Floral trait variation and integration as a function of sexual deception in Gorteria diffusa

Abstract

Phenotypic integration, the coordinated covariance of suites of morphological traits, is critical for proper functioning of organisms. Angiosperm flowers are complex structures comprising suites of traits that function together to achieve effective pollen transfer. Floral integration could reflect shared genetic and developmental control of these traits, or could arise through pollinator-imposed stabilizing correlational selection on traits. We sought to expose mechanisms underlying floral trait integration in the sexually deceptive daisy, Gorteria diffusa, by testing the hypothesis that stabilizing selection imposed by male pollinators on floral traits involved in mimicry has resulted in tighter integration. To do this, we quantified patterns of floral trait variance and covariance in morphologically divergent G. diffusa floral forms representing a continuum in the levels of sexual deception. We show that integration of traits functioning in visual attraction of male pollinators increases with pollinator deception, and is stronger than integration of non-mimicry trait modules. Consistent patterns of within-population trait variance and covariance across floral forms suggest that integration has not been built by stabilizing correlational selection on genetically independent traits. Instead pollinator specialization has selected for tightened integration within modules of linked traits. Despite potentially strong constraint on morphological evolution imposed by developmental genetic linkages between traits, we demonstrate substantial divergence in traits across G. diffusa floral forms and show that divergence has often occurred without altering within-population patterns of trait correlations.

Keywords: Gorteria; insect mimicry; integration.

Figure 1.

Ten floral forms within the G. diffusa species complex showing the full frontal image of the flower, and for each floral form, a close-up of the spotted floret. Floral forms with three-dimensional structures (a–g), floral forms without three-dimensional structures (h–j). Individual floral forms are as follows: (a) Buffels; (b) Spring; (c) Nieuw; (d) Koma; (e) Cal; (f) Okiep; (g) Garies; (h) Soeb; (i) Naries and (j) Oubees. Further descriptions of floral forms can be found in Ellis & Johnson [28].

Figure 2.

Schematic of measured floral traits. (i) Dorsal view of the spotted floret, (ii) side view of a spotted floret, (iii) inset of the floret spot depicting measurements of UV highlights (white circles), (iv) inset of the floret spot with measurements of the three-dimensional structures (black areas), (v) disc floret dissected to reveal petal lobes, (vi) side view of intact disc floret. Measurements were as follows. In the non-spot ray floret trait compartment: a, length of spotted floret; b, width of the spotted floret at 75% of its length; c, angle of the floret tip, d, angle of spotted floret presentation. In the spot trait compartment: e, width of the spot, f, length of spot on midline g, length of spot on floret edge; h, distance to the bottom of the UV highlight; i, length of the UV highlight; j, width of the UV highlight; k, distance to left-hand edge of the three-dimensional structure; l, distance to three-dimensional structure along central axis; m, width of the three-dimensional structure; n, height of the three-dimensional structure. In the disc floret traits compartment: o, length of the disc floret corolla tube; p, width of the disc floret corolla tube; q, length of the pollen presenter; r, length of the free disc floret petal end; s, width of the disc floret petal end.

Figure 3.

Idealized spot arrangements of the different floral forms. Dark grey ovals are the spots, white circles are the highlights, black shapes are the three-dimensional structures, striated black indicates three-dimensional areas without papillate cells, light grey bands are reflective strips. Idealized spot types are lined up on the ‘deception axis’, i.e. floral forms to the left are more sexually deceptive than floral forms on the right. Deception was determined by percentage of mating/inspection visits by Megapalpus capensis. Buffels n = 75; Spring n = 308; Nieuw n = 202; Cal n = 111; Okiep n = 63; Garies n = 45; Soeb n = 17 and Naries n = 9.

Figure 4.

Separation of G. diffusa floral forms on the first two axes of the discriminant function analyses of all measured traits, (a) with and (b) without three-dimensional spot traits. For both datasets, spot traits, and to a lesser extent non-spot ray traits, contribute most to the variance between floral forms explained by the discriminant functions. The most important traits are listed on the axes in descending order of standardized factor coefficients.

Figure 5.

Patterns of covariation within and among floral forms for select trait pairs: (a) floret length versus mid spot length; (b) spot width versus three-dimensional width; (c) edge spot length versus mid spot length and (d) distance to three-dimensional top versus distance to UV. In (a,b) the among-floral-form correlations were not significant despite strong within-floral-form correlations. In (a) the slopes of the within-floral-form correlations between floret and spot dimensions vary significantly between floral forms, whereas in (b) the slopes of the correlations between spot and three-dimensional width do not vary significantly between floral forms despite shifts in the mean ratio of these traits between floral forms. (c,d) Trait pairs relevant to sexual deception (UV-three-dimensional position, and spot shape) which exhibit significant correlations within and between floral forms, despite clear changes between floral forms in mean ratio of the traits. Points are trait means for floral forms, lines are fitted linear correlations within floral forms.

Figure 6.

The influence of degree of sexual deception (proportion of visits by M. capensis males involving mating or inspection responses as opposed to feeding responses) on trait integration in the three trait modules. R-squared values (*p < 0.05) from simple regressions are shown. ANCOVA analysis indicates that degree of deception significantly influences integration when all trait compartments are considered, and that regression slopes differ significantly across trait compartments.