Adaptational Lag Research Articles

Translocation of an arctic seashore plant reveals signs of maladaptation to altered climatic conditions.

Ongoing anthropogenic climate change alters the local climatic conditions to which species may be adapted. Information on species’ climatic requirements and their intraspecific variation is necessary for predicting the effects of climate change on biodiversity. We used a climatic gradient to test whether populations of two allopatric varieties of an arctic seashore herb (Primula nutans ssp. finmarchica) show adaptation to their local climates and how a future warmer climate may affect them. Our experimental set-up combined a reciprocal translocation within the distribution range of the species with an experiment testing the performance of the sampled populations in warmer climatic conditions south of their range. We monitored survival, size, and flowering over four growing seasons as measures of performance and, thus, proxies of fitness. We found that both varieties performed better in experimental gardens towards the north. Interestingly, highest up in the north, the southern variety outperformed the northern one. Supported by weather data, this suggests that the climatic optima of both varieties have moved at least partly outside their current range. Further warming would make the current environments of both varieties even less suitable. We conclude that Primula nutans ssp. finmarchica is already suffering from adaptational lag due to climate change, and that further warming may increase this maladaptation, especially for the northern variety. The study also highlights that it is not sufficient to run only reciprocal translocation experiments. Climate change is already shifting the optimum conditions for many species and adaptation needs also to be tested outside the current range of the focal taxon in order to include both historic conditions and future conditions.

Adaptational lag to temperature in valley oak (Quercus lobata) can be mitigated by genome-informed assisted gene flow

Climate change over the next century is predicted to cause widespread maladaptation in natural systems. This prediction, as well as many sustainable management and conservation practices, assumes that species are adapted to their current climate. However, this assumption is rarely tested. Using a large-scale common garden experiment combined with genome-wide sequencing, we found that valley oak (Quercus lobata), a foundational tree species in California ecosystems, showed a signature of adaptational lag to temperature, with fastest growth rates occurring at cooler temperatures than populations are currently experiencing. Future warming under realistic emissions scenarios was predicted to lead to further maladaptation to temperature and reduction in growth rates for valley oak. We then identified genotypes predicted to grow relatively fast under warmer temperatures and demonstrated that selecting seed sources based on their genotype has the potential to mitigate predicted negative consequences of future climate warming on growth rates in valley oak. These results illustrate that the belief of local adaptation underlying many management and conservation practices, such as using local seed sources for restoration, may not hold for some species. If contemporary adaptational lag is commonplace, we will need new approaches to help alleviate predicted negative consequences of climate warming on natural systems. We present one such approach, "genome-informed assisted gene flow," which optimally matches individuals to future climates based on genotype-phenotype-environment associations.

Local Adaptation and Response of Platycladus orientalis (L.) Franco Populations to Climate Change

Knowledge about the local adaptation and response of forest tree populations to the climate is important for assessing the impact of climate change and developing adaptive genetic resource management strategies. However, such information is not available for most plant species. Here, based on 69 provenances tested at 19 common garden experimental sites, we developed a universal response function (URF) for tree height at seven years of age for the important and wide-spread native Chinese tree species Platycladus orientalis (L.) Franco. URF was recently used to predict the potential growth response of a population originating from any climate and growing in any climate conditions. The developed model integrated both genetic and environmental effects, and explained 55% of the total variation in tree height observed among provenances and test sites in China. We found that local provenances performed better than non-local counterparts in habitats located in central, eastern, and southwestern China, showing the evidence of local adaptation as compared to other regions. In contrast, non-local provenances outperformed local ones in peripheral areas in northern and northwestern China, suggesting an adaptational lag in these areas. Future projections suggest that the suitable habitat areas of P. orientalis would expand by 15%–39% and shift northward by 0.8–3 degrees in latitude; however, the projected tree height of this species would decline by 4%–8% if local provenances were used. If optimal provenances were used, tree height growth could be improved by 13%–15%, along with 59%–71% suitable habitat expansion. Thus, assisted migration with properly selected seed sources would be effective in avoiding maladaptation in new plantations under a changing climate for P. orientalis.

Effect of growth temperature on photosynthetic capacity and respiration in three ecotypes of Eriophorum vaginatum.

Ecotypic differentiation in the tussock‐forming sedge Eriophorum vaginatum has led to the development of populations that are locally adapted to climate in Alaska's moist tussock tundra. As a foundation species, E. vaginatum plays a central role in providing topographic and microclimatic variation essential to these ecosystems, but a changing climate could diminish the importance of this species. As Arctic temperatures have increased, there is evidence of adaptational lag in E. vaginatum, as locally adapted ecotypes now exhibit reduced population growth rates. Whether there is a physiological underpinning to adaptational lag is unknown. Accordingly, this possibility was investigated in reciprocal transplant gardens. Tussocks of E. vaginatum from sites separated by ~1° latitude (Coldfoot: 67°15′N, Toolik Lake: 68°37′, Sagwon: 69°25′) were transplanted into the Toolik Lake and Sagwon sites and exposed to either an ambient or an experimental warming treatment. Five tussocks pertreatment combination were measured at each garden to determine photosynthetic capacity (i.e., V cmax and J max) and dark respiration rate (R d) at measurement temperatures of 15, 20, and 25°C. Photosynthetic enhancements or homeostasis were observed for all ecotypes at both gardens under increased growth temperature, indicating no negative effect of elevated temperature on photosynthetic capacity. Further, no evidence of thermal acclimation in R d was observed for any ecotype, and there was little evidence of ecotypic variation in R d. As such, no physiological contribution to adaptational lag was observed given the increase in growth temperature (up to ~2°C) provided by this study. Despite neutral to positive effects of increased growth temperature on photosynthesis in E. vaginatum, it appears to confer no lasting advantage to the species.

Northward displacement of optimal climate conditions for ecotypes of Eriophorum vaginatum L. across a latitudinal gradient in Alaska.

Plants are often genetically specialized as ecotypes attuned to local environmental conditions. When conditions change, the optimal environment may be physically displaced from the local population, unless dispersal or insitu evolution keep pace, resulting in a phenomenon called adaptational lag. Using a 30-year-old reciprocal transplant study across a 475km latitudinal gradient, we tested the adaptational lag hypothesis by measuring both short-term (tiller population growth rates) and long-term (17-year survival) fitness components of Eriophorum vaginatum ecotypes in Alaska, where climate change may have already displaced the optimum. Analyzing the transplant study as a climate transfer experiment, we showed that the climate optimum for plant performance was displaced ca. 140km north of home sites, although plants were not generally declining in size at home sites. Adaptational lag is expected to be widespread globally for long-lived, ecotypically specialized plants, with disruptive consequences for communities and ecosystems.

Tiller population dynamics of reciprocally transplanted Eriophorum vaginatum L. ecotypes in a changing climate

AbstractMoist tussock tundra, dominated by the sedge Eriophorum vaginatum L., covers approximately 3.36 × 108 km2 of arctic surface area along with large amounts of subarctic land area. Eriophorum vaginatum exhibits ecotypic differentiation along latitudinal gradients in Alaska. While ecotypic differentiation may be beneficial during periods of climate stability, it may be detrimental as climate changes, causing adaptational lag. Following harvest of a 30‐year reciprocal transplant experiment, age‐specific demographic data on E. vaginatum tillers were collected to parameterize a Leslie matrix. Yellow Taxi analysis, based on Tukey's Jackknife, was used to determine mean pseudovalues of tiller population growth rate () for four source populations of E. vaginatum tussocks that were transplanted to each of three gardens along a latitudinal gradient. Source populations responded differentially along the latitudinal gradient. Survival and daughter tiller production influenced differences seen at the mid‐latitude garden, and the overall tiller population performance was generally improved by northward transplanting relative to southward transplanting. A comparison of home‐source and away‐source within the same transplant garden indicates no home‐site advantage. Although populations were still growing when transplanted to home‐sites ( = 1.056), tiller population growth rate increased as ΔGDD became more negative relative to the home site (i.e., as tussocks were transplanted north). These results imply that populations are affected by climate gradients in a manner consistent with adaptational lag. This study documenting the response of high‐latitude ecotypes to climate gradients may be an indication of the possible future effects of climate shift in more southern latitudes.

Disturbances as Hot Spots of Ecotypic Variation: A Case Study with Dryas octopetala

Ecotypic specialization among populations within plant species can result in adaptational lag when the climate changes directionally. However, disturbances, whether caused by direct effects of human activities or indirect effects such as climate change, may represent zones within which natural selection is relaxed. We compared the genetically based variation in leaf morphology in Dryas octopetala within three natural populations arrayed along a snowbank gradient, to that found in a recently colonized gravel pad less than 100 m away (1600 total leaf lengths measured; 4 sites × 10 transects/site × 4 plants/transect × 10 leaves/plant). Elevated among-clone leaf length variation within the disturbed site supported the idea that disturbances may represent “hotspots” of evolutionarily significant genetic variation. In the Arctic, where colonization of disturbances is primarily by native species, adaptive evolution may be more rapid than previously thought due to relaxation of selection and subsequent mixing of previously isolated gene pools in such areas.

Lagging adaptation to warming climate in Arabidopsis thaliana.

If climate change outpaces the rate of adaptive evolution within a site, populations previously well adapted to local conditions may decline or disappear, and banked seeds from those populations will be unsuitable for restoring them. However, if such adaptational lag has occurred, immigrants from historically warmer climates will outperform natives and may provide genetic potential for evolutionary rescue. We tested for lagging adaptation to warming climate using banked seeds of the annual weed Arabidopsis thaliana in common garden experiments in four sites across the species' native European range: Valencia, Spain; Norwich, United Kingdom; Halle, Germany; and Oulu, Finland. Genotypes originating from geographic regions near the planting site had high relative fitness in each site, direct evidence for broad-scale geographic adaptation in this model species. However, genotypes originating in sites historically warmer than the planting site had higher average relative fitness than local genotypes in every site, especially at the northern range limit in Finland. This result suggests that local adaptive optima have shifted rapidly with recent warming across the species' native range. Climatic optima also differed among seasonal germination cohorts within the Norwich site, suggesting that populations occurring where summer germination is common may have greater evolutionary potential to persist under future warming. If adaptational lag has occurred over just a few decades in banked seeds of an annual species, it may be an important consideration for managing longer-lived species, as well as for attempts to conserve threatened populations through ex situ preservation.

Assisted migration to address climate change: recommendations for aspen reforestation in western Canada

Human-aided movement of species populations in large-scale reforestation programs could be a potent and cost-effective climate change adaptation strategy. Such large-scale management interventions, however, tend to entail the risks of unintended consequences, and we propose that three conditions should be met before implementing assisted migration in reforestation programs: (1) evidence of a climate-related adaptational lag, (2) observed biological impacts, and (3) robust model projections to target assisted migration efforts. In a case study of aspen (Populus tremuloides Michaux.) we use reciprocal transplant experiments to study adaptation of tree populations to local environments. Second, we monitor natural aspen populations using the MODIS enhanced vegetation index as a proxy for forest health and productivity. Last, we report results from bioclimate envelope models that predict suitable habitat for locally adapted genotypes under observed and predicted climate change. The combined results support assisted migration prescriptions and indicate that the risk of inaction likely exceeds the risk associated with changing established management practices. However, uncertainty in model projections also implies that we are restricted to a relatively short 20-year planning horizon for prescribing seed movement in reforestation programs. We believe that this study exemplifies a safe and realistic climate change adaptation strategy based on multiple sources of information and some understanding of the uncertainty associated with recommendations for assisted migration. Ad hoc migration prescriptions without a similar level of supporting information should be avoided in reforestation programs.

Adaptation, migration or extirpation: climate change outcomes for tree populations.

Species distribution models predict a wholesale redistribution of trees in the next century, yet migratory responses necessary to spatially track climates far exceed maximum post-glacial rates. The extent to which populations will adapt will depend upon phenotypic variation, strength of selection, fecundity, interspecific competition, and biotic interactions. Populations of temperate and boreal trees show moderate to strong clines in phenology and growth along temperature gradients, indicating substantial local adaptation. Traits involved in local adaptation appear to be the product of small effects of many genes, and the resulting genotypic redundancy combined with high fecundity may facilitate rapid local adaptation despite high gene flow. Gene flow with preadapted alleles from warmer climates may promote adaptation and migration at the leading edge, while populations at the rear will likely face extirpation. Widespread species with large populations and high fecundity are likely to persist and adapt, but will likely suffer adaptational lag for a few generations. As all tree species will be suffering lags, interspecific competition may weaken, facilitating persistence under suboptimal conditions. Species with small populations, fragmented ranges, low fecundity, or suffering declines due to introduced insects or diseases should be candidates for facilitated migration.

Altitudinal genetic variation among Pinus oocarpa populations in Michoacán, Mexico : Implications for seed zoning, conservation, tree breeding and global warming

Pinus oocarpa has a large natural distribution in the sub-tropical forests of Mexico. Populations, however, are rapidly disappearing particularly in the Michoacán State as native forests are converted to avocado ( Persea sp.) orchards. We investigated the patterning of genetic variation among P. oocarpa populations for quantitative traits along an altitudinal gradient by establishing a provenance/progeny test from wind-pollinated seeds collected along an altitudinal transect (1100–1500 m) near Uruapan, Michoacán, Mexico. Genetic variation was analyzed in relation to normalized climate records (temperature, precipitation, degree days >5 °C and annual moisture index) for the provenances and the test site for the contemporary climate and for climates projected for the decades beginning in 2030, 2060, and 2090. Estimates of future climates used output from the Canadian and Hadley General Circulation Models. Results of a field test suggested an altitudinal pattern of genetic differentiation in juvenile height among P. oocarpa populations. Seedlings from populations originating from lower altitudes tended to grow more than seedlings originating from populations at the higher altitudes. However, this trend abates at the lowest altitudinal limit of the species distribution, a probable conservative growth strategy for avoiding drought stress. Thus, the cline appeared to arise from selection along a climatic gradient reflecting in a moisture index (ratio of degree days to precipitation) and is dependent, therefore, on a balance between temperature and moisture. For guiding seed and seedling transfer in ecological restoration, conservation of genetic resources, tree breeding and mitigating the effects of global warming, we suggest guidelines based on delimitation of three altitudinal seed zones of about 200 m in breadth. Alternatively, one can limit transfer to three climatic zones of about 0.75 units of annual moisture index. Predictions of future climates indicate an average annual temperature increase of 3.8 °C by year 2090, and, judging from an increase of an annual moisture index of 26%, an increase in aridity by the end of the century. However, the more difficult period for adaptation of P. oocarpa populations to the new climate should be between 2030 and 2060, when the increase in aridity is expected to be most pronounced. Changes of this magnitude should alter the natural distribution of the species and would create an adaptational lag, as the adaptedness of extant populations deteriorates. Mitigating these effects will require seeds to be transferred upwards in altitude, perhaps as much as 150 m initially.

Bone's mechanostat: a 2003 update.

The still-evolving mechanostat hypothesis for bones inserts tissue-level realities into the former knowledge gap between bone's organ-level and cell-level realities. It concerns load-bearing bones in postnatal free-living bony vertebrates, physiologic bone loading, and how bones adapt their strength to the mechanical loads on them. Voluntary mechanical usage determines most of the postnatal strength of healthy bones in ways that minimize nontraumatic fractures and create a bone-strength safety factor. The mechanostat hypothesis predicts 32 things that occur, including the gross anatomical bone abnormalities in osteogenesis imperfecta; it distinguishes postnatal situations from baseline conditions at birth; it distinguishes bones that carry typical voluntary loads from bones that have other chief functions; and it distinguishes traumatic from nontraumatic fractures. It provides functional definitions of mechanical bone competence, bone quality, osteopenias, and osteoporoses. It includes permissive hormonal and other effects on bones, a marrow mediator mechanism, some limitations of clinical densitometry, a cause of bone "mass" plateaus during treatment, an "adaptational lag" in some children, and some vibration effects on bones. The mechanostat hypothesis may have analogs in nonosseous skeletal organs as well.

The Adaptational System as a Dynamical Feedback System

The characteristics of biological systems of adaptation are developed from the principle that the manifestations of life are modified by and must conform with their environment in order to enable organismic persistence. The two roles of the environment, termed “modifying” and “adaptive”, give rise to the distinction of three elementary and sequentially coupled subsystems characterizing the adaptational system: the modifying system, comparator system, and state regulation system. The third system determines which state alterations are required for adaptation of manifestations (responses) to the demands of the adaptive environment. Adaptational valuation is introduced as a measure of adaptedness of response to adaptive environment. The dynamical aspect of adaptation is shown to be completely described by the timing of feedback. Discrete and continuous forms of adaptation can thus be treated on the same conceptional basis. All steps of the generic system formulation are illustrated with the help of a simple model with additive effects and linear state regulation. The system representation is used to demonstrate how basic intuitive conceptions, such as adaptational lag or adaptational capacity, can be made amenable to precise analysis. Another demonstration concerns recognition of adaptational clues resulting from the distinction between the two environmental classes, modifying and adaptive. Among these clues are challenges of low correlation between the two classes to adaptational systems and the specification of questions of the evolution of phenotypic plasticity.