Linking leaf economic and hydraulic traits with early-age growth performance and survival of Eucalyptus pauciflora.

Selection on plant functional traits may occur through their direct effects on fitness (or a fitness component), or may be mediated by attributes of plant performance which have a direct impact on fitness. Understanding this link is particularly challenging for long-lived organisms, such as forest trees, where lifetime fitness assessments are rarely achievable, and performance features and fitness components are usually quantified from early-life history stages. Accordingly, we studied a cohort of trees from multiple populations of Eucalyptus pauciflora grown in a common-garden field trial established at the hot and dry end of the species distribution on the island of Tasmania, Australia. We related the within-population variation in leaf economic (leaf thickness, leaf area and leaf density) and hydraulic (stomatal density, stomatal length and vein density) traits, measured from two-year-old plants, to two-year growth performance (height and stem diameter) and to a fitness component (seven-year survival). When performance-trait relationships were modelled for all traits simultaneously, statistical support for direct effects on growth performance was only observed for leaf thickness and leaf density. Performance-based estimators of directional selection indicated that individuals with reduced leaf thickness and increased leaf density were favoured. Survival-performance relationships were consistent with size-dependent mortality, with fitness-based selection gradients estimated for performance measures providing evidence for directional selection favouring individuals with faster growth. There was no statistical support for an effect associated with the fitness-based quadratic selection gradient estimated for growth performance. Conditional on a performance measure, fitness-based directional selection gradients estimated for the leaf traits did not provide statistical support for direct effects of the focal traits on tree survival. This suggested that, under the environmental conditions of the trial site and time period covered in the current study, early-stage selection on the studied leaf traits may be mediated by their effects on growth performance, which in turn has a positive direct influence on later-age survival. We discuss the potential mechanistic basis of the direct effects of the focal leaf traits on tree growth, and the relevance of a putative causal pathway of trait effects on fitness through mediation by growth performance in the studied hot and dry environment.

Leaf Economic and Hydraulic Traits Signal Disparate Climate Adaptation Patterns in Two Co-Occurring Woodland Eucalypts.

With climate change impacting trees worldwide, enhancing adaptation capacity has become an important goal of provenance translocation strategies for forestry, ecological renovation, and biodiversity conservation. Given that not every species can be studied in detail, it is important to understand the extent to which climate adaptation patterns can be generalised across species, in terms of the selective agents and traits involved. We here compare patterns of genetic-based population (co)variation in leaf economic and hydraulic traits, climate-trait associations, and genomic differentiation of two widespread tree species (Eucalyptus pauciflora and E. ovata). We studied 2-year-old trees growing in a common-garden trial established with progeny from populations of both species, pair-sampled from 22 localities across their overlapping native distribution in Tasmania, Australia. Despite originating from the same climatic gradients, the species differed in their levels of population variance and trait covariance, patterns of population variation within each species were uncorrelated, and the species had different climate-trait associations. Further, the pattern of genomic differentiation among populations was uncorrelated between species, and population differentiation in leaf traits was mostly uncorrelated with genomic differentiation. We discuss hypotheses to explain this decoupling of patterns and propose that the choice of seed provenances for climate-based plantings needs to account for multiple dimensions of climate change unless species-specific information is available.

Population Divergence along a Genetic Line of Least Resistance in the Tree Species Eucalyptus globulus.

The evolutionary response to selection depends on the distribution of genetic variation in traits under selection within populations, as defined by the additive genetic variance-covariance matrix (G). The structure and evolutionary stability of G will thus influence the course of phenotypic evolution. However, there are few studies assessing the stability of G and its relationship with population divergence within foundation tree species. We compared the G-matrices of Mainland and Island population groups of the forest tree Eucalyptus globulus, and determined the extent to which population divergence aligned with within-population genetic (co)variation. Four key wood property traits exhibiting signals of divergent selection were studied-wood density, extractive content, and lignin content and composition. The comparison of G-matrices of the mainland and island populations indicated that the G-eigenstructure was relatively well preserved at an intra-specific level. Population divergence tended to occur along a major direction of genetic variation in G. The observed conservatism of G, the moderate evolutionary timescale, and close relationship between genetic architecture and population trajectories suggest that genetic constraints may have influenced the evolution and diversification of the E. globulus populations for the traits studied. However, alternative scenarios, including selection aligning genetic architecture and population divergence, are discussed.

Evidence that divergent selection shapes a developmental cline in a forest tree species complex.

Background and Aims: Evolutionary change in developmental trajectories (heterochrony) is a major mechanism of adaptation in plants and animals. However, there are few detailed studies of the variation in the timing of developmental events among wild populations. We here aimed to identify the climatic drivers and measure selection shaping a genetic-based developmental cline among populations of an endemic tree species complex on the island of Tasmania. Methods: Seed lots from 38 native provenances encompassing the clinal transition from the heteroblastic Eucalyptus tenuiramis to the homoblastic Eucalyptus risdonii were grown in a common-garden field trial in southern Tasmania for 20 years. We used 27 climatic variables to model the provenance variation in vegetative juvenility as assessed at age 5 years. A phenotypic selection analysis was used to measure the fitness consequences of variation in vegetative juvenility based on its impact on the survival and reproductive capacity of survivors at age 20 years. Key Results: Significant provenance divergence in vegetative juvenility was shown to be associated with home-site aridity, with the retention of juvenile foliage increasing with increasing aridity. Our results indicated that climate change may lead to different directions of selection across the geographic range of the complex, and in our mesic field site demonstrated that total directional selection within phenotypically variable provenances was in favour of reduced vegetative juvenility. Conclusions: We provide evidence that heteroblasty is adaptive and argue that, in assessing the impacts of rapid global change, developmental plasticity and heterochrony are underappreciated processes which can contribute to populations of long-lived organisms, such as trees, persisting and ultimately adapting to environmental change.

On the persistence of reproductive barriers in Eucalyptus: the bridging of mechanical barriers to zygote formation by F1 hybrids is counteracted by intrinsic post-zygotic incompatibilities.

BACKGROUND AND AIMS: Many previous studies conclude that pre-zygotic barriers such as mechanical isolation account for most reproductive isolation between pairs of taxa. However, the inheritance and persistence of barriers such as these after the first generation of hybridization is rarely quantified, even though it is a vital consideration in understanding gene flow potential. There is an asymmetrical pre-zygotic mechanical barrier to hybridization between Eucalyptus nitens and Eucalyptus globulus, which completely prevents small-flowered E. nitens pollen from mating with large E. globulus flowers, while the reverse cross is possible. We aimed to determine the relative importance of pre- and post-zygotic barriers in preventing gene flow following secondary contact between E. nitens and E. globulus, including the inheritance of barriers in advanced-generation hybrids. METHODS: Experimental crossing was used to produce outcrossed E. nitens, E. globulus and their F1, F2, BCg and BCn hybrids. The strength and inheritance of a suite of pre- and post-zygotic barriers were assessed, including 20-year survival, growth and reproductive capacity. KEY RESULTS: The mechanical barrier to hybridization was lost or greatly reduced in the F1 hybrid. In contrast, intrinsic post-zygotic barriers were strong and persistent. Line-cross analysis indicated that the outbreeding depression in the hybrids was best explained by epistatic loss. CONCLUSIONS: The removal of strong mechanical barriers between E. nitens and E. globulus allows F1 hybrids to act as a bridge for bi-directional gene flow between these species. However, strong and persistent post-zygotic barriers exist, meaning that wherever F1 hybridization does occur, intrinsic post-zygotic barriers will be responsible for most reproductive isolation in this system. This potential transient nature of mechanical barriers to zygote formation due to additive inheritance in hybrids appears under-appreciated, and highlights the often important role that intrinsic post-mating barriers play in maintaining species boundaries at zones of secondary contact.

Heterosis may result in selection favouring the products of long-distance pollen dispersal in Eucalyptus.

Using native trees from near the northern and southern extremities of the relatively continuous eastern distribution of Eucalyptus globulus in Tasmania, we compared the progenies derived from natural open-pollination (OP) with those generated from within-region and long-distance outcrossing. Controlled outcrossing amongst eight parents - with four parents from each of the northern and southern regions - was undertaken using a diallel mating scheme. The progeny were planted in two field trials located within the species native range in southern Tasmania, and their survival and diameter growth were monitored over a 13-year-period. The survival and growth performances of all controlled cross types exceeded those of the OP progenies, consistent with inbreeding depression due to a combination of selfing and bi-parental inbreeding. The poorer survival of the northern regional (♀N♂N) outcrosses compared with the local southern regional outcrosses (♀S♂S) indicated differential selection against the former. Despite this mal-adaptation of the non-local ♀N♂N crosses at both southern sites, the survival of the inter-regional hybrids (♀N♂S and ♀S♂N) was never significantly different from that of the local ♀S♂S crosses. Significant site-dependent heterosis was detected for the growth of the surviving long-distance hybrids. This was expressed as mid-parent heterosis, particularly at the more northern planting site. Heterosis increased with age, while the difference between the regional ♀N♂N and ♀S♂S crosses remained insignificant at any age at either site. Nevertheless, the results for growth suggest that the fitness of individuals derived from long-distance crossing may be better at the more northern of the planting sites. Our results demonstrate the potential for early-age assessments of pollen dispersal to underestimate realised gene flow, with local inbreeding under natural open-pollination resulting in selection favouring the products of longer-distance pollinations. Indeed, heterosis derived from long-distance pollinations may be sufficient to counter local mal-adaptation, at least in the first generation.

Additive and non-additive genetic parameters from clonally replicated and seedling progenies of Eucalyptus globulus.

The first estimates of the importance of epistatic effects within Eucalyptus globulus were obtained from analysis of clonally replicated full-sib progeny tests grown in Portugal. Parents comprised diverse selections from the Portuguese landrace. Variance components were estimated for 4-year-old diameter growth and pilodyn penetration, an indirect measure of wood density, both key traits in the pulpwood breeding objective. The experimental components of variance were used to estimate heritabilities and proportions of the phenotypic variance due to dominance and epistasis. The additive variance was the only significant genetic component affecting either diameter or pilodyn. Estimates of the additive, dominance and epistatic effects accounted for 8-10%, 0-4% and 0.4% of the phenotypic variance in diameter, and for 11-17%, 0% and 5% of the phenotypic variance in pilodyn, respectively. A comparison of residual coefficients of variation within seedling and cloned progenies indicated that C effects within clones were not a serious source of random variability. Despite the test sites encompassing a diverse range of locations, no important genotype by environment interaction was detected. The results suggested that an improvement strategy combining both recurrent selection for additive genetic merit and clonal testing may be adequate for optimizing genetic gains from this genetic base.