Clinal Variation at Phenology-Related Genes in Spruce: Parallel Evolution in FTL2 and Gigantea?

Abstract

Parallel clines in different species, or in different geographical regions of the same species, are an important source of information on the genetic basis of local adaptation. We recently detected latitudinal clines in SNPs frequencies and gene expression of candidate genes for growth cessation in Scandinavian populations of Norway spruce (Picea abies). Here we test whether the same clines are also present in Siberian spruce (P. obovata), a close relative of Norway spruce with a different Quaternary history. We sequenced nine candidate genes and 27 control loci and genotyped 14 SSR loci in six populations of P. obovata located along the Yenisei river from latitude 56°N to latitude 67°N. In contrast to Scandinavian Norway spruce that both departs from the standard neutral model (SNM) and shows a clear population structure, Siberian spruce populations along the Yenisei do not depart from the SNM and are genetically unstructured. Nonetheless, as in Norway spruce, growth cessation is significantly clinal. Polymorphisms in photoperiodic (FTL2) and circadian clock (Gigantea, GI, PRR3) genes also show significant clinal variation and/or evidence of local selection. In GI, one of the variants is the same as in Norway spruce. Finally, a strong cline in gene expression is observed for FTL2, but not for GI. These results, together with recent physiological studies, confirm the key role played by FTL2 and circadian clock genes in the control of growth cessation in spruce species and suggest the presence of parallel adaptation in these two species.I DENTIFYING the loci underlying the variation in quantitative traits and detecting the selection acting on them remains, to this day, one of the main challenges in biology (Rockman 2012;Marjoram et al. 2013). In his Nobel lecture Sidney Brenner (Brenner 2003) predicted that genome-wide association studies (GWAS) would become the main approach to identifying the genetic factors controlling complex traits. The past decade has amply vindicated Brenner's prediction: GWAS have blossomed and identified a large number of single nucleotide polymorphism (SNP) associated to various quantitative traits (Visscher et al. 2012). Limitations of GWAS have, however, started to become evident and different strategies have been offered to alleviate those (Rockman 2012;Marjoram et al. 2013;Vilhjalmsson and Nordborg 2013). In particular, GWAS have limited power unless very large data sets are used. They therefore remain prohibitively expensive, and often not so informative, for nonmodel organisms with limited or nascent genome resources such as conifers. In such organisms a more targeted strategy, combining population genetics, physiology, and expression studies of candidate genes remains a very fruitful approach, at least in the short term. We recently adopted such a strategy in an attempt to unravel the genetic basis of growth cessation, a trait of adaptive value with a strong and well-documented clinal variation, in Norway spruce (Picea abies) (Chen et al. 2012a and references therein). T...

Molecular Proxies for Climate Maladaptation in a Long-Lived Tree (Pinus pinasterAiton, Pinaceae)

“…For instance, by selecting candidates from studies not only in maritime pine but also in other conifers, we assumed that adaptive processes mostly occur by convergent evolution in the same set of genes, while there is evidence suggesting that species adaptation to identical environments may involve separate genes and a certain number of possible paths (e.g., Tenaillon et al 2012). For example, only 2 of the 18 genes surveyed in latitudinal clines of two Eurasian boreal spruces showed identical associations with bud phenology (Chen et al 2012(Chen et al , 2014, while only 3 outlier genes related to climate were shared between two sympatric Picea species in eastern Canada (Prunier et al 2011). Similar results have been reported for adaptation to freshwater in sticklebacks (Deagle et al 2012) and to high elevation in humans (Bigham et al 2010).…”

The extent and meaning of hybridization and introgression between Siberian spruce (Picea obovata) and Norway spruce (Picea abies): cryptic refugia as stepping stones to the west?

“…; Chen et al . ; Table S1, Supporting information) and completed the sampling by adding 20 new populations from hitherto poorly characterized areas such as northeast Russia, the Ob River area and regions east of the Yenisei River (Fig. A; Table S1, Supporting information).…”

Advances and limits of using population genetics to understand local adaptation

“…Population genetic approaches have revealed several examples of convergent local adaptation at the molecular level: within the threespine stickleback (Gaterosteus aculeatus) the EBT locus has been involved in repeated adaptation to freshwater habitats [31], two species of European spruce harbor adaptive latitudinal clines at Ft2 and GI genes [32], and EPAS1 and HBB genes show patterns of high altitude adaptation in both dogs [33] and Tibetan humans [34]. Chen et al [32,36] identified a total of 18 genes harboring SNPs with signatures of latitudinal adaptation in the two species but only 2 genes were detected in both species, and Wang et al [33] identified 14 genes with strong signatures of high altitude adaptation in dogs but only 2 targeted in both dogs and humans. Moreover, the EPAS1 locus does not appear to have been the target of selection in Andean populations [37].…”