Urbanization Alters Phenology, Mating System Allocation, and Life History of Impatiens capensis (Balsaminaceae) via Trait-Specific Plasticity and Genetic Differentiation

Abstract

Urbanization is a major human-mediated driver of environmental change. Plants in urban environments may differ in timing and investment in key life history traits compared to rural plants as a result of genetic differentiation or plastic responses to the urban environment. However, it is unclear for many species whether genetic differentiation or plasticity has shaped urban phenotypes. Impatiens capensis is an annual plant that produces self-pollinating and outcrossing flowers, varying in timing and amount based on environmental conditions. In this study, we characterized differences in floral phenology, mating system allocation, and key life history events between urban and rural populations of I. capensis, in situ and in greenhouse common gardens. We asked whether (1) floral investment varies with urbanization in situ, if (2) the differences between urban and rural populations are maintained (genetic differentiation) or lost/exaggerated (plasticity) in a common garden, if (3) differences can be attributed to shifts in life history strategy, and if (4) urban population traits are more variable (higher coefficient of variation). In situ, we found that urban populations advanced flowering time and invested more in outcrossing flowers compared to rural populations. Within greenhouse common gardens, urban plants maintained advanced flowering and were less variable than rural plants (low CV), indicative of genetic differentiation. In contrast, urban plants lost outcrossing bias in mating system allocation observed in situ, indicating plasticity, although both urban and rural plants were highly variable (high CV) for this trait. Early onset of selfing flowers was tied to earlier germination, but outcrossing onset was not affected by germination time. Flowering probability in urban plants was higher than rural ones in common gardens. Our study demonstrates that urbanization influences plant phenotypes through both genetic differentiation and phenotypic plasticity, but the relative importance of the two mechanisms of change vary among floral traits.

Keywords: common garden; life history; mixed mating system; phenology; plasticity; urbanization.

FIGURE 1

Conceptual diagram of specific hypotheses for Q3: How life history events may influence differences found between urban (U, dashed lines) and rural (R, solid lines) phenotypes of Impatiens capensis . First, H ₀ denotes no difference between population types, as the life history cassettes of germination (blue), selfing flower production (yellow), and outcrossing flower production (red) do not differ between urban and rural populations. Next, H3 hypothesized urban populations have advanced phenology of (A) germination, (B) selfing flower production, and/or (C) outcrossing flower production relative to rural ones. Finally, H4 hypothesized urban populations have an increased probability (denoted by increased cassette height) of (D) germination, (E) selfing flower production, and/or (F) outcrossing flower production relative to rural ones. Note that hypothesized changes are not mutually exclusive and it is likely that a combination of these strategies are present in urban populations.

FIGURE 2

Populations of I. capensis characterized in Pennsylvania USA. Populations were categorized as rural (green circles) or urban (orange triangles). Impervious surface is shown as dark gray pixels and all other land use types are shown as white pixels on the map. Thus, city centers like Pittsburgh are represented by dense clusters of dark gray pixels (ESRI 2024).

FIGURE 3

Density plots with means (vertical lines) of flowering phenology of rural (green solid) and urban (orange dashed) populations (A) in situ and in (B) greenhouse common garden, surveyed early (left panel) and late (right panel) in the flowering season. In both studies, urban populations were significantly more advanced than rural ones in the early, but not late survey. Rural populations were less variable in flowering phenology than urban ones, but both shifted toward senescence in the late survey. (C) Coefficient of variation (CV) ± SE for in situ flowering phenophase was higher in urban populations than rural ones; CV decreased in both populations in the late survey, but more sharply in rural populations. (D) CV ± SE for greenhouse common garden plants was higher for rural plants than urban ones, indicating greater environmental sensitivity in urban plants, although CV declined for both population types in the late survey. Note the different y‐axis ranges for in situ and common garden CVs. Flowering phenology was measured as a phenophase scale of one to eight that ranged from non‐flowering vegetative (i.e., 0), peak flower production (i.e., 5), to fruiting and senescence (i.e., 8). NS p > 0.05, *p < 0.05, **p < 0.01.

FIGURE 4

Outcrossing to selfing ratio displayed as boxplots overlayed with raw data for rural (green circles) and urban (orange triangles) populations in (A) in situ and (B) greenhouse common garden of plants surveyed early (left panel) and late (right panel) in the flowering season. Estimated marginal means are shown as large black symbols. (C) CV ± SE of outcrossing to selfing was not significantly different for in situ urban and rural populations, rather it was highly variable overall. (D) CV ± SE of outcrossing to selfing ratio was higher in urban than in rural plants in the greenhouse common garden, though CV declined for both plant types between the early and late surveys. Note the different y‐axis ranges for CVs.

FIGURE 5

Estimated marginal means (±SE) onset of key life history events for urban and rural plants grown in greenhouse common gardens in 2022 and 2023. When germination (circles) occurred earlier in the year, the timing of selfing onset (squares) was also more advanced, occurring earlier in the year. When germination was more delayed, the selfing onset also shifted later in the year. However, the timing of outcrossing onset (triangles) did not shift significantly with any directional changes in germination or selfing flower production. Interestingly, urban plants displayed a heightened sensitivity to developmental phenology shifts in comparison to rural ones (i.e., earlier germination led to even earlier selfing onset in urban populations).

FIGURE 6

Summary of results following hypothetical Figure 1 in which common gardened urban and rural plants showed differences in germination, selfing, and outcrossing probability, and shift timing of selfing onset as a result of shifting germination timing. This shift in selfing phenology is more pronounced in urban than in rural plants. In contrast, outcrossing is unresponsive to timing of germination or selfing, and instead responds to contemporaneous environmental cues.

FIGURE A1

Binomial data of probability of (A) germination, (B) selfing flower production, and (C) outcrossing flower production for rural (green circles) and urban (orange triangles) populations of I. capensis in common gardens, where size of points is scaled by number of plants with that value. Estimated marginal means (±SE) are shown as black symbols with error bars. The probability of germination was very high, but differed slightly between population types, years, and their interaction (Table 3A, main text). Probability of selfing was higher in urban plants (p = 0.05), but did not differ between years or by the population type*year interaction (Table 3B, main text). Outcrossing flower production differed significantly between years (p < 0.0001), but did not vary significantly between population types (p = 0.09) or the population type*year interaction (Table 3C, main text).

FIGURE A2

Boxplots overlayed with raw data of days between onset of selfing and onset of outcrossing flower production for rural (green circles) and urban (orange triangles) I. capensis in two different years of common gardens. Estimated marginal means (±SE) are shown as black symbols with error bars. Mean time between production of selfing and outcrossing flowers was more variable in 2022 than in 2023, but did not differ by year (p = 0.25), between population types (p = 0.71) or the interaction between population type and year (p = 0.92).