It’s about time – rapid evolution of flowering time in response to insect herbivores

 Amy L. Parachnowitsch
Plant Ecology and Evolution, Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden 75236. email: amyparachnowitsch@gmail.com

When to flower is an important life history decision for angiosperms, one that can influence both the abiotic and biotic environment of reproduction.  Therefore, it is not surprising that flowering time is frequently linked to plant fitness and is under phenotypic selection in many wild populations (Munguía-Rosas et al. 2011).  

A recent study by Agrawal and colleagues (Agrawal et al. 2012) has also highlighted the possibility for rapid evolution in flowering time. These authors set out to test experimentally  whether evening primrose (Oenothera biennis L.) would evolve in response to selection by herbivores.  Their field study is impressive because they examined evolutionary change in experimental populations.  To test for rapid evolution, they created replicate populations of the same O. biennis genotypes.  They then experimentally manipulated insect herbivory in these populations by spraying half with insecticide and monitored changes in genotypic frequency and phenotypic traits for the next three generations.

Oenothera biennis. Photo by AA Agrawal.
Oenothera biennis. Photo by AA Agrawal.

For Oenothera biennis, flowering time is a key trait that predicts specialist pre-dispersal seed predation; later flowering plants avoid such damage.  Even on such a short time scale (4 years), populations relatively herbivore-free evolved earlier flowering times than those with herbivores.  Insect suppression also led to reduced chemical defence in fruits, and changes in community composition with insect suppression also affected evolution in competitive ability of O. biennis.  Taken together, these results emphasise the complex nature of plant-insect interactions and their eco-evolutionary effects. 

What makes the O. biennis example different from many flowering plants is that despite its showy flowers, O. biennis does not rely on pollinators for seed production.  Furthermore, O. biennis has a genetic system to prevent outcrossing, although outcrossing can occur rarely (one such cross was detected in this study).  However, we can exclude pollinators as a major contributor to the evolutionary patterns of flowering time that Agrawal et al. observed.  For outcrossing plants, the importance of flowering time is often considered in terms of its effect on plant-pollinator synchronization and availability of mates.  Therefore, we might predict flowering time to be under pollinator-mediated selection in outcrossing plants. However, my own work and others (Elzinga et al. 2007, Parachnowitsch and Caruso 2008, Parachnowitsch et al. 2012) suggest that herbivores might also be important agents of selection on flowering time, even in systems where pollinators are necessary for seed production.  An exciting future possibility would be to examine this kind of rapid evolution in flowering time in species where multiple interactions are influenced by flowering time.  Ultimately, experimental evolution studies in field conditions such as Agrawal et al. will allow us to understand better the causal agents of selection, and how these interactions lead to evolutionary change.  For now, Agrawal et al. provide an enlightening study furthering our understanding of how ecological interactions can influence rapid evolutionary change and the feedback mechanisms between these processes.

References

Agrawal, A. A., A. P. Hastings, M. T. J. Johnson, J. L. Maron, and J.-P. Salminen. 2012. Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science 338:113-116.

Elzinga, J. A., A. Atlan, A. Biere, L. Gigord, A. E. Weis, and G. Bernasconi. 2007. Time after time: flowering phenology and biotic interactions. Trends in Ecology & Evolution 22:432-439.

Munguía-Rosas, M. A., J. Ollerton, V. Parra-Tabla, and J. A. De-Nova. 2011. Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured. Ecology Letters 14:511-521.

Parachnowitsch, A. L. and C. M. Caruso. 2008. Predispersal seed herbivores, not pollinators, exert selection on floral traits via female fitness. Ecology 89:1802-1810.

Parachnowitsch, A. L., C. M. Caruso, S. A. Campbell, and A. Kessler. 2012. Lobelia siphilitica plants that escape herbivory in time also have reduced latex production. PLoS ONE 7:e37745.

Oenothera biennis L.

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Flowering Newsletter published by the Journal of Experimental Botany
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