Pollinator and habitat-mediated selection as potential contributors to ecological speciation in two closely related species

Abstract

In ecological speciation, incipient species diverge due to natural selection that is ecologically based. In flowering plants, different pollinators could mediate that selection (pollinator-mediated divergent selection) or other features of the environment that differ between habitats of 2 species could do so (environment-mediated divergent selection). Although these mechanisms are well understood, they have received little rigorous testing, as few studies of divergent selection across sites of closely related species include both floral traits that influence pollination and vegetative traits that influence survival. This study employed common gardens in sites of the 2 parental species and a hybrid site, each containing advanced generation hybrids along with the parental species, to test these forms of ecological speciation in plants of the genus Ipomopsis. A total of 3 vegetative traits (specific leaf area, leaf trichomes, and photosynthetic water-use efficiency) and 5 floral traits (corolla length and width, anther insertion, petal color, and nectar production) were analyzed for impacts on fitness components (survival to flowering and seeds per flower, respectively). These traits exhibited strong clines across the elevational gradient in the hybrid zone, with narrower clines in theory reflecting stronger selection or higher genetic variance. Plants with long corollas and inserted anthers had higher seeds per flower at the Ipomopsis tenuituba site, whereas selection favored the reverse condition at the Ipomopsis aggregata site, a signature of divergent selection. In contrast, no divergent selection due to variation in survival was detected on any vegetative trait. Selection within the hybrid zone most closely resembled selection within the I. aggregata site. Across traits, the strength of divergent selection was not significantly correlated with width of the cline, which was better predicted by evolvability (standardized genetic variance). These results support the role of pollinator-mediated divergent selection in ecological speciation and illustrate the importance of genetic variance in determining divergence across hybrid zones.

Keywords: cline; divergent selection; floral traits; pollination; speciation; vegetative traits.

Figure 1.

Divergent selection on two floral traits in Ipomopsis. Relative seeds per flower as a function of (A) standardized corolla length and (B) standardized anther insertion in the two parental sites. Selection differed significantly across sites (p < .01 for site × trait interaction; Table 1). The fitted curves show best-fitting quadratic regressions. Corolla length averaged 27.0 mm for I. aggregata in the I. aggregata site (standardized value = −.42; solid arrow) and 35.3 mm for I. tenuituba in the I. tenuituba site (standardized value = 1.74; dashed arrow). Anther insertion averaged 0.75 mm for I. aggregata in the I. aggregata site (standardized value = −0.66; solid arrow) and 4.92 mm for I. tenuituba in the I. tenuituba site (standardized value = 1.58; dashed arrow). Inset photos show single flowers of the two species positioned above the mean values at their home sites.

Figure 2.

Relative seeds per flower as a function of (A) standardized corolla width and (B) flower color in the two parental sites. Neither trait showed evidence of divergent selection across the two sites. Selection favored wider corollas at the I. aggregata site (p < .05) and was not significant at the I. tenuituba site. Selection overall favored less red flowers (p < .05, Table 3). The fitted curves show best-fitting quadratic regressions. Corolla width averaged 3.52 mm for I. aggregata in the I. aggregata site (standardized value = 0.46; solid arrow) and 3.06 mm for I. tenuituba in the I. tenuituba site (standardized value = −0.85; dashed arrow). Relative reflectance in the red compared to the green averaged 0.61 for I. aggregata in the I. aggregata site (standardized value = 0.59; solid arrow) and 0.14 for I. tenuituba in the I. tenuiutuba site (standardized value = −1.80; dashed arrow).

Figure 3.

Relative survival to flowering as a function of standardized specific leaf area (SLA) in the two parental sites. Selection was directional, favoring lower SLA (p < 0.001; Table 1). Curves show logistic fits separately by site. SLA averaged 186.7 cm²/g for I. aggregata in the I. aggregata site (standardized value = 0.24; solid arrow) and 180.9 cm²/g for I. tenuituba in the I. tenuituba site (standardized value = 0.08; dashed arrow) in this data set. Species differences across the hybrid zone were more extreme in a previous study (180 cm²/g and 150 cm²/g in 2015–2016 at the I. aggregata and I. tenuituba ends of the hybrid zone; Campbell et al., 2018).