Geographic and within-population variation in the globeflower–globeflower fly interaction: the costs and benefits of rearing pollinators’ larvae

Abstract

Interspecific interactions can vary within and among populations and geographic locations, and this variation can influence the nature of the interaction (e.g. mutualistic vs. antagonistic) and its evolutionary stability. Globeflowers are exclusively pollinated by flies, whose larvae feed only on their seeds. Here we document geographic variability in costs and benefits in globeflowers in sustaining their pollinating flies throughout the range of this arctic-alpine European plant over several years. A total of 1,710 flower heads from 38 populations were analysed for their carpel, egg and seed contents. Individual and population analyses control for the confounding influences of variation in both: (1) population traits, such as fly density and egg distribution among flower heads; and (2) individuals traits, such as carpel and egg numbers per flower head. Despite considerable variation in ecological conditions and pollinator densities across populations, large proportions (range 33-58%) of seeds were released after predation, with a benefit-to-cost ratio of 3, indicating that the mutualism is stable over the whole globeflower geographical range. The stability of the mutualistic interaction relies on density-dependent competition among larvae co-developing in a flower head. This competition is revealed by a sharp decrease in the number of seeds eaten per larva with increasing larval number, and is intensified by non-uniform egg distribution among globeflowers within a population. Carpel number is highly variable across globeflowers (range 10-69), and flies lay more eggs in large flowers. Most plants within a population contribute to the rearing of pollinators, but the costs are greater for some than for others. Large globeflowers lose more seed to pollinator larvae, but also release more seed than smaller plants. The apparent alignment of interests between fly and plants (positive relationship between numbers of seed released and destroyed) is shown to hide a conflict of interest found when flower size is controlled for.

Effects of population size on plant reproduction and pollinator abundance in a specialized pollination system

“…Substantial inter‐year differences (see Figs 3a, 3b and 4b) and much variation among populations are found in our own results, despite the populations being from similar geographical and altitudinal localities. Thus, differences in year, altitude and locality across populations might, possibly, confound the detection of such responses in the Despres et al. (2007) study.…”

Floral phenotypic plasticity as a buffering mechanism in the globeflower–fly mutualism

“…large flowers had higher visitation rate), while the length of the flowering stem had no impact on Chiastocheta attraction (Ibanez et al 2010). Furthermore, a large scale survey of 38 natural populations in the French Alps and in the Arctic showed that large flowers hosted more larvae and ultimately dispersed more undamaged seeds than smaller flowers (Després et al 2007). Although there was no difference in fly fitness (larval installation success, larval size and fresh mass) of larvae inhabiting large and small flowers (Després and Cherif 2004).…”

“…plants that are likely to make use of the pollination service without rewarding pollinators with seeds. Large flowers are generally more attractive to egg-laying females (Després et al 2007), and among flowers of different sizes in natural populations, the ones found without developing larvae (actually very few) are always significantly smaller than average (Jaeger et al 2001;Després et al 2007). Small flower genotypes (if they existed) could disrupt the balance of this interaction if they were to obtain sufficient pollen without paying the cost of seed predation.…”

“…A globeflower's corolla size can determine its attractiveness as a host for flies, as indicated by a number of field studies showing positive correlations between flower size (carpels per flower) and egg load per flower (Pellmyr 1989;Johannesen and Loeschcke 1996;Hemborg and Després 1999;Després et al 2007). Large flowers provide more egg-laying sites (Després and Jaeger 1999), and their higher seed number provide a larger food source and potentially relaxed competition among larvae co-developing in a flower (Jaeger et al 2001).…”

“…The cost of hosting larvae can sometimes be very high for individual plants that become over-loaded with eggs, resulting in very low amounts of seeds being released at the end of the season (Després et al 2007). One way of reducing the risk of being overparasitised is to spread seed predation among many flowers on the same plant.…”