Discussion
This study identified two diverged genetic lineages (WTIP and CTIP) in
the seagrass T. hemprichii across the tropical Indo-Pacific. The
observed niche differentiation between the two lineages suggests a
violation of the niche conservatism assumption for species-level SDMs,
and our lineage-level predictions of present and future range
importantly avoid this assumption. Despite differences between the
habitat suitability predictions of the lineage-level and species-level
SDMs, they consistently predict that the CTIP lineage is at greater risk
of range contraction in the future. For this seagrass, but also for
other taxa with intraspecific genetic differentiation, incorporating
information about phylogeographical structure when modelling the impacts
of climate change provides more realistic predictions to better
understand future range shifts (Smith et al. 2019; Zhang et
al. 2021).
Critical marine predictor variables for
seagrasses
Both the lineage-level and species-level SDMs showed that distance to
land, water depth, and annual mean SST represent the most essential
factors in explaining the distributional patterns of T.
hemprichii . The predominant roles of the two geographical predictors
and the negligible roles of marine environmental predictors in the WTIP
lineage-level model (Table 2) may partially explain the marginal impacts
of climate change predicted for this region. The importance of these
three predictors has been emphasized in previous studies ofThalassia species (e.g., Duarte 1991; Lapointe et al.1994; Fourqurean & Zieman 2002; Zhang et al. 2014) and other
seagrasses (e.g., Baumstark et al. 2016; Jayathilake & Costello
2018). For instance, Jayathilake & Costello (2018) used a set of 13
predictors and developed SDMs for 60 seagrass species including T.
hemprichii . They reported the important roles of distance to land and
mean SST in explaining geographical distributions of seagrasses.
Unexpectedly, maximum SST was reported to be critical, but water depth
was less important in their study (Jayathilake & Costello 2018). This
inconsistency in our study might be attributed to (a) different sets of
predictors, and/or (b) different roles of marine predictors in different
seagrass species.
Incorporating intraspecific variation into SDMs for
seagrasses
Seagrasses provide vital ecological services in marine ecosystems and
SDMs have been applied to this taxonomic group for multiple purposes
(see reviews by Robinson et al. 2011; Robinson et al.2017; Melo-Merino et al. 2020). Nonetheless, all previously
reported SDMs on seagrasses were built at the species level and thus
have not considered possible intraspecific variation. For instance,
Chefaoui et al. (2018) developed species-level SDMs for two
seagrasses (Posidonia oceanica and Cymodocea nodosa ) in
the Mediterranean Sea and predicted that the two species are likely to
experience dramatic habitat loss in the future. We fully agree that
species-level SDMs are by definition informative; but given the high
prevalence of intraspecific variation in marine macrophytes (e.g., Kinget al. 2018), and the significance of intraspecific variation in
SDMs (Benito Garzón et al. 2019; Smith et al. 2019; Zhanget al. 2021; Collart et al. 2021), incorporating
intraspecific genetic variation into forecasts of seagrass distribution
should result in more realistic scenarios of the potential consequences
of climate change.
The importance of taxonomic resolution in SDMs has been addressed in
several terrestrial and freshwater species, but much more rarely for
marine species (see review by Smith et al. 2019; Collart et
al. 2021). Species-level SDMs that disregard existing intraspecific
variation can either over- or under-estimate climate change impact on
distributional change. For instance, species-level models for the
lodgepole pine Pinus contorta consistently predicted more extreme
habitat loss than subspecies-level models, regardless of the dispersal
scenario (i.e., no or unlimited dispersal ability) (Oney et al.2013). As another example, although a species-level model for the
reef-building coral Porites lobata predicted over 5% habitat
expansion, when modelling this species as five genetically isolated
subpopulations the prediction was ca. 50% habitat loss (Cacciapaglia &
van Woesik 2018). In the present study, the species model consistently
predicted low impacts of climate change in the CTIP region in comparison
to the lineage model (e.g., the habitat loss vs. stability in the Sunda
Shelf in Fig. 4c vs. Fig. 4d). As for the WTIP region, we found the
opposite pattern. Here, the lineage model predicted stable future
habitats in the southern Red Sea (Fig. 4c), whereas the species model
predicted habitat loss, including to the north of Mauritius (Fig. 4d).
In addition, both species and lineage models predict a southward range
expansion in the southern CTIP, but only the species model clearly
predicts this in the WTIP. Southern expansion is likely correlated with
future temperature increases in areas which are now too cold (Supporting
Information Fig. S5a). We should note that MESS values in the equatorial
regions were slightly negative, which indicates novel future
environmental conditions. This is due in part to higher future SST
values for this region than those used by the present-day SDM
(Supporting Information Fig. S5b)—thus, SDM projections in this region
should be associated with more uncertainty. Further studies involving
both field investigations and associated data updates and methodological
developments for models [e.g., developing ensembles of small models
(Breiner et al. 2018) or using smaller study extent] would
further improve our predictions for climate change impacts on T.
hemprichii in the Tropical Indo-Pacific.
Intraspecific variation and local adaptation in
seagrass
Differences in response to thermal changes related to intraspecific
variation, whether eco-physiological or evolutionary, are
well-documented in seagrasses (King et al. 2018). This variation,
partly based on phenotypic plasticity or local adaptation, ultimately
might permit seagrasses to acclimatize and adapt to changes in climate
(Duarte et al. 2018). The marine predictor variables that played
a predominant role in our SDMs (e.g., annual mean SST and water depth)
could be responsible for both long- and short-term local adaptation ofT. hemprichii to a changing climate (King et al. 2018;
Jahnke et al. 2019b). In support of this, common-garden
experiments have revealed a clear local adaptation to increased
temperatures in Zostera marina (Franssen et al. 2011;
2014), and to a depth gradient in Posidonia oceanica(Marín-Guirao et al. 2016; Jahnke et al. 2019b). Further,
parallel adaptation of Z. marina to thermal clines along the
American and European coasts was demonstrated using a space-for-time
substitution design and gene expression profiling (Jueterbock et
al. 2016). Such adaptive local differentiation induced by divergent
environmental forces (e.g., light, depth and temperature) has led to
structured populations and lineages in seagrasses at various spatial
scales (Dattolo et al. 2014; Jueterbock et al. 2016;
Jahnke et al. 2019b), suggesting that adaptation to local
conditions is a key mechanism for seagrasses to face global climate
change.
In T. hemprichii , natural selection imposed by environmental
heterogeneity might have resulted in the evolution of locally adapted
populations with considerable variation in productivity, growth rate and
competitive interactions (Martins & Bandeira 2001; Lyimo et al.2006; Larkum et al. 2018). Despite clear genetic differentiation
identified between the WTIP and CTIP lineages, we did not ascertain the
adaptive and non-adaptive components of divergence in a common landscape
of the tropical Indo-Pacific. Future studies should focus on
distinguishing neutral genetic differentiation from local adaptation
using reciprocal transplant trials (e.g., common gardens and provenance
trials) (see Joyce & Rehfeldt 2013; Ralph et al. 2018). Also, it
is most important to assess the sub-lethal susceptibility of T.
hemprichii to thermal stress before the strongest impacts of future
climate change are sustained. Intraspecific genetic diversity across
populations can increase a species’ adaptive capacity and result in
cascading effects to the entire ecosystem (Evans et al. 2017). It
is thus important to identify the most temperature-tolerant genotypes
from the WTIP and CTIP lineages, perhaps by manipulating temperature to
quantify the performance of individual genotypes of T. hemprichiiacross thermal gradients. It is also essential to clarify whether
genotype complementarity or dominance enhance the adaptive capacity in a
population (Hughes & Stachowicz 2011).
Conservation implications
The challenge of designing effective actions for seagrass conservation
in the Indo-Pacific exists in the gap between science, policy, and
practice (Fortes 2018). In this study, the separation in geographic
distribution and high niche differentiation between the CTIP and WTIP
lineages suggest that T. hemprichii populations may be locally
adapted (Merilä & Hendry 2014). For species with significant
intraspecific genetic diversity, it is crucial to help maintain the
species’ potential for adaptive responses to climate change by
conserving this diversity (D’Amen et al. 2013). In particular,
lineage differentiation can be explained by recruitment rate (Lyimoet al. 2006; Sherman et al. 2018), nutrient resorption
(Martins & Bandeira 2001), and evolutionary history from the origin
center to the distributional margins (Mukai 1993). Dramatic future
habitat loss in the CTIP was predicted by both the species- and
lineage-level models (Fig. 4), stressing the urgency to develop
monitoring programs to rescue evolutionary and/or ecologically important
units in T. hemprichii , particularly the populations and gene
pools that have persisted through past long-term climate change because
of local adaptation (Bell 2017; Hernawan et al. 2017).
Furthermore, the recognition of high niche differentiation between the
WTIP and CTIP lineages may help to establish coherent principles and
regulating practices by which the different areas that T.
hemprichii inhabits can be protected efficiently.
The biomass, abundance, and productivity of seagrasses are highly
correlated with both habitat suitability (Martins & Bandeira 2001;
Saunders et al. 2013) and epiphytic species biodiversity (Lyimoet al. 2008). Optimizing productivity of T. hemprichii in
a given site or population can help to increase associated community
diversity (Eklöf et al. 2006; Lyimo et al. 2008). Thus, it
is necessary to explore how community diversity and structure correlate
with the genetic composition and structure of the foundational speciesT. hemprichii . Such research can help validate the results of
SDMs in this study and quantify the relationship between T.
hemprichii and its relevant community components (Ikeda et al.2017). Since populations in each of the CTIP and WTIP lineages are
locally adapted, policymakers and stakeholders are encouraged to use
local seed sources of T. hemprichii to ensure management
strategies for successful restoration and conservation purposes.
However, as the WTIP lineage may be more resilient to future climate
change, WTIP seeds could possibly be used to restore CTIP seagrass beds
which are predicted to disappear in the future.
Finally, apart from marine geographical and environmental predictors,
geographical distributions of seagrasses are also determined by other
factors including biotic interactions. For instance, Hyndes et
al. (2016) predicted that accelerating tropicalization can lead to a
potential shift both among the seagrass themselves and among their
associated communities, thereby affecting ecosystem services that
seagrasses provide in this region. The importance of incorporating
biotic interactions into SDMs has long been recognized but it is still
poorly addressed in the marine realm. More mechanistic studies
underlying thermal adaptation by linking ecology to genetics should be
done to better understand how T. hemprichii will adapt to climate
change (Duarte et al. 2018; Hu et al. 2020).