Evolution of a giant genus (II): A phylogenetic case study within Peperomia (Piperaceae)
Final Report Abstract
Systematics, phylogeny and evolutionary biology are terms which are intermingled with each other. Not one single topic can be studied without keeping the others in mind especially when dealing with taxonomic difficult groups due to their species richness. When we started to study the genus Peperomia shortly before the year 2000, Peter Stevens would most likely have had a statement like “Not much is known on the relationships and the evolution of Peperomia” on Angiosperm Phylogeny Web. In 2007, we showed that Verhuellia is not part of or sister to Peperomia as expected, but is revealed as sister to all other Piperaceae, putting character evolution in Piperaceae and in the perianthless Piperales in a different light. It was generally accepted that Peperomia shows the most reduced flowers in Piperales. However, we showed that this is only partially true. As a consequence of the position of the almost equally reduced genus Verhuellia as sister to all other Piperaceae, character evolution with respect to flower morphology and organization in this family and in the perianthless Piperales needed new attention. The androecium at the root node of the perianthless Piperales is hexamerous both without and with the inclusion of Verhuellia. However, stamen number at the root node of Piperaceae differs between the two studies: two with and four without the inclusion of Verhuellia. In contrast to Jaramillo et al. (2004), gynoecial evolution in Piperaceae is not characterized by the reduction from four carpels, as in Zippelia and Manekia, to three in Piper, and one in Peperomia but is trimerous and changes to four carpels in the Manekia– Zippelia clade. The same trend is observed in the Gymnotheca–Saururus clade in Saururaceae and could be interpreted as parallel evolution. This was followed up, investigating in detail the morphology, anatomy and development of the inflorescence as a whole and of the flower, as well as pollen ultrastructure and fruit anatomy in a comparative manner with the other perianthless Piperales lineages. We concluded that Verhuellia is a clearly distinct lineage within Piperaceae as it does not show any intermediate characters between Saururaceae and Piperaceae and that there are only superficial similarities with any other specific group within perianthless Piperales. The inflorescence is an indeterminate spike with sessile flowers, each in the axil of a bract, developing in acropetal, helical succession. Flowers consist of two (occasionally three) stamens with basifixed tetrasporangiate anthers and latrorse dehiscence by a longitudinal slit. The gynoecium lacks a style but has 3–4 stigma branches and a single, basal orthotropous and unitegmic ovule. The fruit is a drupe with large multicellular epidermal protuberances. The pollen is very small, inaperturate and areolate, with hemispherical microechinate exine elements. Unitegmic ovules and inaperturate pollen, which are synapomorphies for the genus Peperomia, are also present in Verhuellia and thus should either be regarded as independent parallel evolution or a reversal to the ancestral state. Not only from a developmental point of view but primarily from a systematic perspective, Verhuellia is a further example of how molecular phylogenetics has helped to understand relationships of the “Tree of Angiosperms” being very much in line with the statement by Peter Stevens mentioned above. The results summarized here had also an impact on the complex historic and partly chaotic taxonomy of Piperaceae, in particular involving Verhuellia. Samain et al. (2008) provided a review of all publications mentioning Verhuellia taxonomy and clarified all nomenclatural obscurities. In addition and as a direct consequence of the molecular phylogenetic findings, the traditional division of the family Piperaceae into two subfamilies Peperomioideae and Piperoideae had to be reconsidered and renamed Verhuellioideae, Zippelioideae, Piperoideae. Beside the family and subfamily level relationships and systematics, much work is still needed below the genus level. E.g. scientists have just started to elucidate relationships based on molecular data, morphological character evolution of the species rich genera Piper and Peperomia – a prerequisite to address questions related to evolutionary biology of the groups, leading to this vast species number (at least 1650 and nearly 2000 species in Peperomia and Piper, respectively. However early on, we realized that research on those genera (here in particular Peperomia) was in need of an infrageneric classification. The classification which was and still is usually adopted is that of Dahlstedt (1900) which divides Peperomia into 9 subgenera, 7 sections and 4 subsections. In 1930, Trealese treated two of Dahlstedt’s sections at the same taxonomic level as Dahlstedt’s subgenera, making a total of 11 primary subdivisions of Peperomia. Later, different authors added a few more subgenera to include some island species. Prior to drawing conclusions derived from aforementioned molecular phylogenetic studies, most of these taxonomic units needed typification and were often in need of the designation of nomenclatural types for names that had not been typified before. Although intensive field work, herbarium studies and lab work has been performed for multiple infrageneneric clades of Peperomia, we have just started to address e.g. biogeographic questions within them. We detected a strong correlation between diversification of a subgenus (Tildenia) and orogenetic events in the distribution centers. In the Andes, distribution was influenced by the Altiplano–Eastern Cordillera System as well as the Amotape-Huancabamba Zone, where the latter served as both migration barrier and migration bridge for different clades within Tildenia. In Mexico, radiation is correlated with the formation of the Trans-Mexican Volcanic Belt. In contrast to most studies of high-elevation taxa which is also the case for Tildenia, we provided support for a south–north colonization towards Central America and Mexico, and provided additional, independent evidence for the latest view on the timing of the Great American Biotic Interchange. The next years will show an accumulation of applying Symmank’s set of methods to many infrageneric monophyletic groups within Piperales lineages.
Publications
- (2007). From forgotten taxon to a missing link? The genus Verhuellia (Piperaceae) revealed by molecules. Annals of Botany 99: 1231-1238
Wanke S., Vanderschaeve L., Mathieu G., Neinhuis C., Goetghebeur P., Samain MS.
- (2008). Verhuellia revisited – unraveling an intricate taxonomic history and a new subfamilial classification of the Piperaceae. Taxon 57: 583-587
Samain, M.S., Wanke, S., Mathieu, G., Neinhuis, C. & Goetghebeur, P.
- (2009). Evolution and systematic value of leaf crystal macropatterns in the genus Peperomia (Piperaceae). International Journal of Plant Sciences 170: 343-354
Horner, H., Wanke, S. & Samain, M.S.
- (2009). Is morphology telling the truth about the evolution of the giant genus Peperomia (Piperaceae)? Plant Systematics and Evolution 278: 1–21
Samain, M.S., Vanderschaeve, L., Chaerle, P., Goetghebeur, P., Neinhuis, C. & Wanke, S.
- (2010). Verhuellia is a segregate lineage in Piperaceae: more evidence from flower, pollen and fruit morphology, anatomy and development. Annals of Botany 105: 677-688
Samain M.S., Vrijdaghs A., Hesse M., Goetghebeur P., Rodriguez F.G., Stoll A., Neinhuis C., Wanke S.
- (2011). Chasing the hare-Evaluating the phylogenetic utility of a nuclear single copy gene region at and below species level. BMC Evolutionary Biology
Naumann, J., Symmank, L., Samain, M-S., Müller, K.F., Neinhuis, C., dePamphilis, C.W. & Wanke, S.
(See online at https://doi.org/10.1186/1471-2148-11-357) - (2011). From the Andean cradle in Peru to the Trans-Mexican Volcanic Belt: the extraordinary journey of the geophytic Peperomia subgenus Tildenia (Piperaceae). Journal of Biogeography 38: 2337–2349
Symmank, L., Samain, M-S, Smith, J.F., Pino, G., Stoll, A., Goetghebeur, P., Neinhuis, C. & Wanke, S.
- (2011). New geophytic Peperomia (Piperaceae) species from Mexico, Belize and Costa Rica. Revista Mexicana de Biodiversidad 82: 357-382
Mathieu, G., Symmank, L., Callejas, R., Wanke, S., Neinhuis, C., Goetghebeur, P. & Samain, M-S.
- (2011). The geophytic Peperomia subgenus Tildenia (Piperaceae) in the Andes with the description of new species in a phylogenetic framework. Plant Ecology and Evolution 144: 148-176
Samain, M-S., Mathieu, G., Pino, G., Symmank, L., Cieza, N., Neinhuis, C., Goetghebeur P. & Wanke S.
- (2012). A comparison of leaf crystal macropatterns in the two sister genera Piper and Peperomia (Piperaceae). American Journal of Botany 99: 983- 997
Horner H.T., Wanke S., Samain M.-S.
(See online at https://doi.org/10.3732/ajb.1200007) - (2012). Growth form evolution in Piperales and its relevance for understanding angiosperm diversification: An integrative approach combining plant architecture, anatomy, and biomechanics. In: Special Issue: Major transitions in angiosperm ecology and functional biology (eds. Field T., Edwards E.). International Journal of Plant Sciences 173: 610-639
Isnard S., Prosperi J., Wanke S., Wagner S., Trueba S., Frenzke L., Samain M-S., Neinhuis C., Rowe N.P.
(See online at https://doi.org/10.1086/665821)
