Is floral diversification associated with pollinator divergence? Flower shape, flower colour and pollinator preference in Chilean Mimulus

Abstract

Background and aims: Adaptation to different pollinators is thought to drive divergence in flower colour and morphology, and may lead to interspecific reproductive isolation. Floral diversity was tested for association with divergent pollinator preferences in a group of four closely related wildflower species: the yellow-flowered Mimulus luteus var. luteus and the red-pigmented M. l. variegatus, M. naiandinus and M. cupreus.

Methods: Patterns of pollinator visitation were evaluated in natural plant populations in central Chile, including both single-species and mixed-species sites. Floral anthocyanin pigments were identified, and floral morphology and nectar variation were quantified in a common garden experiment using seeds collected from the study sites.

Key results: Mimulus l. luteus, M. l. variegatus and M. naiandinus are morphologically similar and share a single generalist bumblebee pollinator, Bombus dahlbomii. Mimulus cupreus differs significantly from the first three taxa in corolla shape as well as nectar characteristics, and had far fewer pollinator visits.

Conclusions: This system shows limited potential for pollinator-mediated restriction of gene flow as a function of flower colour, and no evidence of transition to a novel pollinator. Mimulus cupreus may experience reduced interspecific gene flow due to a lack of bumblebee visitation, but not because of its red pigmentation: rare yellow morphs are equally undervisited by pollinators. Overall, the results suggest that factors other than pollinator shifts may contribute to the maintenance of floral diversity in these Chilean Mimulus species.

Fig. 1.

Study sites, species ranges, and typical flowers of the taxa studied. The distribution of Mimulus l. luteus within Chile is shown in yellow. The Chilean distributions of M. l. variegatus and M. cupreus are indicated by the blue dotted and red dashed line, respectively. A rare yellow morph of M. cupreus is known only from LM. Only two populations of M. naiandinus have been found (one of which is the RT study site), both within the range of M. l. variegatus. The primary range of M. l. luteus is in the eastern, montane region of Chile, but there are some reports of populations in the central and coastal regions as well (von Bohlen, 1995). Ranges are redrawn from von Bohlen (1995); the study taxa have occasionally been found in Argentina but their distributions there are unknown. Study sites are denoted by asterisks, and are abbreviated as: SJ, Volcán San José; RP, Río Pangal; RT, Río Tinguiririca; LM, Laguna del Maule; TC, Termas de Chillan; LL, Laguna del Laja. SCL denotes the location of Santiago, Chile. Below each photograph is the name of the taxon and a list of the study sites at which it occurs.

Fig. 2.

Canonical variate analysis on six floral characters of Chilean Mimulus. Symbols indicate Mimulus cupreus (n = 100), M. l. luteus (n = 142), M. l. variegatus (n = 32), M. naiandinus (n = 27), M. l. luteus × M. naiandinus (n = 34). Loadings for the six variables are shown in the lower left corner, using the following abbreviations: L, corolla tube length; W, corolla width; H, maximum corolla height; S, stigma height; SA, stigma–anther separation; and N, nectar volume.

Fig. 3.

Patterns of stigma closure in Chilean Mimulus over a 24-h period at four locations. Location names are followed by the species present at each location. Sample size in the experimental group is indicated by n. Controls (not shown) have sample sizes of approximately 0·5n. Each line represents data collected in one 24-h period; up to three replicates (on different days) were performed per species per site. Time-points are shown along the x-axis; the y-axis shows the percentage of flowers in the experimental group with closed stigmas.

Fig. 4.

Individual variation in Bombus dahlbomii visits to 16 floral phenotypes in a Mimulus l. luteus × M. naiandinus hybrid swarm. Each square in the grid represents one of 16 possible phenotypes, based on the extent of red pigmentation (x-axis; 1 = minimal, 4 = maximal) and yellow pigmentation (y-axis; 1 = minimal, 4 = maximal). The photographs illustrate the following phenotypes, clockwise from top left: (red, yellow) = (1,4); (4,4); (4,1); (1,1). Squares are shaded according to the frequency of the corresponding phenotype, averaged over two censuses. Census sample sizes were n = 554 open flowers (21 January 2005) and n = 714 open flowers (27 January 2005). The symbols indicate the floral-phenotype mean ± s.e. of 19 individual foraging bouts by B. dahlbomii. Sample sizes for the foraging bouts range from 16–316 flowers visited (mean ± s.e. = 77·1 ± 15·72).