Introduction
Species geographical range is a fundamental unit in macroecology and is
a main predictor of extinction risk across organisms
(Brown et al. 1996, Purvis et al.
2000, Chichorro et al. 2019). As the distribution of a species provides
important information on their ecology and evolution,
understanding what drives the vast
variability in species range size has for long been of interest to
paleontologist, biogeographers, macroecologists and evolutionary
biologists (Brown et al. 1996,
Gaston 2003, Gaston 2009, Gaston & Fuller 2009). Several mechanisms
might underlie species geographical ranges, such as environmental and
physical constraints, differences in niche requirements, population
abundance, latitudinal gradients, differences in body size or trophic
level, colonization-extinction dynamics, species age and dispersal
ability (Gaston 2003). Although all these mechanisms can simultaneously
interact to produce the empirical range sizes, dispersal has received
the most interest, likely because it is one of the most prominent
processes affecting range size
(Hanski et al. 1993, Lester et al.
2007, Sheth et al. 2020). However, despite major efforts to link
dispersal ability to range size, the theoretical expectation of a
positive dispersal-range size relationship has received mixed empirical
support both among and within taxa (Lester et al. 2007, Luiz et al.
2013, Alzate et al. 2019a, Sheth et al. 2020).
Here we define dispersal as any movement of individuals or propagules
potentially leading to gene flow across space (Ronce 2007, Clobert et
al. 2012). Both theoretical and experimental work have shown that
dispersal can positively affect the mechanisms that allow attaining
large geographical ranges (Holt
2003, Holt et al. 2005, Sexton et al. 2009, Alzate et al. 2019b). For
instance, dispersal promotes range expansion by facilitating the
colonization of new habitats and promoting local adaptation (Holt &
Gomulkiewicz 1997, Alzate et al. 2019b). Dispersal also prevents range
contraction by decreasing extinction risk and allowing populations to
persist in suboptimal habitats
(Hufbauer et al. 2015, Alzate et
al. 2019b), as it provides demographic
(Brown & Kondric‐Brown 1977) and
genetic (Holt & Gomulkiewicz
1997) rescue. Furthermore, simulation models (spatial explicit neutral
models) predict a positive effect of dispersal on species range size
(Rangel-Diniz-Filho 2005, Alzate et al. 2019c). An outstanding question
is therefore why positive effects of dispersal on range size are found
in some cases, but not in others.
Discrepancies between expected and observed dispersal-range size
relationships might emerge for different reasons. Firstly, studies
differ in their dispersal ‘definitions’ and therefore also differ in
which phenotypic traits are considered to be associated to dispersal
ability. Which dispersal-related traits to choose is not a trivial
question, particularly because dispersal and dispersal distance are
emergent properties (complex traits) resulting from the interactive
effects of various dispersal-related traits (e.g., morphology,
physiology, behavioural and life history traits), which are highly
dependent on the type of organism studied
(Ronce 2007, Bonte et al. 2012,
Matthysen 2012, Ronce & Clobert 2012, Travis et al. 2012, Sheth 2020,
Green et al. 2021). Moreover, dispersal can occur at different life
stages (e.g., seeds, eggs, juveniles, adults), it is composed by three
phases including departure (i.e., decision to leave the old habitat),
transfer (i.e., displacement from the old to a new habitat) and
settlement (i.e., arrival and settlement in the new habitat), and can be
shaped by external factors and evolve (Ronce 2007, Matthysen 2012).
Although dispersal kernels are in general good proxies for dispersal
abilities across species, there are still difficulties to measure the
tail of the kernel, which is of major importance when scaling up to
distribution dynamics (Clobert et al. 2012). Therefore, different
measures of dispersal may capture different components of the dispersal
process, and may thus affect the resulting dispersal-range size
relationship.
Secondly, true biological differences between study organisms might
determine how dispersal correlates with range size. For instance, it is
possible that the dispersal-range size relationship differs between
active (e.g., reptiles, birds, mammals) and passive dispersers (e.g.,
plants, diatoms, marine molluscs), because dispersal (the transfer
phase) for passive dispersers is outside the control of the individual,
as it depends on external forces (e.g., currents, wind, gravity, other
organisms) with a high stochastic component (Matthysen 2012). Moreover,
the nature of the dispersal medium of marine and terrestrial realms can
lead to differences in dispersal ability between terrestrial and marine
organism. In marine systems, passive rather than active dispersal is
favoured, which may lead to fewer dispersal-related adaptations in
marine than in terrestrial systems (Burgess et al. 2005). The higher
connectivity between marine habitats may also erase the link between
dispersal ability and range sizes (Mora et al. 2012). In terrestrial
systems, dispersal may be more difficult without specialised adaptations
(such as wings to fly, fleshy fruits to attract animal dispersers, etc.)
(Burgess et al. 2015). In addition, human activities can uncouple the
dispersal-range size relationship by decreasing species distributions
(Webb & Gaston 2000). This might be more common on terrestrial than in
marine systems, where large scale human impact has a longer history.
Similarly, dispersal may be less limiting in endotherms than ectotherms,
because endotherms possess broader thermal niches and higher thermal
tolerances due to high metabolic rates compared to ectotherms,
facilitating settlement. Even though endo- and ectotherms might not
differ in the dispersal capacities required during the transfer phase of
dispersal, endothermy might have an advantage during the settlement
phase. Thus, physiological tolerance rather than dispersal ability may
in some cases be the limiting factor when it comes to range size (Pie et
al. 2021).
Thirdly, evolutionary history may affect the current dispersal-range
size relationship by determining time and potential for (past) range
expansion, or the evolution of dispersal-related traits that facilitated
past long-distance dispersal
(Onstein et al. 2019). For
example, range size is likely to vary with species age because species
need time to expand their range
(Willis 1922, Webb & Gaston 2000,
Gaston 2003), and the dispersal-range size relationship may thus be
obscured when studying species of different ages. Furthermore, past
climate changes (e.g., since the last glacial maximum), population
connectivity, and availability of suitable settlement environments, may
have affected the rate of range size expansion (e.g., ‘Reid’s Paradox’),
and may explain distinct dispersal-range size relationships across
biogeographical realms and climate zones that differ in their glaciation
history, for example (Svenning & Skov 2004, Svenning et al. 2008).
Lastly, besides biological and evolutionary reasons, intrinsic
differences between studies, such as study design, methodology, data, or
analytical approach might explain absence of a relationship between
dispersal and range size. Studies examining how dispersal affects range
size differ in taxonomic scope (e.g., ‘genus’, ‘family’, ‘phylum’),
taxonomic unit of analysis (e.g., at ‘genus’ or ‘species’ level), the
measure of species range size (e.g., ‘extent of occurrence’ or ‘area of
occupancy’), range completeness (e.g., ‘partial’ or ‘complete’ measures
of range size), and the number of considered species and
dispersal-related traits to capture variation in the dispersal-range
size relationship. For example, range size measures can under- or
overestimate true range sizes by including or excluding discontinuities
in the spatial distribution of taxa. Similarly, high taxonomic units of
analysis (e.g., ‘genus’ or ‘family’ instead of ‘species’) ignores
within-clade variation in dispersal. The benefit of using comprehensive
data, that is, bigger areas that include complete ranges, over partial
data (i.e., smaller areas that do not include complete ranges) has been
shown for understanding the body size - range size relationship in
animals, with more consistently positive relationships when using
comprehensive data (Gaston & Blackburn 1996).
Despite all possible caveats and warnings about several of these
problems (Blackburn & Gaston 1998, Alzate et al. 2019a, Johnson et al.
2021), a comprehensive methodological framework to study dispersal and
range size is missing. Here we
performed a systematic review to investigate the causes of variation in
the dispersal-range size relationship by collating 478 dispersal-range
size relationships from 86 independent studies. Firstly, we investigated
and synthesized the spread of evidence for the dispersal-range size
relationship between regions, realms and clades. Secondly, we quantified
how differences between studies regarding dispersal and range size
characteristics related to transfer, settlement and evolution, and
potential methodological differences (range size definitions, spatial
corrections and taxonomy) can affect the overall dispersal-range size
relationship (Table 1). Finally, we discuss these results in the context
of the complexity of the dispersal process – from departure, to
transfer, to settlement.
Table 1. Moderator candidates of the dispersal-range size
relationship as synthesized in this study. Variables were classified
into six groups depending on their hypothesized effect on the
dispersal-range size relationship: departure/transfer variables that
directly affect movement/transfer of species, settlement variables or
corrections that influence the potential and realized niche space, time
variables or corrections related to evolutionary history and past
dynamics that may influence range size, and three methodological type
variables that may bias the inference of the dispersal-range size
relationship. Description of each variable and the prediction of why and
how it potentially influences the dispersal-range size relationship is
provided.