Pollinator adaptation and the evolution of floral nectar sugar composition

A long‐standing debate concerns whether nectar sugar composition evolves as an adaptation to pollinator dietary requirements or whether it is ‘phylogenetically constrained’. Here, we use a modelling approach to evaluate the hypothesis that nectar sucrose proportion (NSP) is an adaptation to pollinators. We analyse ~ 2100 species of asterids, spanning several plant families and pollinator groups (PGs), and show that the hypothesis of adaptation cannot be rejected: NSP evolves towards two optimal values, high NSP for specialist‐pollinated and low NSP for generalist‐pollinated plants. However, the inferred adaptive process is weak, suggesting that adaptation to PG only provides a partial explanation for how nectar evolves. Additional factors are therefore needed to fully explain nectar evolution, and we suggest that future studies might incorporate floral shape and size and the abiotic environment into the analytical framework. Further, we show that NSP and PG evolution are correlated – in a manner dictated by pollinator behaviour. This contrasts with the view that a plant necessarily has to adapt its nectar composition to ensure pollination but rather suggests that pollinators adapt their foraging behaviour or dietary requirements to the nectar sugar composition presented by the plants. Finally, we document unexpectedly sucrose‐poor nectar in some specialized nectarivorous bird‐pollinated plants from the Old World, which might represent an overlooked form of pollinator deception. Thus, our broad study provides several new insights into how nectar evolves and we conclude by discussing why maintaining the conceptual dichotomy between adaptation and constraint might be unhelpful for advancing this field.     

Diversity and evolution of floral structure among early diverging lineages in the Ericales

This is a combination of review and original data on floral structure and diversity in the two earliest diverging lineages of the Ericales, i.e. the balsaminoids, comprising Balsaminaceae, Marcgraviaceae and Tetrameristaceae, and the polemonioids, comprising Fouquieriaceae and Polemoniaceae. Each clade is strongly supported in molecular studies, while structural synapomorphies have largely been lacking. For the balsaminoid families, we compare floral morphology, anatomy and histology among selected taxa and find that the entire clade is strongly supported by the shared presence of nectariferous tissue in the floral periphery, thread-like structures on anthers, truncate stigmas, secretion in the ovary, as well as mucilage cells, raphides and tannins in floral tissues. A possible sister group relationship between Balsaminaceae and Tetrameristaceae is supported by the shared presence of post-genital fusion of filaments and ovary and a star-shaped stylar canal. For polemonioids, we document unexpected diversity of floral features in Polemoniaceae, partly providing structural links to Fouquieriaceae. Features include cochlear and quincuncial corolla aestivation, connective protrusions, ventrifixed anthers and nectariferous tissue in the base of the ovary. In addition, we outline future directions for research on floral structure in the Ericales and briefly discuss the general importance of structural studies for our understanding of plant phylogeny and evolution.     

A phylogenetic analysis of 100+ genera and 50+ families of euasterids based on morphological and molecular data with notes on possible higher level morphological synapomorphies

 A data matrix of 143 morphological and chemical characters for 142 genera of euasterids according to the APG system was compiled and complemented with rbcL and ndhF sequences for most of the genera. The data were subjected to parsimony analysis and support was assessed by bootstrapping. Strict consensus trees from analyses of morphology alone and morphology + rbcL + ndhF are presented. The morphological data recover several groups supported by molecular data but at the level of orders and above relationships are only superficially in agreement with molecular studies. The analyses provide support for monophyly of Gentianales, Aquifoliales, Apiales, Asterales, and Dipsacales. All data indicate that Adoxaceae are closely related to Dipsacales and hence they should be included in that order. The trees were used to assess some possible morphological synapomorphies for euasterids I and II and for the orders of the APG system. Euasterids I are generally characterised by opposite leaves, entire leaf margins, hypogynous flowers, “early sympetaly” with a ring-shaped corolla primordium, fusion of stamen filaments with the corolla tube, and capsular fruits. Euasterids II often have alternate leaves, serrate-dentate leaf margins, epigynous flowers, “late sympetaly” with distinct petal primordia, free stamen filaments, and indehiscent fruits. It is unclear which of these characters represent synapomorphies and symplesiomorphies for the two groups, respectively, and there are numerous expections to be interpreted as reversals and parallelisms. Received August 28, 2000 Accepted August 7, 2001     

Early floral development and androecium organization in the sarracenioid clade (Actinidiaceae,Roridulaceae and Sarraceniaceae) of Ericales

The early floral development of Actinidia (A. arguta, A. callosa, A. chinensis and A. kolomikta; Actinidiaceae), Saurauia (S. montana, S. oldhamii, S. pittieri and S. subspinosa; Actinidiaceae), Roridula gorgonias (Roridulaceae) and Heliamphora nutans (Sarraceniaceae) was studied comparatively using scanning electron microscopy. Late stages of androecium development are additionally presented for Clematoclethra scandens (Actinidiaceae), Darlingtonia californica and Sarracenia leucophylla (Sarraceniaceae). Flowers are typically pentamerous and share a number of developmental features: perianth organs emerge in a clockwise or anticlockwise spiral sequence on the floral apex with relatively long plastochrons between successive organs, resulting in conspicuous size differences among perianth organs in early development; the perianth always consists of two differentiated whorls (unlike earlier interpretations of the perianth in Heliamphora); the androecium is polystemonous in most species and is initiated with leading stamens in alternipetalous positions; successive stamen primordia appear in a lateral succession until a ring‐like structure is formed; and the anthers become inverted shortly before anthesis. Later androecial development differs conspicuously between taxa and further proliferation may be centrifugal, centripetal and/or lateral. For Ericales, unusual features of floral development include: petals initiated in a spiral sequence (but later organized in a whorl) with comparatively long plastochrons between individual petals (except Saurauia); common occurrence of perianth organs in double positions in Actinidiaceae; and anthers that become inverted close to anthesis. The floral development in the sarracenioids is additionally compared with that of other families and clades in Ericales, further emphasizing the highly variable patterns of androecium development in the order.     

Calcium plus magnesium indicates digestibility: the significance of the second major axis of plant chemical variation for ecological processes

Plant variation in nutrient concentrations encompasses two major axes. The first is connected to nitrogen (N) and phosphorus (P), reflects growth rate and has been designated as the leaf economics spectrum (LES) while the second follows the gradient in calcium (Ca) and magnesium (Mg) and mirrors cell structural differences. Here, we tested in grasslands whether the sum Ca + Mg concentrations is a better indicator of digestibility than LES constituents. Structural equation modelling revealed that the total effect size of N (0.30) on digestibility was much lower than that of Ca + Mg (0.58). The N effect originated predominantly from sampling date (biomass ageing), while the Ca + Mg effect largely from phylogenetic composition (proportion of monocots). Thus, plant variation in partially substitutable divalent cations seems to play a significant role in biomass digestion by ruminants. This finding contests, together with litter decomposition studies, the prominent role of the LES for understanding both fundamental ecological processes.     

Sequences of 72 plastid genes support the early divergence of Cornales in the asterids

Recent phylogenetic analyses of molecular data have supported different hypotheses of relationships among Cornales,Ericales,and core asterids.Such hypotheses have implications for the evolution of important morphological and embryological features of asterids.In this study we generated plastid genome-scale data of Davidia (Cornales) and Franklinia (Ericales) and combined them with published sequence data of eudicots.Our maximum parsimony,maximum likelihood,and Bayesian analyses generated strongly supported and congruent phylogenetic relationships among the three major lineages of the asterids.Cornales diverges first in asterids; Ericales is sister to the core asterids.Adding two more taxa helps mitigate long branch attraction in parsimony analyses.Sampling 26-28 plastid protein-coding genes may provide satisfactory resolution and support for relationships of eudicots including basal lineages of asterids.     

Comparative floral structure and systematics in the balsaminoid clade including Balsaminaceae,Marcgraviaceae and Tetrameristaceae (Ericales)

Based on molecular phylogenetic studies, Balsaminaceae, Tetrameristaceae (including Pellicieraceae) and Marcgraviaceae form the strongly supported first branching clade in the asterid order Ericales. Marcgraviaceae and Tetrameristaceae were proposed to be closely related in pre‐molecular studies, but the systematic position of Balsaminaceae has been controversial for some time and a relationship with the other two families was never suggested in pre‐molecular/pre‐cladistic times. However, interfamilial relationships in the clade are still unclear because of conflicting phylogenetic hypotheses from molecular analyses. In order to assess the validity of these molecular hypotheses from a morphological point of view, the floral morphology, anatomy and histology of Balsaminaceae, Tetrameristaceae and Marcgraviaceae are comparatively studied in detail. In addition, earlier literature is reviewed. The monophyly of the balsaminoid clade is strongly supported by floral structure, and a series of potential floral synapomorphies is identified for the clade. Prominent features shared by the three families include broad and dorsiventrally flattened filaments, thread‐like structures lining the stomia of dehisced anthers, secretory inner morphological surfaces of the gynoecium, ovules intermediate between uni‐ and bitegmic, incompletely tenuinucellar ovules, fruits with persistent style and stigma, seeds lacking endosperm and several anatomical/histological traits. The families are also distinctive because the bracts and/or sepals are petaloid and nectariferous. Further, the floral structure supports a sister group relationship between Balsaminaceae and Tetrameristaceae rather than any of the other possible interfamilial relationships. These two families share a caducous calyx, post‐genital fusion/coherence of filaments and ovary surface, latrorse anther dehiscence, commissural carpel lobes and ovules with a thickened funiculus and a constricted chalazal region. The occurrence of these features in Ericales is discussed. Future structural studies in other ericalean lineages and additional molecular studies are needed to further test these features with respect to their systematic value for the balsaminoid clade. Some may turn out to be true synapomorphies, whereas others may be recognized as plesiomorphies, as they may be more widely spread in Ericales than currently thought. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173 , 325–386.