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Abstract Plant secondary metabolites are key mechanistic drivers of species interactions. These metabolites have primarily been studied for their role in defense, but they can also have important consequences for mutualisms, including seed dispersal. Although the primary function of fleshy fruits is to attract seed‐dispersing animals, fruits often contain complex mixtures of toxic or deterrent secondary metabolites that can reduce the quantity or quality of seed dispersal mutualisms. Furthermore, because seeds are often dispersed across multiple stages by several dispersers, the net consequences of fruit secondary metabolites for the effectiveness of seed dispersal and ultimately plant fitness are poorly understood. Here, we tested the effects of amides, nitrogen‐based defensive compounds common in fruits of the neotropical plant genusPiper(Piperaceae), on seed dispersal effectiveness (SDE) by ants, which are common secondary seed dispersers. We experimentally added amide extracts toPiperfruits both in the field and lab, finding that amides reduced the quantity of secondary seed dispersal by reducing ant recruitment (87%) and fruit removal rates (58% and 66% in the field and lab, respectively). Moreover, amides not only reduced dispersal quantity but also altered seed dispersal quality by shifting the community composition of recruiting ants (notably by reducing the recruitment of the most effective disperser by 90% but having no detectable effect on the recruitment of a cheater species that removes fruit pulp without dispersing seeds). Although amides did not affect the distance ants initially carried seeds, they altered the quality of seed dispersal by reducing the likelihood of ants cleaning seeds (67%) and increasing their likelihood of ants redispersing seeds outside of the nest (200%). Overall, these results demonstrate that secondary metabolites can alter the effectiveness of plant mutualisms, by both reducing mutualism quantity and altering mutualism quality through multiple mechanisms. These findings present a critical step in understanding the factors mediating the outcomes of seed dispersal and, more broadly, demonstrate the importance of considering how defensive secondary metabolites influence the outcomes of mutualisms surrounding plants.
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Heterochrony and repurposing in the evolution of gymnosperm seed dispersal units
Abstract BackgroundPlant dispersal units, or diaspores, allow the colonization of new environments expanding geographic range and promoting gene flow. Two broad categories of diaspores found in seed plants are dry and fleshy, associated with abiotic and biotic dispersal agents, respectively. Anatomy and developmental genetics of fleshy angiosperm fruits is advanced in contrast to the knowledge gap for analogous fleshy structures in gymnosperm diaspores. Improved understanding of the structural basis of modified accessory organs that aid in seed dispersal will enable future work on the underlying genetics, contributing to hypotheses on the origin of angiosperm fruits. To generate a structural framework for the development and evolution of gymnosperm fleshy diaspores, we studied the anatomy and histochemistry ofEphedra(Gnetales) seed cone bracts, the modified leaves surrounding the reproductive organs. We took an ontogenetic approach, comparing and contrasting the anatomy and histology of fleshy and papery-winged seed cone bracts, and their respective pollen cone bracts and leaves in four species from the South American clade. ResultsSeed bract fleshiness inEphedraderives from mucilage accumulated in chlorenchyma cells, also found in the reduced young leaves before they reach their mature, dry stage. Cellulosic fibers, an infrequent cell type in gymnosperms, were found inEphedra, where they presumably function as a source of supplementary apoplastic water in fleshy seed cone bracts. Papery-winged bract development more closely resembles that of leaves, with chlorenchyma mucilage cells turning into tanniniferous cells early on, and hyaline margins further extending into “wings”. ConclusionsWe propose an evolutionary developmental model whereby fleshy and papery-winged bracts develop from an early-stage anatomy shared with leaves that differs at the pollination stage. The ancestral fleshy bract state may represent a novel differentiation program built upon young leaf anatomy, while the derived dry, papery-winged state is likely built upon an existing differentiation pattern found in mature vegetative leaves. This model for the evolution of cone bract morphology in South AmericanEphedrahence involves a novel differentiation program repurposed from leaves combined with changes in the timing of leaf differentiation, or heterochrony, that can further be tested in other gymnosperms with fleshy diaspores.
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- Award ID(s):
- 1911539
- PAR ID:
- 10652423
- Publisher / Repository:
- BMC
- Date Published:
- Journal Name:
- EvoDevo
- Volume:
- 13
- Issue:
- 1
- ISSN:
- 2041-9139
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1186/s13227-022-00191-8
