Discussion
Using a global dataset of phenotypic differences and differences in
neutral genetic diversity for 1832 populations of 112 species studied
comparatively in marine island and mainland systems, we showed greater
differences in phenotypic traits between islands than between equivalent
populations on the mainland, and no differences in the spatial patterns
of neutral genetic diversity between the two systems.
As expected, mean phenotypic differences were higher between island
populations than between mainland populations. On the mainland, more
populations are likely to benefit from higher connectivity between
habitat patches compared to islands (Pușcaș et al. 2008, Driscoll et al.
2013, Martín-Queller et al. 2017), which could lower the magnitude of
spatial phenotypic variability. In island systems, the effective
isolation due to the saltwater matrix and its consequences e.g., lowered
gene flow, can amplify opportunities for phenotypic differentiation
between populations, which has been linked to accelerated rates of
speciation and high levels of island endemism (Whittaker and
Fernández-Palacios 2006, Kier et al. 2009). The result could also be due
to the potentially larger differences in population sizes between
islands than between mainland populations. On islands, smaller
population sizes are more frequent than on the mainland due to
constraints of island size (Woolfit and Brohman 2005, Triantis et al.
2010). As a result, genetic drift is more frequent on islands (Woolfit
and Brohman (2005), which can set populations on distinct evolutionary
courses and enhance their phenotypic differentiation. Evolutionary
pressure promoted by niche differentiation following colonisation of
islands with different natural history may also underly the stronger
phenotypic differentiation between islands compared to mainland
populations (O’Connell et al. 2019). Due to our modelling framework we
could not derive to what extent the phenotypic differentiation was due
to genetic differentiation, because our genetic diversity metric
quantified differences in neutral genetic diversity between populations.
However, the demonstrated genetic differentiation between islands and
mainland sites (review in Stuessy et al. 2014) strongly suggest that
genetic differentiation may underly the accentuated phenotypic
differences between individual islands compared to mainland systems. The
effect of island system on phenotypic differentiation emerged despite us
analysing oceanic islands together with continental islands. Continental
islands have a different history (they are often closer to the mainland,
benefiting from more frequent immigration opportunities that stabilize
the selection on phenotypic traits) that may have lowered to some extent
the effect of the island system type.
In line with our expectations we found a tendency for increased mean
phenotypic differences between populations with increasing geographic
distance on the mainland, but contrary to our expectations we did not
find a similar trend in island systems, and we found no effect of
macroclimatic distance on the phenotypic differences. While geographic
distance and macroclimatic distance were correlated in our data, which
is frequently the case in spatial analyses (Bahn and McGill 2007, Coutts
et al. 2016), models excluding either the geographic or macroclimatic
distance did not change the results. The lack of any geographic distance
effects on phenotypic differences between islands reinforce that other
spatial constraints as detailed above (isolation due to saltwater,
island size, niche differentiation etc.) may be more effective at
promoting phenotypic variability in island systems compared to the
simple isolation by distance. On the mainland on the other hand, the
signal, albeit weak, of a positive effect of geographic distance on
phenotypes suggests that isolation by distance may play a relatively
more important role in emerging spatial trait variability compared to
island systems (e.g., De Vriendt et al. 2017). The lack of macroclimate
effects in both systems suggests no effect of isolation by macroclimate
in driving mean population-level phenotypic variation. However, evidence
exists for the contrary at least for particular groups of organisms
(e.g. in endotherm, but not in ectotherm vertebrates, mean temperatures
were associated with smaller intraspecific body size globally; Henry et
al. 2023). Therefore, the role of macroclimate in generating isolation
is likely idiosyncratic in terms of the taxonomic groups it affects, and
in contrast to geographic forces (spatial habitat structure, geographic
distance) its effects on spatial phenotypic variability are harder to
generalise. However, as sites for island-mainland population comparisons
are primarily not selected to test variation determined by environmental
differences, we suspect that in our dataset the macroclimatic distance
between populations was too small, as the most frequent paired distance
represented only 2% of the largest potential environmental distance
found in our data (Fig. S3.1). Finally, macroclimate represents only one
dimension of environmental distances between populations, while other
environmental variables that more directly capture the environments
experienced by the populations, such as the heterogeneity of vegetation
types, could be potentially more influential on the measured phenotypic
traits.
There was no effect of the system (island or mainland) on differences
between population-level neutral genetic diversity, except when the
geographic distance was omitted from the model. This is surprising,
because we expected greater variation in neutral genetic diversity
between islands beyond the effect of geographic distance due to e.g.,
disproportionate dispersal difficulties when traversing larger saltwater
barriers, or the hypothesised larger differences in population sizes
between different islands compared to populations on the mainland. The
geographic and macroclimatic distances potentially underlying the
variation in neutral genetic diversity had no system-dependent effects
either, because the interaction between these variables and the system
type was not significant. Other relevant factors for neutral genetic
diversity not tested here such as effective population size or
population dynamics and stability could still differ between island and
mainland systems. Nevertheless, none of the potentially involved factors
caused consistent between-population differences in neutral genetic
diversity in island versus mainland systems in our study. Consequently,
the spatial patterns of neutral genetic diversity are driven, at least
partially, by different mechanisms compared to the spatial patterns of
phenotypic traits, which are clearly governed by forces that differ
between island and mainland systems (Whittaker and Fernández-Palacios
2006, Santos et al. 2016). These results support earlier findings
showing similar levels of population neutral genetic diversity in island
and mainland systems (García-Verdugo et al. 2015, De Kort et al. 2021)
and also provide support for the universality of neutral processes
across systems.
In line with our expectations we captured a weak signal of a positive
influence of geographic distance on the mean differences in neutral
genetic diversity between populations, which was similar across islands
and mainland populations. While spatial isolation is typically a much
stronger driver of genetic differentiation between populations due to
limits to dispersal and genetic drift (Sexton et al. 2014), the effects
of geographic distance on spatial patterns of neutral genetic diversity
seem globally weak and may be more heavily influenced by organismal life
histories combined with environmental conditions, as advanced earlier by
Orsini et al. (2013) and Lira-Noriega and Manthey (2014). Nevertheless,
geographic distance may still determine parallel patterns of neutral
genetic diversity in both island and mainland system, despite the
responses being overall weak.
The effects of environmental distance can override the effects of
geographic distance on differences in neutral genetic diversity between
populations (Lira-Noriega and Manthey 2014), but in our study, contrary
to our expectations, macroclimate had no such effect in either system.
As with the phenotypic differences, contrasting climatic requirements of
different groups of species may make it difficult to distil
generalisations over the course of global approaches. Extending the
sampling design of island-mainland studies to evaluate responses across
larger environmental gradients may be needed to strengthen signals of
global macroclimate effects on neutral genetic diversity, as also
suggested by the range of results in Lira-Noriega and Manthey (2014).
Reconciling island biogeography theories with complementary ecological
and evolutionary theories has a high priority in the future agenda of
island biology (Patiño et al. 2017). Our findings suggest that
comparative tests of general isolation-by-distance and
isolation-by-environment expectations in island and mainland systems, on
populations of the same species, offer promise in achieving such a
reconciliation. In such global comparative analyses, there is an
outstanding amount of unexplained variability (e.g. 40-70% random
species effect in De Kort et al. 2021). This was also the case for our
dataset, with effects due to system type or variation associated with
factors such as taxonomic diversity only capturing a small fraction of
the variation between populations. While macroecological studies
spanning global scales and across kingdoms, such as ours, typically have
large levels of unexplained variation, they are expected to uncover
fundamental spatial phenomena with large effect sizes. We found only
relatively small effects of geographic distance in both island and
mainland systems, indicating that the effect of this simple isolation
measure, commonly used to explain between-population variation, is
difficult to generalise or not as universal as previously thought.
Context dependencies associated with different life histories, such as
dispersal ability of particular species, biotic interactions, variable
population sizes, specific colonisation and isolation histories etc. (De
Kort et al. 2021) may weaken the effects of geographic distance on
phenotypes and genetic diversity. For example, in our island systems the
effect of geographic distance might have been lowered because we
analysed oceanic islands together with continental islands that benefit
more from the spatio-temporal connectivity with the mainland. We also
expected stronger effects of kingdom (plant or animal), species or the
phylogenetic relationships between species as in, e.g. Sexton et al.
(2014), who found differences between plant and animal genetic responses
to geographic and environmental distances. Because this was not the case
in our dataset, we suspect that the low sample size (e.g., only seven
plants in the phenotypic differentiation models) and the large range of
traits each more or less responsive to geographic distance and/or
correlated with each other to different extents might have blurred the
general patterns. The magnitude of the differences between populations
varied largely depending on the response type, but the amount of data
available for particular response types was generally low, with the
exception of body size for the phenotypic traits and heterozygosity for
the neutral genetic diversity (Fig. S2.2). We therefore call for a
careful investigation of context-dependent drivers of population
variability across fundamentally different geographic systems,
commensurate with the life history of particular organisms. Comparative
functional connectivity studies are a promising avenue in this direction
(Juhász and Oborny 2020, Kimberley et al. 2021).
The knowledge transfer between island and mainland systems is still
limited. In a horizon scan of the state-of-the-art of island
biogeography by Patiño et al. 2017, only 10.2% of respondents worked in
both system types. We echo earlier calls (Patiño et al. 2017) for a
better replication of the control mainland populations, which may
massively improve the applicability of island biology studies in
developing global biogeography models. Alternatively, studies could
investigate spatial isolation mechanisms comparatively across different
types of mainland systems ranging from ecological islands to continuous
habitats, while perhaps benefiting from larger datasets.