A seed predator drives the evolution of a seed dispersal mutualism.
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ABSTRACT:
SUBMITTER: Siepielski AM
PROVIDER: S-EPMC2593931 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:How mechanical and biological processes are coordinated across cells, tissues, and organs to produce complex traits is a key question in biology. Cardamine hirsuta, a relative of Arabidopsis thaliana, uses an explosive mechanism to disperse its seeds. We show that this trait evolved through morphomechanical innovations at different spatial scales. At the organ scale, tension within the fruit wall generates the elastic energy required for explosion. This tension is produced by differential contraction of fruit wall tissues through an active mechanism involving turgor pressure, cell geometry, and wall properties of the epidermis. Explosive release of this tension is controlled at the cellular scale by asymmetric lignin deposition within endocarp b cells-a striking pattern that is strictly associated with explosive pod shatter across the Brassicaceae plant family. By bridging these different scales, we present an integrated mechanism for explosive seed dispersal that links evolutionary novelty with complex trait innovation. VIDEO ABSTRACT.
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Project description:Seed predation and seed dispersal can have strong effects on early life history stages of plants. These processes have often been studied as individual effects, but the degree to which their relative importance co-varies with seed predator abundance and how this influences seed germination rates is poorly understood. Therefore, we used a combination of observations and field experiments to determine the degree to which germination rates of the palm Astrocaryum mexicanum varied with abundance of a small mammal seed predator/disperser, Heteromys desmarestianus, in a lowland tropical forest. Patterns of abundance of the two species were strongly related; density of H. desmarestianus was low in sites with low density of A. mexicanum and vice versa. Rates of predation and dispersal of A. mexicanum seeds depended on abundance of H. desmarestianus; sites with high densities of H. desmarestianus had the highest rates of seed predation and lowest rates of seed germination, but a greater total number of seeds were dispersed and there was greater density of seedlings, saplings, and adults of A. mexicanum in these sites. When abundance of H. desmarestianus was experimentally reduced, rates of seed predation decreased, but so did dispersal of A. mexicanum seeds. Critically, rates of germination of dispersed seeds were 5 times greater than undispersed seeds. The results suggest that the relationship between A. mexicanum and H. desmarestianus is a conditional mutualism that results in a strong local effect on the abundance of each species. However, the magnitude and direction of these effects are determined by the relative strength of opposing, but related, mechanisms. A. mexicanum nuts provide H. desmarestianus with a critical food resource, and while seed predation on A. mexicanum nuts by H. desmarestianus is very intense, A. mexicanum ultimately benefits because of the relatively high germination rates of its seeds that are dispersed by H. desmarestianus.
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Project description:The importance of infrequent events for both adaptive evolution and the evolution of species interactions is largely unknown. We investigated how the infrequent production of large seed crops (masting) of a bird-dispersed tree (whitebark pine, Pinus albicaulis) influenced phenotypic selection exerted by its primary avian seed predator-disperser, the Clark's nutcracker (Nucifraga columbiana). Selection was not evident during common years of low seed abundance, whereas it was replicated among areas and favoured traits facilitating seed dispersal during infrequent years of high seed abundance. Since nutcrackers act mostly as seed predators during small seed crops but as seed dispersers during the largest seed crops, trees experienced strong selection from nutcrackers only during infrequent years when the interaction was most strongly mutualistic. Infrequent events can thus be essential to both adaptive evolution and the evolutionary dynamics of species interactions.
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Project description:The family Aizoaceae includes ~1880 species and is one of the more diverse groups within Caryophyllales, particularly in arid areas in the western part of southern Africa. Most species are dwarf succulent-leaf shrubs. In response to the harsh climatic conditions prevalent where they occur, many representatives have evolved special reproductive adaptations. These include hygrochastic capsules (mostly found in Mesembryanthemoideae and Ruschioideae), burr-like indehiscent and one-seeded, winged diaspores, and fast germination of seeds after rain. We focused on anatomical features, evolutionary trends, and the ecological significance of various morpho-anatomical structures found in the seeds. The seeds of 132 species from 61 genera were studied, and 18 diagnostic characters were discovered. All studied characters were compared with those of other families from core Caryophyllales. The seed notch and embryo shape were added to the list of characteristics distinguishing major clades within the family. In addition, the presence of longitudinal ridges and a keel on the seed are additional characters of Aizooideae and combined Ruschioideae-Apatesieae, respectively. Puzzle-like borders of testa cells are a common trait in Ruschioideae and Mesembryanthemoideae. Most taxa in Aizoaceae have a thin seed coat, which is the ancestral state within the family. This may facilitate fast germination. We observed several shifts to a medium-thick or thick seed coat in members of Ruschioideae and Acrosanthoideae. These inhabit fire-prone environments (in vegetation types known as fynbos and renosterveld), where the thickened seed coat may protect against damage by fire. Multi-seeded fruits are the ancestral state within Aizoaceae, with several shifts to one-(two-)seeded xerochastic fruits. The latter are dispersed via autochory, zoochory, or anemochory. This trait has evolved mainly in less succulent subfamilies Acrosanthoideae, Aizooideae, and Sesuvioideae. In highly succulent subfamilies Ruschioideae and Mesembryanthemoideae, fruits are almost exclusively multi-seeded and hygrochastic with ombrohydrochoric dispersal. A reduction in the number of seeds within a dispersal unit is rare. Within Apatesieae and Ruschieae, there are also a few unusual genera whose fruits fall apart into one- to two-seeded mericarps (that are mainly dispersed by wind).
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Project description:Fire is a major disturbance affecting ecosystems worldwide. Phylogenetic studies have shown that the evolution of seed persistence (fire resistance) is associated with fire frequency or severity. However, the existence of specific seed traits resulting from natural selection mediated by fire remains a key question in plant evolution. We evaluated the role of fire in the evolution of seed traits from a microevolutionary perspective, using as a study system a native forb from the Chilean matorral, where fire is a novel, anthropogenic disturbance. We show that anthropogenic fires are shaping the evolution of seed traits such as pubescence and shape. Among-population variation in seed pubescence, shape, and pericarp thickness was strongly associated with fire frequency, and within a population, fire selected those plants with more pubescent seeds, thicker pericarps, and less rounded seeds. Seed pubescence and shape were shown to be heritable traits. Our findings provide insights into the understanding of the evolution of seed traits in fire-prone environments and demonstrate that human-made fires can be driving evolutionary changes in plant species from ecosystems where fires do not occur naturally.
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Project description:Frugivores play differing roles in shaping dispersal patterns yet seed dispersal distance is rarely quantified across entire communities. We model seed dispersal distance using gut passage times and bird movement for the majority (39 interactions) of known bird-tree interactions on the island of Saipan to highlight differences in seed dispersal distances provided by the five avian frugivores. One bird species was found to be a seed predator rather than a disperser. The remaining four avian species dispersed seeds but differences in seed dispersal distance were largely driven by interspecific variation in bird movement rather than intraspecific variation in gut passage times. The median dispersal distance was at least 56 m for all species-specific combinations, indicating all species play a role in reducing high seed mortality under the parent tree. However, one species-the Micronesian Starling-performed 94% of dispersal events greater than 500 m, suggesting this species could be a key driver of long-distance dispersal services (e.g. linking populations, colonizing new areas). Assessing variation in dispersal patterns across this network highlights key sources of variation in seed dispersal distances and suggests which empirical approaches are sufficient for modelling how seed dispersal mutualisms affect populations and communities.
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Project description:BackgroundRecurrent climatic oscillations have produced dramatic changes in species distributions. This process has been proposed to be a major evolutionary force, shaping many life history traits of species, and to govern global patterns of biodiversity at different scales. During range expansions selection may favor the evolution of higher dispersal, and symbiotic interactions may be affected. It has been argued that a weakness of climate fluctuation-driven range dynamics at equatorial latitudes has facilitated the persistence there of more specialized species and interactions. However, how much the biology and ecology of species is changed by range dynamics has seldom been investigated, particularly in equatorial regions.Methodology/principal findingsWe studied a three-species symbiosis endemic to coastal equatorial rainforests in Cameroon, where the impact of range dynamics is supposed to be limited, comprised of two species-specific obligate mutualists--an ant-plant and its protective ant--and a species-specific ant parasite of this mutualism. We combined analyses of within-species genetic diversity and of phenotypic variation in a transect at the southern range limit of this ant-plant system. All three species present congruent genetic signatures of recent gradual southward expansion, a result compatible with available regional paleoclimatic data. As predicted, this expansion has been accompanied by the evolution of more dispersive traits in the two ant species. In contrast, we detected no evidence of change in lifetime reproductive strategy in the tree, nor in its investment in food resources provided to its symbiotic ants.Conclusions/significanceDespite the decreasing investment in protective workers and the increasing investment in dispersing females by both the mutualistic and the parasitic ant species, there was no evidence of destabilization of the symbiosis at the colonization front. To our knowledge, we provide here the first evidence at equatorial latitudes that biological traits associated with dispersal are affected by the range expansion dynamics of a set of interacting species.
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Project description:Invasive vertebrate predators are directly responsible for the extinction or decline of many vertebrate species, but their indirect impacts often go unmeasured, potentially leading to an underestimation of their full impact. When invasives extirpate functionally important mutualists, dependent species are likely to be affected as well. Here, we show that the invasive brown treesnake, directly responsible for the extirpation of forest birds from the island of Guam, is also indirectly responsible for a severe decline in plant recruitment as a result of disrupting the fruit-frugivore mutualism. To assess the impact of frugivore loss on plants, we compare seed dispersal and recruitment of two fleshy-fruited tree species on Guam and three nearby islands with intact disperser communities. We conservatively estimate that the loss of frugivorous birds caused by the brown treesnake may have caused a 61-92% decline in seedling recruitment. This case study highlights the potential for predator invasions to cause indirect, pervasive and easily overlooked interaction cascades.
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