new sense.
Maximum parsimony and, when appropriate, Bayesian inference analyses were performed with combined macromorphological, leaf anatomical, and DNA sequence data. The macromorphological dataset was gathered from 94 Mallotus species. The samples for DNA sequences and leaf anatomy contained 47-49 Mallotus species.
Blumeodendron, Cordemoya and Macaranga were used as outgroups. Continuously varying quantitative morphological characters were included in the analyses, either made discrete with the gap weighting method or coded ‘as such’ in the program Tree analysis using New Technology (TNT). Support was measured with symmetric resampling (SR).
Although our study revealed several relatively small clades, which are stable in different kinds of analyses and often also were supported by SR, the bigger clades and the higher-level relationships in Mallotus are still ambiguous. This is manifested either by large basal polytomies or highly resolved, but unsupported backbones in Mallotus. Based on the results of the present analyses we have refrained from proposing a formal phylogenetic infrageneric classification for Mallotus. However, we have highlighted clades that could be incorporated in such a classification with their putative morphological synapomorphies.
According to the results obtained, three of the six Malltous sections of Airy Shaw are monophyletic: Mallotus, Polyadenii and Stylanthus. On the other hand, sect. Philippinenses is paraphyletic, while sections Axenfeldia and Rottleropsis are polyphyletic. Additionally, the results indicate that sect. Rottleropsis s.l. as circumscribed in Chapter 6 is paraphyletic. Furthermore, the outcome suggest thats sect. Philippinenses is closely related to sect. Mallotus. Subsequently, the five Mallotus species formerly assigned to sect. Hancea form a clade with sections Stylanthus and Polyadenii together with a few other taxa (e.g., M. cauliflorus and M. brevipetiolatus). In the analysis of the qualitative data with reduced taxon sampling (only those taxa included with complete data, i.e., including molecular, macromorphological and anatomical characters), these three clades are grouped together as well (see Chapter 7, Fig. 5). Finally, other new clades (distinguished with the names Glomerulatus, Subulatus, Resinosus, Wrayi and Tiliifolius) were found.
What is the phylogenetic significance of macromorphological and leaf anatomical characters in the delimitation of the sections and their relationships?
Although total evidence analyses using macromorphological, leaf anatomical, and molecular data did not result in a robust phylogeny of Mallotus, the data set could be
Re-shaping spurge pioneers248 Summary and Conclusions 249
used to test the phylogenetic significance of a large number of morphological characters (Chapter 7). The sectional delimitations of Airy Shaw have been questioned, because they are based only on a few, sometimes insufficient characters. For instance, the evaluation of the morphological characters, showed that the leaf venation character was often not suitable for sectional delimitation. The results of the phylogenetic analyses did reveal different morphological synapomorphies for the clades found.
Section Mallotus is supported by the presence of paniculate inflorescences, pistillo- des, spiny fruits, cork warts, stellate hairs, and the absence of tufted hairs. The clade of sect. Mallotus and three sect. Philippinenses species (M. philippensis, M. repandus and M. kongandae) is supported by the presence of stomata on the adaxial leaf surface, enlarged terminal vein tracheids and the absence of outer cuticular ledges. The grouping of this clade together with M. pleiogynus and allies has as synapomorphy the absence of simple hairs (polymorphic in some species). Additionally, most of the members of this clade have a local hypodermis. In most Mallotus species fruits open first septicidally, then loculicidally. However, in the clade of sect. Mallotus and the three sect. Philippinenses species, the opening sequence is reversed to be first loculicidally, then septicidally, a condition additionally present only in two species (Cordemoya subpeltata and M. leucocarpus) unrelated to this clade.
Two synapomorphies support sect. Polyadenii: domatia on the lower surface of the leaf blade and stomata concentrated under the glandular hairs. The latter is only present in two species outside the section: M. decipiens and M. resinosus. Two species in the section, M. plicatus and M. sumatranus, are grouped together. Their shared synapomorphy, the presence of wings on the fruits, might be an adaptation for wind dispersal.
The five species formerly assigned to sect. Hancea form a clade supported by the presence of anisophyllous leaves. This synapomorphy is almost unique for this clade, and outside it is only present in the central Malesian species M. minimifructus.
Furthermore, our results suggest that this group forms a clade together with sections Polyadenii and Stylanthus together with several other taxa (e.g., M. cauliflorus and M. brevipetiolatus), characterized by the presence of glandular hairs on the upper leaf surface. Sect. Stylanthus is supported by the presence of alternate leaves and the fenugreek smell in dried plants.
Among the additional clades obtained (Chapter 7), the Glomerulatus clade contains species characterized by the unique synapomorphy where the pistillate inflorescences have become reduced to glomerules. The species in the Subulatus clade all have umbel- like pistillate inflorescences (usually the inflorescences in the remainder of the Mallotus species are racemes). The synapomorphy for the Resinosus clade is the presence of persistent stipules. The Wrayi clade is characterized by extrafloral nectaries on the nerves of the upper leaf surface. The Tiliifolius clade is supported by the synapomorphy of stellate hairs, and in contrast to sect. Mallotus that solely has stellate hairs, the stellate hairs of the Tiliifolius clade occur in combination with other hairs. In Mallotus s.s., the presence of simple and tufted hairs is more common than the presence of stellate hairs.
Furthermore, a subclade within the Tiliifolius clade, consisting of M. cambodianus, M didymochryseus, M. dispersus, M. eriocarpus, M. tiliifolius, and M. ustulatus is characterized by having a rough upper surface of the leaf blade (usually smooth in the remainer of Mallotus). Three species in this subclade, M. didymochryseus, M. dispersus
and M. tiliifolius, share a similar wetland and/or coastal ecology. Mallotus tiliifolius is found on the edges of mangroves, swampy areas, sandy areas behind the beach, and M. dispersus is found on sand-dunes behind the foreshore. Mallotus didymochryseus grows in the upper story of mixed primary or secondary alluvial lowland or swamp forest.
Future research
The present revisional work on Mallotus has primarily focused on the species occurring in Malesia and Thailand, only a few from outside these regions have been included.
In order to obtain a better idea of the morphological variability within the genus, the c. 30 remaining species from, among others, India, China, Laos, Vietnam, Cambodia, need to be revised.
A new classification of Mallotus should be proposed. Our phylogenetic results reveal the presence of some clades which are consistent throughout most of the analyses and which are supported by morphological synapomorphies. However, as the general support is low, we still cannot use these phylogenies to propose a new classification. For this purpose it is essential to expand the present dataset on many levels. First, by increasing the taxon sampling with the non-Malesian taxa. For instance, the type species of former section Axenfeldia and section Rottleropsis (respectively from India and Myanmar), have not been included and are considered instrumental for nomenclatoral purposes.
Second, by sampling the used DNA markers and leaf anatomy for additional species (the full dataset included macromorphological data for 94 spp., but for many of these species the molecular and leaf anatomical data are still lacking).
Once the support of the phylogeny is improved and a new classification of Mallotus has been proposed, the evolution of the morphological characters within the genus can be more thoroughly studied. Additionally, an important aspect to be studied is the phylogenetic significance of the pioneer/climax species traits of certain taxa. How did these traits originate? Which state is derived? Finally, biogeographical studies can provide information on how the distribution of the genus took place. Especially, to answer the enigma of why only two species are present in continental Africa, when and how did they arrive there, and to verify the hypothesis which suggests that Africa has been colonized by Mallotus at least two times, both from Asia.
