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Do plants cooperate in reproduction? The effect of sharing pollination services on plant reproductive strategies

Periodic Reporting for period 2 - KinCoop (Do plants cooperate in reproduction? The effect of sharing pollination services on plant reproductive strategies)

Reporting period: 2017-08-01 to 2018-07-31

KinCoop studied how plants behave in a social context in terms of their reproductive strategies. Plants can facilitate pollination of their neighbours. I hypothesized that this process of sharing pollination services will influence plant reproduction, driving cooperative reproductive strategies.

KinCoop’s main goal was, thus, to test whether natural selection may favour social behaviours (from selfish to cooperative ones) in plant reproduction by assessing how different social environments, in terms of density and genetic relatedness of neighbours, might influence optimal allocation strategies through the effect of sharing pollinators and the effect this will have on mating patterns and plant fitness.

The development of KinCoop has yielded significant results that will impact on the European Research Area and attitudes of European Society. Namely, the results of KinCoop showed the first evidence that plants recognize kin, modifying consequently their flowering strategies, broadening thus, the vision of how plants reproduce. Therefore, the plant social context may have deep consequences for plant phenotypes but also for plant performance and fitness. Future research should then consider social selection theory into the research agenda of plant populations. All expected milestones have been achieved and the major result obtained during this action has been published in the prestigious multidisciplinary journal: Nature Communication:
Torices, R., J.M. Gómez, J.R. Pannell. 2018 Kin discrimination allows plants to modify investment towards pollinator attraction. Nature Communications 9, 2018

KinCoop tested important questions about social evolution in the context of reproductive strategies that have previously been surprisingly little studied in plants. KinCoop is contributing then to our understanding of how plants cooperate during reproduction to alter plant population dynamics, with potentially useful outcomes for plant conservation, weed control, and crop breeding.
During the development of this project, I have performed several experiments and theoretical studies to achieve main objectives. In addition, I also developed several tasks related to career development, dissemination and public engagement

For the WP1, we aimed to comprehensively explore the way in which the intra-specific social environment influenced the evolution of resource allocation to pollinator attraction in plants. To this end, we have built a new model of evolutionarily stable strategies for obtaining quantitative predictions of the reproductive allocation considering the plant neighbourhood composition. This task has been performed in collaboration with Dr. Mauricio González-Forero, currently working as Marie Sklodowska-Curie Fellow at St. Andrews University in UK. Using this theoretical model, we have found that the density and genetic relatedness of the neighbourhood regulate the optimal investment on floral structures to attract pollinators. Nevertheless, the shape of this functional link between both density and genetic relatedness of the neighbourhood and the optimal investment to pollinator attraction was moulded by different parameters controlling within- and between-group plant competition by pollinators. Namely, our model predicts that plants should cooperate when surrounded by siblings and the investment they do in their flowers help them to compete against other groups rather than to compete with their siblings within the group.

In the WP2, we aimed to investigate in what extent the investment in advertising structures to attract pollinators (petal size, floral colour or nectar secretion) was a plastic response to changes in the social environment. For this, I performed a large common garden experiment under controlled glasshouse conditions involving more than 30,000 seeds and 700 plants where we characterized thousands of flowers. We grew plants in pots under controlled neighbourhoods with two levels of genetic relatedness (either siblings or genetically unrelated strangers) and three levels of density (one, four or seven plants per pot) in a full factorial experimental design. The great success of the this experiment allowed us to collect a vast amount of data. We collected data on reproductive allocation including: plant size in terms of height and biomass, flowering time, number of flowers produced, corolla diameter, flower-tube length, biomass allocated to petals, nectar volume and sugar concentration, quantitative estimation of colour by means of digital photographs, pollen production and ovule numbers.

The main finding of this experiment was that focal plants modified their behaviours depending on the social context. Namely, focal plants invested disproportionally more resources to floral advertisement when they were growing with relatives compared to when they were growing with strangers or alone. This result met the predictions of our theoretical model and support the hypthesis that cooperation in reproduction should be able to evolve in plants. The outstanding significance of these results allowed us to publish them as a paper in the top journal Nature communications. This finding was covered for different general media and thus, the results were highly disseminated between the general public.

For the WP3, I worked in collaboration with Yves Cuendot (former lab technician of Pannell’s group) and Dr. A. González-Megías from University of Granada to develop new microsatellites markers for our model species Moricandia moricandioides L. These markers are critical for assessing mating patterns and male success . Finally, we performed a an experiment in the field (Baza, Spain) to explore the effect of groups of plants on pollinator behaviour. For that, it was necessary to have native pollinators, and we decide to do it in the field during the flowering season. This experiment was performed again with the collaboration of Dr. A. González-Megías who has a long experience with the same model species. This experiment showed that large groups of plants attracted more pollinators but also affected the pollinator behaviour in different aspects such as the number of flowers visited, time spent in the group and number of different individuals visited within the group.
KinCoop have yielded significant results that will impact on the European Research Area and attitudes of European Society. First, the results of KinCoop showed the first evidence that plants might cooperate in reproduction, broadening the vision of how plants reproduce. The social context may have deep consequences for plant phenotypes but also for plant performance and fitness. Future research should therefore consider social selection theory into the research agenda of plant populations.

Therefore, KinCoop results might be relevant to crop science. As the social context affects plant phenotypes and plant productivity, the results of KinCoop will boost the basis of research to improve crop efficiency by applying social theory into agronomic techniques. For that reason, I organized a workshop on the use of social evolution theory on crop improvement. In this workshop, several stakeholders (researchers from universities, from agronomic centres, and from companies of the agriculture sector) met in the EEZA-CSIC during one day to discuss how KinCoop findings could be implemented to improve crop productivity.