Introduction
Marine ecosystems worldwide are experiencing dramatic shifts in
environmental conditions due to climate change, the most evident of
which is a steady increase in sea surface temperature (SST) (Cheunget al. 2013). These changes can affect marine organisms in
different ways, such as by altering the structure of trophic webs (e.g.,
Hyndes et al. 2016), biasing sex ratios in species with
temperature-dependent sex determination (e.g., Miyoshi et al.2020), and redefining the geographical ranges of species (e.g., Pinskyet al. 2020). In order to guide natural resource management under
this changing marine landscape, it is crucial to make future predictions
of suitable habitat for target species as accurately as possible.
Species distribution models (SDMs),
which estimate relationships between species’ presence data and
environmental predictors, have been used extensively to predict
potential changes in species’ distributions under climate change
scenarios (Guisan et al. 2017). The majority of SDMs are
constructed at the species-level or even higher taxonomic levels, and
this is particularly true for applications to marine species (Robinsonet al. 2011; Robinson et al. 2017; Chefaoui et al.2018; Jayathilake & Costello 2018; Melo-Merino et al. 2020). One
fundamental and critical assumption underlying species-level SDMs is
niche conservatism, which assumes that all populations of a species have
analogous environmental requirements and respond in a similar way to a
changing environment (Guisan et al. 2017; Smith et al.2019). But this assumption ignores intra-specific variation, in
particular local adaptation and phenotypic plasticity, which are
frequently observed especially in broadly distributed taxa (e.g.,
Marín-Guirao et al. 2016; Duarte et al. 2018; King et al.2018; Benito Garzón et al. 2019; Peterson et al. 2019;
Zhang et al. 2020b).
SDMs constructed with data for lineages below the species level can
account for possible local adaptations and therefore can provide more
reliable niche estimations and habitat suitability projections for
species with intraspecific variation. For instance, a species-level SDM
for the threatened Japanese crayfish Cambaroides japonicus (De
Haan 1841) predicted that this species might lose a large proportion of
its suitable habitat in the future, whereas lineage-level SDMs for the
same species predicted a weaker impact of climate change overall (Zhanget al. 2021). The importance of taxonomic units (i.e., above and
below the species level) in distribution modelling has recently been
recognized (Benito Garzón et al. 2019; Peterson et al.2019; Smith et al. 2019; Collart et al. 2021), which has
resulted in more SDM applications for terrestrial and freshwater species
that consider intra-specific variation (e.g., Ikeda et al. 2017;
Razgour et al. 2019; Zhang et al. 2021). Conversely,
relatively few SDM studies have investigated this issue in the marine
realm (but see Assis et al. 2018a; Cacciapaglia & van Woesik
2018; Lowen et al. 2019).
Seagrasses are one of the most critical habitat engineers (along with
seaweeds, mangroves, and coral reefs) of tropical coastal marine
environments. They not only harbor rich marine biodiversity in seagrass
meadows, but also provide a number of ecosystem services, such as
primary productivity, habitat restoration, resources for marine life,
and human recreation, among others (Unsworth et al. 2018).
Maintaining these services is key to achieving conservation and economic
goals under global change. Yet, seagrass ecosystems are declining
worldwide at an annual rate of 7% due to multiple natural and
human-mediated disturbances (Orth et al. 2006; Waycott et
al. 2009). It is noteworthy that climate change has received
considerable attention as a major factor for the increasing loss of
seagrass meadows (Jordà et al. 2012; Thomson et al. 2015;
Repolho et al. 2017; Duarte et al. 2018; Smale et
al. 2019). This is particularly true for the tropical Indo-Pacific
bioregion, which supports the most seagrass diversity and a high
diversity of associated flora and fauna (Short et al. 2007) but
has suffered from striking degradation of seagrass coverage (Coleset al. 2011; Rasheed & Unsworth 2011; Grech et al. 2012;
Chefaoui et al. 2018; Olsen et al. 2018; Brodie et
al. 2020). Given the global ecological roles of seagrasses, it is
crucial to make accurate forecasts of their distribution patterns in the
face of climate change, but seagrasses are “among the least-studied
groups” (Melo-Merino et al. 2020) with respect to range shift
projections. The majority (if not all) of SDM studies on seagrasses have
been at the species level and therefore did not incorporate potential
intraspecific variation.
The seagrass Thalassia hemprichii (Ehrenberg) Ascherson
(Hydrocharitaceae) is a perennial climax species that is widely
distributed in the tropical Indo-Pacific bioregion (Green & Short
2003), extending from Australia, the peripheral limit of its eastern
range (Hernawan et al. 2017), to East Africa in the West Indian
Ocean (Jahnke et al. 2019a). It reproduces sexually via seeds and
asexually via vegetative growth of rhizomes. Uprooted adult plants can
potentially float for months and hence colonize distant areas (Wuet al. 2016). In addition, this seagrass forms buoyant seeds that
remain afloat for long enough to disperse a few hundreds of kilometers
(Lacap et al. 2002). A recent survey revealed that seedlings can
also disperse for over a month due to the accumulation of oxygen in the
body tissue (Wu et al. 2016). Thus, T. hemprichii has
excellent long-distance dispersal potential that may play a significant
role in shaping population genetic structure (Lowe & Allendorf 2010).
This species may be particularly vulnerable to climate change because it
exhibits spatial separation of the sexes (dioecious), reinforced by
physiological and morphological differentiation of each sex to variable
microhabitats (Hultine et al. 2016). Recent genetic studies ofT. hemprichii detected genetic lineage divisions in the East and
West Indo-Pacific Ocean (Hernawan et al. 2017; Jahnke et
al. 2019a), but we still do not have a clear understanding of the
distribution of lineages across the entire tropical Indo-Pacific region,
or whether these diverged lineages are expected to respond
differentially to climate change.
In the present study, we used T. hemprichii as a model to: (i)
examine range-wide divergence of genetic lineages in the tropical
Indo-Pacific Ocean; (ii) test if phylogeographical lineages exist, and
if so, quantify niche differentiation between distinct lineages; (iii)
predict climate change impacts on the species’ range with species-level
and lineage-level SDMs. By incorporating potential intra-specific
variation, our SDMs can provide more realistic predictions on how
climate change will shift future distributions of a habitat-forming
seagrass, thus generating valuable knowledge for guiding the long-term
management of this species in the tropical Indo-Pacific coast.