Extrafloral nectaries in Leguminosae: phylogenetic distribution, morphological diversity and evolution

Abstract

Extrafloral nectaries (EFNs) mediating ecologically important ant–plant protection mutualisms are especially common and unusually diverse in the Leguminosae. We present the first comprehensively curated list of legume genera with EFNs, detailing and illustrating their systematic and phylogenetic distributions, locations on the plant, morphology and anatomy, on the basis of a unified classification of EFN categories and a time-calibrated phylogeny, incorporating 710 of the 768 genera. This new synthesis, the first since Mckey (1989)’s seminal paper, increases the number of genera with EFNs to 153 (20% of legumes), distributed across subfamilies Cercidoideae (1), Detarioideae (19), Caesalpinioideae (87) and Papilionoideae (46). EFNs occur at nine locations, and are most prevalent on vegetative plant parts, especially leaves (74%) and inflorescence axes (26%). Four main categories (with eight subcategories) are recognised and include the following: formless, trichomatic (exposed, hollow), parenchymatic (embedded, pit, flat, elevated) and abscission zone EFNs (non-differentiated, swollen scars). Phylogenetic reconstruction of EFNs suggests independent evolutionary trajectories of different EFN types, with elevated EFNs restricted almost exclusively to Caesalpinioideae (where they underwent spectacular morphological disparification), flat EFNs in Detarioideae, swollen scar EFNs in Papilionoideae, and Cercidoideae is the only subfamily bearing intrastipular EFNs. We discuss the complex evolutionary history of EFNs and highlight future research directions.

Large‐scale genomic sequence data resolve the deepest divergences in the legume phylogeny and support a near‐simultaneous evolutionary origin of all six subfamilies

“…Somewhat intermediate is the hypothesis of a shared cryptic precursor trait that can lead to deep homology, where similar traits evolved independently from a shared genetic basis (Shubin et al, 2009;Scotland, 2010). For instance, this could potentially explain the homoplasious distribution of extrafloral nectaries across legumes (Marazzi et al, 2012), which are present in several subfamilies but are different in structure and location, casting doubt on a single origin and prompting the possibility of a shared genetic precursor (Marazzi et al, 2012(Marazzi et al, , 2019.…”

Hybrid capture of 964 nuclear genes resolves evolutionary relationships in the mimosoid legumes and reveals the polytomous origins of a large pantropical radiation

“…The mimosoid clade (LPWG, 2017), formerly subfamily Mimosoideae, comprises ~3300 species in ~87 genera of trees, shrubs, geoxyles, and lianas. Highly typical of the clade, though also found in other members of subfamily Caesalpinioideae, are bipinnate leaves (with few exceptions, most notably the once-pinnate leaves of the genus Inga and the phyllodes of Acacia s.s.; note that taxonomic authorities of all mimosoid genera are included in Table 2) that show extensive quantitative variation in size and numbers of leaflets and pinnae, and usually bear extrafloral nectaries on the petiole, rachis, and/or pinnae (Marazzi et al, 2019). Furthermore, many mimosoids have some form of armature (i.e., stipular spines, spinescent shoots, or prickles).…”

Potential pollen vectors of the mass flowering tree Acacia dealbata, within its natural range in southern Tasmania

“…However, since some bird species were observed to consistently feed on and among the flowers (table 3) they must clearly be deriving some benefit. Brown Thornbills and Silvereyes have previously been documented working among flowers of other Acacia species (Ford & Forde 1976, Knox et al 1985, Vanstone & Paton 1988), but in those cases they were feeding primarily from extrafloral nectaries which are vestigial in A. dealbata (Marazzi et al 2019). However, Silvereyes and a Striated Thornbill Acanthiza lineata also occasionally pecked at flowers of A. pycnantha, and invertebrates and pollen were both suggested as the possible food items targeted (Ford & Forde 1976, Vanstone & Paton 1988.…”

“…Pollen is aggregated into 16 grain polyads which average 46 µm in diameter (Nghiem et al 2018). The flowers do not produce nectar and the extra-floral nectaries are vestigial (Marazzi et al 2019) and offer no reward. The low fruit:flower ratio PLATE 1 -Flowering (26/8/18) and corresponding mature pod crop (1/1/19) on adjacent trees at Site 4.…”

“…Pollen is aggregated into polyads containing 4<32 grains. The flowers do not produce nectar and while extrafloral nectaries are generally present (Boughton 1981), in many species, including A.dealbata, they are only vestigial (Marazzi et al 2019) and offer no reward to visitors. Low reproductive success is also a characteristic of the genus with typically less than one pod produced per flower-head (Wandrag et al 2015).…”