Changes in pollinator fauna affect altitudinal variation of floral size in a bumblebee-pollinated herb

Abstract

Geographic trait variations are often caused by locally different selection regimes. As a steep environmental cline along altitude strongly influences adaptive traits, mountain ecosystems are ideal for exploring adaptive differentiation over short distances. We investigated altitudinal floral size variation of Campanula punctata var. hondoensis in 12 populations in three mountain regions of central Japan to test whether the altitudinal floral size variation was correlated with the size of the local bumblebee pollinator and to assess whether floral size was selected for by pollinator size. We found apparent geographic variations in pollinator assemblages along altitude, which consequently produced a geographic change in pollinator size. Similarly, we found altitudinal changes in floral size, which proved to be correlated with the local pollinator size, but not with altitude itself. Furthermore, pollen removal from flower styles onto bees (plant's male fitness) was strongly influenced by the size match between flower style length and pollinator mouthpart length. These results strongly suggest that C. punctata floral size is under pollinator-mediated selection and that a geographic mosaic of locally adapted C. punctata exists at fine spatial scale.

Keywords: Geographic selection mosaic; local adaptation; mechanical fit; phenotypic selection; pollination efficiency.

Figure 1

The male-phase flower of Campanula punctata and a visiting bumblebee. In this phase, the pollens are adhered on the lateral surface of the style. Several days later, in female phase, the tip of the style unfolds and the stigmatic lobes appear. The match between floral style length and pollinator mouthpart length is important in the plant male fitness (pollen removed by bee visits).

Figure 2

(A) A male-phase flower of Campanula punctata and a visiting bumblebee. In this phase, the pollen grains adhere to the lateral surface of the style. Several days later, when the flower enters the female phase, the tip of the style unfolds and the stigmatic lobes appear. CE, corolla entrance diameter; CW, corolla width; SL, style length; CL, corolla length; PL, pollinator length (distance from the base of the foreleg to the tip of the galea); PH, pollinator height (maximum thorax height). (B) Ventral side of bumblebee and definition of PL measurement.

Figure 3

Relationship between pollinator length (PL) and pollinator height (PH) (mean ± SE) in the four dominant bumblebee species visiting Campanula punctata. Bc, Bombus consobrinus (worker); Bd, B. diversus (worker); Ba, B. ardens (male); Bb, B. beaticola (worker).

Figure 4

Top: Altitudinal change in assemblages of Campanula punctata pollinators (bumblebees). From smallest to largest: Bb, B. beaticola workers and males; Ba, B. ardens males; Bh, B. honshuensis workers; Bu, B. ussuriensis workers; Bd, B. diversus workers; Bc, B. consobrinus workers. Bottom: Altitudinal variation in pollinator height (left) or pollinator length (right) in the 12 populations. See Fig.2 for the dimensions indicated by main pollinator length and height. Each diamond represents a population (white, censused in 2010; black, censused in 2011). Populations Ut-2 and Na-7 are circled with a solid and dashed line, respectively. See Fig.5 for more information.

Figure 5

Altitudinal variation in the four floral size parameters (CE, CW, SL, and CL; see Fig.2) and the PC1 and PC2 scores (mean ± SE). Each circle represents a population (white, censused in 2010; black, censused in 2011). The PC1 score and the four size parameters tended to decrease with altitude. Outlier populations are circled: Ut-2, solid line; Na-7, dashed line.

Figure 6

Scatter plots of PC1 scores versus PC2 scores (mean ± SE, estimated from the floral size parameters). Each symbol represents a population mean, and the bars show the standard errors (white, censused in 2010; black, censused in 2011). We identified three clusters: I, large-flower populations; II, small-flower populations; and III, population Ut-2, which had large, wide flowers (see Table2). Outlier populations are circled: Ut-2, solid line; Na-7, dashed line (see Fig.5).

Figure 7

Male fitness (as indicated by pollen removal) as a function of PL:SL. Fitted single linear and quadratic regression lines are also shown. Bb, B. beaticola worker; Bd, B. diversus worker.