Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured

Abstract

Flowering times of plants are important life-history components and it has previously been hypothesized that flowering phenologies may be currently subject to natural selection or be selectively neutral. In this study we reviewed the evidence for phenotypic selection acting on flowering phenology using ordinary and phylogenetic meta-analysis. Phenotypic selection exists when a phenotypic trait co-varies with fitness; therefore, we looked for studies reporting an association between two components of flowering phenology (flowering time or flowering synchrony) with fitness. Data sets comprising 87 and 18 plant species were then used to assess the incidence and strength of phenotypic selection on flowering time and flowering synchrony, respectively. The influence of dependence on pollinators, the duration of the reproductive event, latitude and plant longevity as moderators of selection were also explored. Our results suggest that selection favours early flowering plants, but the strength of selection is influenced by latitude, with selection being stronger in temperate environments. However, there is no consistent pattern of selection on flowering synchrony. Our study demonstrates that phenotypic selection on flowering time is consistent and relatively strong, in contrast to previous hypotheses of selective neutrality, and has implications for the evolution of temperate floras under global climate change.

Response to joint selection on germination and flowering phenology depends on the direction of selection

“…This lack of constraint is consistent with a negligible correlation between timing of germination and flowering found in earlier work using a variance component approach ( r A  = −0.029, equivalent to r Total , Galloway et al., 2009). Selection in natural populations frequently favors early flowering (Austen, Rowe, Stinchcombe, & Forrest, 2017; Munguía‐Rosas, Ollerton, Parra‐Tabla, & De‐Nova, 2011), a pattern expected to become increasingly common in warm climates (Anderson, Inouye, McKinney, Colautti, & Mitchell‐Olds, 2012), including in C. americana (Haggerty & Galloway, 2011). The ability to evolve early flowering, regardless of the pattern of selection on timing of germination, will enhance C. americana 's ability to respond to changing climates.…”

Links between plant species’ spatial and temporal responses to a warming climate

“…Furthermore, in the analysis of both mean range shifts and shifts in southern range margins, the interaction term between climatic niche conservatism through phenological changes and perennation seemed to be influential, suggesting that annual species have a stronger link between spatial and temporal niche dynamics. Lifetime fitness in annual plants may be more affected by the flowering time in any particular year compared with perennial species, as their fitness relies on only one reproductive season, and flowering during times of favourable conditions may be a more critical issue [42]. This means that the selection on flowering time tends to be stronger in annual plants [42].…”

“…Plant flowering phenology is shaped by the interacting dynamics of both biotic and abiotic factors affecting species' fitness [14,40]. However, accumulated evidence has shown that advancing flowering time with warming maintains, or even increases, fitness [41], particularly in temperate regions [42], causing directional selection favouring earlier flowering [43]. Thus, the northward mean range shifts in species experiencing warming temperatures during flowering have presumably been caused by local extirpation of such species failing to advance their phenology sufficiently.…”

“…Lifetime fitness in annual plants may be more affected by the flowering time in any particular year compared with perennial species, as their fitness relies on only one reproductive season, and flowering during times of favourable conditions may be a more critical issue [42]. This means that the selection on flowering time tends to be stronger in annual plants [42]. Annual plants also have greater potential to adapt to changes in climate because of their short generation time [46].…”

Estimating selection through male fitness: three complementary methods illuminate the nature and causes of selection on flowering time

“…More often than not, fitness through male function is left unexamined. For example, just five of 87 studies reviewed in a recent meta-analysis of selection on flowering time considered any effect on male fitness [1]. Because selection through the two sexual functions can conceivably differ in intensity and direction [2], a focus on seed production alone can lead to a biased view.…”