Brigitte Marazzi

The diversity, ecology and evolution of extrafloral nectaries: current perspectives and future challenges

BACKGROUND Plants in over one hundred families in habitats worldwide bear extrafloral nectaries (EFNs). EFNs display a remarkable diversity of evolutionary origins, as well as diverse morphology and location on the plant. They secrete extrafloral nectar, a carbohydrate-rich food that attracts ants and other arthropods, many of which protect the plant in return. By fostering ecologically important protective mutualisms, EFNs play a significant role in structuring both plant and animal communities. And yet researchers are only now beginning to appreciate their importance and the range of ecological, evolutionary and morphological diversity that EFNs exhibit. SCOPE This Highlight features a series of papers that illustrate some of the newest directions in the study of EFNs. Here, we introduce this set of papers by providing an overview of current understanding and new insights on EFN diversity, ecology and evolution. We highlight major gaps in our current knowledge, and outline future research directions. CONCLUSIONS Our understanding of the roles EFNs play in plant biology is being revolutionized with the use of new tools from developmental biology and genomics, new modes of analysis allowing hypothesis-testing in large-scale phylogenetic frameworks, and new levels of inquiry extending to community-scale interaction networks. But many central questions remain unanswered; indeed, many have not yet been asked. Thus, the EFN puzzle remains an intriguing challenge for the future.

LARGE-SCALE PATTERNS OF DIVERSIFICATION IN THE WIDESPREAD LEGUME GENUS SENNA AND THE EVOLUTIONARY ROLE OF EXTRAFLORAL NECTARIES

Unraveling the diversification history of old, species‐rich and widespread clades is difficult because of extinction, undersampling, and taxonomic uncertainty. In the context of these challenges, we investigated the timing and mode of lineage diversification in Senna (Leguminosae) to gain insights into the evolutionary role of extrafloral nectaries (EFNs). EFNs secrete nectar, attracting ants and forming ecologically important ant–plant mutualisms. In Senna, EFNs characterize one large clade (EFN clade), including 80% of its 350 species. Taxonomic accounts make Senna the largest caesalpinioid genus, but quantitative comparisons to other taxa require inferences about rates. Molecular dating analyses suggest that Senna originated in the early Eocene, and its major lineages appeared during early/mid Eocene to early Oligocene. EFNs evolved in the late Eocene, after the main radiation of ants. The EFN clade diversified faster, becoming significantly more species‐rich than non‐EFN clades. The shift in diversification rates associated with EFN evolution supports the hypothesis that EFNs represent a (relatively old) key innovation in Senna. EFNs may have promoted the colonization of new habitats appearing with the early uplift of the Andes. This would explain the distinctive geographic concentration of the EFN clade in South America.

LOCATING EVOLUTIONARY PRECURSORS ON A PHYLOGENETIC TREE

Conspicuous innovations in the history of life are often preceded by more cryptic genetic and developmental precursors. In many cases, these appear to be associated with recurring origins of very similar traits in close relatives (parallelisms) or striking convergences separated by deep time (deep homologies). Although the phylogenetic distribution of gain and loss of traits hints strongly at the existence of such precursors, no models of trait evolution currently permit inference about their location on a tree. Here we develop a new stochastic model, which explicitly captures the dependency implied by a precursor and permits estimation of precursor locations. We apply it to the evolution of extrafloral nectaries (EFNs), an ecologically significant trait mediating a widespread mutualism between plants and ants. In legumes, a species‐rich clade with morphologically diverse EFNs, the precursor model fits the data on EFN occurrences significantly better than conventional models. The model generates explicit hypotheses about the phylogenetic location of hypothetical precursors, which may help guide future studies of molecular genetic pathways underlying nectary position, development, and function.

Patterns and development of floral asymmetry in Senna (Leguminosae, Cassiinae).

The buzz-pollinated genus Senna (Leguminosae) is outstanding for including species with monosymmetric flowers and species with diverse asymmetric, enantiomorphic (enantiostylous) flowers. To recognize patterns of homology, we dissected the floral symmetry character complex and explored corolla morphology in 60 Senna species and studied floral development of four enantiomorphic species. The asymmetry morph of a flower is correlated with the direction of spiral calyx aestivation. We recognized five patterns of floral asymmetry, resulting from different combinations of six structural elements: deflection of the carpel, deflection of the median abaxial stamen, deflection or modification in size of one lateral abaxial stamen, and modification in shape and size of one or both lower petals. Prominent corolla asymmetry begins in the earl-stage bud (unequal development of lower petals). Androecium asymmetry begins either in the midstage bud (unequal development of thecae in median abaxial stamen; twisting of androecium) or at anthesis (stamen deflection). Gynoecium asymmetry begins in early bud (primordium off the median plane, ventral slit laterally oriented) or midstage to late bud (carpel deflection). In enantiostylous flowers, pronouncedly concave and robust petals of both monosymmetric and asymmetric corollas likely function to ricochet and direct pollen flow during buzz pollination. Occurrence of particular combinations of structural elements of floral symmetry in the subclades is shown.

Diversity in Anthers and Stigmas in the Buzz‐Pollinated Genus Senna (Leguminosae, Cassiinae)

The large genus Senna (Cassiinae, Leguminosae) is an outstanding example of floral structural specialization associated with buzz pollination. This specialization is expressed especially in the androecium (with a high diversity of anther elaborations) and gynoecium (with diversity in stigma shape). The floral structure of 69 species from all major clades of Senna was studied, focusing on heteranthery, anther dehiscence, pore position, extension of the lateral furrow of the thecae, cell wall thickening in the anther tip, and stigma diversity (especially position, form, size, and structure of the orifice and presence of a chamber). Filament union is reported for the first time in the genus; it involves the seven adaxial androecial organs, a pattern unique in legumes. Our investigations identified novel morphological characteristics that are congruent with the clades supported by the molecular phylogeny. Anthers of abaxial stamens with the least differentiated dehiscence pattern, i.e., two separate pores and separate thecae, are found in most major clades (I, III–V, VII). Anthers with apically confluent thecae, forming a shared chamber, and/or with a single pore by confluence of two pores, represent specialized patterns (clades II, IV, VI, VII). Diverse anther tips may reflect different strategies of pollen dispersal; anther pore position may influence pollen flow directions. Anther tip elongation in the abaxial stamens and constriction between the thecae and the anther tip may influence the speed and/or amount of the released pollen.

Plant biotic interactions in the Sonoran desert: Current knowledge and future research perspectives

Premise of research. Biotic interactions have long been considered to be of less importance in structuring desert systems than other ecosystem types, but biotic interactions often play a critical role in meeting the challenges posed by the extreme conditions of desert environments. The Sonoran Desert, in particular, is home to several textbook examples of mutualisms, such as the interactions between the iconic saguaro cactus and its bat pollinators. But what do we know about the diversity, ecology, and evolution of plant-animal, plant-plant, and plant-microbe interactions and their impacts on individual plants and plant species in the Sonoran Desert? Methodology. To address this question, we review the published research on seven common kinds of plant biotic interactions by revisiting the respective literature, identifying gaps in our knowledge, and outlining future research directions. Pivotal results. Numerous gaps in our knowledge of plant biotic interactions in the Sonoran Desert were identified. Studies of insect herbivory, bee pollination, and plant-microbe interactions are poorly represented in the Sonoran Desert literature. Across all categories of interaction, few have examined the impacts of interactions on plant fitness or context-dependent variation in the outcomes and strengths of interactions. For the most part, interactions have been studied at single locations and over short periods of time, resulting in an incomplete understanding of their diversity, ecology, and evolution. Conclusions. Plant biotic interactions shape the habitats in which they occur and play an important role in the maintenance of species diversity. Therefore, we call for increased efforts to fill the gaps in our understanding of plant biotic interactions in the Sonoran Desert, with an emphasis on studies linking interactions to plant fitness and the context-dependent nature of interactions. Without this knowledge we have limited capacity to predict the outcomes of global change on species interactions and to develop measures to conserve the biodiversity of the Sonoran Desert region.

Plant Biotic Interactions in the Sonoran Desert: Conservation Challenges and Future Directions

Biotic interactions are vital to ecosystem functioning. Interactions among individuals lie at the core of population and community dynamics, and therefore play a central role in the existence and persistence of species. Plants form the food base of most terrestrial ecosystems and are therefore not surprisingly involved in a substantial portion of biotic interactions. Plants, animals, and microbes face great challenges to survival in the desert environment, and these interactions play a critical role in the survival of many species. The Sonoran Desert flora is well documented and certain of its iconic interactions are well understood. For example, saguaros and the bats that pollinate them and disperse their fruits have become textbook examples of mutualisms (e.g., Shreve and Wiggins 1964; Turner et al. 2005). However, what do we know about plant-animal, plant-plant, and plant-microbe interactions in the Sonoran Desert more generally? What role do such interactions play in the ecology and evolution of the Sonoran Desert ecosystem? How are these interactions affected by global changes, and how can we conserve interactions? These questions inspired a discussion session convened at the Next Generation Sonoran Desert Researchers (NGSDR) 2012 Summit. Ultimately, participants identified the following five critical needs regarding research and conservation. We need to (1) improve our knowledge of the natural history (diversity, ecology, evolution) of interactions, both as individual entities and as