Peter R. Crane

Fossil evidence of water lilies (Nymphaeales) in the Early Cretaceous

Phylogenetic analyses have identified the water lilies (Nymphaeales: Cabombaceae and Nymphaeaceae), together with four other small groups of flowering plants (the ‘ANITA clades’: Amborellaceae, Illiciales, Trimeniaceae, Austrobaileyaceae), as the first diverging lineages from the main branch of the angiosperm phylogenetic tree, but evidence of these groups in the earliest phases of the angiosperm fossil record has remained elusive. Here we report the earliest unequivocal evidence, based on fossil floral structures and associated pollen, of fossil plants related to members of the ANITA clades. This extends the history of the water lilies (Nymphaeales) back to the Early Cretaceous (125–115 million years) and into the oldest fossil assemblages that contain unequivocal angiosperm stamens and carpels. This discovery adds to the growing congruence between results from molecular-based analyses of relationships among angiosperms and the palaeobotanical record. It is also consistent with previous observations that the flowers of early angiosperms were generally very small compared with those of their living relatives.

Palaeobotanical evidence on the early radiation of magnoliid angiosperms

Early to mid-Cretaceous Potomac Group sediments have yielded a number of well-preserved angiosperm flowers, fruits, seeds, and dispersed stamens. The most diverse assemblage from the Early Cretaceous part of the sequence is from the Puddledock locality, Virginia, eastern USA. This material is of Early to Middle Albian age and is particularly rich in magnoliid and hamamelidid angiosperms. Flowers and fruits from the Puddledock flora are mostly simple and few-parted and so far only two reproductive structures with numerous parts have been recovered. In this paper we focus on floral organs showing magnoliid features, some of which may be compared to extant taxa, at least at the level of order and perhaps family. Other floral organs are more difficult to classify. Fossils from the Puddledock locality document the earliest appearance of calycanthaceous, and possible lauraceous, floral characters. As recorded also from the Early Cretaceous floras of Portugal, several different kinds of epigynous angiosperm and angiosperm-like reproductive structures are present. The discovery of small Circaeaster-like spiny fruits with monocolpate pollen is especially significant.

Flowers on the Tree of Life: New flowers of Laurales from the Early Cretaceous (Early to Middle Albian) of eastern North America

Introduction The increasing number of fossil angiosperm reproductive structures described from Cretaceous strata (e.g. Friis et al., 2006) has provided a wealth of new data for understanding aspects of early flowering-plant evolution. In particular, flowers retrieved from many newly discovered mesofossil floras are often three-dimensionally preserved, which permits detailed morphological and systematic analyses. They have thereby provided information on the phylogenetic diversity and reproductive biology of Cretaceous angiosperms (e.g. Friis et al., 2006, 2010). However, an important feature of the angiosperm fossil record from the Cretaceous is that many fossils, particularly from the Early Cretaceous, cannot readily be accommodated in living taxa at the family or genus level, either because they are too poorly preserved to show the diagnostic features needed for secure systematic placement, or because they show a mosaic of features found in several living groups, indicating that they represent extinct lineages on internal branches of the angiosperm phylogenetic tree. The focus of this paper is on two early fossils of the second kind. While their relationships to extant Laurales are secure, they show features indicating that they fall outside the circumscription of extant families in the order. Studies of relationships among living angiosperms based on analyses of DNA sequences support the recognition of the Laurales as a monophyletic group of seven extant families (Calycanthaceae, Siparunaceae, Gomortegaceae, Atherospermataceae, Hernandiaceae, Monimiaceae, Lauraceae; Renner, 1999, 2005; Renner and Chanderbali, 2000). The Laurales are the sister group to Magnoliales and include between 2840 and 3340 species in about 92 genera (Renner, 2005). The Calycanthaceae are the well-supported sister group to the remainder of the order, the core Laurales (Fig 3.1), within which Atherospermataceae, Gomortegaceae and Siparunaceae also form a well-supported clade (e.g. Renner, 1999, 2005). Relationships among Lauraceae, Monimiaceae and Hernandiaceae are currently not settled securely (Renner and Chanderbali, 2000). Morphological data strongly support a sister relationship of Hernandiaceae and Lauraceae (e.g. Doyle and Endress, 2000; Endress and Doyle, 2009), as do some molecular analyses (e.g. Qiu et al., 1999, 2006). However, in other molecular analyses the pattern of relationships among these three families is not well resolved (e.g. Renner, 1999, 2005; Chanderbali et al., 2001; Soltis et al., 2007).

Early Flowers and Angiosperm Evolution: Introduction to angiosperms

The phylogenetic diversification and ecological radiation of angiosperms (flowering plants) that took place in the Early Cretaceous, between about 135 and 65 million years ago, was one of the major biotic upheavals in the history of life. It had dramatic consequences for the composition and subsequent evolution of terrestrial ecosystems. Ancient Mesozoic vegetation, which was dominated by ferns, conifers, ginkgos and cycads, as well as Bennettitales and other groups of extinct seed plants, was eventually almost entirely replaced by more modern ecosystems dominated by angiosperms. Since the Early Cretaceous, high diversification rates have generated more than 350xa0000 extant angiosperm species. Today there are more living species of angiosperms than all other groups of land plants combined. In their rise to ecological dominance angiosperms have exhibited extraordinary developmental and evolutionary plasticity. This has resulted in overwhelming morphological diversity and a great variety of adaptive types. Angiosperms are far more diverse in vegetative form and in the structure of their reproductive organs than any other group of land plants.

Early Flowers and Angiosperm Evolution: History and evolution of pollination in angiosperms

Pollination, the successful transfer of pollen from the pollen sacs (microsporangia) into proximity with the ovule, is the essential precursor to fertilisation and therefore to sexual reproduction in seed plants. Pollination has been studied most intensively in angiosperms, although few species have been examined in detail compared with the great variety of flowers within the group (e.g. Proctor et al ., 1996; Thien et al ., 2009). Pollination in extant non-angiosperm seed plants has received less attention, but studies over the past few decades now provide a more complete context within which pollination in angiosperms can be evaluated and studied (e.g. Owens et al ., 1998). Interpretation of pollination in extinct plants faces significant difficulties. Only rarely is there relatively direct evidence of flower–pollinator interactions (e.g. insect gut contents, coprolites, insects preserved within flowers, insects carrying pollen) and interpretations of pollination in extinct plants therefore depend heavily on extrapolations to extant taxa based on structural similarities. This often leads to plausible interpretations, but it may also be constraining. There is no a priori reason why the spectrum of plant–pollinator interactions existing today should also include all of those that existed in the past, and inferring floral function from floral structure, even in extant plants, can sometimes be difficult. It is therefore especially challenging to infer pollination in extinct seed plants (e.g. Caytonia , Bennettitales) that have no clear close living relatives.

Early Flowers and Angiosperm Evolution: The environmental context of early angiosperm evolution

The global environment during the earliest phases of angiosperm diversification was radically different from that of today. The geography and distribution of continents was unlike that of our modern world and the Cretaceous was also a time of generally higher sea levels and higher global temperatures. There were low thermal gradients from the equator to the poles (DeConto et al ., 2000a; Gale, 2000; MacLeod et al ., 2000), patterns of rainfall were quite different (Parrish, 1987) and there is no unequivocal evidence of polar ice caps during the Cretaceous and Early Cenozoic (Gale, 2000). The Cretaceous is often considered the classic example of ‘greenhouse’ or ‘supergreenhouse’ conditions in Earth history. These unusual conditions compared with today profoundly influenced the ecology and evolution of life on land as angiosperms underwent their initial radiation and then diversified to become the dominant primary producers in most terrestrial ecosystems. Our modern world provides a poor analogue for the environmental backdrop against which more than half of the evolutionary history of angiosperms unfolded. In this chapter we provide a brief overview of changes in palaeogeography and palaeoclimate through the Cretaceous period, a time interval of 80 million years (Figure 3.1). More detailed accounts can be found elsewhere (e.g. Skelton, 2003b). The aim here is to provide a short summary that places patterns of early angiosperm evolution in their environmental context. Palaeogeography During the later Palaeozoic and Triassic a single supercontinent, Pangaea, was formed through the coalescence of all pre-existing major continental masses. The southern part, Gondwana, consisted of South America, Africa, Apulia (present-day Italy), Arabia, Australia, New Zealand, Antarctica, India, and Madagascar. The northern part, Laurasia, consisted of many smaller and larger continents with North America, Greenland, Europe, Iberia, Siberia, Kazakhstan, Kolyma and China as its main components. Pangaea persisted into the early Mesozoic, but began to break up during the Triassic and Jurassic through a series of processes that continued into the Cretaceous (Figures 3.2–3.5) (Smith et al ., 1981; Scotese et al ., 1988).