Timing of photoperiodic competency causes phenological mismatch in balsam poplar (Populus balsamifera L.).

Plant phenology is expected to be sensitive to climate warming. In boreal trees, spring flush is primarily temperature driven, whereas height growth cessation and autumn leaf senescence are predominantly controlled by photoperiod. Cuttings of 525 genotypes from the full range of balsam poplar were planted into two common gardens (Vancouver and Indian Head, Canada) at similar latitudes, but with differing winter temperatures and growing seasons. There was clinal variation in spring and, particularly, summer and fall phenology. Bud flush and, despite milder climate, bud set and leaf drop were earlier at Vancouver than at Indian Head by 44, 28 and 7 d, respectively. Although newly flushed growth is insensitive to photoperiod, many genotypes at both sites became competent before the summer solstice. At Vancouver, high-latitude genotypes set dormant terminal buds in mid-spring. Most other genotypes grew until midsummer or set bud temporarily and then experienced a second flush. In both gardens and in a growth chamber experiment, earlier bud set was associated with reduced height growth and higher root/shoot ratios. Shoots attained competency ~5 weeks after flushing, which would normally prevent dormancy induction before the solstice, but may be insufficient if spring advances by more than a few weeks.

Comparative nucleotide diversity across North American and European populus species.

Nucleotide polymorphisms in two North American balsam poplars (Populus trichocarpa Torr. & Gray and P. balsamifera L.; section Tacamahaca), and one Eurasian aspen (P. tremula L.; section Populus) were compared using nine loci involved in defense, stress response, photoperiodism, freezing tolerance, and housekeeping. Nucleotide diversity varied among species and was highest for P. tremula (θ(w) = 0.005, π(T) = 0.007) as compared to P. balsamifera (θ(w) = 0.004, π(T) = 0.005) or P. trichocarpa (θ(w) = 0.002, π(T) = 0.003). Across species, the defense and the stress response loci accounted for the majority of the observed level of nucleotide diversity. In general, the studied loci did not deviate from neutral expectation either at the individual locus (non-significant normalized Fay and Wu's H) or at the multi-locus level (non-significant HKA test). Using molecular clock analysis, section Tacamahaca probably shared a common ancestor with section Populus approximately 4.5 million year ago. Divergence between the two closely related balsam poplars was about 0.8 million years ago, a pattern consistent with an isolation-with-migration (IM) model. As expected, P. tremula showed a five-fold higher substitution rate (2 × 10(-8) substitution/site/year) compared to the North American species (0.4 × 10(-8) substitution/site/year), probably reflecting its complex demographic history. Linkage disequilibrium (LD) varied among species with a more rapid decay in the North American species (<400 bp) in comparison to P. tremula (≫400 bp). The similarities in nucleotide diversity pattern and LD decay of the two balsam poplar species likely reflects the recent time of their divergence.

Climate-driven local adaptation of ecophysiology and phenology in balsam poplar, Populus balsamifera L. (Salicaceae).

PREMISE OF THE STUDY: During past episodes of climate change, many plant species experienced large-scale range expansions. Expanding populations likely encountered strong selection as they colonized new environments. In this study we examine the extent to which populations of the widespread forest tree Populus balsamifera L. have become locally adapted as the species expanded into its current range since the last glaciation. METHODS: We tested for adaptive variation in 13 ecophysiology and phenology traits on clonally propagated genotypes originating from a range-wide sample of 20 subpopulations. The hypothesis of local adaption was tested by comparing among-population variation at ecologically important traits (Q(ST)) to expected variation based on demographic history (F(ST)) estimated from a large set of nuclear single nucleotide polymorphism loci. KEY RESULTS: Evidence for divergence in excess of neutral expectations was present for eight of 13 traits. Bud phenology, petiole length, and leaf nitrogen showed the greatest divergence (all Q(ST) > 0.6), whereas traits related to leaf water usage showed the least (all Q(ST) ≤ 0.30) and were not different from neutrality. Strong correlations were present between traits, geography, and climate, and they revealed a general pattern of northern subpopulations adapted to shorter, drier growing seasons compared with populations in the center or eastern regions of the range. CONCLUSIONS: Our study demonstrates pronounced adaptive variation in ecophysiology and phenology among balsam poplar populations. These results suggest that as this widespread forest tree species expanded its range since the end of the last glacial maximum, it evolved rapidly in response to geographically variable selection.

Temperature responses of photosynthesis and respiration in Populus balsamifera L.: acclimation versus adaptation.

To examine the role of acclimation versus adaptation on the temperature responses of CO(2) assimilation, we measured dark respiration (R(n)) and the CO(2) response of net photosynthesis (A) in Populus balsamifera collected from warm and cool habitats and grown at warm and cool temperatures. R(n) and the rate of photosynthetic electron transport (J) are significantly higher in plants grown at 19 versus 27 degrees C; R(n) is not affected by the native thermal habitat. By contrast, both the maximum capacity of rubisco (V(cmax)) and A are relatively insensitive to growth temperature, but both parameters are slightly higher in plants from cool habitats. A is limited by rubisco capacity from 17-37 degrees C regardless of growth temperature, and there is little evidence for an electron-transport limitation. Stomatal conductance (g(s)) is higher in warm-grown plants, but declines with increasing measurement temperature from 17 to 37 degrees C, regardless of growth temperature. The mesophyll conductance (g(m)) is relatively temperature insensitive below 25 degrees C, but g(m) declines at 37 degrees C in cool-grown plants. Plants acclimated to cool temperatures have increased R(n)/A, but this response does not differ between warm- and cool-adapted populations. Primary carbon metabolism clearly acclimates to growth temperature in P. balsamifera, but the ecotypic differences in A suggest that global warming scenarios might affect populations at the northern and southern edges of the boreal forest in different ways.

Enhanced assimilation rate and water use efficiency with latitude through increased photosynthetic capacity and internal conductance in balsam poplar (Populus balsamifera L.).

In outdoor common gardens, high latitude populations of deciduous tree species often display higher assimilation rates (A) than low latitude populations, but they accomplish less height. To test whether trends in A reflect adaptation to growing season length or, alternatively, are garden growth artefacts, we examined variation in height increment and ecophysiological traits in a range-wide collection of Populus balsamifera L. populations from 21 provenances, during unconstrained growth in a greenhouse. Rooted cuttings, maintained without resource limitation under 21 h photoperiod for 90 d, displayed increasing height growth, A, leaf mass per area and leaf N per area with latitude whereas stomatal conductance (g(s)) showed no pattern. Water-use efficiency as indicated by both gas exchange and delta(13)C increased with latitude, whereas photosynthetic nitrogen-use efficiency decreased. Differences in delta(13)C were less than expected based on A/g(s), suggesting coextensive variation in internal conductance (g(m)). Analysis of A-C(i) curves on a subset of populations showed that high latitude genotypes had greater g(m) than low-latitude genotypes. We conclude that higher peak rates of height growth in high latitude genotypes of balsam poplar are supported by higher A, achieved partly through higher g(m), to help compensate for a shorter growing season.

Comparative physiology of allopatric Populus species: geographic clines in photosynthesis, height growth, and carbon isotope discrimination in common gardens.

Populus species with wide geographic ranges display strong adaptation to local environments. We studied the clinal patterns in phenology and ecophysiology in allopatric Populus species adapted to similar environments on different continents under common garden settings. As a result of climatic adaptation, both Populus tremula L. and Populus balsamifera L. display latitudinal clines in photosynthetic rates (A), whereby high-latitude trees of P. tremula had higher A compared to low-latitude trees and nearly so in P. balsamifera (p = 0.06). Stomatal conductance (g s) and chlorophyll content index (CCI) follow similar latitudinal trends. However, foliar nitrogen was positively correlated with latitude in P. balsamifera and negatively correlated in P. tremula. No significant trends in carbon isotope composition of the leaf tissue (δ(13)C) were observed for both species; but, intrinsic water-use efficiency (WUEi) was negatively correlated with the latitude of origin in P. balsamifera. In spite of intrinsically higher A, high-latitude trees in both common gardens accomplished less height gain as a result of early bud set. Thus, shoot biomass was determined by height elongation duration (HED), which was well approximated by the number of days available for free growth between bud flush and bud set. We highlight the shortcoming of unreplicated outdoor common gardens for tree improvement and the crucial role of photoperiod in limiting height growth, further complicating interpretation of other secondary effects.