Seasonal patterns of photochemical capacity and spring phenology reveal genetic differentiation among native Scots pine (Pinus sylvestris L.) populations in Scotland
Highlights
► Scots pine found over a spatially heterogeneous environment in Scotland. ► Little is known about patterns of adaptive genetic variation within the region. ► Variation in photochemical capacity and phenology studied in eight populations. ► Population and family differences found suggest adaption to home environments. ► A revision of current seed transfer guidelines is required.
Introduction
When a species occurs over a spatially heterogeneous environment, divergent selection among different parts of the range often results in the development of genetically differentiated populations which are adapted to the conditions in their home environments (e.g. Linhart and Grant, 1996, Kawecki and Ebert, 2004). Many widespread tree species occur across sharp ecological gradients in temperature and moisture conditions (e.g. Petit and Hampe, 2006) and have developed significant genetic differentiation in quantitative traits among populations. These differences are revealed when provenances are grown together under common-garden conditions and when seed is transferred to sites that differ environmentally from its home site (reviewed in Howe et al., 2003, Savolainen et al., 2007, Aitken et al., 2008). Studying local adaptation in trees has a long history due to the economic importance of many species (Mátyás, 1996), but understanding associations between environmental and phenotypic variation is also required for conservation management of ecologically important species (McKay et al., 2005).
Scotland is the geographically separate, north-western tip of the wide pan-Eurasian distribution of Scots pine (Pinus sylvestris L.; Critchfield and Little, 1966). In Scotland, 84 pinewoods of variable size are currently recognised as native by the British Forestry Commission (Jones, 1999), which together constitute only about 1% of the maximum postglacial coverage (e.g. Mason et al., 2004). Despite significant historical population size decrease, most populations remain diverse at selectively neutral molecular markers, with only a small proportion of the variation due to among-population differences (Forrest, 1980, Kinloch et al., 1986, Provan et al., 1998). Moreover, variation at several candidate genes in Scottish populations was similar to that in more continuous continental populations (Wachowiak et al., 2011). However, little is currently known about patterns of adaptive variation in phenotypic traits among Scottish pinewoods. Early provenance experiments set up by the Forestry Commission in Scotland, starting in the 1920s, suggested differences in performance among some native pinewoods (Lines and Mitchell, 1965) and that performance of continental provenances in Scotland is worse than that of native provenances grown on the same site (Worrell, 1992). It has also been noted that trees transferred from continental to strongly oceanic areas usually perform worse than local populations, possibly due to pathogen stress (e.g. Mason et al., 2004). However, until now, only a few small-scale studies have been performed on phenotypic variation within Scotland (Perks and McKay, 1997, Perks and Ennos, 1999) and it is not known how adaptive traits vary among populations as a result of possible genetic differentiation. Despite the relatively small area covered by Scottish native pinewoods and the relatively short distances between them (the total area of native woodland is approximately 18,000 ha and maximum distance between two pinewoods is less than 200 km), they occur over a range of altitudes and environmentally diverse conditions, with significant gradients in rainfall and temperatures (Salmela et al., 2010). Evidence for environment-driven genetic differentiation in adaptive traits among continental Scots pine populations has been found in previous common-garden studies where sampling has often been done on a much wider geographic scale (e.g. Sarvas, 1962, Wright et al., 1966, Steiner, 1979, Oleksyn et al., 1992, Hurme et al., 1997, Cregg and Zhang, 2001, Andersson and Fedorkov, 2004). Due to the lack of knowledge on patterns of adaptive variation in Scotland, the current seed transfer guidelines are based on earlier work using isozymes and monoterpenes (Forrest, 1980, Kinloch et al., 1986), and divide Scotland into seven geographical zones of biochemical similarity. However, while being valuable tools for studies of population structure and gene flow, such markers often fail to reflect adaptive divergence in phenotype among different populations (Karhu et al., 1996, McKay and Latta, 2002). To underpin policy for the conservation of adaptive genetic variation and the maintenance of evolutionary potential in Scottish populations in future, an extensive assessment of patterns of adaptive variation in relation to local environments is needed.
Seasonality characterises the natural habitats of temperate and boreal zone tree species, where environmental conditions are ideal for growth for a limited period of time. Trees have adapted to such environmental variation by switching between periods of active growth and dormancy in response to changes in temperature or photoperiod (Howe et al., 2003). Photosynthesis shows clear seasonal variation in relation to temperature conditions in northern conifers (Öquist and Huner, 2003): in Scots pine growing in northern Sweden, photosynthetic activity declined along with decreasing autumn temperatures, was inhibited in the middle of winter due to freezing temperatures, and recovered in spring as temperatures started to rise (Ottander et al., 1995). Similarly, the phenology of events such as growth initiation and cessation are also governed by environmental cues (Howe et al., 2003). By timing growth to suit their environment, trees minimise the risk of frost injury at the beginning and the end of their growth periods and maximise their growth potential. Commonly, trees from sites with shorter growing seasons respond to rising temperatures earlier in spring (Steiner, 1979, Beuker, 1994) and cease growing (Oleksyn et al., 1992) and develop cold hardiness earlier in autumn (Hurme et al., 1997) when kept under common-garden conditions. Mismatches between growth phenology and environment can lead to poorer fitness or growth performance: in northern Sweden, transferring seedlings further north has been found to result in increased mortality, and while transfers south increase survival, the transferred trees grow less than the local population due to earlier cessation of growth (Persson and Ståhl, 1990).
Initiation and cessation of growth can be easily scored in a large number of young seedlings and variation in these traits has been extensively studied in forest trees (Howe et al., 2003, Savolainen et al., 2007, Aitken et al., 2008). How the seasonal pattern of photosynthetic activity varies among populations from diverse climates growing under common-garden conditions has not been examined in such great detail. Chlorophyll (a) fluorescence is an efficient and commonly used method allowing a quick evaluation of processes occurring at photosystem II (PSII), the site for the light-driven part of photosynthesis (e.g. Baker and Rosenqvist, 2004). The ratio of two fluorescence parameters, Fv/Fm, is a measure of the maximum quantum yield of primary photochemistry at PSII and is close to 0.8 in healthy plants across various genera (Björkman and Demmig, 1987). Also, a good correlation between Fv/Fm and CO2 fixation has been reported in controlled conditions (Genty et al., 1989), but the relationship can be more complex in natural environments due to other competing processes (Maxwell and Johnson, 2000). PSII is sensitive to environmental stimuli and responses to rising or decreasing temperatures are often reflected in an increase or a decline in Fv/Fm, respectively (Bolhàr-Nordenkampf and Öquist, 1993). Chlorophyll fluorescence has been extensively used in plant physiology and to study stress tolerance among relatively small numbers of genotypes, but has yet to become a popular tool in evolutionary biology for assessing differences in photosynthetic activity in response to environmental signals among multiple populations (for examples, see Parker et al., 2003, Aranda et al., 2005, López et al., 2009).
In this study of an outdoor common-garden trial, our aim was to examine seasonal patterns of photochemical capacity at PSII (estimated as Fv/Fm) under natural climatic conditions in an outdoor common-garden trial of eight native Scots pine populations in Scotland covering a steep gradient in growing season length and annual temperature conditions. We tested the hypothesis that, if genetically differentiated and adapted to the local environment at their home site, then populations would differ in their response to conditions at a common-garden site, and that the patterns of variation would be associated with the environmental characteristics at their home sites. We also recorded timing of growth initiation in spring to test whether phenological differences among populations reflected potential adaptation to local conditions.
Section snippets
Study populations
Eight native Scots pine populations were chosen for the study (Fig. 1). The locations that these populations occupy represent a gradient in the temperature-driven growing season length within Scotland (Table 1). UK Met Office climate data were used to estimate average (1961–1990) growing season length (GSL), mean February and July temperatures, and annual number of air and ground frost days (Perry and Hollis, 2005) at each location. The climate data for the UK are divided into 5 × 5 km grids and
Temperature variation at the experimental site
During the study, temperature dropped below 0 °C for the first time on November 9, but daily average temperatures stayed above freezing until late November (Fig. 2). The coldest day of the period was January 7 (average temperature −6.2 °C). The winter of 2009/2010 was exceptionally cold for Scotland: the long-term (1971–2000) average winter temperature is 2.7 °C, while between December and February 2009/2010 it was estimated by UK Met Office to be 0.24 °C. The seedlings were covered in snow from
Discussion
In this study, we examined variation in seasonal patterns of photochemical capacity in Scots pine seedlings from eight climatically diverse Scottish populations under natural climatic conditions. Fv/Fm showed a distinct seasonal trend, remaining at relatively high levels until December and decreasing towards mid-winter following a period of over 2 weeks with temperatures below or close to 0 °C. Populations responded differently to the change in temperature, with the largest drop in photochemical
Conclusions
In summary, we have demonstrated seasonal variation in photosynthetic activity in Scots pine in Scotland, and found evidence of genetic differentiation in photochemical capacity at low winter temperatures among eight pinewoods. Patterns of variation in Fv/Fm were found to differ from those in boreal populations, possibly due to the milder climate of Scotland. Winter temperatures affected populations differently: photochemical capacity in populations from high-altitude locations was least
Acknowledgements
The authors wish to thank Scottish Forestry Trust for funding (MJS’ PhD studentship), Dave Sim, Joan Beaton, and Ben Moore (Macaulay Institute) for making the seed collections, Lucy Sheppard for lending the Handy PEA device, Alysha Sime for assistance with height measurements, NERC, the Forestry Commission and EU-funded Network of Excellence EVOLTREE for support, UK Met Office for the climate data, and an anonymous reviewer for comments that improved the manuscript.
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