Nectar, floral morphology and pollination syndrome in Loasaceae subfam. Loasoideae (Cornales)

BACKGROUND AND AIMS: Loasaceae subfam. Loasoideae are mostly distributed in South America (sea level to over 4500 m) with a wide range of animals documented as pollinators. The aim was to investigate correlations between nectar parameters, flower morphology, pollination syndrome and phylogeny. METHODS: Nectar was collected from 29 species from seven genera in the subfamily. Concentration and volumes were measured and the amount of sugar calculated. Correlations of nectar data were plotted on a ternary graph and nectar characteristics compared with flower visitors, floral morphology and phylogenetic data. KEY RESULTS: Sugar concentrations are generally higher than reported for most plant families in the literature. The species investigated can be roughly grouped as follows. Group I: plants with approx. 1.5(-3.5) microL nectar with (40-)60-80% sugar and 0.19-2 mg sugar flower-1; with small, white, star-shaped corollas, pollinated by short-tongued bees. Groups II, III and IV: plants with mostly orange, balloon-, saucer-, bowl- or bell-shaped corollas. Group II: plants with approx. 9-14 microL nectar with 40-60% sugar and 4-10 mg sugar flower-1; mostly visited by long-tongued bees and/or hummingbirds. Group III: plants with 40-100 microL nectar with 30-40% sugar and 14-36 mg sugar flower-1, mostly visited by hummingbirds. Group IV: geoflorous plants with 80-90 microL with 10-15% sugar and 8.5-12 mg sugar flower-1, presumably visited by small mammals. Groups II and III include species visited by bees and/or hummingbirds. CONCLUSIONS: Pollinator switches from short-tongued bees via long-tongued bees to hummingbirds appear to have taken place repeatedly in the genera Nasa, Loasa and Caiophora. Changes in nectar amount and concentration appear to evolve rapidly with little phylogenetic constraint.     

Reciprocal developmental changes in the roles of Bcl-w and Bcl-x(L) in regulating sensory neuron survival

We have compared the roles of two anti-apoptotic members of the Bcl2 family, Bcl-w and Bcl-x(L), in regulating the survival of sensory neurons during development. We used microinjection to introduce expression plasmids containing Bcl-w and Bcl-x(L) cDNAs in the sense and antisense orientations into the nuclei of BDNF-dependent nodose neurons and NGF-dependent trigeminal neurons at stages during and after the period of naturally occurring neuronal death. Whilst overexpression of either protein promoted neuronal survival in the absence of neurotrophins and microinjection of antisense constructs reduced neuronal survival in the presence of neurotrophins, the magnitude of these effects changed with age. Whereas Bcl-w overexpression became more effective in promoting neuronal survival with age, Bcl-x(L) overexpression became less effective, and whereas antisense Bcl-w became much more effective in killing neurotrophin-supplemented neurons with age, antisense Bcl-x(L) became much less effective in killing these neurons. There was a marked increased in Bcl-w mRNA and Bcl-w immunoreactive neurons and a decrease in Bcl-x(L) mRNA and Bcl-x(L) immunoreactive neurons in the trigeminal and nodose ganglia over this period of development. Our results demonstrate that both Bcl-w and Bcl-x(L )play an important anti-apoptotic role in regulating the survival of NGF- and BDNF-dependent neurons, and that reciprocal changes occur in the relative importance of these proteins with age. Whereas Bcl-x(L) plays a more important role during the period of naturally occurring neuronal death, Bcl-w plays a more important role at later stages.     

Floral organogenesis and floral evolution of the Lecythidoideae (Lecythidaceae)

The subfamily Lecythidoideae of Lecythidaceae (Brazil nut family) is a dominant group in neotropical forests, especially those of Amazonia. New World members of the family have large showy flowers that are either polysymmetric or monosymmetric. In this study, floral organogenesis of all 10 neotropical genera was examined using SEM. Our observations of floral development are put into the context of a molecular phylogeny based on sequences of the ndhF and trnL-F genes (Am. J. Bot. 94: 289-301). Floral evolution of the subfamily is explained as having undergone four different levels of complexity in regard to floral symmetry. The basal most genera, Grias and Gustavia, have polysymmetric flowers. At level two, represented only by Couroupita, monosymmetry is established through the expression of abaxial dominance and the development of an androecial hood; at this level, abaxial dominance impacts the perianth and androecium, but not the gynoecium. At the third level, monosymmetry is developed in groups of Couratari and Cariniana domestica; but, in the Allantoma/Cariniana decandra lineage, a reversal back to polysymmetric flowers, resulting from a gradual weakening of abaxial dominance, and the loss of the hood has occurred. Finally, in level four, including Bertholletia, Corythophora, Eschweilera, and Lecythis, monosymmetry is so strongly expressed that the gynoecium is also influenced by abaxial dominance. In this group, the hood is complicated in both structure and function, and the floral axis is changed from straight to slightly inclined. This study demonstrates that the development of floral abaxial dominance is the proximate cause of monosymmetry in the Lecythidoideae. We suggest that monosymmetric flowers are more efficiently pollinated, and therefore the bees and bats that pollinate the monosymmetric flowers in this group are ultimately responsible for the monosymmetry.     

Fossil floral and fruit evidence for the evolution of unusual developmental characters in Fagales

Flowers of many living Fagales exhibit unusual developmental characteristics. At anthesis, ovulate flowers have carpels bearing immature orthotropous ovules. After pollination, the ovules increase in size and become anatropous and the ovary enlarges. Simultaneously, the pollen tubes extend from the stigma to the ovules with several phases of growth and quiescence. Finally, after the first fertilization, the remaining ovules abort, resulting in a single‐seeded fruit. Three‐dimensionally preserved potentially fagaceous mesofossil flowers from the Campanian of Massachusetts, USA, provide evidence on the evolution of these characters. The fossils share putative synapomorphies with the Fagales (six tepals, mostly inferior, three‐carpellate ovary with each locule initially containing two pendant ovules, punctate‐rugulate, tricolporate pollen and fruit with a single seed). However, the fossil is bisexual and has nectaries, characters shared with the sister order Cucurbitales, and both lack the fagalean immature orthotropous developmental stage. The fossil shares synapomorphies of an inferior ovary and a single‐seeded indehiscent fruit with both living orders and appears to be transitional. Comparison of ontogenetic changes between the fossil and related fagalean taxa suggests independent stepwise changes in development in which some characters of the modern clades were in place at ～ 75 Myr and others evolved more recently. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 168 , 353–376.     

Impacts of floral gender and whole-plant gender on floral evolution in Ecballium elaterium (Cucurbitaceae)

Investigation of gender specialization in plants has led to several theories on the evolution of sexual dimorphism: reproductive compensation, based on enhanced reproductive efficiency with gender specialization (flowers should be larger on dioecious plants); Bateman's Principle, based on sex-specific selection (display for pollinator attraction in males and seed set in females); and intersexual floral mimicry, based on mimicry of a reward-providing gender by a non-reward providing gender (reduced dimorphism in dioecious plants due to increased spatial separation of male and female flowers). These theories were evaluated in Ecballium elaterium, which contains two subspecies, elaterium (monoecious) and dioicum (dioecious). Our results show that flowers of the dioecious subspecies are larger and allocate more to reproductive organs than do flowers of the monoecious subspecies. Both subspecies are sexually dimorphic (male flowers larger than female flowers). Variance in flower size among populations is greater in the dioecious subspecies. Finally, there is sufficient genetic variation to enable ongoing response to selection; genetic correlation constraints on independent response of female and male flowers may be stronger in the monoecious subspecies. Our findings provide support for aspects of all three theories, suggesting that the evolution of floral dimorphism is based on a complex interplay of factors.     

The developmental floral morphology of Montrichardia arborescens (Araceae) revisited

The spadix of Montrichardia arborescens contains unisexual flowers without a perianth. The pistillate flowers are located in the basal portion of the inflorescence, and the staminate flowers are located in the apical portion. There is a narrow :zone between male flowers and female flowers consisting of atypical flowers. The portion of the atypical flowers facing the staminate zone exhibits staminate characters (stamens), and the portion facing the pistillate zone has an aborted gynoecium. The floral development of Montrichurdia is compared with that of Philodendron and a new interpretation of the morphology of atypical flowers of Montrichardia is proposed. Ontogenetic evidence supports relationships with Philodendron rather than Cercestis. 2001 The Linnean Society of London     

Reversal versus specialization in floral morphological evolution in Petrocosmea (Gesneriaceae)

A widely held hypothesis in evolution is that adaptive specialization constrains the potential direction of future evolutionary change and thus may be irreversible, also known as Dollo's law. However, this hypothesis has long been subject to debate in evolutionary biology. Floral specialization is intriguing as it is usually linked to reproductive isolation and could affect speciation. Here, following the discovery of four new taxa, we observed some interesting phenomena of reversal versus specialization in morphology in a clade with the most specialized flowers in the genus Petrocosmea. In the phylogenetic tree based on sequences of multiple DNA regions, the morphological reversals, especially the regain of a long corolla tube, are nested within the branches characteristic of normally specialized flowers with a short corolla tube and highly specialized zygomorphy. Our results indicate that the highly specialized floral organ of this clade is still actively evolving in multiple branches toward specialization while reversals to different ancestral states occur in some branches. Great disturbance of ecological environment is likely a crucial factor affecting trait reversibility, such as the rapid uplift of the Himalayan–Tibetan plateau. The four new taxa are treated herein taxonomically. The flowers of this clade represent an interesting model to explore the genetic basis underlying the evolutionary reversal versus specialization and the interplay between genetic factors and environmental variables.     

Evidence of rodent pollination inCajophora coronata (Loasaceae)

Vegetative and floral features ofCajophora coronata (Loasaceae) suggest adaptations to pollination by rodents: (1) mammal guard represented by a covering of stinging hairs; (2) geoflory; (3) white corolla; (4) open flowers with copious low concentration nectar; (5) abundant pollen; (6) maximum pollen and nectar presentation in the afternoon hours and in the night. Palynological analysis revealed pollen loads ofC. coronata on the nostrils and whiskers of captured rodents (Graomys griseoflavus, fam.Muridae). Pollen and anther remains were also found in faeces sampled in the surroundings. Additional evidence includes rodent footprints obtained by placing smoked plates beneath the flowers, which revealed flower visitation during the night. These observations are to our knowledge the first evidence of flower visitation by rodents in South America and the first in the New World outside the range of flower bats and bat flowers.     

Comparative floral development in the tribe Mentheae (Nepetoideae: Lamiaceae) and its bearing on the evolution of floral patterns in asterids

A comparative developmental study of flowers was carried out using epi-illumination light microscopy on four genera of Lamiaceae (Nepeta, Rosmarinus, Salvia, andZiziphora), representing all three subtribes of Mentheae. All species examined share unidirectional (adaxial to abaxial) sepal initiation, except Rosmarinus, which has the reverse unidirectional sequence, starting abaxially. Initiated but suppressed bracteoles were detected only in Rosmarinus. In Rosmarinus, Salvia, and Ziziphora, initiation of petals and stamens proceeds unidirectionally from the abaxial side. Floral initiation of Nepeta has bidirectional inception of petals and unidirectional stamen initiation from the adaxial side. Temporal overlap in organ initiation between petal and stamen whorls occurs in all taxa, though this feature is more prominent in Rosmarinus. Significant structural and developmental features that distinguish the four genera include: (1) polysymmetric calyx tube, highly tomentose corolla and deeply four-partitioned ovary in Nepeta; (2) monosymmetric two-lipped calyx and shallowly four-partitioned ovary in Ziziphora; and (3) suppression of adaxial stamens in Salvia and Rosmarinus. Adaxial stamens are absent from Rosmarinus, but reduced stamens remain as staminodia in Salvia. In a phylogenetic context, the late monosymmetry of Nepeta and very early monosymmetry of Rosmarinus could both be regarded as derived conditions compared with the early monosymmetry ofSalvia and Ziziphora.     

Structure of the inflorescence and flower ofPetalonyx linearis (Loasaceae)

Fossil chloranthoid androecia,Chloranthistemon endressii gen. et spec. nov. are described from the Upper Cretaceous (Upper Santonian or Lower Campanian) of Scania, southern Sweden. They are three-lobed and dorsiventrally flattened with all pollen sacs borne laterally and inclined toward the presumed adaxial surface. The central lobe bears two pairs of pollen sacs, the lateral lobes a single pair each. The morphology, anatomy and valvate dehiscence of the fossil androecia is very similar to that seen in extant species ofChloranthus andSarcandra, but the in situ pollen differs from that of all extantChloranthaceae in being spiraperturate. A single chloranthoid androecium from the Lower Cretaceous (Upper Albian) of Maryland, North America has a more generalized structure thanChloranthistemon endressii. It consists of three stamens that are fused at the base, and each stamen bears two pairs of oppositely positioned pollen sacs. Combined with anatomical information from recentChloranthus the Lower Cretaceous specimen suggests that the androecium in the living genus has arisen by fusion and other modifications of three separate stamens each with a normal complement of four pollen sacs. The structure of both the Upper and Lower Cretaceous androecia suggest that these fossilChloranthaceae were insectpollinated. Macrofossil evidence combined with information from dispersed pollen indicates that theChloranthaceae diversified early in angiosperm fossil history and were an important component of Mid-Cretaceous plant communities.     

Phytochemistry and the systematics and ecology of Loasaceae and Gronoviaceae (Loasales)

A screening for iridoid compounds of 78 of 315 species from all major groups in Gronoviaceae and Loasaceae has been carried out. The results were compared to the systematic concepts in the family and distribution and ecology of the taxa. Iridoids are present in at least some species of all genera screened. Some simple, monomeric compounds (e.g., loganin, sweroside) are found in all major groups of the two families and represent the basic iridoid inventory. Other compounds are restricted to certain taxonomic groups: nine-carbon iridoids (e.g., deutzioside) are restricted to Mentzelia (Loasaceae subfam. Mentzelioideae), hetero-oligomeric iridoids (e.g., tricoloroside methyl ester, acerifolioside) are restricted to two small groups in Loasa (Loasa ser. Macrospermae and ser. Floribundae, Loasaceae subfam. Loasoideae), and oleosides (e.g., 10-hydroxyoleoside dimethyl ester) are restricted to the large genus Caiophora sensu Weigend). The distribution of certain iridoid compounds thus confirms some of the generic limits. Iridoid phytochemistry does not correlate with systematic entities above the generic level nor does it in any way correlate with the morphological evolution of taxa. Conversely, the amount and complexity of iridoid compounds present in taxa correlate positively with the aridity of their habitat and the extent of mammalian herbivore pressure.     

Nonheterochronic developmental changes underlie morphological heterochrony in the evolution of the Ardeidae

Evolutionary changes in developmental timing and rates (heterochrony) are a source of morphological variation. Here we explore a central issue in heterochronic analysis: are the alterations in developmental timing and rates the only factor underlying morphological heterochrony? Tarsometatarsal growth through endochondral ossification in Ardeidae evolution has been taken as a case study. Evolutionary changes in bone growth rate (morphological heterochrony) might be either (a) the result of alterations in the mitotic frequency of epiphyseal chondrocytes (process‐heterochrony hypothesis), or (b) the outcome of alterations in the number of proliferating cells or in the size of hypertrophic chondrocytes (structural hypothesis). No correlation was found between tarsometatarsal growth rates and the frequency of cell division. However, bone growth rates were significantly correlated with the number of proliferating cells. These results support the structural hypothesis: morphological acceleration and deceleration are the outcome of evolutionary changes in one structural variable, the number of proliferating cells.     

Comparative floral development in Lithospermum (Boraginaceae) and implications for the evolution and development of heterostyly

? Premise of the study: The evolution and development of floral developmental patterns were investigated in three heterostylous and three homostylous species of Lithospermum to determine whether species that independently acquired the same floral form follow the same pattern of development or different patterns. ? Methods: Using light and scanning electron microscopy, we observed developmental patterns in flowers at different stages of maturity. These patterns were compared within individual species, between heterostylous morphs, and among heterostylous and homostylous species. ? Key results: Although heterostyly has been determined by phylogenetic analysis to have originated independently in each of the heterostylous species, flowers of the long-style morph of each species follow similar patterns of gross development, as do those of the short-style morph. In addition, the flowers of each morph develop in a manner similar to those of their respective homostylous, herkogamous relatives. However, the developmental patterns of the stylar epidermal cells differ among these species and between heterostylous and homostylous species. ? Conclusions: Floral developmental patterns in homostylous species provide evidence that modification of specific traits, such as patterns of stylar growth, can lead to the evolution of heterostyly. The developmental changes that affect the positions of the stigmas and anthers in each morph likely involve either temporal or spatial modifications of gene function. The floral developmental patterns described here and the occurrence of multiple types of herkogamy within some species of Lithospermum provide evidence that heterostylous species in the genus have originated via distinct evolutionary developmental pathways.     

The effect of polyploidy and hybridization on the evolution of floral colour in Nicotiana (Solanaceae)

Background and Aims Speciation in angiosperms can be accompanied by changes in floral colour that may influence pollinator preference and reproductive isolation. This study investigates whether changes in floral colour can accompany polyploid and homoploid hybridization, important processes in angiosperm evolution.Methods Spectral reflectance of corolla tissue was examined for 60 Nicotiana (Solanaceae) accessions (41 taxa) based on spectral shape (corresponding to pigmentation) as well as bee and hummingbird colour perception in order to assess patterns of floral colour evolution. Polyploid and homoploid hybrid spectra were compared with those of their progenitors to evaluate whether hybridization has resulted in floral colour shifts.Key Results Floral colour categories in Nicotiana seem to have arisen multiple times independently during the evolution of the genus. Most younger polyploids displayed an unexpected floral colour, considering those of their progenitors, in the colour perception of at least one pollinator type, whereas older polyploids tended to resemble one or both of their progenitors.Conclusions Floral colour evolution in Nicotiana is weakly constrained by phylogeny, and colour shifts do occur in association with both polyploid and homoploid hybrid divergence. Transgressive floral colour in N. tabacum has arisen by inheritance of anthocyanin pigmentation from its paternal progenitor while having a plastid phenotype like its maternal progenitor. Potentially, floral colour evolution has been driven by, or resulted in, pollinator shifts. However, those polyploids that are not sympatric (on a regional scale) with their progenitor lineages are typically not divergent in floral colour from them, perhaps because of a lack of competition for pollinators.     

The evolution of floral variation without pollinator shifts in Gorteria diffusa (Asteraceae)

One of the most widely accepted explanations for floral diversification in angiosperms is the pollinator-shift model developed by Verne Grant and Ledyard Stebbins. According to this model, the most profound changes in floral traits (such as morphology, color, patterning and scent) occur when plants undergo adaptive shifts between pollinator classes. We tested this model through investigations of geographical variation in floral form and pollinator assemblages in the South African annual daisy Gorteria diffusa. This species has elaborate insect-like ornaments on the capitulum, which attract bee flies belonging to the genus Megapalpus. We found unprecedented levels of geographically structured intraspecific variation and identified 14 discrete forms that vary in the morphology and ornamentation of the capitulum. This variation is not due to phenotypic plasticity because differences among forms were maintained in plants grown from seed in a common garden experiment. Contrary to predictions from the pollinator-shift model, all populations, regardless of floral phenotype, were pollinated primarily by a single species of Megapalpus bee fly. Much of the extensive variation in floral form in G. diffusa therefore appears to have arisen without evolutionary shifts between pollinator types.     

Effects of herbivory on ovum number in Loasa speciosa (Loasaceae)

We examined the direct effect of foliar herbivory on female fitness in the herbaceous plant Loasa speciosa (Loasaceae), measuring ovule number/flower in 46 shoots with different levels of leaf damage. Ovule number/flower was lower in shoots with higher herbivory levels. This result suggests that the known negative impact of herbivory on female plant fitness (i.e. low seed number) can be a direct consequence of the reduction of ovule number.