Introduction
Understanding mechanisms governing spatial patterns of biodiversity at
biogeographical scales is a challenging theme in ecology. Spatial
isolation between populations can decrease connectivity and limit gene
flow and therefore plays a major role in shaping inter-population
variability and speciation processes (Orsini et al. 2013, Sexton et al.
2014, Pironon et al. 2016). Comparative analyses of natural systems
characterised by spatially discontinuous habitats such as islands
separated permanently by saltwater (hereafter referred to as marine
islands) with those where isolation can be driven by increasing
geographic distance between populations within a comparatively benign
landscape matrix (e.g., the mainland) have been encouraged, as they can
advance our understanding of the consequences of spatial isolation for
phenotypes and genotypes (Haila 2002, Laurance 2008, Santos et al. 2016,
Martín-Queller et al. 2017, Patiño et al. 2017, Flantua et al. 2020).
To date, comparing marine island populations to mainland populations has
been a classic approach to understanding the drivers of isolation due to
the obvious geographic separation of islands from the mainland,
particularly for oceanic rather than continental islands (Weigelt and
Kreft 2013). On islands, organisms can be subject to strong selection
pressure due to a large variety of eco-evolutionary forces that include
lowered gene flow, founder effect, genetic drift and high extinction
rates due to smaller population sizes, modified abiotic and biotic
conditions (Santos et al. 2016, Patiño et al. 2017). These factors have
been linked to shifts in body and organ size (the “island rule”,
Foster 1964, Lomolino et al. 2013, Benítez-López et al. 2021), decreased
dispersal (Burns 2018), slower growth rates and increased life span
(Andrews 1976, Lens et al. 2013), and changes in reproductive strategies
and behaviour (Covas 2012, Morinay et al. 2013) in island populations.
Such changes associated with island populations are known as the
“island syndrome” (Whittaker and Fernández-Palacios 2006). In
conjunction with such life history, physiological and behavioural
changes, spatial equilibrial processes (founder effects, restricted
dispersal, small population sizes, higher extinction rates) should
theoretically reduce the neutral genetic diversity of island populations
in comparison to mainland populations. However, while such patterns are
predicted, this observation is not generally applicable across all
island systems (Frankham 1998, Woolfit and Bromhan 2005, García-Verdugo
et al. 2015).
While islands have been the classic focus of isolation effects,
isolation can also emerge on the mainland, due to either large
geographic distances between populations (in continuous and recently
fragmented habitats, Laurance 2008, McIntyre & Hobbs 1999, Watson
2002), or environmental discontinuities between suitable habitat patches
in ecological islands (Csergő et al. 2014, Tapper et al. 2014,
Steinbauer et al. 2016). However, mainland isolation is likely to differ
from classic marine island isolation, as mainland habitat islands lack
an abrupt saltwater barrier and experience higher spatial or temporal
connectivity (Watson 2002, Driscoll et al. 2013, Ó Marcaigh et al.
2021). As a result of this difference, their analogy with marine islands
has been questioned (Flantua et al. 2020). This calls for further
comparative investigations to better understand the spatial mechanisms
governing the biodiversity of island versus mainland systems, and for
the conceptual unification of isolation research across systems (Haila
2002, Laurance 2008, Santos et al. 2016, Patiño et al. 2017, Flantua et
al. 2020).
Geographic distance may be key determinant of spatial isolation, as well
as an important driver of spatial variability, and it is perhaps the
most commonly used metric of geographic isolation (Wright 1943, Orsini
et al. 2013, Sexton et al. 2014). But geographic distance is not an
exclusive determinant of spatial patterns in phenotypic traits and
neutral genetic diversity. While strict isolation by distance emerges
due to limits to dispersal and genetic drift (Wright 1943), the role of
environmental conditions in fostering spatial population variability may
override the direct effects of geographic distance (Kalmar and Currie
2006, Shafer and Wolf 2013, Orsini et al. 2013, Sexton et al. 2016).
Environmental heterogeneity, modified biotic interactions and habitat
disturbance often shape the course of ecological and evolutionary
processes in populations worldwide, and have sculpted much of the
individuality of island populations (Kalmar and Currie 2006, Heaney
2007, Triantis et al. 2010, Lens et al. 2013, Weigelt and Kreft 2013,
Stuessy et al. 2014, Borregaard et al. 2016). Environmental factors are
key determinants of intraspecific body size variation in vertebrate
groups globally (Henry et al. 2023). Increasing evidence indicates that
even the spatial patterns of neutral genetic diversity are heavily
influenced by environmental conditions in addition to the geographic
position of populations (Lira-Noriega and Manthey 2014, de Kort et al.
2021). Despite significant advances in understanding these two major
drivers of biodiversity at different levels of organisation, global
comparative evidence for differential effects in island versus mainland
systems is still lacking.
A complicating circumstance is that significant differences in responses
may exist across different traits or groups of species, some being more
responsive to geographic forces, while others responded more readily to
environmental conditions (Sexton et al. 2014, Pironon et al. 2016,
Orsini et al. 2013, Henry et al. 2023). For example, genetic diversity
of plants responds more readily to geographic, than environmental
drivers compared with animals (Sexton et al. 2014). As a result, a
series of geographic, environmental and taxonomic factors need to be
considered for a better understanding of the links between life
histories and spatial isolation (Dupré and Ehrlén 2002, Sutherland et al
2013) and in order to detect the effect of system type (e.g., island or
mainland) on inter-population variability (García-Verdugo et al. 2015,
De Kort et al. 2021). Due to the difficulties in disentangling these
influencing factors, the development of global biogeographic models of
population variability has been slow, despite major advances in
functional biogeography and population macroecology (overviews in
Schrader et al. 2021a, Schrader et al. 2021b, Buckley and Puy 2022,
Vasconcelos 2023).
Here we conducted a global meta-analysis of multiple plant and animal
populations studied in both island and mainland systems, in which we
test how geographic distance and macroclimatic distance relate to
phenotypic and neutral genetic diversity variation within the
populations of marine island systems and mainland systems (Fig. 1).
While neutral genetic diversity results from spatial processes such as
gene flow, migration or dispersal, it has mostly indirect effect on
fitness through e.g. inbreeding depression or founder effects
(Holderegger et al. 2006). In contrast, phenotypic variability is mainly
influenced by a mixture of adaptive and plastic responses to the
environment, and only partially by neutral (standing) genetic diversity.
Therefore, the two measures provide complementary insights into
processes underlying spatial diversity patterns. While we expected
populations to show greater differences in phenotypic traits and neutral
genetic diversity with increasing distances between populations, we
predicted that these effects would be stronger within island systems,
which show consistent spatial structure compared to the mainland
systems. We further expected greater differences in phenotypic traits
and neutral genetic diversity with increasing macroclimatic differences
between populations, but we did not expect macroclimate effects to
differ between the two system types. Finally, we predicted that
phenotypic traits would show higher levels of spatial variation across
populations compared to neutral genetic diversity, because the former
are more strongly influenced by natural selection.