The great taxonomic diversity of the Orchidaceae is often attributed to adaptive radiation for specific pollinators driven by selection for outcrossing. However, when one looks beyond the product to the process, the evidence for selection is less than overwhelming. We explore this problem by discussing relevant aspects of orchid biology and asking which aspects of reproduction explain the intricate pollination mechanisms and diversification of this family. We reaffirm that orchids are primarily pollination limited, the severity of which is affected by resource constraints. Fruit set is higher in temperate than in tropical species, and in species which offer pollinator rewards than those that do not. Reproductive success is skewed towards few individuals in a population and effective population sizes are often small. Population structure, reproductive success and gene flow among populations suggest that in many situations genetic drift may be as important as selection in fostering genetic and morphological variation in this family. Although there is some evidence for a gradualist model of evolutionary change, we believe that the great diversity in this family is largely a consequence of sequential and rapid interplay between drift and natural selection. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 84, 1–54.

Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification

The flora of the south-western tip of southern Africa, the Cape flora, with some 9000 species in an area of 90,000 km2 is much more speciose than can be expected from its area or latitude, and is comparable to that expected from the most diverse equatorial areas. The endemism of almost 70%, on the other hand, is comparable to that found on islands. This high endemism is accounted for by the ecological and geographical isolation of the Cape Floristic Region, but explanations for the high species richness are not so easily found. The high species richness is accentuated when its taxonomic distribution is investigated: almost half of the total species richness of the area is accounted for by 33 'Cape floral clades'. These are clades which may have initially diversified in the region, and of which at least half the species are still found in the Cape Floristic Region. Such a high contribution by a very small number of clades is typical of island floras, not of mainland floras. The start of the radiation of these clades has been dated by molecular clock techniques to between 18 million years ago (Mya) (Pelargonium) and 8 Mya (Phylica), but only six radiations have been dated to date. The fossil evidence for the dating of the radiation is shown to be largely speculative. The Cenozoic environmental history of southern Africa is reviewed in search of possible triggers for the radiations, climatic changes emerge as the most likely candidate. Due to a very poor fossil record, the climatic history has to be inferred from larger scale patterns, these suggest large-scale fluctuations between summer wet (Palaeocene, Early Miocene) and summer dry climates (Oligocene, Middle Miocene to present). The massive speciation in the Cape flora might be accounted for by the diverse limitations to gene flow (dissected landscapes, pollinator specialisation, long flowering times allowing much phenological specialisation), as well as a richly complex environment providing a diversity of selective forces (geographically variable climate, much altitude variation, different soil types, rocky terrain providing many micro-niches, and regular fires providing both intermediate disturbances, as well as different ways of surviving the fires). However, much of this is based on correlation, and there is a great need for (a) experimental testing of the proposed speciation mechanisms, (b) more molecular clock estimates of the age and pattern of the radiations, and (c) more fossil evidence bearing on the past climates.

The radiation of the Cape flora, southern Africa

There is a voluminous literature on pollination and dispersal, very little of which deals with the consequences of reproductive failure and its most extreme consequence: extinction. The risk of plant extinctions can be assessed by considering the probability of dispersal or pollinator failure, reproductive dependence on the mutualism and demographic dependence on seeds. Traits for ranking species rapidly according to these three criteria are indicated. Analysis of case studies suggests that plants often compensate for high risk in one of the three categories by low risk in another. For example, self-incompatible plants with rare specialist pollinators often propagate vegetatively. Some systems, including elements of the Cape flora and lowland tropical rain forest, lack compensatory traits and the risk of plant extinction from failed mutualism is high. 'What escapes the eye, however, is a much more insidious kind of extincnction: the extinction of ecological interactions' Janzen (1974).

Do mutualisms matter? Assessing the impact of pollinator and disperser disruption on plant extinction

A review of comparative levels of reproductive success among nectariferous and nectarless orchids worldwide was compiled from a comprehensive survey of fruit set from 117 orchid species in the literature and from our own field studies. It confirms the hypothesis that nectariferous orchids are more successful in setting fruit than are nectarless species. Overall fruit set figures for nectarless and nectariferous orchids were 19.5 and 49.3% for North America, 27.7 and 63.1% for Europe, 41.4 and 74.4% for the temperate southern hemisphere, and 11.5 and 24.9% for the tropics, demonstrating that the dichotomy is consistent across all geographical areas. On average, the provision of nectar doubles the probability of fruit set in both temperate and tropical areas, but tropical orchids are remarkable in that all (whether nectarless or nectariferous, or terrestrial or epiphytic) display low fruit productivity (<50%). Fruiting failure in the tropics may be balanced by higher productivity per capsule, since tropical orchid fruits contain on average 150 times more seeds than temperate ones. Hybridization occurs more frequently among nectarless orchids in Britain and Europe than among nectariferous ones, and there is a significant positive association between orchid rarity and lack of nectar reward in the British Isles. Sexual reproduction in the Orchidaceae is predominantly pollinator dependent, but this can sometimes be successfully circumvented by asexual seed production (agamospermy) or, more frequently, by automatic self-pollination (autogamy). The proportion of highly successful nectarless orchids from all geographic areas is very low and comparable with that of orchids offering rewards other than nectar (∼14% of species in each case) emphasizing that high reproductive success is only associated with nectar reward (53% of species). It is suggested that the evolution of nectar production within the family has been the most frequent means of escaping the reproductive limitations of low pollinator visitation frequencies.

Fruit set, nectar reward, and rarity in the Orchidaceae.

Orchids display many unsurpassed floral specializations, as both rewarders and frauds in their interaction with animal pollinators. Accumulating evidence indicates that their floral evolution is driven by pollinator traits and that expenditure for maximized sexual reproduction is parcelled out over their lifetimes in strategies for coping with pollinator and resource limitations. Recent advances in orchid pollination biology center mainly on floral evolutionary processes, pseudocopulation and other deceptive pollination systems, and flower and fruit production in relation to costs of sexual reproduction.

Ke. Steiner

Papers

The pollination of Disperis (Orchidaceae) by oil-collecting bees in southern Africa