Wood evolution: Baileyan trends and Functional traits in the fossil record

ABSTRACTWe revisited questions about changes in the incidences of functional wood anatomical traits through geologic time and compared the incidences of these traits in the fossil record with modern wood anatomical diversity patterns in order to test classical (“Baileyan”) and more recent ecophyletic hypotheses of xylem evolution. We contrast patterns through time for tropical and higher (paleo)latitudes. Data are from the InsideWood database. There are striking differences between woods from high and mid latitudes versus tropical (paleo)-latitudes. At temperate and subtropical latitudes (Laurasia and high latitude Gondwana), the epoch by epoch time series supports the Baileyan transformation series of vessel-bearing woody angiosperms (basal woody angiosperms and eudicots): “primitive” features such as scalariform perforations, exclusively solitary vessels, apotracheal diffuse parenchyma and heterocellular rays abound in the Cretaceous and become much less frequent in the Cenozoic, especially post-Eocene. In contrast, in the paleotropics hardly any changes occur in the incidences – each epoch has an equally “modern” spectrum of wood anatomical attributes. Although climatic gradients from the poles to the equator were less steep in the Cretaceous than in the late Cenozoic, the wood anatomical differences between mid-high latitude woods and tropical woods were much more pronounced in the Cretaceous than in later epochs. This seeming paradox is discussed but we cannot resolve it.We suggest that tropical conditions have accelerated xylem evolution towards greater hydraulic efficiency (simple perforations), biological defense and hydraulic repair (elaborate paratracheal parenchyma patterns) as evidenced by late Cretaceous tropical latitude woods having near modern incidences of almost all traits. At higher paleolatitudes of both the Northern and Southern Hemisphere “ancestral” features such as scalariform perforations were retained in cooler and frost-prone regions where they were not selected against in mesic habitats because of lower demands on conductive efficiency, and could even be advantageous in trapping freeze-thaw embolisms. The fossil wood record remains too incomplete for testing hypotheses on the wood anatomy of the earliest angiosperms. The low incidence of so-called “xerophobic” woods sensu Feild with scalariform perforations with numerous (over 40) closely spaced bars in the Cretaceous tropical fossil record is puzzling. At higher paleolatitudes such woods are common in the Cretaceous.Ring porosity, an indicator of seasonal climates and deciduousness, occurs at low levels in the Cretaceous and Paleogene at higher paleolatitudes only, and reaches modern levels in the Miocene. In Neogene and Recent temperate Northern Hemisphere, wide vessels are virtually restricted to ring-porous woods. In the tropics, there is a low incidence of ring porosity throughout all epochs.The fossil record indicates that ecophysiological adaptation to tropical or temperate conditions was already evident in the Cretaceous with considerable latitudinal differences.

Una mirada de la situación actual de la anatomía de la madera

The primary objective of this contribution is to present a view of how and to what extent comparative systematic wood anatomy has changed over the past fifty years and what research priorities should be for the future. Wood anatomy has resolved itself into a series of subdisciplines, each of which deals with particular questions. Thus, wood anatomical study has passed successively from a consideration of wood data based upon well-defined and largely unchallenged principles to a more flexible view of wood evolution based on structure-function relationships at the cellular level and the establishment of correlations between anatomy and ecology. The questions and phenomena to be investigated are so complex and variable that, in many cases, they can be analyzed only through the active cooperation of a group of experts.

An overview of the hydraulic systems in early land plants

One of the key functions of wood is hydraulic conductivity, and the general physical properties controlling this are well characterized in living plants. Modern species capture only a fraction of the known diversity of wood, which is well preserved in a fossil record that extends back over 400 million years to the origin of the vascular plants. Early fossil woods are known to differ in many key respects from woods of modern gymnosperms (e.g., tracheid size, secondary wall thickenings, lignin chemistry, cambium development) and recent discoveries are shedding new light on the earliest stages of wood evolution, raising questions about the performance of these systems and their functions. We provide an overview of the early fossil record focusing on tracheid morphology in the earliest primary and secondary xylem and on cambial development. The fossil record clearly shows that wood evolved in small stature plants prior to the evolution of a distinctive leaf-stem-root organography. The hydraulic properties of fossil woods cannot be measured directly, but with the development of mathematical models it is becoming increasingly feasible to make inferences and quantify performance, enabling comparison with modern woods. Perhaps the most difficult aspect of hydraulic conductance to quantify is the resistance of pits and other highly distinctive and unique secondary wall features in the earliest tracheids. New analytical methods, in particular X-ray synchrotron microtomography (PPC-SRμCT), open up the possibility of creating dynamic, three-dimensional models of permineralized woods facilitating the analysis of hydraulic and biomechanical properties.

How wood evolves: a new synthesis

Recent advances in wood physiology, molecular phylogeny, and ultrastructure (chiefly scanning electron microscopy, SEM), as well as important new knowledge in traditional fields, provide the basis for a new vision of how wood evolves. Woody angiosperms have, in the main, shifted from conductive safety to conductive efficiency (with many variations and modifications) and from ability to resist cavitation (low vulnerability) to ability to refill vessels. The invention of the vessel was a kind of dimorphism (vessel elements plus tracheids) that permitted division of labor and many kinds of wood repatterning that suit conductive safety–efficiency trade-offs. Angiosperms were primarily adapted to mesic habitats but were not failures or “unstable.” They have survived to the present in such habitats well, along with older structural adaptations (e.g., the scalariform perforation plate) that are still suited to such habitats. These “primitive” features are evident in earlier branchings of phylogenetic trees based on multiple genes. Older features may still be functional and thus persist, although newer formulations are overriding in effect. There are, however, numerous instances of “breakouts” in a number of clades (ecological iterations and bursts of speciation and diversification related to new ways of dealing with water economy), whereas in other branchings, other clades show ecological stasis over long periods of time. Newer physiological and anatomical mechanisms have permitted entry into habitats with marked fluctuation in moisture availability. Wood evolves progressively, and literal character state reversal may be unusual: genomic and developmental information holds answers to these changes. Wood is a complex tissue, and each of the histological components shows polymorphism as an evolutionary mechanism. Cell types within wood evolve collaboratively. Shifts in wood features (e.g., simplification of the scalariform perforation plate) are commonly homoplastic. Manifold changes in habit and in leaf physiology, morphology, and anatomy accompany wood evolution, and wood should be studied with relationship to real-world ecology, information that cannot be gleaned from literature or other secondary sources. Heterochrony (protracted juvenilism, accelerated adulthood) characterizes angiosperm xylem extensively, far more so than in other vascular plants, and these mechanisms have resulted in many remarkable changes (e.g., monocots have permanently juvenile xylem, woody trees represent accelerated adulthood). Understanding the many successful features of angiosperm wood evolution must ultimately rest on syntheses.

Wood anatomy of Cussonia and Seemannaralia (Araliaceae) with systematic and ecological implications

The wood structure of two related African genera, Cussonia Thunb. (15 of 21 species) and the monotypic Seemannaralia R.Vig. (Araliaceae) is examined. The considerable diversity in wood anatomical characters within these taxa is mostly related to environmental factors; taxonomic groupings or phylogenetic relationships seem to be less important. The shortening of vessel elements and fibres, an increase in vessel number per group, a decrease in vessel diameter and a reduction in the number of bars of perforation plates, are associated with the more temperat species. The changes in vessel grouping show a significant correlation with rainfall. The placement of the simple-leaved Cussonia species in the subgenus Protocussonia and the isolated position of C. paniculata Eckl. & Zeyh., the only member of the subgenus Paniculatae, are supported. Many Cussonia species share a very low fibre to vessel element length ratio. Despite the basal position of Seemannaralia relative to Cussonia revealed by molecular data (Plunkett et al. 2004), its wood structure is more specialised in terms of the Baileyan major trends in wood evolution. This discrepancy may be the effect of a long-term adaptation of tropical ancestors of Seemannaralia to drier biomes.