Rapid evolution of an adaptive cyanogenesis cline in introduced North American white clover (Trifolium repens L.)

Abstract

White clover is polymorphic for cyanogenesis (HCN production after tissue damage), and this herbivore defence polymorphism has served as a classic model for studying adaptive variation. The cyanogenic phenotype requires two interacting biochemical components; the presence/absence of each component is controlled by a simple Mendelian gene (Ac/ac and Li/li). Climate-associated cyanogenesis clines occur in both native (Eurasian) and introduced populations worldwide, with cyanogenic plants predominating in warmer locations. Moreover, previous studies have suggested that epistatic selection may act within populations to maintain cyanogenic (AcLi) plants and acyanogenic plants that lack both components (acli plants) at the expense of plants possessing a single component (Acli and acLi plants). Here, we examine the roles of selection, gene flow and demography in the evolution of a latitudinal cyanogenesis cline in introduced North American populations. Using 1145 plants sampled across a 1650 km transect, we determine the distribution of cyanogenesis variation across the central United States and investigate whether clinal variation is adaptive or an artefact of population introduction history. We also test for the evidence of epistatic selection. We detect a clear latitudinal cline, with cyanogenesis frequencies increasing from 11% to 86% across the transect. Population structure analysis using nine microsatellite loci indicates that the cline is adaptive and not a by-product of demographic history. However, we find no evidence for epistatic selection within populations. Our results provide strong evidence for rapid adaptive evolution in these introduced populations, and they further suggest that the mechanisms maintaining adaptive variation may vary among populations of a species.

Urbanization drives the evolution of parallel clines in plant populations

“…Adaptive clines in cyanogenesis can arise because of spatial gradients in either the defensive benefits or the self-toxicity costs of cyanogenesis [21]. We tested two non-exclusive hypotheses that could explain the results of our natural population surveys: (i) cyanogenesis is more beneficial in rural areas because of increased herbivory, and (ii) cyanogenesis is more costly in urban areas because of colder winter ground temperatures.…”

“…0.4; see below); (v) less than 10 cm snowfall in the previous 5 days to allow sufficient time for the effects of urbanization on snow melt to occur. We focused our analyses on January and February because January isotherms have previously been implicated as major factors driving the evolution of clines in T. repens cyanogenesis [19,21], and there were insufficient images from January alone for robust analysis. For images that met these criteria (list of images archived on Dryad), we extracted the NDSI [32] for each of our study populations using the point sampling tool in QGIS 2.12 [33].…”

“…While distance to an urban centre might explain evolutionary patterns, it is important to distinguish large-scale factors associated with urbanization from finer-scale local factors [21]. To accomplish this, we retrieved 2015 human population density estimates from the NASA GPW4 dataset (resolution ¼ 1 km) [30].…”

“…cyanogenic glycosides and linamarase) are stored separately in cells to avoid self-toxicity, and only form HCN when they are brought together following tissue damage. Previous research found that cyanogenesis is most frequent in populations at low latitudes and elevations [19,20], and it has been hypothesized that herbivores select for cyanogenesis in these warm environments [17,21]. In cold climates, cyanogenesis is selected against because freezing temperatures lyse cells and trigger HCN release, causing self-toxicity in cyanogenic plants [17,22,23].…”

The roles of genetic drift and natural selection in quantitative trait divergence along an altitudinal gradient in Arabidopsis thaliana

“…Local adaptation often leads to the formation of clinal or ecotypic variation that can evolve over surprisingly short distances (e.g., Brady et al, 2005). Clinal variation can establish fast, repeatedly and with ongoing gene flow, as has for example been shown for cyanogenesis clines in white clover (Kooyers and Olsen, 2012) and for climateassociated morphological clines in invasive plants (Monty and Mahy, 2009). Understanding local adaptation requires the identification of genetically based traits under divergent selection.…”