Rapid evolution caused by pollinator loss in Mimulus guttatus

Abstract

Anthropogenic perturbations including habitat loss and emerging disease are changing pollinator communities and generating novel selection pressures on plant populations. Disruption of plant-pollinator relationships is predicted to cause plant mating system evolution, although this process has not been directly observed. This study demonstrates the immediate evolutionary effects of pollinator loss within experimental populations of a predominately outcrossing wildflower. Initially equivalent populations evolved for five generations within two pollination treatments: abundant bumblebee pollinators versus no pollinators. The populations without pollinators suffered greatly reduced fitness in early generations but rebounded as they evolved an improved ability to self-fertilize. All populations diverged in floral, developmental, and life-history traits, but only a subset of characters showed clear association with pollination treatment. Pronounced treatment effects were noted for anther-stigma separation and autogamous seed set. Dramatic allele frequency changes at two chromosomal polymorphisms occurred in the no pollinator populations, explaining a large fraction of divergence in pollen viability. The pattern of phenotypic and genetic changes in this experiment favors a sequential model for the evolution of the multitrait "selfing syndrome" observed throughout angiosperms.

Figure 1

(A) Trait differences between outcrossing and selfing Mimulus congeners—anterior perspective of flowers from M. guttatus (left) and M. nasutus (right). (B) Diagram of floral measurements. Mimulus guttatus flower, dorsal view, with upper corolla removed to show reproductive structures. Floral measures reported in study depicted with brackets.

Figure 2

Population fitness over five generations of evolution. Per capita seed production (mg) for each population and generation calculated by dividing bulked seed collected from each population by the number of adult plants. As a consequence, standard errors could not be estimated.

Figure 3

Character divergence and chromosomal polymorphism effects. Population trait means (Generation 7) are given for (A) corolla width, (B) self seed, (C) anther–stigma separation, and (D) pollen viability after five generations of selection for the No Bee (A1, A2), Bee (B1, B2), and source populations. Means sharing letters above bars are not significantly different from one another (Tukey–Kramer posthoc). Error bars are ± 1 SEM. In panels (C, D), the predicted effects of the two chromosomal polymorphisms are depicted with arrows for each population (direction and magnitude of trait change expected given the allele frequency difference from the source population). Values at arrow origins are predicted units of trait change. Panel (C) includes only the Inversion whereas (D) is combined effects of Inversion and Drive on pollen viability.

Figure 4

Bivariate plot of the negative relationship between mean anther–stigma separation and mean self seed by experimental population for Generation 7. Error bars are ± 1 SEM.

Figure 5

Mean autogamy positively covaries with heritability for this trait in Generation 7 plants. Error bars are ± 1 SEM.