Wood functional disparity lags behind taxonomic ...

Review of Palaeobotany and Palynology 246 (2017) 251–257

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Wood functional disparity lags behind taxonomic diversification in angiosperms Hugo I. Martínez-Cabrera a,⁎, Jingming Zheng b, Emilio Estrada-Ruiz c a b c

Museo de Múzquiz, A. C., Zaragoza 209, C.P. 26340, Melchor Múzquiz, Coahuila, Mexico College of Forestry, Beijing Forestry University, Beijing 100083, PR China Laboratorio de Ecología, Departamento de Zoología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional, 11340 México D.F., Mexico

a r t i c l e

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Article history: Received 17 June 2017 Received in revised form 26 July 2017 Accepted 27 July 2017 Available online 01 August 2017 Keywords: Disparity Diversification Evolution Fossil wood Functional traits Wood development

a b s t r a c t Early angiosperm fossil record shows a remarkably low wood structural diversity relative to that exhibited by reproductive structures. As wood anatomical traits are related to plant function, paucity of early wood structural differentiation suggests a delay of functional diversification relative to the explosive taxonomic accumulation of the group. We assembled a wood anatomy dataset of over 1000 extant species from Argentina, Brazil, China, Mexico, USA and Suriname to determine the disparification patterns of the cell types associated with the three main wood functional axes: conduction, support and storage. We found that most traits had a temporal shift in their evolutionary patterns, with early conservatism followed by high lability towards the present. Our results indicate that a surge in functional wood traits lability took place after the initial taxonomic diversification in the early Cretaceous and support the observed low wood structural diversity observed in the early angiosperm fossil record. Increased trait lability likely allowed evolutionary flexibility by lifting developmental constraints and boosted the evolution of different cell types involved in multiple wood functions and their associated ecological role. The diversification in wood function coincides with the escalation of angiosperm tree size and leaf hydraulic capacity and likely contributed to the subsequent ecological expansion of the angiosperms. © 2017 Elsevier B.V. All rights reserved.

1. Introduction The rise in the ecological dominance of angiosperms is in part a product of enhanced xylem and leaf hydraulic capacities and niche diversification that started during the mid to Late Cretaceous (Feild et al., 2011). An increase in angiosperm conductive capacity paired with a generalized increase in angiosperm size (Upchurch and Wolfe, 1993) likely contributed to maximize carbon fixation and brought unprecedented transpiration rates that influenced many aspects of ecosystem functioning (Upchurch and Wolfe, 1993; Upchurch et al., 1998, 2015; Boyce et al., 2010; Peralta-Medina and Falcon-Lang, 2012). There is some evidence suggesting that this functional expansion that made angiosperms dominate the terrestrial landscape only took place after the initial taxonomic explosion of the group (Feild et al., 2004). A study including a large number of fossil wood records also suggests that despite the fast diversification of the angiosperms in the mid-Cretaceous, they only became ecological dominant until the latest Cretaceous (Peralta-Medina and Falcon-Lang, 2012). Diversity of pollen, leaves and reproductive structures supports a major diversification event of the angiosperms around 90– 130 million years ago (Crane et al., 1995, 2000) and, by the Late ⁎ Corresponding author. E-mail address: [email protected] (H.I. Martínez-Cabrera).

http://dx.doi.org/10.1016/j.revpalbo.2017.07.008 0034-6667/© 2017 Elsevier B.V. All rights reserved.

Cretaceous, angiosperm pollen dominated most low latitude palynofloras (60 to 80% of the species). Increased pollen diversity is often used as an indicator of angiosperm ecological diversification and it is supported by the highly developed reproductive and foliar structural diversity (Crane and Lidgard, 1989). However, the timing of angiosperm wood structural diversification seems to differ since, despite their abundance in many localities, there are few fossil wood types at the beginning of the Late Cretaceous (100 mya, Cenomanian). Strikingly, after 60–70 million years (Turonian–Santonian) of angiosperm evolution, only 50 wood types have been described for the Northern Hemisphere (Wheeler and Lehman, 2009). Moreover, during the Early Cretaceous (Aptian–Albian) two main wood types (Paraphyllanthoxylon and Icacinoxylon/Platanoxylon) dominated many woody paleofloras (e.g., Suzuki, 1982; Thayn et al., 1983, 1985; Wheeler and Baas, 1991; Suzuki et al., 1996; Takahashi and Suzuki, 2003; Wheeler and Lehman, 2009). It is important, however, to highlight that Cretaceous charcoalified assemblages (e.g., Oakley and Falcon-Lang, 2009; Falcon-Lang et al., 2012), which up to date have been not extensively studied, might result in greater wood diversity. For instance, in the Santonian wood assemblage from Upatoi Creek, Georgia, seven new types of wood with scalariform perforation plates (Falcon-Lang et al., 2012). In a comprehensive study of Early Cretaceous angiosperm fossil woods from Europe, Philippe et al. (2008) did not find angiosperms

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during most of the Early Cretaceous (Barremian–Aptian). It was not until the Albian that the first angiosperm woods appeared in the European fossil record (Hungary and United Kingdom, respectively; Crawley, 2001; Barale et al., 2002). In the Cenomanian (earliest Late Cretaceous), diversity of genera in Europe increased to seven new wood types relative to the Albian with an accompanying increase in wood anatomical diversity (Lignier, 1907; Crawley, 2001; Falcon-Lang et al., 2001; Philippe et al., 2008). The increase in angiosperm wood frequency that occurred towards the Cenomanian was accompanied by a parallel increase in anatomical diversity (Philippe et al., 2008). Despite this noticeable, but modest, increase in anatomical diversity, the relationships of most of these woods to extant families is unknown, and many have a combination of features that occur in more than one family or order (Herendeen, 1991). Such is the case of Paraphyllanthoxylon that is regularly placed in Lauraceae (Herendeen, 1991), but it has also been compared to Phyllanthaceae and Euphorbiaceae (Malpighiales), Elaeocarpaceae (Oxalidales), and Anacardiaceae– Burseraceae (Sapindales) (Thayn and Tidwell, 1984; Herendeen, 1991; Martínez-Cabrera et al., 2006; García-Hernández et al., 2016). The paucity of records of Early Cretaceous woods may be because most had thin-walled fibers and low-density wood (Philippe et al., 2008). A thin-walled fiber not only reduce chance of preservation, and thus explain the lack of early angiosperm records, but also is a feature tightly related with the ecological space occupied by plants, as they determine key life history strategies. Charcoalified assemblages could enrich the Cretaceous fossil record in the future since woods with thinwalled fibers have greater potential for preservation (Falcon-Lang et al., 2012). Fiber wall-thickness is one of the main determinants of wood density, which in turn is related to growth and survival rates and life span. Early angiosperms have been suggested to be short statured plants that thrived in wet, disturbed areas (Wing and Boucher, 1998; Morley, 2003; Coiffard et al., 2007) and therefore they likely inhabited a very restricted functional space characterized by fast growth rates, short lifespans and low resistance to cavitation. The lack of wood anatomical diversity in Early Cretaceous angiosperms suggests a delay in wood structural/functional differentiation, relative to the taxonomic diversification, and could be the result of this initial restriction in their ecological niche space. A similar delay in functional diversification has been inferred for leaves as they expanded their initial hydraulic capacity (vein density) only towards the Late Cretaceous (Feild et al., 2011). During the first 30 million years of their evolution, angiosperms had a vein density similar to that of contemporary ferns and gymnosperms, but they increased their hydraulic niche first during the midCretaceous, going beyond the hydraulic capacity of contemporaneous ferns and gymnosperms, and then at the Cretaceous–Paleogene boundary when they reached the hydraulic capacity levels of modern magathermal forest plants (Feild et al., 2011). A second source of evidence indicating that wood structure might have slow rates of evolution is the significant levels of phylogenetic conservatism of some wood anatomical traits (e.g., Zanne et al., 2010; Zheng and Martínez-Cabrera, 2013). It is, however, unclear if this trend is the result of constant conservatism through time or, as suggested by the early fossil wood record, there is an initial lack of differentiation among closely related species followed by a burst in functional diversification in the latest Cretaceous. Early phylogenetic conservatism may explain the delay in anatomical differentiation relative to reproductive structures. When phylogenetic conservatism is strong, species may experience difficulties to colonize and to adapt to new environments (Losos, 2008), while rapidly evolving traits may fuel the spread into new adaptive zones (e.g., Kozak and Wiens, 2010a) and clades can experience greater diversification success (Holt, 1990). Therefore, determining temporal patterns of phylogenetic trait conservatism-lability may help us to ascertain the processes that constrained xylem anatomy and functional strategies during the early evolution of the angiosperms, and when and why the evolutionary constraints were lifted contributing to the diversification of wood function that powered the eventual niche expansion of the angiosperms.

Here, using a dataset for wood traits of 1053 extant angiosperms we set out to determine the temporal patterns of wood disparification (accumulation of functional diversity among closely related species) of three interrelated axes of xylem structural variation linked to support, storage and water conduction. We tested the hypothesis of early trait conservatism. This hypothesis is suggested by the limited structural differentiation and low diversity of the early angiosperm wood fossil record. The three axes of variation we studied provide information on particular structural and ecological aspects of wood. 1) The support axis, which is mainly driven by fiber traits (e.g., Martínez-Cabrera et al., 2009), is linked to wood density, plant biomechanics and therefore is related to life history traits (growth rate, life span, survival; Roderick, 2000; Muller-Landau, 2004), successional stage (Saldarriaga et al., 1988; Swaine and Whitmore, 1988), ecosystem productivity, and global carbon cycling (Chave et al., 2009). 2) The hydraulic axis is anatomically driven by vessel characteristics and influences water conduction efficiency and cavitation resistance (Zimmermann, 1983). This functional axis also relates to gas exchange, carbon fixation rates and growth rates (Tyree, 2003; Poorter et al., 2009). 3) The storage axis, determined by parenchyma traits, is related to a multitude of functions including plant defense (Deflorio et al., 2008), storage and transport of carbohydrates (Hoch et al., 2003), and possibly to horizontal water transport which might be linked to embolism repair (Bucci et al., 2003; Salleo et al., 2004). Because wood anatomical traits are ultimately linked to ecological strategies of plants and ecosystem function (e.g., water transport, growth, carbon and nitrogen cycling), the temporal pattern of diversification of these aspects of wood function will help to better understand angiosperm niche evolution and its relationship with historical ecosystem change.

2. Materials and methods We examined the temporal patterns in wood functional disparity in two trait datasets that we used in previous publications. One comprises species from the Americas and includes cell dimensions and hydraulic properties (Martínez-Cabrera and Cevallos-Ferriz, 2008; Martínez-Cabrera et al., 2009, 2011; Schenk et al., 2009), the other is a Chinese dataset including proportion of cross sectional areas occupied by each cell type (Zheng and Martínez-Cabrera, 2013). Both datasets are presented in as supplementary material. We determined the temporal patterns of anatomical differentiation in fiber and vessel dimensions, theoretical conductivity (Kt) and vulnerability index (VI) using data from 272 species from the Americas (USA, Argentina (Martínez-Cabrera et al., 2009; Schenk et al., 2009), Mexico, Brazil and Suriname (Martínez-Cabrera and Cevallos-Ferriz, 2008; Martínez-Cabrera et al., 2011)). This database comprises trees and shrubs collected for largescale studies and therefore they are ecologically (from tropical rain forest to desert vegetation) and phylogenetically diverse. The anatomical traits for the species from USA and Argentina (Martínez-Cabrera et al., 2009, 2011; Schenk et al., 2009) were measured in radial sectors of the two most recent growth rings. For these 63 species, vessel lumen diameters were calculated as the diameters of circles with the same area of individual vessel lumens (Kolb and Sperry, 1999) and were based on at least 200 vessels per sample (Martínez-Cabrera et al., 2009; Schenk et al., 2009). For the Mexican, Brazilian and Surinamese tree communities (209 species), tangential vessel diameter was measured directly from the slides and was based on at least 25 randomly selected vessels (IAWA, 1989). For these sites, vessel density was determined in at least 10 fields of view; in the Argentinean and North American sites, traits were determined in entire radial sectors. Fiber diameter, fiber and vessel wall thickness and fiber wall to lumen ratio was measured on at least 25 (MartínezCabrera and Cevallos-Ferriz, 2008 dataset) cells and up to 200 cells (Martínez-Cabrera et al., 2009, 2011; Schenk et al., 2009). Potential conductivity per cross sectional sapwood area was calculated using a modiP 4 fied Hagen–Poiseuille equation ( K t ¼ ðπρ=128ηÞ ni¼1 di ; Tyree and


Ewers, 1991): where ρ is the density of the fluid in km·m−3; η is the dynamic viscosity of the fluid in MPa·s−1; n is the number of vessels; and d is the diameter of the vessels. Vulnerability Index (VI) was calculated as vessel diameter/vessel density (Carlquist, 1977). We also determined patterns of disparification in the proportions of cross sectional area occupied by vessels, fibers, rays, axial parenchyma and cell wall in 781 tree species from China (Zheng and MartínezCabrera, 2013) whose anatomy was described earlier (Yang and Lu, 1993; Yang and Yang, 2001; Yang et al., 2009). Most of the species were sampled in the Eastern Monsoonal climate zone in China and include elements from temperate, sub-tropical and tropical forests (Zhao, 1995). Wood anatomical traits were measured from the outermost portions of the sampled discs. The proportion of cross-sectional area occupied by vessels, fibers, rays, axial parenchyma and cell wall was measured using an optical microscope and an attached image analyzer (Zeng et al., 1985) in fields of view of 1 mm2. In ring-porous woods, the proportion of area occupied by each cell type was determined by measuring four fields of view, two each in early wood and late wood. In diffuse-porous woods, the proportion of each cell type was calculated from three fields of view from the early, middle and late growth portions of the growth rings. The proportions of various tissues were calculated as the mean values of these fields of view. Total cell wall area was the total dark area in a field of view and represents the cell wall of all cell types. In addition, to visualize the functional axes of variation in each dataset, we carried out principal component analyses (PCA) to then run a disparity analysis on the species PCA scores in the first three principal components to determine temporal lability patterns of functional morphospace. The phylogenetic relationships among species were reconstructed using the program PHYLOMATIC (Webb and Donoghue, 2005). Polytomies were treated as soft and the resulting tree was randomly resolved. Branch lengths of the resulting trees were calculated using the branch length-adjusting algorithm (bladj) implemented in the program PHYLOCOM (Webb et al., 2007). The phylogenetic trees were calibrated using angiosperm node ages provided in Wikstrom et al. (2001). The root of both trees corresponds to the divergence between Magnoliids and eudicots (estimated age = 161 million years). To quantify the functional diversification over time we used disparity through time method (DTT, Harmon et al., 2003) for each trait and PC axes. The DTT analyses were run for individual variables and the scores of the first three PC axes for both datasets. DTT for each trait is calculated from the standardized mean pairwise Euclidean distance between species. At each node in the phylogeny the mean relative disparity was calculated for all clades with ancestral lineages present at that point in time, then these disparities are plotted as a function of relative time. Values near 0 indicate that greater divergence in trait values occurred among clades rather than within clades and therefore is an indication of conservatism in closely related species. If trait variation is partitioned within the axial parenchyma area

PCA 2

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members of subclades (values near 1) indicate trait lability. Disparity analysis allows visualizing temporal shifts in patterns of trait conservatism-lability. The degree to which the calculated mean disparity deviated from the null expectations under unconstrained Brownian motion evolution was evaluated by performing 1000 simulations of each trait on the ultrametric tree. To compare the relative disparity with the null hypothesis, we used the morphological disparity index (MDI), which is the area between the calculated and median of the simulated disparities at each level in the phylogeny (Harmon et al., 2003). Negative values of MDI (i.e. a negative difference between the observed disparity and the median of the simulated values) indicate that variation is predominantly partitioned among subclades, while positive values indicate that variance is predominantly partitioned within clades. 3. Results In PCA including the cell-type area data, the first three principal component analysis explained 88% of the variation. In this analysis (Fig. 1A), the first PC axis represents a trade-off between space devoted to conduction (vessel area) and investment in support (fiber and wall areas), while the second PC represents a previously described tradeoff between axial and radial parenchyma (Martínez-Cabrera et al., 2009; Zheng and Martínez-Cabrera, 2013). In PCA of the cell dimensions data (the Americas dataset), the three first principal components explained 72% (Fig. 1B). The first PC axis represents in this analysis the trade-off between conduction capacity (vessels diameter, Kt and vulnerability index) and support (fibers wall-thickness and vessel density). The second PC reflects the negative relationship between fiber diameter and fiber wall to lumen ratio and it is therefore a mechanical support axis. Most of the traits and PC functional axes showed a temporally heterogeneous disparity pattern, with low disparity (relative to the null expectations) early to then increase between 120 and 80 million years ago (Aptian–Campanian) (Figs. 2, 3). This pattern indicates low levels of anatomical, and likely functional, differentiation among closely related species early in the history of angiosperms (most of the evolution occurred among clades at this point), followed by a burst in functional evolution among closely related species. Only fiber diameter (Fig. 3E) and ray area (Fig. 3K) had constantly high disparity throughout the history of the angiosperms (high anatomical differentiation among closely related species). Some traits, especially those related to the water conduction functional axis, such as vessel density, Kt and VI have more recent peaks of disparity. For the last two traits, these peaks occurred during the last 32 million years. Vessel density, diameter, Kt, VI, fiber wall-thickness, and parenchyma area and the first two PC axes of the American dataset, not only had low early disparity values, but it was lower than the expected under the null hypothesis. The mean MDI

B

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vessel density

vessel wall-thickness

vessel diameter

fiber wall-thickness

VI K t wall area

ray area

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fiber wall to lume ratio

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Fig. 1. Loading plots of anatomical traits on the first two principal component axes in the Chinese (A) and the Americas (B) datasets.

4. Discussion Previous studies have found low levels of wood trait divergence among closely related species, suggesting that some of the wood functions (Zheng and Martínez-Cabrera, 2013) and wood functional traits (Martínez-Cabrera et al., 2009, 2011; Zanne et al., 2010) are phylogenetically conserved. Here we found a heterogeneous pattern of functional variation throughout time consistent with a phase of wood anatomical conservatism early in the history of angiosperms followed by increased lability towards the present. In consequence, we suggest that the pattern of overall high conservatism in wood traits evidenced in other studies (Zanne et al., 2010; Zheng and Martínez-Cabrera, 2013), is driven by the high levels of early trait conservatism. This early lack of structural disparity within clades might explain the reduced number of wood morphotypes found in the early angiosperm fossil record and the apparent lack of anatomical differentiation among groups (i.e. morphotypes probably representing more than one taxonomic unit, see Herendeen, 1991). Conceivably, early conservatism could be one of the reasons of the restricted ecological niche of angiosperms during their first 50 million years of existence. Molecular evidence suggests that early basal angiosperm lineages were small trees, shrubs and vines and that likely occupied disturbed areas and could have grown in alluvial plains (Wing and Boucher, 1998; Morley, 2003; Coiffard et al., 2007). This ecological niche would entail a functional strategy consistent with a fast growth rate and low resistance to embolism and therefore low investment in support tissue as most of the Early Cretaceous angiosperms have thin-walled fibers (Philippe et al., 2008). This strategy could have restricted the distribution of the angiosperms during the first part of the Early Cretaceous, as it was a globally dry period (Skelton et al., 2003), hindering for some time the opportunities for the ecological and functional expansion of the angiosperms. In this sense, the lack of opportunities for diversification due to restrictions in habitat availability, together with the early trait conservatism we detected, likely precluded the incursion of the group into new niches and limited the morphospace evolution of the group. The later burst in trait lability of wood functional traits in concert with the escalation of the leaf hydraulic function (Feild et al., 2011), tree and canopy size (Upchurch and Wolfe, 1993), woodiness (e.g., Philippe et al., 2008) and biomass (Upchurch and Wolfe, 1993) of the angiosperms that occurred towards the mid to Late Cretaceous, helped angiosperms to spread into new adaptive zones and experience even greater diversification success. Accelerated trait evolution (i.e. trait lability) often promotes lineages to successfully explore new environments (e.g., Kozak and Wiens, 2010b) and experience higher rates of diversification (Holt, 1990). Although vessel conduction efficiency played a major role in the rising of the ecological dominance of the group (Feild and Wilson, 2012) and its influence in the global ecosystem (Upchurch and Wolfe, 1993; Boyce et al., 2010), there is another aspect of vessel evolution that had a profound impact in the wood structural evolution of angiosperms.

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(the difference between the observed disparity and the median of the simulated values) for all traits and PC axes were positive, indicating that trait evolution has taken place through within-clade differentiation (Table 1). Although, as mentioned above, the early MDI values of many of the traits is negative, suggesting an early lack of functional and anatomical differentiation among closely related species.

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Fig. 2. Relative disparity plots for PC functional axes representing. A) the trade-off between cross sectional area invested in conduction and support; B) and between axial and radial parenchyma areas; C) represents the trade-off between Kt and vulnerability index with fiber wall-thickness and D) is the support axis in the American dataset. The continuous line represents the measured relative disparity and the dashed line is the median expected disparity based on simulations. Larger positive area between the observed disparity curve (solid line) and the median of the simulated values (dashed) indicates higher degree of structural differentiation among close relatives. Negative area between the two curves indicates that variation is partitioned among subclades rather than among close relatives. RT = relative time, MY = million years ago.

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Fig. 3. Relative disparity plots for some wood anatomical traits. A) vessel density; B) vessel diameter; C) Kt; D) vulnerability index; E) fiber diameter; F) fiber wall-thickness; G) fiber wall to lumen ratio, H) vessel area, I) wall area; J) fiber area; K) ray area; L) parenchyma area.

The functional expansion of the short-statured Early Cretaceous angiosperms that resulted in their ecological niche widening, did not exclusively relied on the increased hydraulic capacity of vessels relative to tracheids. In fact, it is improbable that reduction in flow resistivity of vessels alone explains the successful ecological expansion in the group since basal vessel bearing and vesselless angiosperms have similar area specific hydraulic conductivity (Sperry et al., 2007). Instead, the functional advantage of the wood of basal angiosperms with vessels over vesselless is that similar hydraulic capacity is reached by devoting

lower cross sectional area to water conduction (they have conduit basis lower resistivity of vessels relative to tracheids). Thus, it seems that the reduced allocation of space to conducting area lifted, or at least relaxed, developmental constraints and propelled evolution of other cell types (evolution of heteroxylly) involved in radial biomechanics, radial transport and storage without sacrificing conduction efficiency (Sperry et al., 2007; Feild et al., 2011; Feild and Wilson, 2012). The evolution of the other cell types (in particular their proportions and spatial arrangement) and their associated ecological function likely opened new

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Table 1 Morphological disparity indices (MDI). American dataset

Chinese dataset

Trait

MDI

Trait

MDI

Vessel diameter Vessel density KT Vessel wall thickness Vulnerability index Fiber diameter Fiber wall thickness Fiber wall to lumen ratio PC1 PC2 PC3

0.116 0.045 0.029 0.084 0.032 0.281 0.195 0.104 0.048 0.173 0.097

Vessel area Cell wall area Fiber area Ray area Axial parenchyma area PC1 PC2 PC3 – – –

0.221 0.387 0.213 0.300 0.036 0.249 0.146 0.229 – – –

evolutionary venues over which functional, structural and ecological diversification occurred (Feild and Wilson, 2012). Our results indicate that this process of anatomical expansion among closely related species occurred by the mid to Late Cretaceous and therefore it took place several million years after the origin of the angiosperms. Feild and Wilson (2012) suggest that the advantage of specialization of cells related to support, storage and conduction of heteroxylous relative to the homoxylous basal angiosperms could be restricted to wet habitats since the former are more vulnerable to embolisms but with similar resistivity and suggest that vessel evolution in early stages was more driven by cavitation risk than by transport efficiency. Therefore, they suggest that the well-described trade-off between transport efficiency and safety evolved only with the radiation of the core angiosperms. Our analysis does not allow us to determine whether or not there have been shifts in conduction capacity. Instead, we found that traits related with conduction efficiency (vessel diameter, potential conductivity and vulnerability index) were among the traits with longer periods of early conservatism, and therefore indicate that the expansion of the water conduction strategies among closely related species occurred more recently. A perhaps more striking results is the constantly high level of disparity, relative to the null expectations, of ray area and fiber diameter. Especially the high early disparity levels of ray area suggest that the early functional expansion of the radial system might have played a prominent role in the ecology of the angiosperms. Ray structural differentiation, particularly the increment of ray tissue of angiosperms relative to the gymnosperms, is often seen as one of the its key innovation (Carlquist, 1975) as it influences radial transport and storage (Sauter and van Cleve, 1994), radial biomechanics (Mattheck and Kubler, 1995; Burgert et al., 1999; Burgert and Eckstein, 2001), and has been related to the enhanced resprouting capacity of early angiosperms in response to disturbance (Feild et al., 2004; Morris et al., 2015). The early lability of fiber diameter would seem counterintuitive in light of the current knowledge of the habit and ecology of early angiosperms. Fiber diameter determines fiber wall-thickness and fiber wall to lumen ratio and therefore influences wood density (MartínezCabrera et al., 2009), which is key functional traits that integrates variation in other life history traits (e.g., Poorter et al., 2009). Given the presumed weak woodiness of the early angiosperms (Philippe et al., 2008), which is also observed in extant basal angiosperm lineages (Feild and Wilson, 2012), a more constrained pattern of within clade differentiation (i.e. conservatism) would be expected since their habit and anatomy seems to be limited. Our analysis, however, only allows to follow patterns of trait similarity among closely related species, and not to trace trait values in time and therefore even within restricted morphospaces (size of the total morphospace for a particular time slice) there could be high levels of partition among closely related species. Because of the high prevalence of early conservatism, our results have also profound implications for the use of fossil wood in

paleoclimate reconstruction since it touches the basic assumption of trait environmental convergence and its constancy trough time (biological uniformitarism). Prevalence of high phylogenetic signal early in the history of angiosperms imply that a large proportion of trait variation is explained by phylogeny, rather than by environment alone and, even if adaptive environmental convergence is present today, larger errors in paleoclimate estimates should be expected as we go deeper in time. Our results in this regard support the findings of an extensive survey of fossil wood anatomy (Wheeler and Baas, 1991), suggesting a nonconstant relationship between some wood anatomical traits and climate through time. Many of the ecologically informative traits (e.g., some vessel distribution patterns, helical thickenings in vessel walls, vessel groupings, and elaborated paratracheal axial parenchyma distributions) only appeared in the fossil record during the Paleogene, therefore limiting their utility until after this period (Wheeler and Baas, 1991). Acknowledgments We thank Elisabeth Wheeler and two anonymous reviewers for their helpful comments on a previous version of the manuscript. This research was funded by the CONACyT (240241) and the SIP-IPN (20170872) grants to EER. Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.revpalbo.2017.07.008. References Barale, G., Barbacka, M., Philippe, M., 2002. Early Cretaceous flora of Hungary and its palaeoecological significance. Acta Palaeobot. 42, 13–27. Boyce, C.K., Lee, J.E., Feild, T.S., Brodribb, T.J., Zwieniecki, M.A., 2010. Angiosperms helped put the rain in the rainforests: the impact of plant physiological evolution on tropical biodiversity. Ann. Mo. Bot. Gard. 97, 527–540. Bucci, S.J., Scholz, F.G., Goldstein, G., Meinzer, F.C., Sternberg, L.D.S.L., 2003. Dynamic changes in hydraulic conductivity in petioles of two savanna tree species: factors and mechanisms contributing to the refilling of embolized vessels. Plant Cell Environ. 26, 1633–1645. Burgert, I., Eckstein, D., 2001. The tensile strength of isolated wood rays of beech (Fagus sylvatica L.) and its significance for the biomechanics of living trees. Trees 15, 168–170. Burgert, I., Bernasconi, A., Eckstein, D., 1999. Evidence for the strength function of rays in living trees. Holz Roh Werkst. 57, 397–399. Carlquist, S., 1975. Ecological Strategies of Xylem Evolution. Univ. Calif. Press, Berkeley. Carlquist, S., 1977. Ecological factors in wood evolution: a floristic approach. Am. J. Bot. 64, 887–896. Chave, J., Coomes, D., Jansen, S., Lewis, S.L., Swenson, N.G., Zanne, A.E., 2009. Towards a worldwide wood economics spectrum. Ecol. Lett. 12, 351–366. Coiffard, C., Gomez, B., Thévenard, F., 2007. Early Cretaceous angiosperm invasion of Western Europe and major environmental changes. Ann. Bot. 100, 545–553. Crane, P.R., Lidgard, S., 1989. Angiosperm diversification and paleolatitudinal gradients in Cretaceous floristic diversity. Science 246, 675–678. Crane, P.R., Friis, E.M., Pedersen, K.R., 1995. The origin and early diversification of angiosperms. Nature 374, 27–33. Crane, P.R., Friis, E.M., Pedersen, K.R., 2000. The origin and early diversification of angiosperms. Shaking the Tree: Readings From Nature in the History of Life, pp. 233–250. Crawley, M., 2001. Angiosperm woods from British Lower Cretaceous and Palaeogene deposits. Spec. Pap. Palaeontol. 66, 1–100. Deflorio, G., Johnson, C., Fink, S., Schwarze, F.M.W.R., 2008. Decay development in living sapwood of coniferous and deciduous trees inoculated with six wood decay fungi. For. Ecol. Manag. 255, 2373–2383. Falcon-Lang, H.J., Kvaček, J., Uličný, D., 2001. Fire-prone plant communities and palaeoclimate of a Late Cretaceous fluvial to estuarine environment, Pecínov quarry, Czech Republic. Geol. Mag. 138, 563–576. Falcon-Lang, H.J., Wheeler, E.A., Baas, P., Herendeen, P., 2012. A diverse charcoalified assemblage of Cretaceous (Santonian) angiosperm woods from Upatoi Creek, Georgia, U.S.A. Part 1. Morphotypes with scalariform perforation plates. Rev. Palaeobot. Palynol. 184, 49–73. Feild, T.S., Wilson, J.P., 2012. Evolutionary voyage of angiosperm vessel structure-function and its significance for early angiosperm success. Int. J. Plant Sci. 2012, 596–609. Feild, T.S., Arens, N.C., Doyle, J.A., Dawson, T.E., Donoghue, M.J., 2004. Dark and disturbed: a new image of early angiosperm ecology. Paleobiology 30, 82–107. Feild, T.S., Brodribb, T.J., Iglesias, A., Chatelet, D.S., Baresch, A., Upchurch Jr., G.R., Gomez, B., Mohr, B.A.R., Coiffard, C., Kvacek, J., Jaramillo, C., 2011. Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution. Proc. Natl. Acad. Sci. 108, 8363–8366.

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