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Phylogenetic niche conservatism (PNC) shapes the distribution of organisms by constraining lineages to particular climatic conditions. Conversely, if areas with similar climates are geographically isolated, diversification may also be limited by dispersal. Neotropical xeric habitats provide an ideal system to test the relative roles of climate and geography on diversification, as they occur in disjunct areas with similar biotas. Sicariinae sand spiders are intimately associated with these xeric environments, particularly seasonally dry tropical forests (SDTFs) and subtropical deserts/scrublands in Africa (Hexophthalma) and the Neotropics (Sicarius). We explore the role of PNC, geography and biome shifts in their evolution and timing of diversification. We estimated a time-calibrated, total-evidence phylogeny of Sicariinae, and used published distribution records to estimate climatic niche and biome occupancy. Topologies were used for estimating ancestral niches and biome shifts. We used variation partitioning methods to test the relative importance of climate and spatially autocorrelated factors in explaining the spatial variation in phylogenetic structure of Sicarius across the Neotropics. Neotropical Sicarius are ancient and split from their African sister-group around 90 (57–131) million years ago. Most speciation events took place in the Miocene. Sicariinae records can be separated in two groups corresponding to temperate/dry and tropical/seasonally dry climates. The ancestral climatic niche of Sicariinae are temperate/dry areas, with 2–3 shifts to tropical/seasonally dry areas in Sicarius. Similarly, ancestral biomes occupied by the group are temperate and dry (deserts, Mediterranean shrub, temperate grasslands), with 2–3 shifts to tropical, seasonally dry forests and grasslands. Most of the variation in phylogenetic structure is explained by long-distance dispersal limitation that is independent of the measured climatic conditions. Sicariinae have an ancient association to arid lands, suggesting that PNC prevented them from colonizing mesic habitats. However, niches are labile at a smaller scale, with several shifts from deserts to SDTFs. This suggests that PNC and long-distance dispersal limitation played major roles in confining lineages to isolated areas of SDTF/desert over evolutionary history, although shifts between xeric biomes occurred whenever geographical opportunities were presented.
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Molecular Phylogenetics and Evolution https://doi.org/10.1016/j.ympev.2019.106569
© 2019. Licensed under the Creative Commons CC-BY-NC-ND 4.0 license: http://creativecommons.org/licenses/by-nc-nd/4.0/
Phylogeny of Neotropical Sicarius sand spiders suggests frequent
transitions from deserts to dry forests despite antique, broad-scale
niche conservatism
I.L.F. Magalhaes1,2, D.M. Neves3,4, F.R. Santos5, T.H.D.A. Vidigal2, A.D. Brescovit6
and A.J. Santos2
1División Aracnología, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Buenos Aires,
Argentina.2Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas
Gerais, Minas Gerais, Brazil. 3Department of Ecology and Evolutionary Biology, University of Arizona,
Tucson AZ, USA. 4Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de
Minas Gerais, Minas Gerais, Brazil. 5Departamento de Biologia Geral, Instituto de Ciências Biológicas,
Universidade Federal de Minas Gerais. 6Laboratório Especial de Coleções Zoológicas, Instituto
Butantan, São Paulo, Brazil. Correspondence: Ivan L. F. Magalhaes, Av. Ángel Gallardo 470,
C1405DJR, Buenos Aires, Argentina. E-mail: magalhaes@macn.gov.ar.
Highlights
Sand spiders are mostly restricted to African and Neotropical dry forests and
xeric scrublands.
Divergence between African and Neotropical forms occurred during the
Cretaceous.
Speciation events of taxa from Neotropical dry biomes took place in the
Miocene.
Lineages from deserts invaded dry forest habitats 23 times in their history.
Niches are conserved in broad scale (dry vs. mesic) but labile in small scale (dry
vs. dry).
Magalhaes et al.
Niche conservatism and phylogeny of Sicarius
2
Abstract
Phylogenetic niche conservatism (PNC) shapes the distribution of organisms by constraining lineages
to particular climatic conditions. Conversely, if areas with similar climates are geographically
isolated, diversification may also be limited by dispersal. Neotropical xeric habitats provide an ideal
system to test the relative roles of climate and geography on diversification, as they occur in disjunct
areas with similar biotas. Sicariinae sand spiders are intimately associated with these xeric
environments, particularly seasonally dry tropical forests (SDTFs) and subtropical deserts/scrublands
in Africa (Hexophthalma) and the Neotropics (Sicarius). We explore the role of PNC, geography and
biome shifts in their evolution and timing of diversification. We estimated a time-calibrated, total-
evidence phylogeny of Sicariinae, and used published distribution records to estimate climatic niche
and biome occupancy. Topologies were used for estimating ancestral niches and biome shifts. We
used variation partitioning methods to test the relative importance of climate and spatially
autocorrelated factors in explaining the spatial variation in phylogenetic structure of Sicarius across
the Neotropics. Neotropical Sicarius are ancient and split from their African sister-group around 90
(57131) million years ago. Most speciation events took place in the Miocene. Sicariinae records can
be separated in two groups corresponding to temperate/dry and tropical/seasonally dry climates. The
ancestral climatic niche of Sicariinae are temperate/dry areas, with 23 shifts to tropical/seasonally
dry areas in Sicarius. Similarly, ancestral biomes occupied by the group are temperate and dry
(deserts, Mediterranean shrub, temperate grasslands), with 23 shifts to tropical, seasonally dry forests
and grasslands. Most of the variation in phylogenetic structure is explained by long-distance dispersal
limitation that is independent of the measured climatic conditions. Sicariinae have an ancient
association to arid lands, suggesting that PNC prevented them from colonizing mesic habitats.
However, niches are labile at a smaller scale, with several shifts from deserts to SDTFs. This suggests
that PNC and long-distance dispersal limitation played major roles in confining lineages to isolated
areas of SDTF/desert over evolutionary history, although shifts between xeric biomes occurred
whenever geographical opportunities were presented.
Keywords: Atacama, Dry Diagonal, phylogenetic niche conservatism, Pleistocene Arc Hypothesis,
seasonally dry tropical forests, Sicariidae
Magalhaes et al.
Niche conservatism and phylogeny of Sicarius
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1. Introduction
Patterns of variation in species diversity, from communities to biomes, have long
intrigued biogeographers. Different biomes have different biotic composition, and to
understand how such diversity was attained it is crucial to assess the relative importance
of biome conservatism vs. biome switching (Crisp et al., 2009). The biome conservatism
hypothesis predicts that lineages tend to retain their ancestral ecological traits, and that
colonization of novel biomes over evolutionary history is rare. This is mainly due to
phylogenetic niche conservatism (PNC), which has been defined as an evolutionary
process in which related species are more similar in the ecological niche they occupy
than would be expected by chance (Losos, 2008). Empirical evidence for the biome
conservatism hypothesis, however, is controversial and largely focused on testing biome
conservatism vs. switching in plant lineages (but see Antonelli et al., 2018). Studies
addressing the potential contribution of conservatism in Neotropical biomes are
relatively scant (see Donoghue & Edwards 2014 for a review). One of such few studies
showed, for instance, an unexpected high degree of biome switching between wet
forests and savannas in South American plant lineages (Simon et al., 2009). This
indicates that biome conservatism might not be as common as suggested in the
literature. On the other hand, niches are always conserved to some extent, and it is
expected that related species occupy similar biomes (Wiens & Graham, 2005). Thus, to
better understand the distribution of organisms we should not only investigate if the
niches are conserved or not, but also identify at what level niche shifts happened.
Besides wet forests and savannas, the Neotropical region also houses a
considerable extent of drought-associated biomes (henceforth dry biomes). These
biomes harbour unique species and lineage diversity (Pennington et al., 2009;
DRYFLOR, 2016), but are often overlooked in studies aiming at understanding the
assembly of the Neotropical biota. Studying dry biomes is no easy task because they
occur in several disjunct areas, or nuclei, scattered along the Neotropical region
(Pennington et al., 2000; Werneck, 2011; see also Fig. 1). Despite their current
geographical isolation, a significant part of the biota of these nuclei is shared among
them, at least at the generic or family levels (Prado & Gibbs, 1993; Pennington et al.,
2000; Werneck, 2011; Magalhaes et al., 2017). Some authors have argued that such
fragmented distribution has persisted over long enough evolutionary timescales to have
influenced the evolution and biogeography of dry biomes (Pennington et al., 2009). This
Magalhaes et al.
Niche conservatism and phylogeny of Sicarius
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led to the prediction that, due to historical dispersal limitation associated with island
biogeographic rules, there is high geographical structure in phylogenetic relatedness in
dry biomes (Pennington et al., 2009). This pattern holds for plant lineages (Lavin,
2006), with closely-related taxa tending to occupy the same nuclei. This suggests that
dispersal limitation plays a prominent role in the assembly of the biota of Neotropical
dry biomes. However, dry biomes are a heterogeneous assemblage, ranging from
warmer, seasonally dry tropical forests (SDTFs) to subtropical deserts, where climatic
conditions are more unpredictable. This finer-scale variation in climatic conditions
could also have shaped the diversification of organisms associated with dry biomes,
especially if these are evolving under strong phylogenetic niche conservatism.
Nonetheless, this question remains unexplored.
The evolutionary timing is a third factor that should be taken in to account to
understand processes of biome shift or conservatism. Older lineages likely have had
more opportunities to either shift between biomes or to colonize distant areas with
similar conditions. The timing of assembly of Neotropical dry biomes is still a matter of
discussion. It has been hypothesized that these dry biomes share a significant portion of
their biota because they have been connected in the past. Influential studies have
suggested that these connections may have taken place in the drier, colder periods of the
Pleistocene the Pleistocene arc hypothesis (PAH) (Prado & Gibbs 1993, Pennington et
al. 2000). This hypothesis predict that lineages from different SDTF nuclei should have
diverged recently, no later than the Pleistocene. However, many phylogenetic studies of
taxa associated to SDTFs have found divergence times that are much deeper than the
ones expected by the PAH, mostly in the Miocene (Pennington et al., 2004; Werneck et
al., 2012; Beati et al., 2013; Magalhaes et al. 2014; Côrtes et al., 2015). While it seems
likely that Neotropical dry biomes have been connected in the past, the timing and
causes of such events remain unclear. Dated phylogenies would not only shed light on
this question, but also put niche conservatism in a time scale and allow quantifying the
number of niche shifts in a given period of evolutionary time.
A sound phylogenetic basis is fundamental to addressing these biogeographical
questions. There are several dated, large-scale phylogenetic studies of plants associated
with dry environments, particularly SDTFs (e.g. Pennington et al., 2004; Côrtes et al.,
2015). However, there is only a handful of phylogenies focusing on animals from
Neotropical dry biomes,(e.g. Werneck et al. 2012; Beati et al., 2013; Palma et al., 2014;
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Niche conservatism and phylogeny of Sicarius
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Lanna et al., 2018; Fonseca et al., 2018). The majority of these studies included only a
few focal species, are geographically restricted, and do not cover the wide range of
climatic conditions within the dry biomes. The focal group of this study, the sand
spiders (subfamily Sicariinae), are a particularly interesting model to study the evolution
dry biomes. These spiders are widespread and restricted to several SDTF nuclei, deserts
and xeric scrublands in America and Africa. These medium to large spiders have special
setae that adhere to soil particles, so they are able to camouflage on the ground to
ambush their prey. The subfamily includes two genera: the 21 species of Sicarius
Walckenaer, 1867 occur in South and Central America, while the eight species of
Hexophthalma Karsch, 1879, are restricted to southern Africa (Magalhaes et al., 2017;
Lotz, 2018). Sicariids seem to be very poor dispersers: their diversity is highly
structured geographically (Binford et al. 2008, Magalhaes et al., 2014; 2017) and they
do not disperse by ballooning (rafting in the wind using silk strands, often over long
distances) (see Binford et al. 2008). The divergence between the Sicarius and
Hexophthalma has been estimated to have occurred before the separation of South
America and Africa (Binford et al., 2008). Thus, these genera have long evolutionary
history spanning most of the major geological events that could have shaped current
Neotropical and southern African biodiversity. Their ancient association with a wide
array of dry environments suggests that niche conservatism might play an important role
in their evolution. All of this suggests they would be excellent models to test the relative
roles of niche conservatism and dispersal limitation in the diversification of a dry-
associated group of organisms.
To increase our understanding of the biogeographic history of Neotropical dry
biomes, we examined the timing of diversification of Sicariinae lineages and explored
the relative importance of historical dispersal limitation and phylogenetic niche
conservatism in explaining their current distribution. We focused particularly on
Sicarius because this genus is more diverse, occupies a wider range of climatic
conditions and biomes, and has a more disjunct distribution, and thus is an ideal model
to explore these questions. We gathered a comprehensive, specialist-based dataset on
the distribution of Sicariinae species, characterized the climatic space occupied by these
spiders, and generated a robust, dated phylogeny for the subfamily based on multiple
gene regions and morphological data. Specifically, we established three hypotheses to
test whether patterns of phylogenetic niche conservatism and dispersal limitation shaped
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Niche conservatism and phylogeny of Sicarius
6
the evolutionary history of Sicarius: (H1) phylogenetic niche conservatism was a major
force shaping the distribution of Sicarius, and lineages inhabiting SDTFs and deserts are
reciprocally monophyletic; (H2) due to historical dispersal limitation within each of
these two groups closely related species occur in geographically close areas; and (H3)
divergence among Sicarius species pre-date the Pleistocene, suggesting that
phylogenetic niche conservatism has persisted over long evolutionary timescales.
2. Material and methods
2.1. Sicariinae distribution, biome occupancy and characterization of
climatic niche. Georeferenced records of Sicarius and Hexophthalma were obtained
from Magalhaes et al. (2017) and Lotz (2012), representing virtually all the published
records of the subfamily to date (available as online Supp. file S8). We took two
complementary approaches to investigate the biomes and climatic niches occupied by
Sicariinae spiders. To characterize biome occupancy, we sorted Sicariinae records using
the biome classification of Olson et al. (2001), with two modifications following
Echeverría-Londoño et al. (2018): the Caatinga and the Chaco have been re-classified as
a tropical dry forest and a xeric shrubland, respectively. To summarize fine-scale
climatic variation, we extracted values for 21 environmental variables for each unique
record: altitude, the 19 bioclimatic variables available at WorldClim (Hijmans et al.,
2005; see a complete list of the variables in the legend of Supp. Figure S1), and an
annual aridity index (Zomer et al., 2006). We then performed a principal component
analysis (PCA) based on a correlation matrix to reduce the dimensionality of the
variable matrix using PAST 2.17c (Hammer et al., 2001). The results indicate that the
first component (PC1) constrains 42.9% of the variation in climatic data associated with
Sicariinae records (PC1; see Fig. 1 and section 3.1 below). Because the second
component constrained a smaller variation in climatic data, and to avoid overfitting in
the variation partitioning analysis, only PC1 was used in further analysis (see section
2.5 below).
2.2. Collection and analysis of sequence data. Specimens for DNA extraction
(see Supp. file S9) were preferably collected in 96º ethanol and kept at -20 ºC, or
collected at 7080º ethanol and kept at room temperature for at most four years before
DNA extraction. DNA was extracted from leg muscle using a Promega Wizard®
Genomic DNA Purification Kit. Four target regions have been amplified and sequenced,
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Niche conservatism and phylogeny of Sicarius
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two mitochondrial and two nuclear: (1) part of the Cytochrome c-Oxidase subunit I
(COI) gene; (2) a fragment including the 3’ end of the 16S ribosomal subunit gene
(16S), containing the entire tRNA-leucine gene and the 5’ end of the nitrate
dehydrogenase 1 gene; (3) part of the Histone 3, subunit A (H3) gene; and (4) part of
the 28S large ribosomal subunit gene (28S). Primers and PCR conditions for amplifying
COI and H3 follow Magalhaes et al. (2014), and for 16S and 28S follow Binford et al.
(2008). In some cases, the 16S fragments were amplified using the pair N1J736 (5'-
AAG-AGT-TTG-ATT-GCR-TCS-T-3') and LRN1634-SIC (5'-YGT-GST-AAG-GTA-
GCA-TAA-T-3') (G.J. Binford, unpublished), with an annealing temperature of 4850
ºC. All primer sequences and annealing temperatures are provided as online Supp. file
S10. PCR success was checked on 1% agarose gel stained with GelRed® (Biotium).
PCR products were purified using a NaCl + 20% 8000 polyethyleneglycol solution and
washes in 80º ethanol, and then sequenced in both directions (COI, 16S, H3) or using
internal primers (28S) on an ABI 3130xl Genetic Analyzer (Applied Biosystems). Some
sequences from Binford et al. (2008) available from GenBank were used to complement
our data (see Supp. file S9). Newly generated sequences are available from GenBank
(MN216032MN216141, COI; MN242267MN242348, 16S; MN207491MN207584,
H3; MN219594MN219633, 28S).
2.3. Phylogenetic analyses. Sequences of each marker were aligned using
Muscle (Edgar, 2004) in MEGA 6 (Tamura et al., 2013). We checked all gene regions for
saturation using a homogeneity test in TreePuzzle 5.2 (Schmidt et al. 2002). The
nucleotides in the third codon position of the COI fragment of some sequences failed
the homogeneity test, and thus this position was analysed in a separate partition. For
each of the four fragments sequenced, best-fitting models of evolution were selected
using jModeltest 2.1.10 (Darriba et al. 2012) based on maximum-likelihood optimized
trees, and using AIC as a selection criterion. The final matrix with the four concatenated
markers contains 4327 aligned positions (COI, 1009 bp; H3, 324; 16S-tLeu-ND1, 924;
28S, 2070) (see Supp. file S11). We assembled two matrices, one sampling multiple
individuals per species (large dataset: 145 terminals, 54.6% missing data or gaps) and
another reduced one, with a single individual per species, for the dating analysis using
BEAST (small dataset: 35 terminals, 40.9% missing data or gaps).
We were able to gather morphological data and sequences of up to four
molecular markers for 19 out of 21 Sicarius species and seven Hexophthalma species.
Magalhaes et al.
Niche conservatism and phylogeny of Sicarius
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Thirteen Loxosceles species, Drymusa serrana (Drymusidae) and Ochyrocera diablo
(Ochyroceratidae) were included as outgroups, and the trees have been rooted using
Physocyclus globosus (Pholcidae). In most cases, samples cover several portions of the
geographical range of each Sicariinae species. Sicarius species for which we have no
sequence data include the narrow-ranged S. andinus from Peru and S. utriformis from
Galapagos. The matrix of morphological characters of Magalhaes et al. (2017) has been
used in conjunction with the sequence data for the total-evidence analyses. As BEAST
2.5.2 (Bouckaert et al. 2014) does not handle ordered multistate discrete characters, we
have re-coded these as binary characters; we also included three terminals not
previously included in the matrix, S. vallenato, D. serrana, and O. diablo. This
modified morphological matrix contains 112 characters (see Supp file. S13).
Topologies for the large dataset were obtained using Bayesian inference in
MrBayes 3.2 (Ronquist et al., 2012). Nucleotide substitution models were specified for
each partition based on the results of jModelTest and a MKv + Γ model was specified
for the morphological partition. Preliminary runs had shown that S. andinus was acting
as a rogue taxon due to the lack of sequence data, so we ran an additional analysis
excluding this terminal to re-evaluate clade support in its absence. We also ran an
analysis based only on the sequence data (and excluding the two species for which we
had no sequences). For each dataset, two runs with four Markov chains each (one
heated) were sampled at 3000 intervals along 30 million generations; the first 25%
samples were discarded as burn-in, and a majority-rule consensus of the remaining trees
was obtained using the sumt command in MrBayes 3.2. Stationarity and mixing of the
chains were checked in Tracer 1.7 (Rambaut et al., 2018). All Bayesian analyses were
performed remotely using the CIPRES portal (Miller et al., 2010). Sequence alignments
and inputs for Bayesian analyses are available as online Supp. file S11.
2.4. Divergence dating. Clade ages were estimated while accounting for
phylogenetic uncertainty in BEAST 2.5.2 using the small dataset. Absolute ages can only
be obtained by fixing calibration points (e.g. with fossils), by using a known
substitution rate, or a combination of both. Here we explore the sensitivity of age
estimates by testing different calibration schemes. There are no records of Sicariinae
fossils, but its sister group, Loxosceles, is represented in Miocene amber inclusions from
Dominican Republic (Wunderlich, 1988) that are at least 15 million years (My) old
(Iturralde-Vinent & MacPhee, 1996). We also calibrate the divergence between
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Niche conservatism and phylogeny of Sicarius
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Drymusidae and Ochyroceratidae based on the age of Priscaleclercera Wunderlich, a
genus from Burmese amber estimated to be at least 98.17 My old (Shi et al. 2012).
Additionally, Bidegaray-Batista & Arnedo (2011) estimated substitution rates for
several genes commonly employed in phylogenetic studies using a dataset of
Dysderidae spiders. To incorporate this information in our analyses (i.e., fossil and
substitution rates), we took four approaches (Table 1):
1) Fossil, including two calibration points: (a) a uniform prior (bounds of 15
450 million years) for the age of the split between L. laeta and L. deserta
based on Dominican amber Loxosceles; this assumes the fossil species
belong in the L. laeta species group, which is supported by the male palpal
morphology: fossils have a long, slender, curved embolus similar to extant L.
rufipes and related species (see Wunderlich, 1988); (b) a uniform prior
(bounds of 98.17450 million years) for the age of the split between
Drymusa and Ochyrocera based on Priscaleclercera: this fossil genus shares
with extant ochyroceratids the possession of six eyes, a protruding clypeus, a
bulb with fused tegulum and subtegulum with a complex apical portion, bulb
situated terminally to the cymbium, and cymbium bearing a stout macroseta
(see Wunderlich, 2017). We used a uniform prior distribution on node ages
because this makes the least assumptions regarding the time of appearance of
the clade in relation to the known fossils. We use 450 as a conservative hard
maximum because the first fully terrestrial arthropods appear in the fossil
record no earlier than 435 My ago (Wolfe et al., 2016), and thus it is very
unlikely that the groups treated here had appeared by that time (a reasoning
proposed by Benton & Donoghue, 2007).
2) H3, incorporating the substitution rate of this gene estimated by Bidegaray-
Batista & Arnedo (2011) as a prior to its clock rate. We set the H3.ucld.mean
prior to have a normal distribution with a mean of 0.00108 and a SD of
0.000244, so that the 95% confidence interval matches the interval in
Bidegaray-Batista & Arnedo (2011). We have refrained from including the
estimated substitution rates of other genes because they are not directly
comparable between our study and that of Bidegaray-Batista & Arnedo
(2011): we have analysed the third codon position of COI separately, have
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Niche conservatism and phylogeny of Sicarius
10
analysed 16S and ND1 under a single partition, and have amplified a
different portion of the 28S gene due to the set of primers used.
3) Fossil+H3, combining the two approaches described above.
4) Fossil+H3+Gondwana, combining the approach Fossil+H3 with uniform
priors (bounds of 100450 million years) for the time of the splits between
Sicarius and Hexophthalma, and L. vonwredei and South American
Loxosceles; this run was intended to enforce the separation between African
and American taxa to be at least 100 million years old, which is a
conservative estimate of the last physical connection of the two continents
(some authors argue that they have been separated for at least 120 million
years; reviewed in Upchurch, 2008).
In all cases, at least three Markov chains were run for 30 million generations,
sampling parameters every 3,000 generations. Site and clock models were unlinked
across the different markers, nucleotide models were specified as per the results of
jModelTest, and a single tree partition was used. We ran preliminary runs comparing
different tree priors and clock models for the Fossil+H3 dataset: (a) Yule tree prior +
exponential relaxed clock, (b) Yule tree prior + lognormal relaxed clock, (a) birth-death
(BD) tree prior + exponential relaxed clock, (a) BD tree prior + lognormal relaxed
clock. Comparison of the likelihood using the AICm method (Baele et al. 2012) in
Tracer 1.6 indicated that the BD tree prior + exponential clock is favoured, and thus the
tree prior was set to a speciation birth-death process and the clock model of all
partitions was set to an exponential relaxed clock. At any rates, topology and age
estimates are qualitatively identical regardless of tree and clock priors (data not shown),
indicating that the choice of a particular combination of them does not affect our results.
Convergence and stationarity of chains and ESS values were checked in Tracer 1.7. The
first 10% states were discarded as burn-in in LogCombiner 2.5.2, and maximum clade
credibility trees with median heights were obtained using TreeAnnotator 2.5.2.
Uncertainty in age estimates was assessed by evaluating their highest posterior density
(HPD) intervals.
2.5. Reconstruction of ancestral niche and ancestral biomes. For each
Sicariinae species included in our dataset, we calculated the average of PC1 values
across all individual records of that species. We also coded species according to the
biomes where they occur: (1) tropical and subtropical moist broadleaf forests, (2)
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Niche conservatism and phylogeny of Sicarius
11
tropical and subtropical dry broadleaf forests, (3) temperate broadleaf and mixed
forests, (4) tropical and subtropical grasslands, savannas, and shrublands, (5) temperate
grasslands, savannas, and shrublands, (6) montane grasslands and shrublands, (7)
Mediterranean forests, woodlands, and shrub and (8) deserts and xeric shrublands.
Species occurring in more than one biome were coded as polymorphic (except when a
biome was represented by only one or two records per species). We optimized the
values of PC1 and biome occurrence on the trees obtained using the small dataset.
Ancestral states were reconstructed under maximum parsimony using the Trace
Character History option in Mesquite 3.04 (Maddison & Maddison, 2017).
2.6. Decomposition of phylogenetic relatedness. We investigated whether the
distribution patterns of Sicariinae lineages across the Neotropics were mainly limited by
climate (e.g. closely related lineages occupy similar climatic conditions regardless of
spatial proximity) or spatially autocorrelated factors (spatial structure that is
independent of the measured climatic factor). First, we decomposed the phylogenetic
relationships of Sicarius lineages into eigenvectors through a principal coordinates
analysis (PCoA), which represent the phylogenetic distances among taxa while
correcting for statistical dependence. To represent the spatial component, we
summarized the distribution of each species by averaging the latitude and longitude of
its records to generate a geographic distance matrix among the species. We then used
this matrix to generate spatial eigenvectors stemming from principal coordinates of
neighbour matrices (PCNMs; Borcard et al., 2004). Briefly explained, the first step of
this analysis is to compute the PCoA of a matrix built from geographic distances among
all sampling sites and truncated for distances larger than a cut-off set a priori to retain
only neighbouring distances. The eigenvalues of this PCoA describe orthogonal multi-
scale spatial variables. In other words, PCNMs are distance-based variables capable of
describing spatial organisation among sites at different spatial scales. As explained
elsewhere (Borcard & Legendre, 2002; Peres Neto, et al., 2006), larger eigenvalues are
associated with broader spatial scale structures while smaller eigenvalues represent fine-
scale spatial structures. We then obtained the relative contribution of climatic (PC1; see
Fig. 1) and spatially autocorrelated factors (PCNMs) in explaining variation in
phylogenetic relatedness across the Neotropics by (1) compiling significant spatial
variables through a forward selection method for generalized linear models, with a
permutation-based test for each variable added (Borcard et al., 2011); and (2)
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Niche conservatism and phylogeny of Sicarius
12
partitioning the variation of the phylogenetic eigenvectors with respect to the significant
spatial and environmental variables (Desdevides et al. 2003; Blanchet et al. 2008;
Borcard et al. 2011; Legendre et al. 2012). We also mapped phylogenetic eigenvectors
on to the phylogeny by interpolating states at internal branches through a maximum
likelihood ancestral state reconstruction (Schluter et al., 1997). Finally, we explored the
results visually by plotting in geographic space (1) the distribution of Sicarius lineages,
(2) their decomposed phylogenetic relatedness, and (3) the variation of significant
spatial and environmental variables. The variable selection and variation partitioning
were conducted using the fields (Nychka et al., 2015) and vegan (Oksanen et al., 2016)
packages in R. We conducted the phylogenetic and geographical mapping using the R
packages phytools (Revell, 2012) and maptools (Lewin-Koh & Bivand, 2012),
respectively.
3. Results
3.1. Characterization of climatic space and biome occupancy. All variables
indicative of higher temperatures and precipitation correlate positively with PC1, while
those indicative of higher daily/annual variation in temperatures and precipitation
correlate negatively (Supp. Fig. S1). Biologically, we interpret higher values of PC1 as
representing areas with hotter, wetter, and more stable climates. A visual inspection of
the frequency histogram of PC1 values associated with Sicariinae records indicates a
clear bimodal distribution allowing us to define two discrete groups (Fig. 1C). When
confronted with the geographic origin of the records (Fig. 1B), it is clear that the group
of records associated with values of PC1 lower than 0.5 represent temperate dry areas,
and the group with values of PC1 higher than 0.5 represent tropical, seasonally dry
areas. Regarding biome occupancy, Sicariinae records come mainly from dry biomes,
such as Mediterranean forests, woodlands, and shrub (217 records), deserts and xeric
shrublands (196 records) and tropical and subtropical dry broadleaf forests (126
records) (Table 2). Interestingly, there is a broad correlation between biomes and the
two groups inferred from climatic data (Table 2, Supp. Fig. S3): records from areas with
PC < 0.5 are most commonly found in Mediterranean forests and shrub, deserts and
xeric shrublands and temperate grasslands, while records from areas with PC > 0.5 are
most common in dry and moist tropical and subtropical forests and tropical grasslands
and savannas.
Magalhaes et al.
Niche conservatism and phylogeny of Sicarius
13
3.2. Phylogenetic analyses. Both Hexophthalma and Sicarius are strongly
supported (Figs 23, Supp. Fig. S2). Most of the smaller Sicarius clades identified in
the morphological analysis of Magalhaes et al. (2017) have been recovered here with
good support, but the deeper relationships of the genus have been resolved differently
upon the inclusion of sequence data. The two species from the Monte (xeric scrublands
of Argentina), S. mapuche and S. rupestris, form a clade (A) that is sister to all other
Sicarius. The remaining species are divided in three large groups. The first (clade B)
includes S. gracilis, S. peruensis (both from coastal Peru) and S. utriformis (Galapagos),
the second (clade C) includes S. yurensis and S. thomisoides from the Sechura and
Atacama deserts, respectively, and the third (clade D) includes all the remaining
species; relationships between clades B, C and D are unresolved or have negligible
support. Clade D is subdivided in a group with three small species from the Chilean
coast (clade E) and a clade (F) formed by S. boliviensis from the Chiquitano dry forests
of Bolivia, S. andinus from inter-Andean dry valleys in Peru, S. levii from the
Argentinian Monte, S. rugosus from dry forests in Central America, S. vallenato from
the dry north of Colombia and the six species from the Brazilian Caatinga dry forests
(clade J). The phylogenetic position of S. vallenato is here assessed for the first time and
the species is recovered as sister to S. rugosus with high support (clade I), and this pair
forms a clade (H) with the Caatinga species (clade J). The position of S. andinus is
highly unstable as we lack sequence data for this species and it shows no clear
morphological synapomorphies with other Sicarius. Our analysis most frequently places
it as sister to S. boliviensis, but the support is very low; removing S. andinus from the
analysis results in much greater nodal support across clade D (Figs 2, 3). The
relationships among Sicarius species have a strong geographical component: usually,
closely related species occur in adjacent geographical areas. For example, the three
species from Peru, Ecuador and the Galapagos (clade B), the three small species from
the Chilean coast (clade E), and the six species from the Brazilian Caatinga (clade J)
form well-supported monophyletic groups. The dated tree obtained using BEAST (Fig. 3)
has an essentially similar topology as that recovered by MrBayes (Fig. 2); the smaller
tree obtained with BEAST (Fig. 3) was used for further analyses (reconstruction of
ancestral niches and variation partitioning).
3.3. Divergence dating. The results from the four different dating schemes are
summarized in Table 1. Using only fossil data or only the H3 substitution rate to
Magalhaes et al.
Niche conservatism and phylogeny of Sicarius
14
calibrate the molecular clock results in similar mean ages, although the confidence
intervals are much wider when using the substitution rate alone. Combining the fossil
calibration and H3 rates results in slightly older mean clade ages with relatively wide
confidence intervals. Since this approach makes the best use of previous knowledge, we
have chosen this as our working hypothesis (Fig. 3). Including a biogeographic
calibration taken from the break-up of western Gondwana results in much older
estimates for clade ages (Table 1). As the hypotheses we test in this paper are mainly
biogeographic, it might result in circular reasoning to choose this last calibration
scheme as our working hypothesis. These results are included here for comparison only
and should be taken with extreme caution. However, they indicate that the divergences
among Sicariinae might be even older than the ones obtained under other calibration
schemes.
Our estimates (Fig. 3; Table 1) indicate that the first split within Sicariidae
occurred at least 113.5 million years ago (Mya) (74.3163.5, 95% highest posterior
density interval; HPD). Regarding continental disjunctions, the split between African L.
vonwredei and the clade containing New World Loxosceles took place at 72.1 Mya
(HPD 42.5107.6), while the split between Hexophthalma and Sicarius is older and
dates to 89.7 Mya (HPD 57.6131.1). Sicarius has been diversifying in the New World
for at least 55.6 million years (HPD 34.280.7), and most speciation events took place
in the Miocene (Fig. 3). For instance, Sicarius yurensis (from the Sechura desert) and S.
thomisoides (from the Atacama Desert) diverged at 23.8 Mya (HPD 9.5 40). The split
between S. peruensis and S. utriformis was estimated to be at least 9.7 Mya (1.222.2).
The Caatinga clade has been diversifying for at least 20.2 million years (HPD 11.6
30.5). Sicarius rugosus and S. vallenato diverged at 16.2 Myr (6.227.6). All consensus
trees resulting from MrBayes or BEAST analyses are available as online Supp. File S12.
3.4. Reconstruction of ancestral niche and ancestral biomes. Optimizations
based on parsimony (Fig. 3) suggest that the ancestral climatic niche of Sicariinae
spiders are temperate/dry areas. This results mainly from the fact that Hexophthalma
exclusively inhabits localities with this climate, and that Sicarius coming from warmer,
seasonally dry habitats are deeply nested in clades containing mostly species inhabiting
temperate/dry areas (Fig. 3). Our optimizations suggest that Sicarius have shifted from
temperate/dry areas to tropical/seasonally dry areas at least 23 times during its
evolutionary history. The shifting lineages are S. utriformis and clade F. The
Magalhaes et al.
Niche conservatism and phylogeny of Sicarius
15
optimization at the base of clade F is ambiguous, making it difficult to untangle its
biogeographic history: either there were two independent invasions of
tropical/seasonally dry areas (one in S. boliviensis+S. andinus, and the other in clade H),
or the ancestor of the entire clade has shifted to tropical/seasonally dry areas a single
time, and the lineage containing S. levii has later returned to a temperate/dry
environment. It should be noted that while most populations of S. gracilis are found in
the Peruvian coastal desert, at least some populations inhabit SDTFs of northern Peru
and southern Ecuador, and this may represent a fourth shift of temperate/dry areas to
tropical/seasonally dry areas that was not captured by our optimization (Fig. 3).
The reconstruction of ancestral biomes yields essentially similar results (Supp.
Fig. S3). The earliest lineages of Sicariinae occupy deserts and xeric scrublands,
Mediterranean shrub or temperate grasslands. At least 23 shifts to dry tropical forests
were inferred, one of them in S. gracilis. Again, the optimization at the base of clade F
is ambiguous, with either (1) a shift to tropical dry forests at its base, with S. levii later
re-invading xeric scrublands, or (2) two independent shifts to dry forests, one in S.
boliviensis+S. andinus and the other in clade H.
3.5. Decomposition of phylogenetic relatedness. The first three PCoA axes
(henceforth PCoA13) constrain 60% of the variance in phylogenetic relatedness in
Sicarius lineages found across the Neotropics, and there was a negligible increase in
constrained variance by adding a fourth PCoA axis (< 10%). PCoA1 constrains 27% of
the variance and segregates lineages found in deserts (blue-green spectrum in Fig. 4a)
from lineages found in SDTFs (red spectrum in Fig. 4a,b) and in the northern
Argentinean Monte (yellow spectrum in Fig. 4a,b). The first and sixth PCNM axes,
which describe positive large to intermediate-scale spatial autocorrelation, account for
67% of the deviance in PCoA1, with 20% of this occurring independently of the
environmental fraction summarized by the PC1 (see Supp. Table S7 for variation
partitioning fractions). The second PCoA axis constrains 18% of the variance and
segregates lineages found in the southern Argentinian Monte from lineages in the
northern Atacama deserts, and these two clades from all others (red spectrum in Fig.
4c,d) . The second and third PCNM axes, which describe positive large-scale spatial
autocorrelation, account for 50% of the deviance in PCoA2. There is no evidence of
intrinsic environmental conditions (namely PC1) controlling the variation in
phylogenetic relatedness summarized by the second PCoA axis. PCoA3 constrains 15%
Magalhaes et al.
Niche conservatism and phylogeny of Sicarius
16
of the variance in phylogenetic relatedness. Within the desert-southern Monte group
(blue-green spectrum in Fig. 4a,b), PCoA3 segregates lineages found in the southern
Atacama Desert (red-green spectrum in Fig. 4e,f) from all others. Within the SDTF-
northern Monte group (red-yellow spectrum in Fig. 4a,b), PCoA3 segregates lineages
found in Chiquitania (S. boliviensis), inter-Andean valleys (S. andinus) and northern
Monte (S. levii) (green spectrum in Fig. 4e,f) from all others. The first PCNM axis
accounts for 30% of the deviance in the third PCoA axis, with 11% of this occurring
independently of the environmental fraction summarized by the PC1 (Supp. Table S7).
These results indicate that phylogenetic relatedness summarized by the first and
third PCoA axes decreases with large and intermediate-scale geographic distances, and
increasing distances are partially associated with variation in aridity. Thus, lineages
from adjacent SDTF (or desert) nuclei are more closely related than lineages from (i)
distant SDTF nuclei, (ii) distant desert nuclei, and (iii) any combination of distant desert
and SDTF nuclei. There is no evidence of intrinsic environmental conditions (namely
PC1) controlling the variation in phylogenetic relatedness summarized by the second
PCoA axis, indicating that lineages from adjacent deserts and SDTFs are more closely
related than lineages from (i) distant desert nuclei, and (ii) distant SDTF nuclei (Fig. 4,
Supp. Table S7).
4. Discussion
Estimated divergence between species of spider groups that occur in different
continents are frequently much younger than the break-up of ancient landmasses, and
their present distribution is best explained by recent long-distance dispersal (e.g.,
euophryine salticids, Zhang & Maddison, 2013; nephiline araneids, Kuntner et al. 2013;
lycosids, Piacentini & Ramírez, 2019; but see Chousou-Polydouri et al. 2019 for
evidence of continental vicariance in orsolobids). In contrast, our results indicate that
extant Sicariinae started diversifying at least 90 million years ago, with confidence
intervals overlapping the estimates of the western Gondwana break-up (see Upchurch,
2008). This suggests that the split between African and American Sicariinae has been
driven by continental drift, with no subsequent cross-Atlantic dispersal events. More
interestingly, the old divergences within Sicarius indicate that these spiders have a long
history of association to South American xeric environments. Deep divergences
(Miocene or earlier) have been reported for some organisms associated with SDTFs and
Magalhaes et al.
Niche conservatism and phylogeny of Sicarius
17
portions of the Dry Diagonal (Pennington et al. 2004; Särkinen et al., 2012; Werneck et
al., 2012; Lanna et al., 2018; Fonseca et al., 2018), and our results add to the growing
body of evidence that Neotropical xeric and seasonally dry environments have stood as
cohesive biogeographic units for a long evolutionary time.
It has been suggested that SDTFs experienced expansions in their range during
Pleistocene cool periods (Prado & Gibbs, 1993; Pennington et al., 2000). Since most
Sicarius species is restricted to a single SDTF nucleus, our results indicate that Sicarius
were not able to take these opportunities to expand their ranges and colonize distant
xeric areas, or that there have been no Pleistocene SDTF expansions at all. In agreement
with this second scenario, phylogeographic studies do not show evidence of population
expansion of dry biome taxa during the Pleistocene (Werneck et al., 2012; Magalhaes et
al., 2014; Vieira et al., 2015; Thomé et al., 2016; Bartoleti et al., 2017). Our results are
the first evidence that this pattern also holds at the interspecific level. Sicarius spiders
are incapable of ballooning, and their geographic structure suggests they are poor long-
distance dispersers (see below). Thus, it is unlikely they have been able to cross large
patches of unsuitable habitats. Considering their wide, disjunct current distribution, it
seems that presently isolated Neotropical xeric areas have been connected in the past
and acted as corridors for the dispersal of Sicarius. Basing on our estimates of
divergence times (Fig. 3), these connections most likely took place in early to mid-
Miocene. We therefore emphasize that future studies should test hypotheses considering
climatic and geological events older than Pleistocene cooling periods to explain the
connections among SDTF/deserts (e.g. marine transgressions; C4 grassland expansions;
Andean / Brazilian plateau uplifts; see also Werneck, 2011).
Sicariinae are exclusively found in arid and semi-arid regions (Fig. 1, online
Supp. Figs S3, S4, S5). They have been diversifying for at least 90 Myr and were never
able to colonize mesic habitats during this long evolutionary time. This indicates that
phylogenetic niche conservatism (PNC) is playing a major role in their evolution by
confining the entire clade to xeric habitats (Figs 1, 3, Supp. Fig. S3). Whatever they are,
the biological limitations that prevent these spiders from living in mesic habitats are
probably the major factor explaining their current distribution. Given that PNC plays
such a strong role in their evolution, we expected that there would also be few shifts
between dry biomes. Within xeric environments, however, niches are more labile, and
these spiders have been able to shift between dry areas with distinct climates. Our
Magalhaes et al.
Niche conservatism and phylogeny of Sicarius
18
optimizations recover at least 2 or 3 shifts from temperate, dry to warmer, seasonally
dry tropical areas (Fig. 3). This indicates that colonization of areas with novel climates
was frequent within the genus, as 14% of the 21 speciation events represented in Fig. 3
were associated with a major climatic shift. Interestingly, our results recover shifts from
drier biomes (deserts, Mediterranean shrub) to SDTFs (Fig. S3), which have higher
precipitation. Previous studies focusing on biome shifts of arid-associated organisms
have found a converse pattern, with species from deserts repeatedly originating from
ancestors inhabiting more humid climates (Heibl et al., 2012; Rix et al., 2017; Cardillo
et al., 2017).
What roles do geography and climate play in shaping the history of Sicarius in
Neotropical dry biomes? The diversity of Sicarius is strongly structured geographically,
with closely related species mainly occurring in adjacent areas (Figs 2, 3, 4). This strong
geographic structure is also observed in gene trees at the intraspecific level (online
Supp. Fig. S6; Magalhaes et al., 2014). Theoretical models indicate that geographically
structured clades can show high phylogenetic signal in climatic niche merely because of
stochastic geographic processes taking place during speciation (Coelho et al. 2019). As
a consequence, one might overestimate the importance of phylogenetic niche
conservatism if geography is not taken into account. For instance, we have recovered
one lineage entirely associated to dry forests that are currently isolated: S. rugosus from
Central America, S. vallenato from Colombia, and the six species from the Brazilian
Caatinga (Fig. 3, clade H). Could this clade be evolving under strong PNC in a smaller
scale, since the eight species occupy similar biomes and climatic niches, but are
dispersed over a vast geographical area? Here, we addressed this question by explicitly
testing the correlation of geography and climate with the phylogeny. We find that most
of the variation in phylogenetic relatedness in Sicarius is not explained by the measured
climatic conditions (PC1) alone, but rather by a combination of climate and other
spatially structured factors (Fig. 4, Supp. Table S7). This indicates that phylogenetic
distance among taxa is correlated with geographic distance, and this correlation is even
greater when climatic distance is taken into account. We hypothesize that although PNC
in climate plays a role in confining clades to either deserts or SDTFs, spatially
structured factors, either stochastic or deterministic (e.g., unmeasured spatially
structured environmental conditions), were likely more important in Sicarius evolution.
In agreement with this, some Sicarius lineages from a given desert are more closely
Magalhaes et al.
Niche conservatism and phylogeny of Sicarius
19
related to lineages from adjacent SDTFs than they are to those of geographically distant
deserts (e.g. S. gracilis and S. peruensis; S. levii and S. boliviensis). In addition, our
phylogeny suggests that desert lineages have shifted to SDTF multiple times over their
evolutionary history. Overall, it seems that Sicarius from each nucleus of SDTF/desert
have been evolving in isolation from other regions, with old, endemic clades
diversifying in geographically restricted areas.
Our results resemble a similar pattern recovered in plants associated with SDTF
nuclei in the Andes, appropriately termed ―evolutionary islands‖ (Särkinen et al., 2012).
In contrast, lowland SDTF nuclei (e.g. Caatinga and Chiquitania) are less isolated and
share a significant part of their plant biota (Prado & Gibbs, 1993; Neves et al., 2015).
For these nuclei along these lowland SDTFs, climatic conditions are more important
predictors of plant community composition than other spatially structured factors
(Neves et al., 2015). Here we show a converse pattern, whereby not only species, but
entire spider lineages associated with lowland SDTF nuclei are strongly structured
geographically and have not been able to colonize other xeric areas. This structure is not
explained by climatic differences alone, but rather by spatially structured factors that are
prevalent between these nuclei, and likely persisted since most Sicarius lineages
diverged in the Miocene. For example, the Cerrado is a mesic and fire-affected
environment which has been estimated to have originated in the Miocene (Simon et al.
2009) and is an important barrier between the Caatinga and Chiquitano nuclei. Of
course, these results raise new questions. For example, how did a taxon of spiders with
limited dispersal potential manage to colonize a remote oceanic archipelago (S.
utriformis in the Galapagos)?
By using Sicariinae spiders as a model group, we explored how the biota of
Neotropical xeric environments assembled and diversified. We show that these spiders
have an ancient evolutionary history, with most speciation events taking place in the
Miocene. If dry biomes have been connected during Pleistocene glacial periods,
Sicarius were unable to take advantage of this to colonize other geographic areas.
Furthermore, not once in their ancient evolutionary history have Sicariinae spiders been
able to colonize mesic habitats, indicating that their adaptation to xeric habitats is the
most important determinant of their distribution. At a smaller scale, however, the
pattern is converse: niches are labile and shifts between different xeric biomes happened
several times throughout their evolutionary history. The limited dispersal capabilities
Magalhaes et al.
Niche conservatism and phylogeny of Sicarius
20
and the strong biome phylogenetic conservatism of sicariine spiders resulted in each
SDTF/desert nucleus becoming an ―evolutionary island‖ that has persisted in isolation
from other areas for millions of years.
5. Acknowledgements
A. Dippenaar and P. Marais (AcAT, South Africa), L. Esposito and D. Ubick
(CAS, USA), L. Carvalho (CHNUFPI, Brazil), P. Motta (DZUB, Brazil), M. Ramírez
(MACN, Argentina), A. Kury (MNRJ, Brazil), R. Pinto da Rocha (MZSP, Brazil) and
R. Orellana (UNSAAC, Peru) kindly lent specimens from the collections under their
care. We thank A.O. Porta, A. Taucare Ríos, B.T. Faleiro, C. Calitra, C. Veloso, F.M.
Hughes, G.F.B. Pereira, H.A. Iuri, J. Ochoa, J. Cabra García, L.N. Piacentini, L.S.
Carvalho, M. Stockmann, R. Botero Trujillo and T.J. Porto for sharing Sicarius
specimens or help in the field. P. Martins, M. Ramírez and R. Sage allowed
reproduction of their gorgeous photos of live specimens. Collecting was performed
under permits by SEMA-Bahia and ICMBio (Brazil), Subsecretaría de Ecología de La
Pampa, SAyDS-Río Negro and APN (Argentina), DGFFS (Peru), and CONAF (Chile).
M.J. Ramírez, C.J. Grismado and D. Silva helped with obtaining collecting permits for
Argentina and Peru. G.J. Binford kindly shared sequences of unpublished primers. D.T.
Rezende helped with GIS data. Some COI sequences were obtained with help of the
MACN Barcoding Laboratory (amplification) and the Canadian Centre of DNA
Barcoding (sequencing and submission to BOLD). This contribution is part of the first
author’s thesis in Ecology (PPG-ECMVS); an early version of the manuscript benefited
from comments by F.P. Werneck, who was part of the evaluating committee. Later
versions were improved by comments by U. Oliveira, G.H.F. Azevedo, several
anonymous referees and the editor, M.A. Arnedo.
6. Funding
This study was supported by CONICET (doctoral fellowship to ILFM and grant
PIP 2012-0943, iBOL Argentina 2012), FONCyT (PICT 2015-0283), CNPq
(301776/2004-0 to ADB; 308613/2016-3 to FRS; 407288/2013-9, 405795/2016-5,
306222/2015-9 to AJS), FAPEMIG (PPM-00651-15), INCT-HymPAr
(http:/www.hympar.ufscar.br/), FAPESP (2011/50689-0) and National Science
Foundation (DEB-1556651 to DMN).
Magalhaes et al.
Niche conservatism and phylogeny of Sicarius
21
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Online supplementary material
Files S1S7. Supplementary figures S1S6 and table S7, including PCA loadings (S1),
tree topology obtained only with sequence data (S2), optimization of ancestral biomes
(S3), histograms of aridity and precipitation values associated to Sicariinae records (S4
S5), COI gene trees for several species of Sicarius (S6) and variation partitioning
fractions (Table S7).
File S8. Spreadsheet with georeferenced Sicariinae records and their associated values
of climatic variables and principal components.
File S9. Voucher data of Sicariidae specimens used for this study, and data associated
with sequence data mined from GenBank.
File S10. Primer sequences and annealing temperatures for amplifying the markers used
in this study.
File S11. Alignments and input files.
File S12. Consensus tree files from MrBayes and BEAST.
Author contributions
AJS and ILFM designed the study. ADB, AJS and ILFM performed fieldwork. ADB,
AJS, THDAV and FRS provided reagents and equipment for molecular work. ILFM
identified specimens, gathered sequences and specimen records, gathered climatic niche
and biome data, and performed phylogenetic analyses. DMN designed and performed
variation partitioning analyses. ILFM, DMN and AJS led the writing of the first version
of the manuscript. All authors worked on the final version of the text.
-1.6
-0.8
0.8 1.6 2.4
PC1-2
1
2
3
PC2
temperate/dry
(b)
-1.8 -0.6 0.6 1.8
16
48
80
112
144
Fr neuqe cy
PC1
(c) Hexophthalma
Sicarius
H.hah
H.goa
H.spa
H.alb H.dam
H.dol
H.tes
S.and
S.bol
S.car
S.cru
S.dia
S.fum
S.gra
S.jeq
S.lan
S.lev
S.map
S.orn
S.per
S.rug
S.rup
S.sac
S.tho S.tro
S.utr S.val
S.yur
tropical/seasonally dry
Figure 1. Distribution records of Sicariinae in climatic and geographic space. (a) First two axes of a
principal components analysis of 21 climatic variables extracted for Sicariinae records. Each dot
represents a single Sicariinae record; the average position of each species is shown as black dots. The first
principal component (PC1; 42.9% of the total variation) is positively correlated with temperature and
precipitation, and negatively correlated with daily/annual variation in temperature and precipitation (see
also Supp. Figure S1). Two groups can be separated along the PC1, corresponding to temperate/dry
climates (PC1 < 0.5) and tropical/seasonally dry climates (PC1>0.5). (b) Geographic distribution of the
two groups observed in A. Circles represent the temperate/dry group (with darker shades representing
lower values of PC1). Squares represent the tropical/seasonally dry group (with darker shades
representing higher values of PC1). (c) Frequency histogram of Sicariinae records plotted against the
value of PC1, showing the distinct break between the two groups.
Figure 2. A densely sampled, total-evidence phylogeny of Sicariinae spiders obtained under Bayesian
inference using MrBayes 3.2 based on morphology and sequence data (COI, 16S-tLeu-ND1, 28S, H3).
Numbers next to nodes represent posterior probabilities (PP); nodes with PP 0.99 are marked with a
star. Clade supports in grey refer to a run excluding S. andinus, which behaves as a rogue taxon. Clades
marked with letters are discussed in the text. Photo credits: R. Sage (S. yurensis), M.J. Ramírez (S.
fumosus), P.H. Martins (S. cariri), others by ILFM.
H goanikontesensis
0.01020304050607080
H spatulata
H hahni
S mapuche
S rupestris
S gracilis
S peruensis
S utriformis
S thomisoides
S yurensis
S fumosus
S crustosus
S lanuginosus
S andinus
S boliviensis
S levii
S rugosus
S vallenato
S saci
S tropicus
S cariri
S diadorim
S jequitinhonha
S ornatus
PC1 value
-1.11 to -1
-1 to -0.5
-0.5 to 0.0
0.0 to 0.5
0.5 to 1
1 to 1.5
1.5 to 2
2 to 2.57
Miocene
Eocene
Cretaceous
Sicarius
Hexophthalma
1
2
3
5
3, 6
6
7
8
2
9
10
11
*
*
**
0.48
*0.94
0.58
*
**
a
1-0.92 0.65
0.94-0.70
0.95-0.69
1-0.81
*
1-0.96 *
*
*
0.99-0.70
b
c
d
e
f
j
3, 4
ghi
Figure 3. Phylogeny of Sicariinae spiders, their geographic distribution, and a parsimony-based
optimization of average values of the first principal component of climatic data (PC1; see Fig. 1). Above:
dated phylogenetic hypothesis for the relationships among Sicariinae spiders estimated analyzing a
reduced taxon set using BEAST 2.5.2 based on morphology and sequence data (COI, 16S-tLeu-ND1, 28S,
H3). Numbers next to nodes represent posterior probabilities (PP); nodes with PP ≥ 0.99 are marked with
a star. Clade supports in grey refer to a run excluding S. andinus, which behaves as a rogue taxon. Clades
marked with letters are discussed in the text. The molecular clock has been calibrated using fossils
(Loxosceles from Dominican amber, ochyroceratids from Burmese amber) and estimated substitution
rates for the H3 gene. Below: geographic distribution of Sicariinae spiders taken from the literature (black
dots), locations sampled for this study (white dots) and localities of complementary sequences from
GenBank (grey dots). Tropical dry forests highlighted in green, subtropical deserts and scrublands
highlighted in pink. The position of the Dry Diagonal, formed by the Caatinga, Cerrado and Chaco, is
indicated between the two dashed lines. Legend: (1) African xeric scrublands, (2) Argentinian Monte, (3)
Peruvian coastal desert, (4) Ecuadorian/Peruvian coastal dry forests, (5) Galapagos xeric scrubland, (6)
Chilean matorrales, (7) Peruvian Andean dry forests, (8) Chiquitano dry forests (9) Central American dry
forests, (10) Colombian dry forests, (11) Caatinga dry forests.
mapuche
rupestris
gracilis
peruensis
utriformis
thomisoides
yurensis
fumosus
crustosus
lanuginosus
andinus
boliviensis
levii
rugosus
vallenato
saci
tropicus
cariri
diadorim
jequitinhonha
ornatus
(a) -34.2 50.33
PCoA1
mapuche
rupestris
gracilis
peruensis
utriformis
thomisoides
yurensis
fumosus
crustosus
lanuginosus
andinus
boliviensis
levii
rugosus
vallenato
saci
tropicus
cariri
diadorim
jequitinhonha
ornatus
(c) -62.2 41.49
PCoA2
mapuche
rupestris
gracilis
peruensis
utriformis
thomisoides
yurensis
fumosus
crustosus
lanuginosus
andinus
boliviensis
levii
rugosus
vallenato
saci
tropicus
cariri
diadorim
jequitinhonha
ornatus
(e) -47.9 24.15
PCoA3
PCNM1
Min: -0.22
Max: 0.32
(b) (d) (f)
PCNM2
Min: -0.23
Max: 0.46
PCNM1
Min: -0.22
Max: 0.32
temperate
dry
tropical
seasonal
Figure 4. Decomposition of phylogenetic relatedness in Sicarius lineages across the Neotropics. Scores
from the first three axes of the principal coordinates analysis (PCoA) are mapped on to the phylogeny by
interpolating states at internal branches through a maximum likelihood ancestral state reconstruction (a, c,
e). Scores from the first two axes of the principal coordinates of neighbourhood matrix (PCNM), the most
significant in the forward selection (see Results), are mapped across geographic space (b, d, f), and
represent eigenvectors describing spatial structure in phylogenetic relatedness. Position of lineages in (b),
(d) and (f) is given by its mean latitudinal and longitudinal distribution. (a) PCoA1 constrains 27% of the
variance and segregates lineages found in deserts (blue-green spectrum) from lineages found in SDTFs
(red spectrum in Fig. 4a,b) and in the northern Argentinean Monte (yellow spectrum. (b) Geographical
variation of phylogenetic relatedness summarized by the first PCoA axis. Colours of circles plotted across
geographic space are identical to the colours of terminal branches in the PCoA1 phylogeny (dashed lines).
Size of circles indicates variation in the first PCNM axis. (c) PCoA2 constrains 18% of the variance and
segregates lineages found in the southern Argentinian Monte from lineages in the northern Atacama
deserts, and these two clades from all others (red spectrum). (d) Geographical variation of phylogenetic
relatedness summarized by the second PCoA axis. Colours of circles plotted across geographic space are
identical to the colours of terminal branches in the PCoA2 phylogeny. Size of circles indicates variation
in the second PCNM axis. (e) PCoA3 constrains 15% of the variance in phylogenetic relatedness. Within
the desert-southern Monte group (blue-green spectrum in Fig. 4a,b), PCoA3 segregates lineages found in
the southern Atacama Desert (red-green spectrum) from all others. Within the SDTF-northern Monte
group (red-yellow spectrum in Fig. 4a,b), PCoA3 segregates lineages found in Chiquitania (S.
boliviensis), inter-Andean valleys (S. andinus) and northern Monte (S. levii) (green spectrum) from all
others. (f) Geographical variation of phylogenetic relatedness summarized by the third PCoA axis.
Colours of circles plotted across geographic space are identical to the colours of terminal branches in the
PCoA3 phylogeny. Size of circles indicates variation in the first PCNM axis.
Tables
Table 1. Uncertainty associated with the estimates of ages of some clades of Sicariidae. For each clade and calibrating scheme, we present the
mean value and 95% highest posterior density interval obtained through Bayesian inference using BEAST 2.5.2. Four different calibrating schemes
have been used. (1) Fossil, with a constraint based on Miocene Loxosceles fossils from Dominican amber (see Wunderlich, 1988) and Cretaceous
ochyroceratid fossils from Burmese amber (see Wunderlich 2017). (2) H3, using substitution rates of the H3 gene estimated for dysderids (see
Bidegaray-Batista & Arnedo, 2011), (3) fossil + H3, a combination of the two latter approaches, and (4) fossil + H3 + Gondwana, a combination of
the two described approaches plus a biogeographical constraint based on the separation of Africa and South America (see Upchurch, 2008). All
values are given in millions of years.
Split / Calibration method
Fossil
H3
Fossil+H3
Fossil+H3+Gondwana
DrymusidaeScytodidae
113.8 (98.2147.4)
101.7 (41.1164.6)
127.1 (98.2179.6)
174.8 (99.6246.6)
L.laetaL.deserta
44.9 (22.269.5)
45.6 (2174.8)
53.3 (27.682.6)
83.2 (49.2116.7)
SicariinaeLoxoscelinae
94.6 (60.1135.9)
97.4 (51.9150.8)
113.5 (74.3163.5)
167 (124.2219.2)
HexophthalmaSicarius
74.2 (45.6108.2)
77.3 (41.8120.9)
89.7 (57.6131.1)
132.2 (100173.1)
L.vonwredeiNew World Loxosceles
60 (33.289.6)
61.9 (30.597.3)
72.1 (42.5107.6)
115 (100144.9)
H.spatulataremaining Hexophthalma
59.3 (33.188.3)
61.8 (31.598.1)
71.6 (42.7107.2)
105.5 (70.1147.2)
S.rupestris+S.mapucheremaining Sicarius
46.1 (26.968.9)
48.4 (25.775.3)
55.6 (34.280.7)
81.4 (56.2112.8)
S. thomisoides + S. yurensis
19.9 (7.635.3)
20.9 (836.3)
23.8 (9.540)
35.1 (14.557.8)
S.fumosusS.crustosus+S.lanuginosus
21.4 (10.234.4)
22.7 (1037.6)
26 (12.841.7)
37.7 (20.157.8)
S. utriformis + S. peruensis
7.9 (0.917.6)
8.5 (119.1)
9.7 (1.222.2)
14 (1.930.8)
Caatinga clade
16.8 (9.225.9)
17.6 (927.7)
20.2 (11.630.5)
29.8 (18.941.9)
S. leviiCaatinga clade
30 (16.845.5)
31.6 (16.549.5)
36.6 (21.754.1)
53.2 (35.273.6)
S. rugosusS. vallenato
13.4 (522.8)
14.2 (524.6)
16.2 (6.227.6)
23.8 (10.438.9)
Table 2. Classification of 743 Sicariinae records using the biome limits of Olson et al. (2001) with modifications described in the text. Records
are sorted into two groups estimated from climatic variables (PC1 values lower or higher than 0.5, respectively). Biome numbers follow Olson
et al. 2001: 1= tropical and subtropical moist broadleaf forests, 2= tropical and subtropical dry broadleaf forests, 3= tropical and subtropical
coniferous forests, 4= temperate broadleaf and mixed forests, 7= tropical and subtropical grasslands, savannas, and shrublands, 8= temperate
grasslands, savannas, and shrublands, 9= flooded grasslands, 10= montane grasslands and shrublands, 12= Mediterranean forests, woodlands,
and shrub and 13= deserts and xeric shrublands.
Biome
1
2
3
4
7
8
9
10
12
13
Total
PC1 < 0.5
2
3
0
37
11
54
0
41
217
189
554
PC1 > 0.5
26
123
1
0
18
0
1
2
0
7
178
Total
28
126
1
37
29
54
1
43
217
196
732
Molecular Phylogenetics and Evolution
Phylogeny of Neotropical Sicarius sand spiders suggests frequent transitions from
deserts to dry forests despite antique, broad-scale niche conservatism
Magalhaes ILF, Neves DM, Santos FR, Vidigal THDA, Brescovit AD, Santos AJ
Online supplementary material S1–S7
Supplementary figures S1–S6 and table S7, including PCA loadings (S1), tree topology obtained
only with sequence data (S2), optimization of ancestral biomes (S3), histograms of aridity and
precipitation values associated to Sicariinae records (S4–S5), COI gene trees for several species of
Sicarius (S6) and variation partitioning fractions (Table S7).
Supplementary figure S1. Loadings of the first principal component of a principal components analysis of
environmental variables associated to Sicariinae records (see Fig. 1). Bio1 = annual mean temperature, bio2 =
mean diurnal range, bio3 = isothermality, bio4 = temperature seasonality, bio5 = maximum temperature of
warmest month, bio6 = minimum temperature of coldest month, bio7 = temperature annual range, bio8 = mean
temperature of wettest quarter, bio9 = mean temperature of driest quarter, bio10 = mean temperature of warmest
quarter, bio11 = mean temperature of coldest quarter, bio12 = annual precipitation, bio13 = precipitation of
wettest month, bio14 = precipitation of driest month, bio15 = precipitation seasonality (coefficient of variation),
bio16 = precipitation of wettest quarter, bio17 = precipitation of driest quarter, bio18 = precipitation of warmest
quarter, bio19 = precipitation of coldest quarter, alt = elevation, ai_yr = aridity index.
S_thomisoides_576
S_ornatus_041
L_similis_178
S_tropicus_452
S_diadorim_404
S_mapuche_IFM1431
S_fumosus_555
S_peruensis_522
S_levii_IFM0315
S_rugosus_GJB08
S_thomisoides_516
L_ericsoni_174
S_rupestris_IFM0316
S_thomisoides_572
S_levii_IFM0090
Sicarius_sp_Corralito_GJB08
S_tropicus_377
S_ornatus_042
Ochyrocera_diablo_GenBank
S_rupestris_IFM0089
S_lanuginosus_GDR4020
S_peruensis_1_GJB08
S_peruensis_520
L_amazonica_GJB08
S_gracilis_523
S_gracilis_114
S_fumosus_563
S_fumosus_553
S_diadorim_092
Drymusa_serrana_GJB2008
S_thomisoides_517
S_fumosus_552
S_mapuche_IFM1430
S_peruensis_2_GJB08
S_boliviensis_491
S_fumosus_551
S_levii_PC_GJB08
S_thomisoides_547
S_yurensis_704
S_fumosus_560
S_rupestris_IFM0321
S_thomisoides_573
S_cariri_083
S_gracilis_513
S_thomisoides_518
L_laeta_Chile
S_cariri_190
S_levii_IFM0085
S_rupestris_IFM0322
S_boliviensis_082
S_peruensis_521
S_crustosus_566
S_mapuche_IFM1016
S_cariri_383
S_diadorim_528
S_rupestris_IFM0320
S_levii_Catamarca_GJB08
S_mapuche_IFM0530
S_levii_Salta_GJB08
L_laeta_GJB08
H_goanikontesensis_577
L_simillima_IFM1441
L_simillima_GJB08
S_crustosus_IFM0094
H_hahni_IFM1440
Sicarius_sp_PicunLeufu_GJB08
S_levii_IFM0317
S_fumosus_565
S_rupestris_IFM0378
S_levii_IFM0093
Sicarius_sp_Arroyito_GJB08
S_rupestris_IFM0091
S_jequitinhonha_062
S_thomisoides_548
S_fumosus_561
S_peruensis_519
S_thomisoides_575
H_spatulata_579
S_fumosus_554
L_intermedia_143
S_ornatus_331
S_fumosus_558
S_fumosus_562
S_crustosus_IFM0095
H_cf_dolichocephala_IFM1439
S_rupestris_IFM0088
S_rupestris_IFM0362
S_thomisoides_510
S_fumosus_556
S_levii_IFM0371
S_fumosus_564
Hexophthalma_aff_hahni_GJB08
S_thomisoides_549
S_mapuche_IFM0529
S_fumosus_557
H_goanikontesensis_578
L_deserta_GJB08
S_tropicus_342
Physocyclus_globosus_GenBank
S_boliviensis_492
L_hirsuta_GJB08
L_vonwredei_GJB08
S_fumosus_550
S_cariri_410
L_rufescens_GJB08
S_thomisoides_156
S_crustosus_568
L_caribbaea_GJB08
S_tropicus_244
S_thomisoides_515
S_cariri_427
Hexophthalma_sp1_GJB08
Sicarius_sp_Merlo_GJB08
S_ornatus_527
S_thomisoides_508
S_tropicus_325
S_crustosus_569
S_yurensis_IFM0086
S_fumosus_559
S_yurensis_512
S_peruensis_506
L_intermedia_GJB08
H_albospinosa_GJB08
S_ornatus_526
L_chapadensis_049
L_diaguita_IFM1279
S_crustosus_567
S_rupestris_IFM0365
S_levii_IFM0319
S_vallenato_IFM1075
S_saci_015
S_crustosus_IFM0957
S_rupestris_IFM0364
S_tropicus_389
S_thomisoides_574
S_saci_022
S_ornatus_337
S_jequitinhonha_010
L_amazonica_018
S_saci_034
H_spatulata_IFM1600
S_levii_Quijades_GJB08
S_boliviensis_081
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Supplementary figure S2. Phylogenetic hypothesis for the relationships among Sicariinae
s
piders estimated using Bayesian inference based on sequence data only (COI, 16S-tLeu-ND1
,
28S, H3). Numbers next to nodes represent posterior probabilities.
Supplementary figure S3. (A) Plot of the two first axes of a principal component analysis of climatic variables
extracted for Sicariinae records. Data points are colored according to their biome of origin according to the
classification of Olson et al. (2001) with slight modifications described in the text. (B) Map of biomes mentioned
in the text. The convex hulls delimit the two climatic groups described in the text. (C) A parsimony-based
optimization of the ancestral biomes on the phylogenetic hypothesis inferred using B
EAST
, which implies 2–3
shifts from deserts and xeric scrublands to dry tropical forests.
Supplementary figure S4. Frequency histogram of 10000 points taken randomly from Central/South America
(blue) and Sicariinae records (red) plotted against their associated aridity index.
Supplementary figure S5. Frequency histogram of 10000 points taken randomly from Central/South America
(blue) and Sicariinae records (red) plotted against their associated precipitation of the driest month.
Supplementary figure S6. Phylogenetic trees estimated under Bayesian inference using sequences of the
cytochrome c oxidase subunit I for several species of Sicarius. Maps with the geographic origin of the sequenced
individuals are placed to the right of each tree. Numbers next to nodes represent posterior probabilities. Groups
of sequences have been arbitrarily defined based on tree structure. Within-group and between-groups genetic
distances using the Kimura two-parameters (K2P) model of evolution are noted near each tree. Scale bars for the
maps: 200km.
Supplementary table 7. Variation partitioning by generalized linear models to determine how
much of the spatial variation in phylogenetic relatedness across the Neotropics, summarized by the
first three axes of the Principal Coordinates Analysis (PCoA), was accounted for by the
environmental variable measured. Fraction ‘climate’ represents nonspatial environmental variation
summarized by the first axis of a Principal Component Analyses (see Methods section); fraction
‘spatially structured climate’ represents the overlap between the environmental and spatial
components; fraction ‘Spatial Autocorrelation’ represents the spatial structure not captured by the
measured environmental variable. ns = non-significant; na = non-applicable.
PCoA1 PCoA2 PCoA3
Climate (PC1) -0.01 ns -0.04
Spatially Structured Climate 0.47 na 0.19
Spatial Autocorrelation 0.20 0.50 0.11
Unexplained 0.34 0.50 0.74
... To illustrate our argument, we explore the effect of uncertainty in the biogeographic history of Neotropical sand spiders (Sicarius). These spiders represent an ideal system for this test because they are moderately diverse (21 species) and all species have been included in a dated total-evidence phylogeny [30]. The genus has a disjunct distribution, and each species is restricted to one or two arid areas surrounded by mesic habitats; phylogeographic and phylogenetic patterns suggest they are very poor dispersers [31][32][33]. ...
... The first is the timing of arrival of Sicarius in the Galapagos archipelago. The Galapagos are currently inhabited by a single species of sand spider, Sicarius utriformis (Butler), which is sister to S. peruensis (Keyserling) from the Peruvian coastal deserts [30,33]. Although the oldest emerged islands are ~3.5 million years (Myr) old [34], geological evidence suggests that the archipelago existed for at least 14.5 Myr, when it was composed of paleo-islands that are now submerged [35,36]. ...
... Although the oldest emerged islands are ~3.5 million years (Myr) old [34], geological evidence suggests that the archipelago existed for at least 14.5 Myr, when it was composed of paleo-islands that are now submerged [35,36]. The age of divergence between S. utriformis and S. peruensis has a 95% confidence interval between 1.2 and 22.2 Myr (median 9.7; [30]), and thus it is possible that this pair of species split before the current islands were formed, but during the time the archipelago was formed by paleo-islands. This makes this system ideal to test the effect of the uncertainty of age estimates in biogeographic inference. ...
Article
Full-text available
Event-based biogeographic methods, such as dispersal-extinction-cladogenesis, have become increasingly popular for attempting to reconstruct the biogeographic history of organisms. Such methods employ distributional data of sampled species and a dated phylogenetic tree to estimate ancestral distribution ranges. Because the input tree is often a single consensus tree, uncertainty in topology and age estimates are rarely accounted for, even when they may affect the outcome of biogeographic estimates. Even when such uncertainties are taken into account for estimates of ancestral ranges, they are usually ignored when researchers compare competing biogeographic hypotheses. We explore the effect of incorporating this uncertainty in a biogeographic analysis of the 21 species of sand spiders (Sicariidae: Sicarius) from Neotropical xeric biomes, based on a total-evidence phylogeny including a complete sampling of the genus. Using a custom R script, we account for uncertainty in ages and topology by estimating ancestral ranges over a sample of trees from the posterior distribution of a Bayesian analysis, and for uncertainty in biogeographic estimates by using stochastic maps. This approach allows for counting biogeographic events such as dispersal among areas, counting lineages through time per area, and testing biogeographic hypotheses, while not overestimating the confidence in a single topology. Including uncertainty in ages indicates that Sicarius dispersed to the Galapagos Islands when the archipelago was formed by paleo-islands that are now submerged; model comparison strongly favors a scenario where dispersal took place before the current islands emerged. We also investigated past connections among currently disjunct Neotropical dry forests; failing to account for topological uncertainty underestimates possible connections among the Caatinga and Andean dry forests in favor of connections among Caatinga and Caribbean + Mesoamerican dry forests. Additionally, we find that biogeographic models including a founder-event speciation parameter (“+J”) are more prone to suffer from the overconfidence effects of estimating ancestral ranges using a single topology. This effect is alleviated by incorporating topological and age uncertainty while estimating stochastic maps, increasing the similarity in the inference of biogeographic events between models with or without a founder-event speciation parameter. We argue that incorporating phylogenetic uncertainty in biogeographic hypothesis-testing is valuable and should be a commonplace approach in the presence of rogue taxa or wide confidence intervals in age estimates, and especially when using models including founder-event speciation.
... Given approximately polytomous relationships within Appalachia (see below), this point estimate would correspond to a crown group age for the Appalachian radiation, and thus implies older divergences at the base of Hypochilus, perhaps during the Cretaceous. We note here that many other non-entelegyne araneomorph spider lineages are at least this ancient (both within extant families and sometimes within extant genera), as estimated from molecular clock analyses (e.g., sicariids - Magalhaes et al. 2019;leptonetids -Ledford et al. 2021), but also known directly from Upper Cretaceous Burmese amber fossils (e.g., psilodercids - Magalhaes et al. 2021). Also, the combination of Cretaceous fossil evidence in the context of living spider families suggests that non-entelygyne araneomorph lineages (akin to Hypochilus and Hypochilidae) dominated spider diversity at this time (Wunderlich 2008;Magalhaes et al. 2020). ...
Article
Full-text available
Hypochilus is a relictual lineage of Nearctic spiders distributed disjunctly across the United States in three montane regions (California, southern Rocky Mountains, southern Appalachia). Phylogenetic resolution of species relationships in Hypochilus has been challenging, and conserved morphology coupled with extreme genetic divergence has led to uncertain species limits in some complexes. Here, Hypochilus interspecies relationships have been reconstructed and cryptic speciation more critically evaluated using a combination of ultraconserved elements, mitochondrial CO1 by-catch, and morphology. Phylogenomic data strongly support the monophyly of regional clades and support a ((California, Appalachia), southern Rocky Mountains) topology. In Appalachia, five species are resolved as four lineages ( H. thorelli Marx, 1888 and H. coylei Platnick, 1987 are clearly sister taxa), but the interrelationships of these four lineages remain unresolved. The Appalachian species H. pococki Platnick, 1987 is recovered as monophyletic but is highly genetically structured at the nuclear level. While algorithmic analyses of nuclear data indicate many species (e.g., all H. pococki populations as species), male morphology instead reveals striking stasis. Within the California clade, nuclear and mitochondrial lineages of H. petrunkevitchi Gertsch, 1958 correspond directly to drainage basins of the southern Sierra Nevada, with H. bernardino Catley, 1994 nested within H. petrunkevitchi and sister to the southernmost basin populations. Combining nuclear, mitochondrial, geographical, and morphological evidence a new species from the Tule River and Cedar Creek drainages is described, Hypochilus xomote sp. nov. We also emphasize the conservation issues that face several microendemic, habitat-specialized species in this remarkable genus.
... For species adapted to colder habitats, their range limits may contract as fewer areas are suitable (Cole et al. 2011, Rubidge et al. 2012, Smale and Wernberg 2013. Lastly, a range shift may occur, with species moving away from inhospitable areas and towards more suitable areas (Parmesan and Yohe 2003, Berriozabal-Islas et al. 2018, Magalhaes et al. 2019). ...
Thesis
Full-text available
With a warming climate and changes in land use during the last decades, ticks have been observed to occur at increasingly higher latitudes and altitudes in the northern hemisphere. With the range expansion of ticks comes the potential for new diseases to emerge in previously uninfected areas, as well the number of cases of existing ones to increase. The effects of climate change are expected to be disproportionally pronounced a high latitudes, and are expected to continue for the foreseeable future. However, the dynamics of tick range expansion and their altitudinal occurrence near their northern distribution limit remain poorly understood. This thesis examines the altitudinal occurrence and host-parasite relations of two tick species, the exophilic generalist Ixodes ricinus and the endophilic specialist I. trianguliceps, by investigating the burdens found on small mammals along two altitudinal gradients in two locations in southern Norway. Based on previous studies in Norway, the highest altitude at which I. ricinus was found was 583 m.a.s.l., but in this thesis we found that I. ricinus occur considerably higher than previously thought, up to an altitude of at least 1000 m.a.s.l. The effects of altitude were less pronounced on the occurrence of I. trianguliceps, indicating that the endophilic ecology of this species may enable it to survive at higher altitudes compared to the exophilic I. ricinus. A follow-up study expanding the range of the altitudinal gradient may reveal the actual distribution limit of ticks in these areas. Furthermore, this study also investigated how ticks may utilize other hosts in areas characterized by multi-annual, high-amplitude rodent cycles, and how such cycles may inhibit the further progression of ticks. We found that non-cyclical shrew populations may have the potential to maintain tick populations in periods of low rodent availability, therefore enabling ticks to sustain a further upward progression, despite the periodic unavailability of some host species. A study encompassing one or more complete rodent cycles may shed more light on the roles of small mammals other than rodents in their capacity to act as a stable reserve of tick hosts, as well as on the specifics of the rodent cycles in these areas, and the influence of warming temperatures. Lastly, we tested whether the choice of capture method (live or lethal trapping) may result in different perceived tick burdens, in order to determine whether the use of live trapping was unavoidable to accurately assess tick burdens. We found no significant differences in larval I. ricinus burdens on hosts captured between the two trap types, and we therefore propose that in light of animal welfare, lethal trapping of small mammals in studies assessing tick burdens is favored, as animals are not subjected to capture stress, while accuracy is maintained. The combined results in this thesis may serve as a starting point for further studies investigating the range expansion of ticks and tick-borne diseases in northern regions.
... However, at present, the spatial distribution of these formations is patchy, and probably during the natural retraction process of this ecosystem some species, both flora (Prado & Gibbs 1993;Pennington et al. 2000;Prado 2000;Pennington et al. 2004;Collevatti et al. 2013;Côrtes et al. 2015;Arruda et al. 2018) and fauna (e.g. ants, bees, birds, lizards, spiders) (Zanella 2000;Werneck & Colli 2006;Silva et al. 2017;Magalhaes et al. 2019;Corbett et al. 2020) may have undergone evolutionary processes such as vicariance and long-distance dispersal limitation (Prado & Gibbs 1993;Mayle 2004). ...
Article
en Tropical dry forests (TDFs) are one of the most threatened ecosystems worldwide. Two hypotheses have been proposed to explain the origin of TDFs in South America: the Amazonian TDF hypothesis and the Pleistocene Arc hypothesis (PAH). There is a need to evaluate the distribution patterns of different organisms across the TDF distribution. We tested the following hypotheses: the species composition is determined by historical-evolutionary events, and therefore, the TDFs have a similar species composition as predicted by the PAH. Alternatively, the species composition is determined by recent ecological processes, and therefore, the TDFs have a sharing of species to their respective adjacent dominant habitat, with no support for the PAH. We expect that climatic factors drive the species richness, abundance and species dissimilarity (β-diversity) between TDFs and adjacent habitats across the latitudinal gradient. We sampled dung beetles across six Brazilian states in TDF fragments and adjacent dominant habitats and obtained the climatic conditions across the gradient. We used the β-diversity partition and generalised linear models to test our hypotheses. We sampled 8,625 dung beetles representing 102 species. Sorensen dissimilarity was higher among TDFs than between TDFs and adjacent habitats and was mostly due to the substitution of species. Annual mean temperature had a positive effect on abundance in TDFs but did not affect species richness. Species substitution (Podani’s approach) between TDFs and adjacent habitats decreased with mean diurnal range of temperature, while nestedness patterns (Baselga’s approach) increased with annual precipitation. Depending on the approach used (Baselga’s vs. Podani’s), we can obtain different results across the latitudinal gradient. The composition and structure of dung beetle assemblages in TDFs are mostly determined by more recent regional-to-local ecological processes since each TDF has a unique evolutionary history and a different dung beetle species composition. Our results do not support the Pleistocene Arc hypothesis. RESUMO pt As Florestas Tropicais Secas (FTSs) são um dos ecossistemas mais ameaçados do mundo. Duas hipóteses foram propostas para explicar a origem das FTSs na América do Sul: a hipótese da FTS Amazônica e a hipótese do Arco do Pleistoceno (PAH). É necessário avaliar os padrões de distribuição de diferentes organismos ao longa da distribuição da FTS. Testamos as seguintes hipóteses: a composição das espécies é determinada por eventos histórico-evolutivos e, portanto, as FTSs têm uma composição de espécies semelhante à prevista pela PAH. Alternativamente, a composição das espécies é determinada por processos ecológicos recentes e, portanto, as FTSs têm um compartilhamento de espécies com seus respectivos habitats dominantes adjacentes, sem suporte para a PAH. Esperamos que os fatores climáticos conduzam a riqueza de espécies, abundância e dissimilaridade de espécies (diversidade β) entre FTSs e habitats adjacentes em todo o gradiente latitudinal. Amostramos besouros escarabeíneos em seis estados brasileiros em fragmentos de FTS e habitats dominantes adjacentes e obtivemos as condições climáticas ao longo do gradiente. Usamos a partição de diversidade β e modelos lineares generalizados para testar nossas hipóteses. Amostramos 8.625 escarabeíneos que representam 102 espécies. A dissimilaridade de Sorensen foi maior entre FTSs do que entre FTSs e habitats adjacentes e foi principalmente devido à substituição de espécies. A temperatura média anual teve um efeito positivo sobre a abundância em FTSs, mas não afetou a riqueza de espécies. A substituição de espécies (abordagem de Podani) entre FTSs e habitats adjacentes diminuiu com a variação diurna média de temperatura, enquanto os padrões de aninhamento (abordagem de Baselga) aumentaram com a precipitação anual. Dependendo da abordagem utilizada (Baselga’s vs. Podani’s), podemos obter resultados diferentes em todo o gradiente latitudinal. A composição e a estrutura das assembleias de escarabeíneos em FTSs são principalmente determinadas por processos ecológicos regionais a locais mais recentes, uma vez que cada FTS tem uma história evolutiva única e uma composição de espécies diferente de escarabeíneos. Nossos resultados não suportam a hipótese do Arco do Pleistoceno.
... They suggested that biogeographical relationships between both diagonals are weak. Indeed, Magalhaes et al. (2019) showed some connections between both SADDs in spiders, but Caatinga lineages seem to be more related to dry forest species from Mesoamerica and Colombia. For small mammals, Kelt et al. (2000) reported high faunistic similarity within regions of the wSADD, but no similarity of these with the Caatinga. ...
... Depending on the species' adaptability to a warmer climate and the ability to disperse, species may either (i) increase their distribution range due to conditions becoming more favourable in areas that were previously inhospitable [3,4]; (ii) contract in range as their habitat becomes increasingly unsuitable [5,6]; or (iii) move away from areas that have become unsuitable towards habitats that have become more favourable [7,8]. To date most species appear to expand their natural distribution range, and for the majority of species both a northward [9,10] and an upward [11][12][13] range expansion seems to be the most common movement pattern. ...
Article
Full-text available
Background During the last decades a northward and upward range shift has been observed among many organisms across different taxa. In the northern hemisphere, ticks have been observed to have increased their latitudinal and altitudinal range limit. However, the elevational expansion at its northern distribution range remains largely unstudied. In this study we investigated the altitudinal distribution of the exophilic Ixodes ricinus and endophilic I. trianguliceps on two mountain slopes in Norway by assessing larval infestation rates on bank voles ( Myodes glareolus ). Methods During 2017 and 2018, 1325 bank voles were captured during the spring, summer and autumn at ten trapping stations ranging from 100 m to 1000 m.a.s.l. in two study areas in southern Norway. We used generalized logistic regression models to estimate the prevalence of infestation of both tick species along gradients of altitude, considering study area, collection year and season, temperature, humidity and altitude interactions as extrinsic variables, and host body mass and sex as intrinsic predictor variables. Results We found that both I. ricinus and I. trianguliceps infested bank voles at altitudes up to 1000 m.a.s.l., which is a substantial increase in altitude compared to previous findings for I. ricinus in this region. The infestation rates declined more rapidly with increasing altitude for I. ricinus compared to I. trianguliceps , indicating that the endophilic ecology of I. trianguliceps may provide shelter from limiting factors tied to altitude. Seasonal effects limited the occurrence of I. ricinus during autumn, but I. trianguliceps was found to infest rodents at all altitudes during all seasons of both years. Conclusions This study provides new insights into the altitudinal distribution of two tick species at their northern distribution range, one with the potential to transmit zoonotic pathogens to both humans and livestock. With warming temperatures predicted to increase, and especially so in the northern regions, the risk of tick-borne infections is likely to become a concern at increasingly higher altitudes in the future.
... During the last decades increasing temperatures have been shown to have an impact on the distribution of species across a wide range of taxonomic groups [1,2]. Depending on the species' adaptability to a warmer climate and the ability to disperse, species may either 1) increase their distribution range due to conditions becoming more favourable in areas that were previously inhospitable [3,4], 2) contract in range as their habitat becomes increasingly unsuitable [5,6], or 3) move away from areas that have become unsuitable towards habitats that have become more favourable [7,8]. To date most species appear to expand their natural distribution range, and for the majority of species both a northward [9,10] and an upward [11][12][13] range expansion seems to be the most common movement pattern. ...
Preprint
Full-text available
Background: During the last decades a northward and upward range shift has been observed among many organisms across different taxa. In the northern hemisphere, ticks have been observed to have increased their latitudinal and altitudinal range limit. However, the elevational expansion at its northern distribution range remains largely unstudied. In this study we investigated the altitudinal distribution of the exophilic Ixodes ricinus and endophilic I. trianguliceps on two mountain slopes in Norway by assessing larval infestation rates on bank voles (Myodes glareolus). Methods: During 2017 and 2018, 1325 bank voles were captured during spring, summer and autumn at 10 trapping stations ranging from 100 m to 1000 m.a.s.l. in two study areas in southern Norway. We used generalized logistic regression models to estimate the prevalence of infestation of both tick species along altitude, considering study area, collection year and season, temperature, humidity and altitude interactions as extrinsic variables; and host body mass and sex as intrinsic predictor variables. Results: We found that both I. ricinus and I. trianguliceps infested bank voles at altitudes up to 1000 m.a.s.l., which is a substantial increase in altitude compared to previous findings for I. ricinus in this region. The infestation rates declined more rapidly for I. ricinus compared to I. trianguliceps, indicating that the endophilic ecology of I. trianguliceps may provide shelter from limiting factors tied to altitude. Seasonal effects limited the occurrence of I. ricinus during autumn, but I. trianguliceps was found to infest rodents at all altitudes during all seasons of both years. Conclusions: This study provides new insights into the altitudinal distribution of two tick species at their northern distributional range, one with the potential to transmit zoonotic pathogens to both humans and livestock. With warming temperatures predicted to increase, and especially so in the northern regions, the risk of tick-borne infections is likely to become a concern at increasingly higher altitudes in the future.
Book
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Trabajo interdisciplinario de botánicos, liquenólogos, entomólogos, aracnólogos, herpetólogos, ornitólogos y conservacionistas, desarrollado en el marco del Proyecto FIC-R "Plan de Recuperación Reserva Nacional La Chimba" (2019-2020) a través de diversas campañas de terreno y colaboraciones con especialistas. Documenta más de 300 especies nativas confirmadas, con la preparación de 185 fichas técnicas, relevando además la presencia de 13 especies en riesgo de extinción según la clasificación del Ministerio del Medio Ambiente, Chile, tres de ellas En Peligro Crítico de extinción. VIDEO LANZAMIENTO: https://www.youtube.com/watch?v=xN8NDiGExAw&t=2844s // DESCARGA EN ALTA RESOLUCIÓN: https://recuperemoslachimba.cl/guia-campo/
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Aim As a continental island, much of the biota of New Zealand was initially thought to have been shaped by vicariance. Recent studies, however, have highlighted the role of dispersal, with some even suggesting that the entire biota is the product of dispersal events following emergence of the islands. This study focuses on the interplay between dispersal and vicariance, specifically asking whether the spider family Orsolobidae has Gondwanan origins on New Zealand. Location The spider family Orsolobidae was sampled from all continents where they occur (Africa, Australia, New Zealand and South America), comprising a total of 66 specimens representing the phylogenetic diversity of the family. Methods DNA sequences were obtained from six fragments that were subsequently aligned and analysed with MrBayes3.2 and beast 1.8. The phylogeny was calibrated with fossils used as node calibrations, as well as with the substitution rate of Histone H3. Results The orsolobid fauna of each land mass except Australia forms a monophyletic group in our analyses. The divergence dating analysis suggests that diversification of Orsolobidae started at a minimum of 80 Ma, while the New Zealand clade dates from a minimum of 40 Ma. Main conclusions Thus, while many taxa have colonized the islands by dispersal, certain lineages, including the Orsolobidae, have clearly been capable of persisting through times of reduced land area.
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Aim To assess the effects of historical events on the tempo and mode of diversification of the lizard Polychrus acutirostris along the South American diagonal of open formations (DOF). Location Caatinga and Cerrado biomes in Brazil. Methods We sequenced fragments of one mtDNA and three nuDNA genes of 68 individuals from 33 localities. We used population assignment methods to access genetic structure and estimate lineage boundaries. Next, we estimated lineage relationships, intraspecific diversity, environmental niche similarity and demographic history. Finally, we tested 12 diversification scenarios using an approximate Bayesian computation (ABC) approach. Results We recovered three non‐overlapping, geographically structured lineages corresponding to Caatinga, north‐east Cerrado and south‐west Cerrado, with the major divergence event dating to the Late Neogene. We also recovered a complex scenario of divergence associated with gene flow and niche divergence. Main conclusions We show a complex history of diversification along the South American DOF. Our findings support the role of environmental features as the likely drivers of P. acutirostris intraspecific diversification during the Late Neogene.
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The American tropics (the Neotropics) are the most species-rich realm on Earth, and for centuries, scientists have attempted to understand the origins and evolution of their biodiversity. It is now clear that different regions and taxonomic groups have responded differently to geological and climatic changes. However, we still lack a basic understanding of how Neotropical biodiversity was assembled over evolutionary timescales. Here we infer the timing and origin of the living biota in all major Neotropical regions by performing a cross-taxonomic biogeographic analysis based on 4,450 species from six major clades across the tree of life (angiosperms, birds, ferns, frogs, mammals, and squamates), and integrate >1.3 million species occurrences with large-scale phylogenies. We report an unprecedented level of biotic interchange among all Neotropical regions, totaling 4,525 dispersal events. About half of these events involved transitions between major environmental types, with a predominant directionality from forested to open biomes. For all taxonomic groups surveyed here, Amazonia is the primary source of Neotropical diversity, providing >2,800 lineages to other regions. Most of these dispersal events were to Mesoamerica (∼1,500 lineages), followed by dispersals into open regions of northern South America and the Cerrado and Chaco biomes. Biotic interchange has taken place for >60 million years and generally increased toward the present. The total amount of time lineages spend in a region appears to be the strongest predictor of migration events. These results demonstrate the complex origin of tropical ecosystems and the key role of biotic interchange for the assembly of regional biotas.
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Bayesian inference of phylogeny using Markov chain Monte Carlo (MCMC) (Drummond et al., 2002; Mau et al., 1999; Rannala and Yang, 1996) flourishes as a popular approach to uncover the evolutionary relationships among taxa, such as genes, genomes, individuals or species. MCMC approaches generate samples of model parameter values - including the phylogenetic tree -drawn from their posterior distribution given molecular sequence data and a selection of evolutionary models. Visualising, tabulating and marginalising these samples is critical for approximating the posterior quantities of interest that one reports as the outcome of a Bayesian phylogenetic analysis. To facilitate this task, we have developed the Tracer (version 1.7) software package to process MCMC trace files containing parameter samples and to interactively explore the high-dimensional posterior distribution. Tracer works automatically with sample output from BEAST (Drummond et al., 2012), BEAST2 (Bouckaert et al., 2014), LAMARC (Kuhner, 2006), Migrate (Beerli, 2006), MrBayes (Ronquist et al., 2012), RevBayes (Höhna et al., 2016) and possibly other MCMC programs from other domains.
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The described Afrotropical species of the genus Hexophthalma Karsch, 1879 (under the genus name Sicarius Walckenaer, 1847), of the spider family Sicariidae Keyserling, 1880, were recently reviewed. In the present paper the Afrotropical species of the genus Hexophthalma are revisited. After a thorough examination of all the available specimens from nine major collections, the species H. testacea (Purcell, 1908) is here synonymized with H. hahni (Karsch, 1878), three new species are described – H. binfordae sp. nov., H. goanikontesensis sp. nov. (both from Namibia) and H. leroyi sp. nov. (from South Africa) – and the male of H. dolichocephala (Lawrence, 1928) is described for the first time. The distribution of the species is also revised and a new updated key to the species is compiled.
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