Introduction
Mountainous tropical regions are hyperdiverse
(Fjeldså et al., 2012;
Rahbek, et al., 2019a; Rahbek, et al., 2019b). Besides climate
heterogeneity producing different habitats in a patchy distribution, it
has been argued that two additional factors particularly increase
diversity in tropical mountains. First, because tropical taxa have
narrow physiological tolerances to temperature, tropical mountain passes
are more effective barriers to dispersal than those in temperate
regions, thus promoting speciation through physical disruption of gene
flow (Janzen, 1967;
Polato et al., 2018; Sheldon et al., 2018). Second, coupling
altitudinal gradients with tropical latitudes allows populations within
tropical mountains to persist relatively in situ despite global
climate fluctuations (Mastretta-Yanes, et al., 2018; Rahbek, et al.,
2019a; Rahbek, et al., 2019b). These processes of isolation and
long-term persistence have been widely used to explain diversification
among tropical mountain peaks across the world
(e.g., Fjeldså et al.,
2012; He et al., 2019; Knowles, 2001; Mastretta-Yanes et al., 2018;
McCormack et al., 2009; Uscanga et al. in review). However,
recent evidence suggests that neutral processes within a single mountain
could also play an important role in generating endemism
(Bray & Bocak,
2016), but diversification at the single mountain scale and short
geographic distances has seldom been explored.
Studying evolutionary processes in mountain ranges across fine spatial
scales is challenging due to their complexity with regard to topography
and geological and climatic history. However, the insular nature of
sky-islands reduces the complexity of mountainous regions, thus
providing more simplified systems to analyze evolutionary processes.
Within true oceanic islands, habitat discontinuity has been demonstrated
to have an important role in driving geographical diversification
(García‐Olivares et
al., 2019; Goodman et al., 2012). Additionally, Salces‐Castellano et
al. (2020) have demonstrated that, when dispersal ability and climate
tolerance are restricted, strong geographic isolation over distances of
only a few kilometers can be found for multiple co-occurring arthropod
species of an oceanic island. These results suggest that besides
allopatric diversification between different islands, island systems
could also promote high levels of intra-island geographical
diversification, acting as a local-scale diversity source. If
geographical diversification were occurring within individual
sky-islands in this way, following the expectations of the neutral
theory of biodiversity, it would be expected to find similar spatial
patterns of differentiation from the haplotype to the community levels
(Baselga et al., 2013).
Arthropod communities are ideal systems to test evolutionary processes
at fine spatial scales within sky-islands because they are locally
abundant and diverse and relatively easy to sample massively. They also
harbour a broad diversity of groups with different dispersal abilities,
e.g. including winged and non-winged species and varying body-sizes.
However, taxonomic identification to the species level of rich
communities of arthropods with traditional methods is challenging
(Favreau et al,. 2006, Yu et al., 2012). In this sense, new high
throughput sequencing approaches applied to the study of arthropods are
revolutionizing the understanding of complex arthropod communities
(Andujar et al., 2015;
Arribas et al., 2016; Ji et al., 2013; Yu et al., 2012). Specially
promising is the use of whole community metabarcoding (cMBC) for the
bulk sequencing of the mitochondrial COI gene of mixed communities
(Andújar et al., 2018). Recent improvements for denoising metabarcoding
datasets (e.g., Edgar, 2016; Callahan et al., 2016) and evaluating the
prevalence of sequencing errors and co-amplified pseudogenes (Andújar et
al., 2020) raised the prospect of read-based, haplotype-level analyses
with mitochondrial COI cMBC data, which represents a step change for the
study of diversity patterns through whole-community genetic analyses
(Andújar et al., 2018;
Arribas et al., 2020).
Haplotype data from hyperdiverse arthropod communities can be used
directly for analyses of genetic diversity, or aggregated into
species-level entities for analyses of species diversity, allowing for
the joint analysis of turnover (beta diversity) at multiple hierarchical
levels. Local assemblages may diverge simply due to the lack of
population movement which, when assessed for entire communities, results
in a largely regular decay of community similarity with spatial distance
for the typically neutral haplotype variation of the mitochondrial COI
gene (Baselga et al., 2013). Under a scenario where dispersal
constraints are a dominant driver of spatial variation in community
structure, assemblage turnover at the species level should mirror these
haplotype patterns, albeit at a higher level of similarity (Baselga et
al., 2013; Baselga, Gómez-Rodríguez, & Vogler, 2015). This analytical
approach has been exploited to determine whether the composition across
multiple beetle taxa assemblages is predominantly driven by dispersal
(Baselga et al., 2013; Baselga, Gómez-Rodríguez, & Vogler, 2015) and
has been proposed as a useful way to compare relative dispersal
constraints between lineages from different taxonomic groups
(Gómez-Rodríguez et al., 2019, Múrria et al., 2017). These, and other
studies using a multi-hierarchical approach, have focused from regional
to continental-scale distances. However recent work has also exploited
this framework to analyze community assemblage at finest geographic
scales (<15 km) using cMBC data, while also allowing to
explore hyperdiverse communities, like soil mesofauna (Arribas et al.,
2020). Therefore, applying the cMBC approach to the hyperdiverse
arthropod faunas of tropical mountains offers much potential for
understanding their community structure and the processes that have
shaped it.
Here, we evaluate fine-spatial community patterns within the arthropod
fauna of a tropical sky-island forest, to better understand the roles of
dispersal limitation and landscape features as drivers of the diversity
found in tropical mountains. To do this, we performed a systematic
sampling consisting of 840 pitfall traps across Abies religiosaforests within the Nevado de Toluca, a sky-island from the Transmexican
Volcanic Belt (TMVB). We generated haplotype-level metabarcoding data
for 42 arthropod communities distributed in sampling blocks separated
from 50 m to 19 km, and evaluate patterns of richness, turnover and
distance decay in community similarity at multiple hierarchical levels
(haplotype, putative species (OTU) and supra-specific levels). As we are
interested in the effect of ecological and topographic features on
dispersal limitation, in addition to testing for the effect of
isolation-by-distance (IBD), we also performed an
isolation-by-resistance (IBR) analysis. This allows cost dispersal given
by landscape features to be incorporated, yielding biologically more
informative distance decay relationships than Euclidean distance alone
(McRae, 2006). Our
analytical framework thus allows us to assess the role of dispersal
constraint within a local spatial setting on tropical mountain
diversity.