Department of Ecology and Genetics, Uppsala University
This is a flowering highlight that only indirectly concerns flowering. Furthermore the study does not address the molecular basis of flowering as is often the case in these columns but instead is highly relevant to the understanding of its adaptive basis. Indeed the study by Yeaman et al. (2016) may well herald a new era in the analysis of local adaptation. While there is ample evidence of local adaptation for flowering time and other putatively adaptive traits (Savolainen et al., 2013) it has proven harder to identify the genes associated with it. There are various methods to do so, all of them with strengths and weaknesses. One popular approach is to test for statistical association between flowering time variation and genetic polymorphisms along the genome. A major issue with this approach is that the signal of local adaptation can be confounded by population genetic structure.
For example, if one samples plants along a latitudinal gradient in Scandinavia, any difference between individuals from the North and the South could reflect the fact that Scandinavia was recolonized along two main routes after the Last Glacial Maximum (18,000 years ago), one entering Scandinavia from the south and the other from the north. So plants from northern Scandinavia can differ from their southern counterparts simply because they have different origins and differences between them cannot automatically be assigned to adaptation to the local environment. Of course, there are methods to correct for population structure, but if adaptation and demographic history go hand in hand, removing one may well end up removing the other leading to false negatives.
How did Yeaman et al. (2016) address this thorny issue? Well, they chose not to address it directly; instead they took a different road. Here is the main thrust of their reasoning. Lodgepole pine (Pinus contorta) and interior spruce (Picea glauca, Picea engelmannii and their hybrids) are two common conifer species in western Canada. Pines and spruces diverged some 140 million years ago, and we therefore do not expect to see shared polymorphism left between the two species. Being a complex species interior spruce has a particularly intricate population structure. So rather than risking a high number of false negatives by attempting to correct for population structure they assessed the relationship between genome-wide SNP variation, on the one hand, and 17 phenotypic traits assessed in growth chamber and 22 environmental variables, on the other hand, in both species. This was done without correcting for population structure. For each species they then obtained a list of top candidate genes. Of course many of them are likely false positives. But which ones are false positives and which ones true candidate genes?
In order to find out which genes could be good candidate genes for local adaptation, and incidentally test for convergent local adaptation, the authors looked for genes that are top candidates in both species. Top candidates were defined as genes with an exceptional proportion of their total SNPs being associated to either phenotype or environment. Depending on how stringent the False Discovery Rate (FDR) is the number of genes with strong signature of convergent local adaptation varied between 6 and 83. For a FDR=0.05 the number was 47. Many of those 47 top candidates had conserved patterns of differential expression in both species and/or were enriched for transcription factors and genes involved in biological regulation. Several of the convergent genes such as Pseudo-response regulator 5 (PPR5) that regulates the circadian clock or FY that indirectly regulates FLOWERING LOCUS C are part of the pathways controlling flowering time in Arabidopsis thaliana and are prime candidates for being involved in the control of phenology in trees.
So, after all, this study is not that far from the usual topic of this column. But, in my view, its foremost value is its very innovative use of comparative genomics. It is not the first comparative study of local adaptation in trees (see Chen et al., 2012, 2014) but it is certainly the first to be carried out on a genomic scale and on highly diverged species. I do not doubt that it will have a strong impact on future studies of local adaptation for phenological traits, in general, and on flowering time, in particular. Associated with functional studies the general approach developed by Yeaman et al. (2016) could lead to new insights on the evolution of the basic molecular mechanisms associated with local adaptation.
Yeaman S., Hodgins KA, Lotterhos KE, Suren H, Nadeau S, Degner JC, et al. 2016. Convergent local adaptation to climate in distantly related conifers. Science 353(6306), 1431–1433.
Chen J, Källman, T, Ma X, Gyllenstrand N, Zaina G, Morgante M, et al. 2012. Disentangling the roles of history and local selection in shaping clinal variation of allele frequencies and gene expression in Norway spruce (Picea abies). Genetics 191, 865–881.
Chen J, Tsuda Y, Stocks M, Källman T, Xu N, Kärkkäinen K, et al. 2014. Clinal variation at phenology-related genes in spruce: parallel evolution in FTL2 and Gigantea? Genetics 197(3), 1025–1038.
Savolainen O, Lascoux M, & Merilä J. 2013. Ecological genomics of local adaptation. Nature Reviews Genetics 14(11), 807–820.