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.