Dispersal limitations drive community structure across
multi-hierarchical levels at fine geographical scales
To investigate whether dispersal limitations shape distance-decay
relationships within a mountain, we performed an IBD and IBR analyses on
Diptera and Collembola, which have contrasting dispersal capabilities
(winged and unwinged, respectively). The unified neutral theory of
biodiversity predicts that similarity in species composition decreases
with distance due to dispersal limitation
(Hubbell, 2001). To
test this, we examined if DDRs at multi-hierarchical levels can be
explained by the dispersion limitation in addition to distance.
Specifically we analyzed which landscape variables (Figure S5)
influenced DDRs in arthropods of contrasting dispersal abilities
(Collembola and Diptera), considering our entire sampling in Nevado de
Toluca (19 km max distance among sampling points) and finer geographic
scales within the East (<5 km) and West (<2 km)
subsets of our sampling. We found that decay of similarity of
communities decreases with spatial distance at the level of haplotypes,
all CLs (0.5 to 7.5% lineages) and putative molecular species by GMYC
(Figure 5). This occurs both in Collembola and Diptera, but is more
marked in Collembola whose dispersal abilities are more limited.
Interestingly, for Collembola our results also hold both considering our
entire sampling as well as finer (<2 km) geographic distances
(Figure 5, 6) which is consistent with genetic studies within Collembola
showing genetic differentiation over very short geographic distances
(Cicconardi et al., 2013; Faria et al., 2019).
High dispersal ability is expected to enhance community similarity
(Baselga et al.,
2012). Our results support this, because the fit of the decay is higher
in the wingless Collembola (r 2 = 0.704 andr 2 = 0.599 at the haplotype and GMYC levels,
respectively; Table S3; Figure 5a) than in the winged Diptera
(r 2 = 0.293 and r 2 =
0.195 at the haplotype and GMYC levels, respectively; Table S4; Figure
5c). Similar patterns of higher distance decay relationships at
multi-hierarchical levels in poorly dispersing organisms than in better
dispersers were found in European water beetles
(Baselga et al.,
2013), Iberian leaf beetles
(Baselga et al.,
2015) and European beetles (Gómez-Rodríguez & Baselga, 2018) at much
larger (hundreds of km) geographical scales than here (but see
Gómez-Rodríguez et al., 2019 where the pattern was not clear for
terrestrial molluscs). Communities of good dispersers are more
homogeneous not only because they can disperse larger distances, but
also because they can more easily overcome geographical barriers between
suitable habitat
(Thompson & Townsend,
2006; Vellend, 2010). Thus, if dispersal abilities matter, then
landscape features impeding dispersal may also play a role in
structuring diversity, which can be explicitly tested including
landscape features in analyses such as IBR.
IBR quantifies ‘effective distances’ between communities that may yield
more biologically informative DDRs than Euclidean distance
(McRae, 2006; McRae et
al., 2008). Our results show positive significant correlation with
different explanatory power depending on the surface used, with
altitudinal differences better explaining similarity decay than distance
alone (“flat” landscape), slope or vegetation type. The resistance
surface “flat” (i.e., IBD) has slightly less explanatory power for
Collembola (r 2 = 0.704 at the haplotype level,r 2 = 0.599 at GMYC; Table S3; Figure 5a) than
“Altitude 3,000” (r 2 = 0.723 at the haplotype
level, r 2 = 0.644 at GMYC; Table S3; Figure
5b), the best fitting resistance surface. This resistance surface
corresponds to the elevation at which the Nevado de Toluca volcano
massif begins (Figure S5; Table S2), suggesting that Collembola followed
a pattern of IBD and that their limited dispersal is not impacted by
landscape features. For Diptera, the highest explanatory power was
provided by the resistance surface “Altitude B”
(r 2 = 0.319 at the haplotype level,r 2 = 0.228 at GMYC; Table S4; Figure 5d). This
resistance surface assumes maximum conductance at the mean altitude of
our sampling and a gradual decrease until reaching altitudes outside of
our sampling range, but still where Abies forest can be found
(Table S2). This suggests that besides being able to disperse larger
distances, Diptera moves through relatively unsuitable conditions
(different altitudes) less efficiently. Therefore, for Diptera it is not
distance alone that drives community structure, but also landscape
features. Thus, although our sampling blocks are separated by short
distances from 50 m to 19 km, connectivity among sites for Diptera
depends upon the elevation model used to set the conductance values
(Table S2; Figure S5). This is congruent with Janzen’s prediction of
“mountain passes being higher the tropics” (Janzen, 1967), and adds to
the recent empirical data
(Polato et al., 2018)
corroborating it. However, although our results show that landscape
connectivity contributes to dispersal limitation, geographic distance
seems to play a more dominant role both for both orders. This is
consistent with dispersal limitation acting over evolutionary time, as
has been suggested to explain the small spatial scale diversification ofScarelus beetles within tropical mountains (Bray & Bocak, 2016).
Distance decay patterns at the species level could reflect environmental
heterogeneity spatially correlated (i.e., between western and eastern
sides of the Nevado de Toluca). While some degree of environmental
distance could impact on the obtained biodiversity patterns (but see
above on the homogeneity of the sampling study habitat), our results on
i) spatial patterns of community dissimilarity recurrently found for
multiple hierarchical levels, including haplotypes which are expected to
behave neutraly across environmental gradients; ii) high values of
turnover and local endemicity at multiple spatial scales and iii) the
consistent multihierarchical pattern of distance decay in community
similarity at reduce scales (within mountain sites) for less dispersive
species, while substantially diluted for the more dispersive ones, point
to dispersal limitation within this single single sky-island as a major
driver of community assemblage.
Multi‐hierarchical approaches are useful to assess whether variation in
biological assemblages driven by dispersion follow a fractal geometry
where the same neutral processes underlie the distribution of haplotypes
and higher clustering levels
(Baselga et al., 2013,
2015). Fractal patterns have been revealed in aquatic beetles, leaf
beetles, and terrestrial molluscs, highlighting an important role for
neutral processes in the spatial structuring of biodiversity
(Baselga et al., 2013,
2015; Gómez-Rodríguez et al., 2019). Our results also reveal the
existence of a fractal pattern for DDRs, with similarity decreasing with
spatial distance from the level of haplotypes to 7.5% CLs (Table S6).
These patterns represent a considerably finer geographic scale than that
reported in previous studies (from 820 km to 4,500 km as in
Baselga et al., 2013,
2015). DDRs decreased with distance at even finer geographic scales
(<5 and <2 km) in Collembola (Table S5, Figure 6 and
S6), revealing that for arthropods with low dispersal ability, DDRs can
occur at very fine geographic distances and at all multi-hierarchical
levels, within the geographic confines of a sky island. Further to this,
we reveal that DDRs can also emerge within arthropod groups that are
typically considered as good dispersers (Diptera), but at comparatively
larger geographic distances (Figure 5). Our results align well with
analyses performed in Iberian forest and grassland mesofauna, where DDRs
were found at all hierarchical levels, also in less than 15 km, for soil
taxa with low dispersal abilities
(Arribas et al.,
2020). Given these short distances, our findings are important not only
for understanding evolution, but also for biomonitoring efforts aiming
to detect changes in community assembly, even in relatively short
distances among sampling points.