INTRODUCTION
Climate change is a key pressure on ecosystem persistence and function (Urban, 2015; Brondizio et al., 2019). The shift in climate trends will have an impact on ecosystem structure, potentially making organisms more susceptible to the effects of extreme climate events (Pacifici et al., 2015; Harris et al., 2018). Precipitation patterns are changing in heterogenous ways, with some areas becoming wetter and others drier; and while global surface temperature is predicted to rise by 1–4 °C on average by the end of the current century, the level of temperature rise is also heterogeneous depending on various factors (e.g., latitude, elevation); in addition, the frequency of extreme events such as heatwaves, wildfires, floods and droughts have increased over recent decades in several regions of the world (IPCC, 2021). Because these changes are spatially assorted, predicting climate change impacts across affected landscapes and response patterns from organisms is often challenging.
Mediterranean-type climates (MTC) are defined by reliable precipitation and temperature regimes, with predictable summer periods of low rainfall and hot temperatures, and winter periods of high rainfall and moderate temperatures. Changes in regions with MTC have already been observed with large ecosystem impacts. Ecological studies in the Mediterranean basin consistently identify more frequent drought periods, together with warmer temperatures, as main drivers for declines in oaks (Quercus spp. ) (Corcobado et al., 2014; Gentilesca et al., 2017) and pines (Pinus spp.) (Camarero et al., 2018). In the south-west Western Australia biodiversity hotspot, the 2010-11 extreme drought and heatwave conditions resulted in large scale forest collapses in eucalypts (Matusick et al., 2013). While some variation in climatic factors exists in natural systems (Staudinger et al., 2013), the rapid and extreme shifts associated with anthropogenic climate change are challenging for most organisms to persist (Levin & Poe 2017; Carlo et al., 2018).
If new climatic scenarios are no longer suitable for species to maintain their normal ecology and physiology, they either develop new adaptations, shift their geographical range or in worst case scenarios, go extinct (Bellard et al., 2012; Soto-Correa et al., 2012). Species may persist through enhanced physiological tolerance, phenotypic plasticity and/or genetic adaptation (Anderson et al., 2011; Christmas et al., 2016). Maintenance of standing genetic variation (allelic variation at a locus held within existing population) is a key factor for adaptation to changing conditions in native habitats (Guzella et al., 2018, Chhatre et al., 2019) and for persistence through environmental stressors over generations (Sexton et al., 2011; Kremer et al., 2012). Genetic variation is critical for ecological adaptive capacity - the potential and ability to adjust to, and persist through, external factors - and consequently, the evolutionary potential of the species (Reed et al., 2011). Evolution to a specific environment through natural selection results in patterns of local adaptation, when a local population experiences higher fitness compared to non-local counterparts (Kawecki & Ebert, 2004).
Measuring local adaptation has benefited through recent improvements in DNA sequencing and statistical methodology, making it possible to investigate genetic divergence and the effects of environmental factors on the process of local genetic adaptation (Honjo & Kudoh, 2019; Gougherty et al., 2020). Environmental association analyses (EAA) have been gaining traction in the last decade (Ahrens et al., 2018), allowing identification of possible candidate genes for adaptation to the environment from tens of thousands of single-nucleotide polymorphisms (SNPs) sampled throughout the whole genome from samples collected from populations across environmental gradients. For example, EAAs have been used to explore adaptive genetic variation on diverse and widespread woody plant genera, like Quercus (Martins et al., 2018; Gugger et al., 2021), Populus (Ingvarsson & Bernhardsson, 2020; Gougherty et al., 2021) and Corymbia (Ahrens et al., 2019a). These studies have identified functional genes involved in adaptation to climatic factors that can be interpreted as divergent selection linked to population-specific environmental variables (i.e., local adaptation to climate). However, different climate factors identify different sets of adaptive candidates, and few studies have focused on how these sets of adaptive candidates sort across the landscape. If candidate SNPs independently sort across the landscape, then managing these species to maintain adaptive capacity to climate change may prove to be difficult.
Identifying the genetic basis of local adaptation and selective factors is still challenging, particularly for species with limited genomic resources and polygenic control of climate adaptations (Mayol et al., 2019; Capblancq et al., 2020). Non-synonymous mutations in gene regions result in amino acid changes, which often yields changes in gene functions (Kryazhimskiy & Plotkin, 2008). These changes in genes can be under selection among populations spread across that environment. Groups of genes found to be significantly associated with environment can be categorised into broader functional groups using gene ontology (GO) enrichment analysis (The Gene Ontology Consortium, 2019). GO terms have been used to predict polygenic adaptive biological processes and molecular functions associated with candidate SNPs in tree species (Jordan et al., 2017; Collevatti et al., 2019). However, few studies investigate how genes of similar function develop patterns of adaptation across complex landscapes. If genes with related functions are found to be adaptive, this might be indicative of additive genetic variation controlling adaptation to the environment.
This study investigated the putative patterns of local adaptation associated with climate gradients across complex landscapes. To test hypotheses associated with signals of adaptation, we focused onEucalyptus marginata Donn ex. Sm. (jarrah) because of its high genetic diversity and low population differentiation (Wheeler et al., 2003) and its ecological importance in the biodiverse hotspot of south-west Western Australia (SWWA). This region has prolonged periods of extensive drying, with an estimated reduction of 20% in rainfall, from the 1970s to the present (Water Corporation, 2020), documented impacts of drought and heatwave events (Matusick et al., 2013), and the future (2030) climate is projected to show increased frequency and intensity of extremes (BOM & CSIRO, 2020).
Furthermore, jarrah provenance trials have demonstrated genetic variation in functional traits associated to precipitation factors (O’Brien et al. 2007; Koch & Samsa 2007), indicating potential local adaptation to drought stress. Ecological studies have also confirmed that water availability is critical for jarrah seedling survival and persistence (Stoneman et al., 1994; McChesney et al., 1995; Standish et al., 2015). Considering these studies on jarrah, we hypothesize that (1) populations show strong genetic patterns of local adaptation to climate; (2) precipitation is a stronger determinant of genetic adaptation compared to temperature; (3) functionally related genes show similar signatures of adaptation; and (4) adaptive variants are independently sorting across the landscape. Lastly, we use this information to create predictive maps of adaptive variation across the landscape to facilitate informed strategies for forest management that incorporate response to future climate. We go on to assess how active management strategies, such as assisted gene migration (Hoffman et al., 2015; Prober et al., 2015; Aitken & Bemmels, 2016) may be employed to build adaptive capacity to climate change.