Differences in flowering time maintain species boundaries in a continental radiation ofViburnum

Abstract

Premise We take an integrative approach in assessing how introgression and Pleistocene climate fluctuations have shaped the diversification of the core Lentago clade of Viburnum, a group of five interfertile species with broad areas of sympatry. We specifically tested whether flowering time plays a role in maintaining species isolation. Methods RAD‐seq data for 103 individuals were used to infer the species relationships and the genetic structure within each species. Flowering times were compared among species on the basis of historical flowering dates documented by herbarium specimens. Results Within each species, we found a strong relationship between flowering date and latitude, such that southern populations flower earlier than northern ones. In areas of sympatry, the species flower in sequence rather than simultaneously, with flowering dates offset by ≥9 d for all species pairs. In two cases it appears that the offset in flowering times is an incidental consequence of adaptation to differing climates, but in the recently diverged sister species V. prunifolium and V. rufidulum, we find evidence that reinforcement led to reproductive character displacement. Long‐term trends suggest that the two northern‐most species are flowering earlier in response to recent climate change. Conclusions We argue that speciation in the Lentago clade has primarily occurred through ecological divergence of allopatric populations, but differences in flowering time were essential to maintain separation of incipient species when they came into secondary contact. This combination of factors may underlie diversification in many other plant clades.

Phylogeography and the Evolutionary History of Sunflower (Helianthus annuus L.): Wild Diversity and the Dynamics of Domestication

“…Indeed, many such species have been found to have undergone dramatic range contractions into southern refugia during glacial periods and rapidly expanded northward as climates warmed following the LGM [23][24][25]57]. This general pattern of northward expansion from lower latitude refugial areas has also been observed in a number of widespread species, whose contemporary distributions span both glaciated and unglaciated North America: e.g., herbs (Asclepias exaltata [58], Campanulastrum americanum [59], Trillium erectum and T. grandiflorum [60,61], and Symplocarpus foetidus [62]); shrubs (Dirca paulustris [63], Viburnum lantanoides [64], Viburnum nudum complex [65], and the Lentago clade of Viburnum [66]); and trees (e.g., Acer rubrum and sacharum [67,68], Carya cordiformis and ovata [69,70], Fagus grandifolia [67,71], and Pinus strobus [72,73]).…”

Joint phylogenetic estimation of geographic movements and biome shifts during the global diversification ofViburnum

“…First, basic taxonomic issues remain, and we anticipate the discovery of additional Viburnum species as we apply molecular approaches at the population level. A case in point is our resurrection of V. nitidum, which was hidden on the coastal plain of the Southeastern US (Spriggs et al, 2019). Second, we are painfully aware of how little we know about extinct viburnums.…”

Phenological displacement is uncommon among sympatric angiosperms

“…Either of these processes should select for the evolution of staggered, minimally overlapping flowering schedules, especially between closely related taxa. Indeed, divergence in flowering time among sympatric plants have been documented in numerous studies (e.g., (Levin, 2006;Lowry et al, 2008;Spriggs et al, 2019;Stiles, 1977;Stinson, 2004)).…”

“…Reproductive character displacement -the modification of reproductive traits in sympatric populations of related species -is widely considered to be a key mechanism facilitating co-occurrence, reproductive isolation, and ecological and evolutionary divergence (J A Coyne & Orr, 2004; Jerry A Coyne, 1992;Grant & Grant, 2011;Mayr, 1947). This is especially true for the timing (phenology) of flowering, which is strongly linked to fitness and often highly variable even among closely related taxa (Briscoe Runquist, Chu, Iverson, Kopp, & Moeller, 2014;Brody, 1997;Domínguez & Dirzo, 1995;Galloway, 2002;Kelly & Levin, 2000;Lacey, Roach, Herr, Kincaid, & Perrott, 2003;Lowry, Rockwood, & Willis, 2008;Park et al, 2018;B Rathcke & Lacey, 1985;Sletvold, Moritz, & Ågren, 2015;Spriggs et al, 2019;Stinson, 2004).…”

“…Flowering phenology is a heritable trait on which selection can act rapidly (Allard & Hansche, 1964;Bergh, 1976;Izawa, 2007). Despite its relevance, empirical evidence for phenological character displacement in plants remains limited to a small number of case studies (e.g., (Briscoe Runquist et al, 2014;Lowry et al, 2008;Spriggs et al, 2019). This greatly limits our ability to understand the general relevance of phenological displacement governing plant interactions and distributions.…”