Mutualists and antagonists drive among-population variation in selection and evolution of floral display in a perennial herb

Abstract

Spatial variation in the direction of selection drives the evolution of adaptive differentiation. However, few experimental studies have examined the relative importance of different environmental factors for variation in selection and evolutionary trajectories in natural populations. Here, we combine 8 y of observational data and field experiments to assess the relative importance of mutualistic and antagonistic interactions for spatial variation in selection and short-term evolution of a genetically based floral display dimorphism in the short-lived perennial herb Primula farinosa. Natural populations of this species include two floral morphs: long-scaped plants that present their flowers well above the ground and short-scaped plants with flowers positioned close to the ground. The direction and magnitude of selection on scape morph varied among populations, and so did the frequency of the short morph (median 19%, range 0-100%; n = 69 populations). A field experiment replicated at four sites demonstrated that variation in the strength of interactions with grazers and pollinators were responsible for among-population differences in relative fitness of the two morphs. Selection exerted by grazers favored the short-scaped morph, whereas pollinator-mediated selection favored the long-scaped morph. Moreover, variation in selection among natural populations was associated with differences in morph frequency change, and the experimental removal of grazers at nine sites significantly reduced the frequency of the short-scaped morph over 8 y. The results demonstrate that spatial variation in intensity of grazing and pollination produces a selection mosaic, and that changes in biotic interactions can trigger rapid genetic changes in natural plant populations.

Keywords: adaptive evolution; divergent selection; floral trait; herbivory; natural selection.

Fig. 1.

(Lower) Frequency distribution of the proportion of the short-scaped morph in 69 populations of P. farinosa on Öland, southeastern Sweden in 2001. (Upper) The photos show the long scaped morph (Left) and the short-scaped morph (Right). Photo: J.Å.

Fig. 2.

Relative fitness of the short-scaped morph (ln[mean number of intact mature fruits produced by short-scaped plants divided by mean number of intact mature fruits produced by long-scaped plants]) in P. farinosa populations on Öland, southeastern Sweden in 2000 (n = 37 populations) and 2001 (n = 46 populations). Populations in which the difference in fruit production between scape morphs was statistically significant (according to contrasts in mixed-model ANOVA) are indicated in red (S > L) and blue (S < L); statistically nonsignificant differences are indicated in green.

Fig. 3.

Spatiotemporal variation in relative fitness of the short-scaped morph in five P. farinosa populations sampled over 5 y.

Fig. 4.

Effects of grazer exclusion and supplemental hand-pollination on relative fitness of the short-scaped morph of P. farinosa in a field experiment conducted in four populations: (A) control, (B) grazers excluded, (C) plants receiving supplemental hand-pollination, and (D) grazers excluded and plants receiving supplemental hand-pollination. Population × treatment combinations for which the 95% confidence interval of relative fitness (estimated through bootstrapping 1000 times) did not overlap zero are indicated.

Fig. 5.

Change in the proportion of the short-scaped morph from 2004 to 2012 in control plots and exclosures established in nine populations of P. farinosa. Difference in change between the two treatments tested with paired t test.