The two opposite pathways in the evolution of flowers
The definition of what a flower is remains an important question in botany. One generally makes a distinction between flowers and inflorescences, although this distinction is not always clear, as in the case of pseudanthia. Pseudanthia are compact inflorescences of small or reduced flowers that mimic a real flower. The structure of a flower is made up from a variable number of building blocks, generally with sepals (a calyx), petals (corolla), stamens (androecium), and carpels (gynoecium). The number and arrangement of the building blocks is generally highly conservative and depends on the size and evolutionary history of the flower. The best way to describe the structure of flowers is by the use of floral diagrams.
However, despite their conservative nature, flowers evolve constantly and this evolution can go in two opposite directions. These changes will affect the number of building blocks that will determine how flowers can evolve. Changes in the flower structure are dependent on the pollination system. On the one hand there is a trend to reduction, leading to a loss of organs, and on the other there is a trend to increased complexity, leading to highly elaborate flowers.
A reduction of flowers is generally generated by a drive to abiotic pollination, especially wind pollination. This is accompanied in flowers by reduced size, loss of petals or even the whole perianth, reduction in the number of carpels and ovules, and unisexuality. Male flowers become aggregated in dense catkins and stamens have long filaments to expose the anthers to the wind, which picks up the large amount of dry pollen. Female flowers are fewer in number, on the same or a different plant, and consist of few or a single carpel with long hairy stigmas, in order to catch airborne pollen. The evolution towards wind pollination appears to be a progressive process, with several transitional stages in reduction. Examples are given for two plant families, viz. Gunneraceae and Restionaceae.
In Gunneraceae there is a reduction series between different species, starting with hermaphrodite flowers such as Gunnera manicata having sepals and petals. Other species are invariably unisexual, with a progressive reduction of petals and sepals in male flowers. In pistillate flowers petals are usually lost, but sepals remain generally present, subtending huge styles.
Restionaceae represent a large southern hemisphere family close to Poaceae. As in grasses, flowers are wind pollinated and grouped in dense spikes but unlike grasses flowers are unisexual and dioecious. Reductions in female flowers are expressed in the staminodes and in the number of carpels. Some genera have three fertile carpels. In other genera there is a progressive sterilization of one-two carpels, either
loss of the anterior carpel, ending in 2-styled-flowers,
(2) through the reduction and loss of the anterior and one posterior carpel, ending in a single lateral style, and
(3) through the reduction and loss of the two posterior carpels, leading to a single anterior carpel.
Staminodes become aborted at different stages of their development, and are ultimately lost completely. Reductions in Restionaceae appear to be guided by a strong compression of flowers between bract and spike axis and a trend to a highly efficient vortex pollination, where bracts shape a spiral air cirulation leading pollen grains to the receptive stigmas. As a result all excessive organs are either reduced or lost.
Higher complexity is generally linked to complex biotic pollination mechanisms involving specialized pollinating animals. Several trends lead to increased complexity, such as size increase, higher merism, stamen and carpel multiplications, and the development of various appendages (corona or spurs).
A higher stamen number allows the production of more pollen and the attraction of larger pollinators. However, most flowers of angiosperms have two or a single stamen whorl, and thus not sufficient building blocks to produce more pollen. An increase in stamen number is brought about by the division of single primary stamen primordia in many secondary stamens. This can lead to fascicles of stamens in the flower, but often separate primordia converge into a single ring primordium producing even more stamens. More stamens can also arise by the expansion of a floral cup or hypanthium providing space for an increase.
Stamen increases can be highly complex, as in Loasaceae where flowers can either have multiple stamens arising on a ring primordium or on separate primordia (Mentzelia) or are confined to the antepetalous area, while the antesepalous stamens develop as staminodial structures (e.g. Cajophora, Loasa). The staminodes arise in groups of five, forming a coloured nectar container.
In Lecythidaceae flowers are either regular with many stamens formed on a ring primordium, or are zygomorphic with an androecium consisting of fertile stamens covered by a flap or hood consisting of sterile stamens. As a result only larger bees can access food sources in the flower and have to push their way between flap and receptacle. The genus Napoleonaea has a complex system consisting of a combination of two whorls of staminodial structures and a whorl of pleated petals. The fertile stamens are situated within the inner erect staminodial whorl and can only be accessed through small slits. Flowers are pollinated by small insects, such as thrips.
Malvaceae have highly variable flowers with an androecium derived from two initial stamen whorls. While the antepetalous stamens have a general tendency to multiply in pairs or in higher numbers arranged in two columns, the antesepalous stamens are either staminodes or they converge in triplets with one antepetalous column on each side. Stamen increase is accompanied by growth of an androecial tube around the ovary and repeated divisions of primordia leading to stamens with half anthers.
Contrary to stamen increases, flowers have evolved many other ways to increase their complexity. Coronas are coloured appendages that can arise anywhere in the flower, greatly adding to the attraction or playing specific roles in pollination strategies. In Passiflora flowers are relatively simple with five stamens and three carpels. Growth of a floral cup allows for the development of a multilayered corona of threads, creating an effective barrier for a nectary and surpassing the original attraction of the perianth. Asclepiadoideae of Apocynaceae also develop a corona; the corona arises on the back of the stamens which have their anthers attached to the style. The corona is funnel-shaped and provides access to nectar that ascends through capillarity, while the anthers have evolved specialized pollinia for effective pollination.
Evolutionary trends to reduction or increase can also be reversed, when pollination systems change during evolution. A good example is a return from wind pollination to insect pollination, leading to a secondary increase in complexity. Depending on the availability of building blocks as a result of a reduction in the flower, different outcomes are possible. Salix is the sister group of Populus, a genus that is wind pollinated with unisexual flowers. However, Salix has reverted to insect pollination while retaining most characteristics of wind pollinated flowers (unisexual flowers, catkins). Attraction of bees is made possible through the transformation of the reduced perianth into nectaries. In Caryophyllales, original petals have been lost in evolution, while the original five sepals have been retained.
Different families evolved strategies to attract pollinators, either through coloration of sepals or bracts, or a secondary increase of stamens and the development of outer petal-like staminodes provides attraction in the flower. A return to animal pollination can also drive strongly reduced unisexual flowers into complex pseudoflowers. This is particularly obvious in the family Euphorbiaceae building up inflorescences resembling flowers and behaving as flowers. In Euphorbia bracts are fused into cup-shaped structures bordered with glands and enclosing a single female flower of three carpels and several male flowers of a single stamen.
The examples presented above illustrate only a minor part of evolutionary possibilities in flowers, driven by diverging pollination strategies. The number of building blocks present in flowers determine the outcome of the evolution, as a loss of building blocks reduces the number of blocks available for further evolution. Understanding the processes at play in evolution of floral structures are extremely important, as they allow us to understand the links that exist between different group of plants, something that is not always clearly shown in our modern molecular phylogenies.