|The male flowers of Amborella are crowded with stamens.
Photo by Scott Zona, posted on Wikipedia
Amborella is in the same position relative to angiosperms in genera, as Acorus is to other monocots. I argued in a recent post (What's so primitive about Acorus?), however, that being at the tip of a very long evolutionary branch does not necessarily mean being exactly the same as the very first members of that branch. It is likely in fact that some changes have been made as conditions and competition changed over the tens of millions of years since that ancient phylogenetic split. I identified several ways in which Acorus was probably more advanced than some other archaic monocots that branched off slightly later.
|The female flower of Amborella
contains several carpels and a few
sterile stamens. The carpels are
ascidiate and unsealed. An opening
just below the stigma is blocked
only by a drop of fluid.
Photo by Sangtae Kim
To be sure, Amborella trichopoda, has retained a number of truly archaic features. For one thing, it has the most primitive wood (consisting only of tracheids), of any living angiosperm (Carlquist & Schneider 2001). It also has very basic flowers, as we'll see below.
Amborella occurs in the rain forests of New Caledonian, a gentle environment isolated from both climate change and the hotbeds of aggressive evolution on the continents. Other relics of past ages survive in similar habitats, including the nearly-as-ancient order Austrobaileyales.
If we include the Austrobaileyales and the Nymphaeales with Amborella in our analysis, we can create a more general picture of the ancestral angiosperm. Together these three clades are referred to as the ANITA grade, and contrast with the higher angiosperms of the magnolids, eudiots, and monocots. Each can be assumed to have a different mix of ancestral and specialized characteristics. The likely characteristics of the ancestral flower have been in fact derived from a study of this group (Endress 2001).
In this model, the ancestor of all known angiosperms had bisexual flowers consisting of simple, separate organs: tepals, stamens and carpels, which were spirally arranged and indefinite in number. Advancements from this model, such as carpels fused into a compound pistil, stamens in whorls of definite numbers, and tepals in two distinct whorls of sepals and petals, show up in various higher groups at different times.
Three other aspects of the carpels are also part of the model:
1. carpels are unsealed. They are open just below the stigmatic region, and entry of dirt, pathogens and small animals is blocked only by a drop of fluid. This contrasts with most modern carpels, which are completely sealed by a tight suture.
2. carpels are ascidiate, i.e. urn-shaped. The wall of the carpel is smooth and seamless, like a sock pulled up around its contents. This contrasts both with earlier accepted models of the first angiosperm carpels, and those of most modern angiosperms, which are plicate (folded). In the plicate model, a row of ovules along each margin of an ancient, leaf-like structure were brought inside as the margins joined together in a tight suture.
3. carpels contain just a few ovules placed opposite the backbone of the carpel, though there is some variation. Amborella has just one ovule, some waterlilies have many.
|The carpel of Amborella is ascidate and unsealed at the top,
though the stigma region shows a folded structure
consistent with the plicate model of the carpel.
Drawing from Bailey & Swamy (1948)
|In the plicate, or folded-leaf
model, the first carpels folded
or rolled together, bringing rows
of marginal ovules inside. The
two edges eventually became
tightly sealed by an interlocking
Drawing from the 1879
textbook by Asa Gray
The flowers are also unisexual, with pollen-producing flowers on separate plants from those that bear ovule-producing flowers. Such an arrangement is likely a means of avoiding self-pollination (Ferrandiz et al. 2010). Similar patterns can be seen in a variety of other plants, such as date palms. The fact that the female flowers contain sterile stamens between the tepals and the carpels is compelling evidence that the ancestors of Amborella did indeed have bisexual flowers. This has recently been confirmed by Sauchet et al. (2017).
The fruits of Amborella are described as small drupes. These are fleshy fruits with large seeds filled with food reserves, typically adapted for germination in shady forests. Drupes are found among many different families of flowering plants, but to my knowledge are always the endpoints of evolution from more generalized ancestors with flexible ovule production. In the Rose family, for example, drupes are found in the genus Prunus (plums, cherries, etc.), a specialized genus in a family that includes a wide variety of fruit types.
|The bisexual flowers of Austrobaileya have a
number of carpels, each containing two rows of
ovules, as well as flattened, blade-like stamens.
In sum, Amborella is likely specialized in its floral display, unisexual flowers, and single-seeded carpels. In other ways, it does show its age: wood without vessels, simple, separate flower parts of indefinite numbers, and unsealed carpels. Its present very limited distribution in forests of New Caledonia attest to its archaic status and its proximity to extinction. The few ways in which it has specialized are probably the keys to it still being with us.
This discussion leads to a deeper question of the nature of the first angiosperm carpels, which evolved well before the common ancestor of living angiosperms. Were they ascidiate or plicate? The ascidiate carpel itself may be an adaptation for making berries and drupes, maybe nuts and achenes as well, but does not lend itself to carpels that must reopen as capsules, follicles or legumes. So were the very first carpels fleshy berries? I'll take that up in a future post.
Bailey I. W. and Swamy B. G. L. 1948 Amborella trichopoda Baill., a new morphological type of vesselless dicotyledon. Journal of the Arnold Arboretum 29: 245–254.
Endress, P. K. 2001. The Flowers in Extant Basal Angiosperms and Inferences on Ancestral Flowers
International Journal of Plant Sciences 162 (5): 1111- 1140
Thien, L. B. , T. L. Sage, T. Jaffré, P. Bernhardt, V. Pontieri, P. H. Weston, D. Malloch, H. Azuma, S. W. Graham, M. A. McPherson, H. S. Rai, R. F. Sage and J-L. Dupre. 2003. The Population Structure and Floral Biology of Amborella trichopoda (Amborellaceae) Annals of the Missouri Botanical Garden 90 (3): 466-490.