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Pollinator-driven speciation in painted petal irises

Félix Forest
28 February 2014

Félix Forest, Head of Molecular Systematics at Kew, describes the co-evolution of pollinators and painted petal irises in the Greater Cape of South Africa.

It was on the way to Nieuwoudtville, a small town about four hours drive north of Cape Town in the Northern Cape Province of South Africa, that I first witnessed the elegance of long-proboscid fly pollination. The graceful fly I saw was hovering above a clump of cream-coloured flowers, with its long proboscid dangling straight beneath it, delicately inserting it down the equally long floral tube of a Lapeirousia species to reach the sweet nectar contained at the bottom of its flower. The wonder of this first encounter remained with me and has fuelled the particular interest I have for the evolution of pollination systems and their role in driving the formation of new plant species. Understanding the evolution of plant-pollinator associations is essential for their long-term conservation, particularly at a time when pollinator decline and its impact on biodiversity as a whole and ecosystem services is becoming increasingly critical.

Long-proboscid fly pollination is relatively common in the Cape and Namaqualand. Several species of fly are involved in this mutualism with a multitude of plant species, but many more weird and wonderful pollination modes are found in this biodiversity hotspot, which has been a focus of my research for many years. The Greater Cape Floristic Region of South Africa is a small area home to more than 9,000 species of vascular plants, of which about 70% are found nowhere else on Earth. The adaptation to different pollinators and the presence of a large number of specialised pollination systems has been hypothesised as one of the main factors promoting the formation of new species in this region.

Photo of Lapeirousia dolomitica

Lapeirousia dolomitica, pollinated by long-proboscid flies from the family Nemestrinideae

Many scientists have considered pollinators as potentially playing an important role in the diversification of flowering plants, including Charles Darwin who came to this conclusion after studying pollination in orchids. Considering the diversity of pollination syndromes and the incredible diversity of floral forms and colours observed in some plant groups, it becomes difficult to ignore the fact that pollinators may play a fundamental role in the speciation process in several of these plant assemblages.

To explore the role of pollinators in speciation, my colleagues and I turned our attention to the iris family (Iridaceae). This group of plants is well-known, due to its ubiquitous presence in our gardens and in the cut-flower displays in shops and supermarkets. Iris, Gladiolus, Freesia, Crocosmia, and Crocus are probably the best-known genera in horticulture, but many more have made their niche in the gardener’s world. The family is particularly well represented in sub-Saharan Africa, with no less than 1,200 of the 2,000 species the group comprises found in this region. What makes this family even more attractive for those interested in the evolution of pollination systems is that no fewer than 17 different pollination systems have been reported in this group, including pollination by bees, birds, butterflies, moths, wasps, beetles and of course long-proboscid flies.

Photo of Lapeirousia silenoides

Lapeirousia silenoides, pollinated by long-proboscid flies from the family Nemestrinideae

In our recently published study, we focussed on the genus, a small group comprising 27 species, mostly confined to the south western part of the African continent, and commonly known as painted petal irises. Despite its small size, no less than seven different pollination systems have been observed in this group, including two different guilds of long-proboscid fly pollination from families Nemestrinidae (tangled-veined flies) and Tabanidae (horse flies). In spite of this large diversity of pollinators, a previous study had concluded that the diversification of species in this group was driven by the diversity of soils on which these species occur and that pollinator shifts (changes in pollinators during evolutionary history) played only a secondary role in the speciation process. We re-examined the conclusions of this study by constructing a molecular phylogenetic tree of the group, a diagram depicting the relationships betweenLapeirousia species based on DNA sequence data.

Diagram depicting the relationships between Lapeirousia species based on DNA sequence data

Diagram depicting the relationships between Lapeirousia species based on DNA sequence data

Download the diagram of Lapeirousia phylogeny

Interestingly, we also found that pollination by long-proboscid flies was the ancestral condition in the genus, which is unusual as other studies of groups with varied pollination systems generally show that long-proboscid fly pollination has evolved from bee or generalist syndromes. This corroborates the assessment of biogeographical patterns that we also performed in this study in that most species of Lapeirousia (24 out of 27) are found along the west coast and near interior of southern Africa. The distribution of Lapeirousia essentially overlaps with the distribution of the long-proboscid flies involved in the pollination of many of its species.

Map of long-proboscid flies and Lapeirousia in South Africa

Map of long-proboscid flies and Lapeirousia in South Africa

Comparing our phylogenetic tree with the current geographical distribution of the species, suggests that the genus Lapeirousia evolved first in the Cape region of South Africa. In other words, the evolution of long-proboscid fly pollination in Lapeirousia coincides with the origin of the group in the Cape region, where the long-proboscid flies that pollinate many of them are mostly restricted.

There are several ongoing studies at Kew on the evolution of pollination systems in Iridaceae, but also in other plant groups. One of these studies is focusing on the Iridaceae genus Tritoniopsis, a group similar to Lapeirousia in size and diversity of pollinators, and which is particularly interesting due to the presence of bimodal pollination systems in many species. These species possess morphological features allowing the use of two different pollinator groups. How these evolved is a mystery but, hopefully, not for long.

An increasing number of studies are investigating the evolution of pollination syndromes at the population level (with particular pollination syndromes or with trait adaptations to different pollinators), and at the species level. Despite all these efforts, there are many aspects of the intimate relationships between plants and their pollinators that remain to be explored, and more questions are arising than answers, but it is a very exciting field of research with many amazing stories still to tell.

- Félix -


References

  • Forest, F., Goldblatt, P.,  Manning, J. C., Baker, D., Colville, J. F., Devey, D.S., Jose, S., Kaye, M. & Buerki, S. (2014). Pollinator shifts as triggers of speciation in painted petal irises (Lapeirousia: Iridaceae). Annals of Botany 113: 357-371. Available online
  • Goldblatt P. & Manning, J.C. (1996). Phylogeny and speciation in Lapeirousia subgenus Lapeirousia (Iridaceae: Ixioideae). Annals of the Missouri Botanical Garden 83: 346-361. Available online
  • Goldblatt P. & Manning, J.C. (2000). The long-proboscid fly pollination system in southern Africa. Annals of the Missouri Botanical Garden 87: 146-170. Available online
  • Goldblatt P. & Manning, J.C. (2006). Radiation of pollination systems in the Iridaceae of sub-Saharan Africa. Annals of Botany 97: 317-344. Available online
  • Johnson, S.D. (2010). The pollination niche and its role in the diversification and maintenance of the southern African flora. Philosophical Transactions of the Royal Society B-Biological Sciences 365: 499-516. Available online
  • Manning J.C. & Goldblatt, P. (1997). The Moegistorhynchus longirostris (Diptera: Nemestrinidae) pollination guild: Long-tubed flowers and a specialized long-proboscid fly pollination system in southern Africa. Plant Systematics and Evolution 206: 51-69. Available online

Images of long-proboscid flies:

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