Floral scent of the Mediterranean fig tree: significant inter-varietal difference but strong conservation of the signal responsible for pollinator attraction

Abstract

For thousands of years, humans have domesticated different plants by selecting for particular characters, often affecting less-known traits, including the volatile organic compounds (VOCs) emitted by these plants for defense or reproduction. The fig tree Ficus carica has a very wide range of varieties in the Mediterranean region and is selected for its traits affecting fruits, including pollination, but the effect of human-driven diversification on the VOCs emitted by the receptive figs to attract their pollinator (Blastophaga psenes) is not known. In the present study, VOCs from receptive figs of eight varieties in northern Morocco, were collected at different times within the manual pollination period and analyzed by gas chromatography-mass spectrometry. Genetic analyses using microsatellite loci were performed on the same varieties. Despite strong inter-varietal differences in the quantity and relative proportions of all VOCs, the relative proportions of the four pollinator-attractive VOCs showed limited variation among varieties. There was no significant correlation between genetic markers and chemical profiles of the different varieties. While diversification driven by humans has led to differences between varieties in VOC profiles, this paper suggests that throughout the process of domestication and varietal diversification, stabilizing selection has maintained a strong signal favoring pollinator attraction.

Figure 1

Diagram showing the timing of manual pollination and of collection of volatile organic compounds (VOCs) from receptive figs for the eight varieties of Ficus carica studied. The time of the year is indicated by the black arrow at the top of the diagram. For each variety, the first manual pollination time is indicated and each individual tree was pollinated two to three more times over a period of two to three weeks. Varieties with the same color (grey: Beginning; yellow: Middle; blue: End) experienced the first manual pollination at the same time. Three VOC collection sections of the same six individual trees per variety were made (indicated by the drawing of the figs). For each of these sections, the mean (± standard errors) per individual tree of the temperatures inside (in) and outside (out) the bag containing the figs are presented in degrees Celsius.

Figure 2

Comparison among the eight varieties of Ficus carica of the total estimated quantities and relative proportions of volatile organic compounds (VOCs) emitted by receptive figs. The box plot of estimated total quantifies (log-transformed) of all VOCs (a) and of the four pollinator-attractive VOCs (b) are presented, together with the results of pairwise comparisons of estimated total quantities within each variety using least-squares means comparisons. Different letters indicate statistically significant differences. Non-metric multidimensional scaling ordination (NMDS) of the relative proportions based on Bray–Curtis distance are presented for all VOCs (c, Stress = 0.113) and for the four pollinator-attractive VOCs (d, Stress = 0.066) (circle: 2017, triangle: 2018). In addition, results of pairwise comparisons of the relative proportions using PERMANOVA are presented for all VOCs (e) and for the four VOCs responsible for pollinator attraction (f). p < 0.01: _**p < 0.05: _*p > 0.05: NS.

Figure 3

Genetic (a) and chemical (b) dendrograms. Independent matrices coding genetic distances between varieties were calculated from allele frequency data by neighbor-joining based on Nei distance. Chemical dendrogram was created by using neighbor joining based on the Bray–Curtis distance matrix for the averaged relative proportions of VOCs per variety.

Figure 4

Comparison of the estimated quantities of all volatile organic compounds (VOCs) (a) and of the four VOCs responsible for pollinator attraction (b) at the three different times within the manual pollination period for each of the eight varieties. Data were log-transformed. Results of pairwise comparisons of estimated total quantifies within each variety using least-squares means comparisons are presented, with different letters indicating statistically significant differences.

Figure 5

Relative proportions of the four pollinator-attractive volatile organic compounds (VOCs) at the three different time within the manual pollination period of the eight varieties (a, b, c, d, e, f, g and h). Results of pairwise comparisons between times were performed with correction of p-values using the “fdr” procedure. Different letters indicate statistically significant differences. When no letter is indicated, the global test was not statistically significantly different.