A plastic response towards enhanced reproduction is expected in stressful environments, but it is assumed to trade off against vegetative growth and efficiency in the use of available resources deployed in reproduction [reproductive efficiency (RE)]. Evidence supporting this expectation is scarce for plants, particularly for long-lived species. Forest trees such as Mediterranean pines provide ideal models to study the adaptive value of allocation to reproduction vs. vegetative growth given their among-population differentiation for adaptive traits and their remarkable capacity to cope with dry and low-fertility environments. We studied 52 range-wide Pinus halepensis populations planted into two environmentally contrasting sites during their initial reproductive stage. We investigated the effect of site, population and their interaction on vegetative growth, threshold size for female reproduction, reproductive-vegetative size relationships and RE. We quantified correlations among traits and environmental variables to identify allocation trade-offs and ecotypic trends. Genetic variation for plasticity was high for vegetative growth, whereas it was nonsignificant for reproduction. Sizecorrected reproduction was enhanced in the more stressful site supporting the expectation for adverse conditions to elicit plastic responses in reproductive allometry. However, RE was unrelated with early reproductive investment. Our results followed theoretical predictions and support that phenotypic plasticity for reproduction is adaptive under stressful environments. Considering expectations of increased drought in the Mediterranean, we hypothesize that phenotypic plasticity together with natural selection on reproductive traits will play a relevant role in the future adaptation of forest tree species.
The study represents the first report of genetic variability among populations for differences in the threshold size for first reproduction between male and female sexual functions in a tree species. The relatively uniform size at which individuals begin reproducing through their male function probably represents the fact that pollen dispersal is also relatively invariant among sites. However, the genetic variability in the timing of female reproduction probably reflects environment-dependent costs of cone production. The results also suggest that early sex allocation in this species might evolve under constraints that do not apply to other conifers.
Serotiny is a heritable trait in P. halepensis, and selection acts on it, giving rise to contrasting serotiny levels among populations depending on the fire regime, and supporting the role of fire in generating genetic divergence for adaptive traits.
Preserving intraspecific genetic diversity is essential for long-term forest sustainability in a climate change scenario. Despite that, genetic information is largely neglected in conservation planning, and how conservation units should be defined is still heatedly debated. Here, we use maritime pine (Pinus pinaster Ait.), an outcrossing long-lived tree with a highly fragmented distribution in the Mediterranean biodiversity hotspot, to prove the importance of accounting for genetic variation, of both neutral molecular markers and quantitative traits, to define useful conservation units. Six gene pools associated to distinct evolutionary histories were identified within the species using 12 microsatellites and 266 single nucleotide polymorphisms (SNPs). In addition, height and survival standing variation, their genetic control, and plasticity were assessed in a multisite clonal common garden experiment (16 544 trees). We found high levels of quantitative genetic differentiation within previously defined neutral gene pools. Subsequent cluster analysis and post hoc trait distribution comparisons allowed us to define 10 genetically homogeneous population groups with high evolutionary potential. They constitute the minimum number of units to be represented in a maritime pine dynamic conservation program. Our results uphold that the identification of conservation units below the species level should account for key neutral and adaptive components of genetic diversity, especially in species with strong population structure and complex evolutionary histories. The environmental zonation approach currently used by the pan-European genetic conservation strategy for forest trees would be largely improved by gradually integrating molecular and quantitative trait information, as data become available.
1. Mediterranean ecosystems are biodiversity hotspots located between temperate mesic climates and semi-deserts and deserts. Mediterranean climates are characterized by a drought season but its length and severity can be highly variable across regions. In this review, we explored population genetic variation in functional traits and fitness in Mediterranean oak and pine species. We tested the hypothesis that increased drought tolerance has evolved as an adaptation to xeric and warm areas of the Mediterranean climate while increased competitive abilities have been favoured in more mesic regions, following a productivity-persistence trade-off within species.2. We first reviewed the literature and performed a meta-analysis of studies on Pinus sp. and Quercus sp. from Mediterranean climates, and then analysed a set of unpublished data from Spanish common garden experiments of species from the Mediterranean Basin, searching for evidence of trait genetic variation among populations, local adaptation and trait-environment associations.3. The meta-analysis showed that 82.9% (95% CI 75.7-89.4) of traits per study showed significant population genetic differentiation and that 52. 5% (35.6-69.2) of traits in studies with two or more Mediterranean environments exhibited population-by-environment interaction. Population differences in traits related to drought tolerance, cold hardiness and fitness were usually correlated with provenance precipitation and temperature gradients, suggesting that adaptation to different climatic regimes is an important process driving intraspecific genetic divergence. Within the Spanish trial network, however, predicted fitness functions based on climatic transfer distance failed to reveal significantly higher fitness of populations at experimental sites with climates closer to their provenances' ones.Neither the literature review nor the new analyses of the Spanish trial network provided evidence of a negative association between growth-and persistencerelated traits at the intraspecific level. 4. Synthesis. Population genetic differentiation in functional traits and fitness is common in Mediterranean species, driven, at least in part, by the adaptation to contrasting temperature and precipitation regimes. Because of experimental constraints or biological reality, our study failed to detect a trade-off between | 1023
Growth-limiting environments exacerbated the precocious release of seeds, contrary to the ecotypic trend found for the aerial cone bank, suggesting a counter-gradient plasticity. This plastic response is potentially maladaptive under a scenario of frequent wildfires.
Heterozygosity-fitness correlations (HFCs) have been used to understand the complex interactions between inbreeding, genetic diversity and evolution. Although frequently reported for decades, evidence for HFCs was often based on underpowered studies or inappropriate methods, and hence their underlying mechanisms are still under debate. Here, we used 6100 genome-wide single nucleotide polymorphisms (SNPs) to test for general and local effect HFCs in maritime pine (Pinus pinaster Ait.), an iconic Mediterranean forest tree. Survival was used as a fitness proxy, and HFCs were assessed at a four-site common garden under contrasting environmental conditions (total of 16 288 trees). We found no significant correlations between genome-wide heterozygosity and fitness at any location, despite variation in inbreeding explaining a substantial proportion of the total variance for survival. However, four SNPs (including two non-synonymous mutations) were involved in significant associations with survival, in particular in the common gardens with higher environmental stress, as shown by a novel heterozygosity-fitness association test at the species-wide level. Fitness effects of SNPs involved in significant HFCs were stable across maritime pine gene pools naturally growing in distinct environments. These results led us to dismiss the general effect hypothesis and suggested a significant role of heterozygosity in specific candidate genes for increasing fitness in maritime pine. Our study highlights the importance of considering the species evolutionary and demographic history and different spatial scales and testing environments when assessing and interpreting HFCs.
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