Genetic architecture of pollination syndrome transition between hummingbird-specialist and generalist species in the genus Rhytidophyllum (Gesneriaceae)

Abstract

Adaptation to pollinators is a key factor of diversification in angiosperms. The Caribbean sister genera Rhytidophyllum and Gesneria present an important diversification of floral characters. Most of their species can be divided in two major pollination syndromes. Large-open flowers with pale colours and great amount of nectar represent the generalist syndrome, while the hummingbird-specialist syndrome corresponds to red tubular flowers with a less important nectar volume. Repeated convergent evolution toward the generalist syndrome in this group suggests that such transitions rely on few genes of moderate to large effect. To test this hypothesis, we built a linkage map and performed a QTL detection for divergent pollination syndrome traits by crossing one specimen of the generalist species Rhytidophyllum auriculatum with one specimen of the hummingbird pollinated R. rupincola. Using geometric morphometrics and univariate traits measurements, we found that floral shape among the second-generation hybrids is correlated with morphological variation observed between generalist and hummingbird-specialist species at the genus level. The QTL analysis showed that colour and nectar volume variation between syndromes involve each one major QTL while floral shape has a more complex genetic basis and rely on few genes of moderate effect. Finally, we did not detect any genetic linkage between the QTLs underlying those traits. This genetic independence of traits could have facilitated evolution toward optimal syndromes.

Keywords: Floral evolution; Genotyping by sequencing; Geometric morphometrics; Plant mating systems; Pollination syndrome; QTL.

Figure 1. Measure of shape variation in the hybrid population and parents.

(A) Flowers from both parents (top row), the self-pollinated F1 and samples from the F2 population; (B) position of landmarks on corolla pictures- red stars represent landmarks and small orange stars are semi-landmarks.

Figure 2. Diagram presentation of the four morphological measurement approaches.

Figure 3. Principal component analyses of shape.

(A) PCA performed on wild specimens from species with different pollination syndromes (method i—Pollination syndrome differences); Large and small dots represent species mean shapes and individual shapes, respectively, and individuals that belong to a given species are linked to it with a line. (B) PCA performed on the hybrid population (method iii–Morphological variation in the hybrid population) where triangles represent self-pollinated parents’ progeny. Numbers between brackets are percentage of shape variance represented by each axis.

Figure 4. Shape variation associated with each principal component.

Each point represent a landmark (or semi-landmark) position on the profile of the corolla, as shown in Fig. 1B. Sd, standard deviation, c = 1 for hybrid population PCA, 0.5 for between syndrome PCA and 0.2 for between parents PCA.

Figure 5. Distribution and correlation among traits in the hybrid population.

Diagonal: traits distribution, the vertical lines correspond to the values of parent R. rupincola (red), parent R. auriculatum (green) and the self-pollinated F1 (purple). Lower left triangle, correlation among traits, if covariation is significant after Sidak correction, the regression line was plotted; Upper right triangle, regression coefficient, in bold if correlation is significant.

Figure 6. Linkage map and position of QTLs.

QTLs positions are marked with 2-LOD confidence region, numbers right to the linkage groups represent markers position in cM. Unique names for QTLs correspond to the names given in Table 2.