The Evolutionary Ecology OF underground Fruits

Final Report Summary - TEE-OFF (The Evolutionary Ecology OF underground Fruits)

The aim of TEE-OFF was to study the evolutionary ecology of the most extreme case of limited dispersal in plants: geocarpy, the production of subterranean fruits.
The experimental system are Mediterranean legumes in the genera Lathyrus and Vicia with underground and aerial fruits (i.e. amphicarpic; Figs. 1-3). The latter are expected to facilitate migration and gene flow while non-dispersing, underground fruits are predicted to maximize local adaptation.
Dispersal within the maternal site or at very short distances has traditionally been associated with heterogeneous environments where the cost of dispersal is high because patches suitable for settlement are relatively rare. This hypothesis is well supported by theoretical models but it has never been formally tested. For instance, it has never been empirically verified whether taxa with non-dispersing fruits are locally adapted to different, more heterogeneous habitats than their “dispersing” relatives.
An alternative (albeit not mutually exclusive) explanation for the evolution of underground fruits is that maternal plants develop fruits underground to avoid predation. This hypothesis was put forward by C. Darwin as early as 1880 . Although some models support scenarios in which predator pressure can lead to the emergence of limited dispersal strategies, it has never been empirically tested to date whether seed predation can indeed force plants to limit dispersal, potentially leading to the production of underground seeds.
In the case of legumes, it has been hypothesized that many of the specific fruit and seed features have evolved as means to scape insect predators in general and beetles (weevils and bruchids) in particular. This hypothesis is plausible because a plant with seeds that were less prone to predation will gain an immediate fitness advantage. Still, the extent to which predators can shape the dispersal structures of plants remains little studied.
In this grant we tested the role of local adaptation and predators in the evolution of limited dispersal strategies. We used a phylogenetically informed framework consisting of two amphicarpic legumes (L. amphicarpos and V. amphicarpa; Figs. 1-3) and their closest relatives that have only aerial dispersal. With manipulative and observational studies we are trying to establish a) the extent to which dispersal imposes constraints on the geographical distribution of plants; b) if specific dispersal syndromes provide an evolutionary advantage in certain environments and c) how dispersal morphology changes in response to predation.
Dispersal and the geographic distribution of plants
This part of the project was severely curtailed by the firing of the molecular lab manager by the general manager of the UGR. This unfortunate and unjustified event drove the population and functional genetics work to a halt. However, all plant samples were collected as proposed, DNA extracted and molecular markers selected. We are in a position to resume and complete as soon as the necessary resources are in place.
Environmental dependency of dispersal
The adaptive value of dispersal in different environmental conditions as well as under different mating conditions has been investigated using a combination of common garden experiments and mathematical modeling. The latter was undertaken with the help of M. A. Muñoz and J. Hidalgo from the department of Physics of the UGR in what proved to be a fruitful interdisciplinary collaboration. Our results common garden results seem to indicate that amphicarpic plants have higher fitness under water stress conditions, although these results need to be validated. The theoretical work showed that mixed dispersal strategies, such as those exhibited by amphicarpic plants, are adaptive whenever environmental conditions are unpredictable and inbreeding depression is low. Limited dispersal, such as complete geocarpy, is adaptive only under very specific conditions, only if the environment is highly unpredictable, the probability of establishment at the maternal site is very high (maybe due to facilitation) and inbreeding depression is negligible (Fig. 4).
Dispersal morphology and predation
The role of geocarpy as a predator avoidance mechanism has been tested using field observations and manipulative experiments in the common garden. Our results are somewhat puzzling. Against what was hypothesized by Darwin, underground fruits exhibit higher rates of predation in the field and do not ensure fitness under predator pressure (Fig. 5). However, underground pods seem to facilitate escape from a certain class of seed predators (bruchids; Colleoptera, Chrysomellidae), which seem to attack only the aerial fruits (Fig. 6).

Figure legends
Figure 1
Vicia amphicarpa (purple flowers) and Lathyrus amphicarpos (red flowers) growing together in a pasture in Zahara de la Sierra, Cádiz, Spain
Figure 2
Flower anatomy of L. amphicarpos. a) - c) Aerial flower. a) & e) general abaxial view; b) & f) Corolla parts 1- Banner, 2- Wings, 3- Keel; c) & g) Lateral views of stamens and pistil; d) Detailed view of the subterranean stamens
Figure 3
Detailed view of subterranean and aerial fruits of L. amphicarpos a) Subterranean pod, 1 - Abaxial view, 2- Lateral view; b) Aerial pod 1- Lateral view, 2- Abaxial view.
Figure 4
Modeling of the adaptive value of dispersal syndromes a) Limited dispersal is only viable if inbreeding depression δ is >0; b) Ratio of dispersing and non-dispersing fruits α that result in an evolutionary stable strategy (ESS) under different levels of inbreeding δ and environmental variation (σ; horizontal axis); observe that when the environmental variability is low, the dispersing syndrome is favored (red region). On the other hand, mixed strategies are selected for in the scenarios of large environmental variability (green region). Notice that the parameter space in which the non-dispersing syndrome is selected for is negligible (light blue region). The dotted line indicates the levels of inbreeding depression and environmental variability that necessarily lead to the extinction of the population in a few generations (<30) generations. density: population density; pint: probability of establishment at the maternal site.

Figure 5
Reduction in fitness caused by herbivory. %Fitness was estimated as the ratio of fruits produced by an individual plant relative to the maximum number of fruits produced by any plant of the same species. Asterisks denote a significant reduction in fitness as a consequence of herbivory. The only two species that suffered a significant reduction in fitness were the two amphicarpic taxa. C: control; H: herbivory; LA: Lathyrus amphicarpos; LC: L. cicera; VA: Vicia amphicarpa; VS: V. sativa

Figure 6
Adult of Bruchus tristiculus (Bruchinae, Chrysomelidae, Coleoptera) inside an aerial Lathyrus seed.

Final Report Summary - TEE-OFF (The Evolutionary Ecology OF underground Fruits)

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