TY - JOUR
T1 - Diversity and evolution of a trait mediating ant-plant interactions
T2 - Insights from extrafloral nectaries in Senna (Leguminosae)
AU - Marazzi, Brigitte
AU - Conti, Elena
AU - Sanderson, Michael J.
AU - Mcmahon, Michelle M.
AU - Bronstein, Judith L.
N1 - Funding Information:
We thank M. Johnson and K. Coppola (greenhouse and plant care), A. Agellon (assistance with SEM), A. Grantham (assistance with paraffin microtome sections), H.-P. Linder (use of light microscope with digital camera), L. Paganucci de Queiroz ( photos and samples of Senna martiana), D. Cardoso (photos of S. bracteosa), A. Weaving/Ardea.com (photos of S. italica), Peter Endress and the Bronstein and Conti labs (stimulating discussions), Jeff Karron and two anonymous reviewers (valuable comments on the manuscript), and the Arizona-Sonora Desert Museum, Campus Arboretum of the University of Arizona, Desert Botanical Garden and Desert Legume Program (cultivated specimens). This work was supported by the Swiss National Science Foundation ( postdoctoral fellowship PA00P3-126248 to B.M.) and the National Geographic Research Program (8775-10 to B.M. with J.L.B., M.M.M. and M.J.S.). The Swiss Academy of Sciences supported early field-collecting trips (to B.M.).
PY - 2013/6
Y1 - 2013/6
N2 - Background and Aims Plants display a wide range of traits that allow them to use animals for vital tasks. To attract and reward aggressive ants that protect developing leaves and flowers from consumers, many plants bear extrafloral nectaries (EFNs). EFNs are exceptionally diverse in morphology and locations on a plant. In this study the evolution of EFN diversity is explored by focusing on the legume genus Senna, in which EFNs underwent remarkable morphological diversification and occur in over 80% of the approx. 350 species. Methods EFN diversity in location, morphology and plant ontogeny was characterized in wild and cultivated plants, using scanning electron microscopy and microtome sectioning. From these data EFN evolution was reconstructed in a phylogenetic framework comprising 83 Senna species. Key Results Two distinct kinds of EFNs exist in two unrelated clades within Senna. 'Individualized' EFNs (iEFNs), located on the compound leaves and sometimes at the base of pedicels, display a conspicuous, gland-like nectary structure, are highly diverse in shape and characterize the species-rich EFN clade. Previously overlooked 'non-individualized' EFNs (non-iEFNs) embedded within stipules, bracts, and sepals are cryptic and may represent a new synapomorphy for clade II. Leaves bear EFNs consistently throughout plant ontogeny. In one species, however, early seedlings develop iEFNs between the first pair of leaflets, but later leaves produce them at the leaf base. This ontogenetic shift reflects our inferred diversification history of iEFN location: ancestral leaves bore EFNs between the first pair of leaflets, while leaves derived from them bore EFNs either between multiple pairs of leaflets or at the leaf base. Conclusions EFNs are more diverse than previously thought. EFN-bearing plant parts provide different opportunities for EFN presentation (i.e. location) and individualization (i.e. morphology), with implications for EFN morphological evolution, EFN-ant protective mutualisms and the evolutionary role of EFNs in plant diversification.
AB - Background and Aims Plants display a wide range of traits that allow them to use animals for vital tasks. To attract and reward aggressive ants that protect developing leaves and flowers from consumers, many plants bear extrafloral nectaries (EFNs). EFNs are exceptionally diverse in morphology and locations on a plant. In this study the evolution of EFN diversity is explored by focusing on the legume genus Senna, in which EFNs underwent remarkable morphological diversification and occur in over 80% of the approx. 350 species. Methods EFN diversity in location, morphology and plant ontogeny was characterized in wild and cultivated plants, using scanning electron microscopy and microtome sectioning. From these data EFN evolution was reconstructed in a phylogenetic framework comprising 83 Senna species. Key Results Two distinct kinds of EFNs exist in two unrelated clades within Senna. 'Individualized' EFNs (iEFNs), located on the compound leaves and sometimes at the base of pedicels, display a conspicuous, gland-like nectary structure, are highly diverse in shape and characterize the species-rich EFN clade. Previously overlooked 'non-individualized' EFNs (non-iEFNs) embedded within stipules, bracts, and sepals are cryptic and may represent a new synapomorphy for clade II. Leaves bear EFNs consistently throughout plant ontogeny. In one species, however, early seedlings develop iEFNs between the first pair of leaflets, but later leaves produce them at the leaf base. This ontogenetic shift reflects our inferred diversification history of iEFN location: ancestral leaves bore EFNs between the first pair of leaflets, while leaves derived from them bore EFNs either between multiple pairs of leaflets or at the leaf base. Conclusions EFNs are more diverse than previously thought. EFN-bearing plant parts provide different opportunities for EFN presentation (i.e. location) and individualization (i.e. morphology), with implications for EFN morphological evolution, EFN-ant protective mutualisms and the evolutionary role of EFNs in plant diversification.
KW - Ant-plant mutualism
KW - Fabaceae
KW - Senna
KW - ant protection
KW - extrafloral nectaries
KW - functional morphology
KW - homology
KW - key innovation
KW - morphological evolution
KW - ontogeny
KW - phylogeny
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U2 - 10.1093/aob/mcs226
DO - 10.1093/aob/mcs226
M3 - Article
C2 - 23104672
AN - SCOPUS:84878317023
SN - 0305-7364
VL - 111
SP - 1263
EP - 1275
JO - Annals of botany
JF - Annals of botany
IS - 6
ER -