Dorothy A. Steane

In plants where seed dispersal is limited compared with pollen dispersal, hybridisation may enhance gene exchange and species dispersal. We provide genetic evidence of hybridisation contributing to the expansion of the rare Eucalyptus risdonii into the range of the widespread Eucalyptus amygdalina. These closely related tree species are morphologically distinct, and observations suggest that natural hybrids occur along their distribution boundaries and as isolated trees or in small patches within the range of E. amygdalina. Hybrid phenotypes occur outside the range of normal dispersal for E. risdonii seed, yet in some hybrid patches small individuals resembling E. risdonii occur and are hypothesised to be a result of backcrossing. Using 3362 genome‐wide SNPs assessed from 97 individuals of E. risdonii and E. amygdalina and 171 hybrid trees, we show that (i) isolated hybrids match the genotypes expected of F₁/F₂ hybrids, (ii) there is a continuum in the genetic composition among the isolated hybrid patches from patches dominated by F₁/F₂‐like genotypes to those dominated by E. risdonii‐backcross genotypes, and (iii) the E. risdonii‐like phenotypes in the isolated hybrid patches are most‐closely related to proximal larger hybrids. These results suggest that the E. risdonii phenotype has been resurrected in isolated hybrid patches established from pollen dispersal, providing the first steps in its invasion of suitable habitat by long‐distance pollen dispersal and complete introgressive displacement of E. amygdalina. Such expansion accords with the population demographics, common garden performance data, and climate modelling which favours E. risdonii and highlights a role of interspecific hybridisation in climate change adaptation and species expansion.

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.

Understanding the capacity of forest tree species to adapt to climate change is of increasing importance for managing forest genetic resources. Through a genomics approach, we modelled spatial variation in climate adaptation within the Australian temperate forest tree Eucalyptus globulus, identified putative climate drivers of this genomic variation, and predicted locations of future climate refugia and populations at-risk of future maladaptation. Using 812,158 SNPs across 130 individuals from 30 populations (i.e., localities) spanning the species’ natural range, a gradientForest algorithm found 1177 SNPs associated with locality variation in home-site climate (climate-SNPs), putatively linking them to climate adaptation. Very few climate-SNPs were associated with population-level variation in drought susceptibility, signalling the multi-faceted nature and complexity of climate adaptation. Redundancy analysis (RDA) showed 24% of the climate-SNP variation could be explained by annual precipitation, isothermality, and maximum temperature of the warmest month. Spatial predictions of the RDA climate vectors associated with climate-SNPs allowed mapping of genomically informed climate selective surfaces across the species’ range under contemporary and projected future climates. These surfaces suggest over 50% of the current distribution of E. globulus will be outside the modelled adaptive range by 2070 and at risk of climate maladaptation. Such surfaces present a new integrated approach for natural resource managers to capture adaptive genetic variation and plan translocations in the face of climate change.

Eucalyptus globulus is native to southeastern Australia, including the island of Tasmania, but is one of the most widely grown hardwood forestry species in the world and is naturalized on several continents. We studied its naturalization in California, where the species has been planted for over 150 years. We sampled 70 E. globulus trees from 53 locations spanning the entire range of the species in California to quantify the genetic variation present and test whether particular genotypes or native origin affect variation in naturalization among locations. Diversity and native affinities were determined based on six nuclear microsatellite markers and sequences from a highly variable chloroplast DNA region (J_LA+). The likely native origin was determined by DNA-based comparison with a range-wide native stand collection. Most of California’s E. globulus originated from eastern Tasmania. Genetic diversity in California is greatly reduced compared with that of the native Australian population, with a single chloroplast haplotype occurring in 66% of the Californian samples. Throughout California, the degree of E. globulus naturalization varies widely but was not associated with genotype or native origin of the trees, arguing that factors such as local climate and disturbance are more important than pre-introduction evolutionary history.

Hybridization is increasingly recognized as an integral part of the dynamics of species range expansion and contraction. Thus, it is important to understand the reproductive barriers between co-occurring species. Extending previous studies that argued that the rare Eucalyptus risdonii was expanding into the range of the surrounding E. amygdalina by both seed and pollen dispersal, we here investigate the long-term fitness of both species and their hybrids and whether expansion is continuing. We assessed the survival of phenotypes representing a continuum between the two pure species in a natural hybrid swarm after 29 years, along with seedling recruitment. The performance of pure species as well as of artificial and natural hybrids was also assessed over 28 years in a common garden trial. In the hybrid zone, E. amygdalina adults showed greater mortality than E. risdonii, and the current seedling cohort is still dominated by E. risdonii phenotypes. Morphologically intermediate individuals appeared to be the least fit. Similar results were observed after growing artificial first-generation and natural hybrids alongside pure species families in a common garden trial. Here, the survival, reproduction, health and growth of the intermediate hybrids were significantly less than those of either pure species, consistent with hybrid inferiority, although this did not manifest until later reproductive ages. Among the variable progeny of natural intermediate hybrids, the most E. risdonii-like phenotypes were the most fit. This study contributes to the increasing number of reports of hybrid inferiority in Eucalyptus, suggesting that post-zygotic barriers contribute to the maintenance of species integrity even between closely related species. However, with fitness rapidly recovered following backcrossing, it is argued that hybridization can still be an important evolutionary process, in the present case appearing to contribute to the range expansion of the rare E. risdonii in response to climate change.

Genetic studies are increasingly detecting cryptic taxa that likely represent a significant component of global biodiversity. However, cryptic taxa are often criticized because they are typically detected serendipitously and may not receive the follow‐up study required to verify their geographic or evolutionary limits. Here, we follow‐up a study of Eucalyptus salubris that unexpectedly detected two divergent lineages but was not sampled sufficiently to make clear interpretations. We undertook comprehensive sampling for an independent genomic analysis (3,605 SNPs) to investigate whether the two purported lineages remain discrete genetic entities or if they intergrade throughout the species’ range. We also assessed morphological and ecological traits, and sequenced chloroplast DNA. SNP results showed strong genome‐wide divergence (F_ST = 0.252) between two discrete lineages: one dominated the north and one the southern regions of the species’ range. Within lineages, gene flow was high, with low differentiation (mean F_ST = 0.056) spanning hundreds of kilometers. In the central region, the lineages were interspersed but maintained their genomic distinctiveness: an indirect demonstration of reproductive isolation. Populations of the southern lineage exhibited significantly lower specific leaf area and occurred on soils with lower phosphorus relative to the northern lineage. Finally, two major chloroplast haplotypes were associated with each lineage but were shared between lineages in the central distribution. Together, these results suggest that these lineages have non‐contemporary origins and that ecotypic adaptive processes strengthened their divergence more recently. We conclude that these lineages warrant taxonomic recognition as separate species and provide fascinating insight into eucalypt speciation.

Eucalyptus globulus subsp. globulus Labill. (Tasmanian Blue Gum), native to southeast Australia, is a benchmark species for the pulp and paper industry. We genotyped 397 trees from 16 populations of E. globulus representing the native diversity in Australia using 24 microsatellite loci. Eight genetically distinct groups were detected, consistent with genetic groupings detected in previous quantitative and molecular studies. A sample of 29 Portuguese individuals was added to help clarify the origin of the Portuguese landrace. The results suggest a southern and eastern Tasmania origin for the Portuguese landrace. This genetic framework will enable researchers to investigate the provenance of individuals of unknown pedigree and assess the levels of representation of E. globulus natural variation in the Portuguese landrace.

Transects that traverse substantial climate gradients are important tools for climate change research and allow questions on the extent to which phenotypic variation associates with climate, the link between climate and species distributions, and variation in sensitivity to climate change among biomes to be addressed. However, the potential limitations of individual transect studies have recently been highlighted. Here, we argue that replicating and networking transects, along with the introduction of experimental treatments, addresses these concerns. Transect networks provide cost‐effective and robust insights into ecological and evolutionary adaptation and improve forecasting of ecosystem change. We draw on the experience and research facilitated by the Australian Transect Network to demonstrate our case, with examples, to clarify how population‐ and community‐level studies can be integrated with observations from multiple transects, manipulative experiments, genomics, and ecological modeling to gain novel insights into how species and systems respond to climate change. This integration can provide a spatiotemporal understanding of past and future climate‐induced changes, which will inform effective management actions for promoting biodiversity resilience.

As climates change, restoration programmes need to maximize the capacity of regenerating ecosystems to adapt to new environments, particularly when planting long-lived trees. By using a combined phenotypic and genomic approach, we assessed evidence of adaptation capacity in Eucalyptus loxophleba ssp. lissophloia, a mallee eucalypt important for restoration and oil production in Western Australia. Assessment of leaf traits in nine wild populations across a rainfall gradient showed that two traits were correlated with long-term moisture availability. Populations in more arid environments had lower specific leaf area and lower stomatal conductance, consistent with a stable plastic or adaptive response. Other leaf size and shape traits were correlated with short-term climate variables, suggesting a dynamic plastic response. Genome-wide scans with 4851 DArTseq markers and outlier analysis detected 50 markers showing signals of disruptive selection, consistent with local adaptation. Sixteen markers showed allele frequencies correlated with aridity; three were also associated with differences in stomatal conductance. Multivariate analysis and marker-environment associations signalled secondary directions of adaptation associated with maximum temperatures and soil phosphorus. We suggest that adaptation and acclimation are both likely determinants of functional phenotype in E. loxophleba, and argue that aridity is a critical driver of adaptation in this widespread species.

Widespread species spanning strong environmental (e.g., climatic) gradients frequently display morphological and physiological adaptations to local conditions. Some adaptations are common to different species that occupy similar environments. However, the genomic architecture underlying such convergent traits may not be the same between species. Using genomic data from previous studies of three widespread eucalypt species that grow along rainfall gradients in southern Australia, our probabilistic approach provides evidence that adaptation to aridity is a genome-wide phenomenon, likely to involve multiple and diverse genes, gene families and regulatory regions that affect a multitude of complex genetic and biochemical processes.