Ancestral xerophobia: a hypothesis on the whole plant ecophysiology of early angiosperms

Abstract

Today, angiosperms are fundamental players in the diversity and biogeochemical functioning of the planet. Yet despite the omnipresence of angiosperms in today's ecosystems, the basic evolutionary understanding of how the earliest angiosperms functioned remains unknown. Here we synthesize ecophysiological, paleobotanical, paleoecological, and phylogenetic lines of evidence about early angiosperms and their environments. In doing so, we arrive at a hypothesis that early angiosperms evolved in evermoist tropical terrestrial habitats, where three of their emblematic innovations - including net-veined leaves, xylem vessels, and flowers - found ecophysiological advantages. However, the adaptation of early angiosperm ecophysiology to wet habitats did not initially promote massive diversification and ecological dominance. Instead, wet habitats were permissive for the ecological roothold of the clade, a critical phase of early diversification that entailed experimentation with a range of functional innovations in the leaves, wood, and flowers. Later, our results suggest that some of these innovations were co-opted gradually for new roles in the evolution of greater productivity and drought tolerance, which are characteristics seen across the vast majority of derived and ecologically dominant angiosperms today.

Integrating Early Cretaceous Fossils into the Phylogeny of Living Angiosperms: ANITA Lines and Relatives of Chloranthaceae

“…One hypothesis for resolving the conflict between molecular and fossil data (Feild et al 2004(Feild et al , 2009), mentioned in connection with Appomattoxia, is based on the fact that the terrestrial ANITA lines are "xerophobic" plants restricted to wet, shaded forest understory habitats and evidence that such habitats were rare in the Triassic and Jurassic, when climates were relatively arid across the tropics (Ziegler et al 2003). The ANITA lines make up less than 0.1% of living angiosperm species, and analyses by Magalló n and indicated that rates of angiosperm diversification were initially low and did not speed up until origin of the mesangiosperm clade.…”

“…By contrast, Amborella and Austrobaileyales are restricted to wet, shaded forest understory sites. Feild et al (2004Feild et al ( , 2009) reconstructed such habitats as ancestral for angiosperms and argued that the rarity of such environments in the Triassic and Jurassic could explain why angiosperms escaped detection if they existed at that time, as indicated by many molecular dating analyses (Magalló n 2010; Smith et al 2010;Clarke et al 2011;see Doyle 2012). If Appomattoxia is near the base of the tree, it could challenge this view of ecology of the first angiosperms or else indicate that members of the basal grade were able to break out of the ancestral niche and adapt to dry climates more easily than might be expected.…”

Fossil evidence for a herbaceous diversification of early eudicot angiosperms during the Early Cretaceous

“…Teeth of this type are sites of guttation; the loss of water at tooth apices prevents flooding of the leaf mesophyll under conditions of high soil moisture, high humidity and low evaporative demand [53][54][55]. Environments such as forest understory and riparian corridors in tropical and temperate climates typically host plants with hydathodal teeth [49,[56][57][58][59][60][61]; but hydathodal teeth also occur in some marginally or semi-aquatic ranunculalean herbs that grow under bright, subareal conditions [39].…”

Recognising angiosperm clades in the Early Cretaceous fossil record

“…Bell et al 2010;Smith et al 2010;Clarke et al 2011), but this raises the question of why they are not seen in the fossil record until the Cretaceous. One hypothesis (Feild et al 2004(Feild et al , 2009) is based on the fact that the living ANITA lines (except for Nymphaeales, which are derived in being aquatic) are ecologically restricted to wet forest understorey habitats, as in New Caledonia and Queensland today, and low in diversity (only 0.1% of angiosperm species). This suggests that pre-Cretaceous ANITA-grade angiosperms could have escaped detection because wet habitats suitable for them were geographically restricted, because arid and semiarid conditions prevailed across most of the tropics (Rees et al 2000;Ziegler et al 2003).…”