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A seed predator drives the evolution of a seed dispersal mutualism.

ABSTRACT: Although antagonists are hypothesized to impede the evolution of mutualisms, they may simultaneously exert selection favouring the evolution of alternative mutualistic interactions. We found that increases in limber pine (Pinus flexilis) seed defences arising from selection exerted by a pre-dispersal seed predator (red squirrel Tamiasciurus hudsonicus) reduced the efficacy of limber pine's primary seed disperser (Clark's nutcracker Nucifraga columbiana) while enhancing seed dispersal by ground-foraging scatter-hoarding rodents (Peromyscus). Thus, there is a shift from relying on primary seed dispersal by birds in areas without red squirrels, to an increasing reliance on secondary seed dispersal by scatter-hoarding rodents in areas with red squirrels. Seed predators can therefore drive the evolution of seed defences, which in turn favour alternative seed dispersal mutualisms that lead to major changes in the mode of seed dispersal. Given that adaptive evolution in response to antagonists frequently impedes one kind of mutualistic interaction, the evolution of alternative mutualistic interactions may be a common by-product.

SUBMITTER: Siepielski AM

PROVIDER: S-EPMC2593931 | biostudies-literature | 2008 Aug

REPOSITORIES: biostudies-literature

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A seed predator drives the evolution of a seed dispersal mutualism.

Siepielski Adam M AM Benkman Craig W CW

Proceedings. Biological sciences 20080801 1645

Although antagonists are hypothesized to impede the evolution of mutualisms, they may simultaneously exert selection favouring the evolution of alternative mutualistic interactions. We found that increases in limber pine (Pinus flexilis) seed defences arising from selection exerted by a pre-dispersal seed predator (red squirrel Tamiasciurus hudsonicus) reduced the efficacy of limber pine's primary seed disperser (Clark's nutcracker Nucifraga columbiana) while enhancing seed dispersal by ground-f ...[more]

PMID: 18460433

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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).

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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A seed predator drives the evolution of a seed dispersal mutualism.

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A seed predator drives the evolution of a seed dispersal mutualism.

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