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Journal of Biogeography. 2022;00:1–13.
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1wileyonlinelibrary.com/journal/jbi
Received: 18 November 2021
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Revised: 17 Februar y 2022
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Accepted: 17 March 2022
DOI: 10.1111/jbi.14373
RESEARCH ARTICLE
Microplate tectonics and environmental factors as distribution
drivers in Western Mediterranean freshwater planarians
Laia Leria1 | Marta Riutort1 | Rafael Romero1 | Xavier Ferrer2 | Miquel Vila- Farré3
This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in
any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.
© 2022 The Authors. Journal of Biogeography published by John Wiley & Sons Ltd.
Handling editor: Aristeidis Par makelis
1Department de Genètica, Microbiologia
i Estadística and Institut de Recerca de
la Biodiversitat (IRBio), Universitat de
Barcelona, Barcelona, Catalonia, Spain
2Department de Biologia Evolutiva,
Ecologia i Ciències Ambientals and Institut
de Recerca de la Biodiversitat (IRBio),
Universitat de Barcelona, Barcelona, Spain
3Department of Tissue Dynamics and
Regeneration, Max Planck Institute for
Multidisciplinary Sciences, Göttingen,
Germany
Correspondence
Miquel Vila- Farré, Deparment of Tissue
Dynamics and Regeneration, Max
Planck Institute for Multidisciplinary
Sciences, 37077, Göttingen, Am Fassberg
11, Germany.
Email: mvilafa@mpinat.mpg.de
Funding information
Ministerio de Ciencia e Innovación, Grant/
Award Number: BES- 2012- 057645;
Ministerio de Economía y Competitividad,
Grant/Award Number: PGC2018- 093924-
B- 100 and CGL2015
Abstract
Aim: Species biogeography mainly focuses on palaeogeographical events, while en-
vironmental factors are generally overlooked despite their importance in species
diversification. Here, we use an integrative approach to understand how palaeogeo-
graphical and environmental processes shape species distribution and focus on fresh-
water planarians as the model system.
Location: Western Mediterranean.
Tax o n: Dugesia.
Methods: We inferred the phylogenetic relationships of most known Dugesia species
in the area using six molecular markers. We then estimated their divergence times and
reconstructed their ancestral distribution ranges. We also performed environmental
niche modelling analyses using Dugesia subtentaculata as a model to evaluate the ef-
fects of several hydro- environmental variables and the likely existence of interspecific
competition on Dugesia distributions.
Results: Our results provide a new phylogenetic scheme for Dugesia from the Western
Mediterranean and show that the time splits between the lineages and their putative
ancestral distribution ranges are correlated with microplate tectonic dynamics within
the region during the Oligocene– Miocene period. Our environmental niche modelling
analyses indicate that the type of land cover and the slope of the terrain are the most
important abiotic factors driving the distribution of Dugesia from this region. Finally,
we found a partial niche overlap between D. subtentaculata and two other common
planarian species from the Iberian Peninsula.
Main conclusions: The microplate tectonic dynamics of the Western Mediterranean
during the Oligocene– Miocene period, together with the position of the mountain
ranges and posterior climate changes, may have played crucial roles in driving the
biogeographical history of Dugesia in this region. Moreover, both interspecific com-
petition and changes in fluvial characteristics driven by human activities may affect
the current diversity and distribution of Dugesia in the Western Mediterranean. This
study highlights the importance of integrating different types of information to study
the biogeographical history of a species.
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LERIA et al.
1 | INTRODUC TION
The Mediterranean Basin is one of the most biologically rich regions
on Earth (Mittermeier et al., 2011). The region has a rather com-
plex palaeogeographical history that includes various tectonic pro-
cesses, in addition to changes in sea level (Hsü et al., 1973; Krijgsman
et al., 1999; Mather, 2009; Rosenbaum et al., 2002). Plate tectonic
movements in the Western Mediterranean during the Oligocene–
Miocene period are among the most widely studied processes,
as they not only resulted in the creation of most of the Western
Mediterranean islands, but also shaped the entire contemporary
Western Mediterranean coastline (Rosenbaum et al., 2002).
The main tectonic process of the Western Mediterranean during
the Oligocene– Miocene period began around 25 Mya when the land
mass that is today northeastern Iberia and southern France detached
from the continent. It migrated south and subsequently broke into
several smaller fragments known as microplates. These microplates
presently correspond to the Kabylies, the Betic region, the Riff,
Calabria, Corsica, Sardinia and the Balearic Islands, and they split
from each other at different time periods while migrating across the
Mediterranean Sea until reaching their present positions. In addition
to the large geographical consequences of this tectonic process, it is
an important driver of the current distribution and diversity of many
animal species from the Western Mediterranean region, including
snails, lizards, earthworms, spiders and planarians (Bidegaray- Batista
& Arnedo, 2011; Lázaro et al., 20 11; Mendes et al., 2017; Opatova
et al., 2016; Pérez- Losada et al., 2011; Pfenninger et al., 2010).
In addition to tectonic movements, environmental factors can
also shape the distribution of species (Monge- Nájera, 2008). These
types of factors can be divided into two main categories, biotic and
abiotic. Those abiotic factors specific from each species' habitat,
such as the type of soil for edaphic organisms or the water charac-
teristics for aquatic ones, can provide relevant hints into the biogeo-
graphical history of a species (Bailey et al., 2018). Concerning biotic
factors, interspecific competition plays an essential role in shaping
the distribution of species. For example, competition theory pre-
dicts that when two sympatric species share identical niches, one
will eventually exclude the other, or selective pressure will cause
niche differentiation, allowing both species to coexist geographically
(Brown & Wilson, 1956; Chase, 2011).
Freshwater planarians (Platyhelminthes, Tricladida) are free- living
organisms that depend on the continuity of freshwater bodies to sur-
vive and disperse, and they are susceptible to desiccation (with few
exceptions) and high salinity (Vila- Farré & Rink, 2018). To disperse,
they use an active gliding movement along the submerged substrate
mediated by ventral cilia, rather than swimming or passively dispers-
ing through the water current (Ball & Reynoldson, 1981). For these
reasons, planarians in general, and particularly freshwater planarians,
are considered to be ideal model organisms for studying processes
that have shaped the diversity and distribution of species, as exempli-
fied in several studies (e.g. Lázaro et al., 2011; Solà et al., 2013).
The genus Dugesia is the most species- rich freshwater planar-
ian genus in the Western Mediterranean with 16 known species,
and all but two (D. sicula and D. gonocephala) are endemic to this re-
gion (Figure 1; Table S1). Previous studies have found that Western
Mediterranean species are the sister clade of Eastern Mediterranean
species (Lázaro et al., 2009; Solà et al., 2013). However, D. sicula is
an exception; although it is present throughout the Mediterranean, it
belongs to an African group of Dugesia that recently col onised the are a
(probably mediated by human activities) (Lázaro et al., 2009; Lázaro
& Riutort, 2013). Unfortunately, the phylogenetic relationships within
the Western Mediterranean clade of species remain unresolved,
mainly because of the limited genetic information contained in molec-
ular markers used and incomplete taxon sampling. Therefore, the pa-
laeogeographical processes that may have shaped its present diversity
and distribution have not yet been clarified. In addition, there is limited
information available for evaluating the roles of different environmen-
tal factors on the species distribution of Dugesia (Roca et al., 1992).
Interspecific competition for food has been proposed as an
essential factor that regulates population density and influences
its distribution in some planarian species (Vila- Farré & Rink, 2018).
A recent study in the Iberian Peninsula showed that Dugesia spe-
cies can coexist with other freshwater planarian genera and occa-
sionally with other Dugesia spp. (Leria et al., 2020). Of all Western
Mediterranean Dugesia, the distribution range of Dugesia subten-
taculata has been more widely studied (Leria et al., 2020). This fact,
together with its likely competition with Polycelis felina and Dugesia
sicula (Leria , 2019, and M. Riutort personal communication) make D.
subtentaculata an excellent model for studying the impacts of both
abiotic and biotic environmental factors on Dugesia distributions.
The present study aimed to disentangle how palaeogeograph-
ical processes and environmental factors interact to drive the bio-
geographical histor y of species. With this objective, we focused on
Dugesia freshwater planarians from the Western Mediterranean as
a model and aimed to answer the following questions: (1) Did the
microplate tectonics of the Western Mediterranean play a role in the
biogeographical history of Dugesia? (2) Which hydro- environmental
factors were more important in driving the distribution of Dugesia
species? (3) Can interspecific competition influence the current di-
versity and distribution of the genus? We used information from six
molecular markers to infer a time- calibrated phylogeny that included
most of the known Dugesia sp e c i e s from the Wester n Me d i t e r rane a n ,
and we reconstructed the ancestral ranges of their distributions. We
also conducted an environmental niche modelling analysis for D.
subtentaculata from the Iberian Peninsula to evaluate the influence
of different hydro- environmental factors on its distribution and the
KEY WORDS
abiotic factors, biogeography, Dugesia, interspecific competition, Mediterranean hotspot,
niche modelling
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LERIA et al .
likely existence of interspecific competition between D. subtentacu-
lata, D. sicula and P. felina.
2 | MATERIALS AND METHODS
2.1 | Taxon sampling
The present study used molec ula r data fo r 11 of the 15 autochthon ous
Dugesia species from the Western Mediterranean (Figure 1; Table S2).
D. brigantii and D. leporii have not be en found sin ce their initial descr ip-
tion, and D. ilvana and D. maghrebiana are found in regions that were
difficult to sample; therefore, these four species were precluded from
this study. Furthermore, D. sicula was not included in the molecular
analysis because although it occurs in the area, it does not belong to
the Western Mediterranean Dugesia clade (Lázaro et al., 2009; Solà
et al., 2022). We also used molecular information for five Dugesia spe-
cies from the eastern Mediterranean region as an outgroup.
Please see the Extended Materials and Methods in the
Supplementary Information for more extensive descriptions of the
methods described in the following subsections.
2.2 | DNA sequences and datasets
For the analyses, we used previously published sequences correspond-
ing to six different molecular markers per species: (a) 28S ribosomal RNA
gene (28S), (b) internal transcribed spacer 1 (ITS), (c) 18S ribosomal RNA
gene (18S), (d) cytochrome c oxidase I (Cox1), (e) an anonymous marker
(Dunuc3) and (f) a disulfide isomerase (Dunuc5) (Leria et al., 2020; Solà
et al., 2022). Only eight sequences were newly obtained for the pre-
sent study, and they corresponded to Cox1 of D. tubqalis and 18S of D.
aurea, D.corbata, D. subtentaculata and D. vilafarrei (see Supplementary
Information for details on sequence amplification).
All individuals were represented by a single sequence per mo-
lecular marker, except for D. subtentaculata, which was represented
by two different Cox1 sequences originating from one individual
(Peralejos de las Truchas) that corresponded to the two most diver-
gent Cox1 haplotypes within that individual. It has been suggested
that this intraindividual genetic diversity is a consequence of fissip-
arous reproduction (Leria et al., 2019). GenBank accession numbers
are listed in Table S2.
The DNA sequences of the different markers were arranged in
two concatenated datasets, named Dataset 1 and Dataset 2, which
FIGURE 1 Distribution map of all known Dugesia species from the Western Mediterranean region. The outlined geographical regions
correspond to the different areas included in the analysis of ancestral range reconstruction (excepting Greece, which was used for the outgroup).
The geographical distribution of those species known to occur in many different localities from extensive regions (viz., D. benazzii, D. gonocephala,
D. sicula and D. subtentaculata) has been represented with a coloured area instead of specific points. Species marked with an asterisk have not
been included in the present study. References for the distribution of each species are detailed in Table S1. Map projection: geographical
D. subtentaculata
D. aurea
D. corbata
D. vilafarrei
D. ilvana *
D. tubqalis
Dugesia sp.
D. benazzii
D. hepta
D. gonocephala
D. liguriensis
D. etrusca
D. leporii *
D. magrebiana *
D. brigantii *
D. sicula *
Europe
Iberian Peninsula
Betics
Riff
Africa
Kabylies
Balearic
Islands
Corso -
Sardinian
Archipelago
400 km
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LERIA et al.
differed only with respect to the Cox1 sequence of the D. subten-
taculata individual from Peralejos de las Truchas. Datasets 1 and 2
include the haplotypes MK385877 and MK385895, respectively.
2.3 | Molecular data analyses
The DNA sequences of each gene were separately aligned using
MAFFT online (Katoh & Standley, 2013) with the automatic
model selection option. The existence of sequence saturation
was evaluated using the program DAMBE (Xia et al., 2003; Xia
& Lemey, 2009; Xia & Xie, 2001). The phylogenetic relationships
between Dugesia species were inferred using Bayesian Inference
implemented in MrBayes 3.2 (Ronquist et al., 2012) and maximum
likelihood implemented in RaxML 7.0.3 (Stamatakis, 2006) and
IQ- TREE 1.6.12 (Nguyen et al., 2015). Two maximum likelihood
methods were used because they use different sequence evolu-
tion models to infer the trees, resulting in different phylogenetic
outputs (see Extended Methods in the Suppor ting Information for
further details about the models). The approximate times of diver-
gence between the lineages were estimated using the software
BEAST v.1.8.4 (Drummond et al., 2012). The well- known biogeo-
graphical event corresponding to the Mid- Aegean Trench (frag-
mentation of the Aegean Peninsula into oriental and an occidental
regions between 9 and 12 Mya) was used as a calibration point
(Dermitzakis & Papanikolaou, 1981). Fi nally, to recons truct the an-
cestral geographical ranges of the different Dugesia species from
the Western Mediterranean region, the previously obtained time-
calibrated phylogenies were input into the software RASP 4.2 (Yu
et al., 2015). We assigned nine different areas for this analysis: (A)
Africa pro parte, (Ba) the Balearic Islands, (Be) Betics, (E) Europe
pro parte, (G) Greece, (I) the Iberian Peninsula pro parte, (K)
Kabylies, (R) the Riff and (S) Corso- Sardinian Archipelago (see the
divisions in Figure 1). To reduce the length of names, we excluded
the ‘pro parte’ epithet from the area names that refer to a part
of Africa, Europe and the Iberian Peninsula (see Supplementary
Information for details about such areas).
2.4 | Environmental data analyses
Information about the distribution of the three species included in
the environmental analyses (viz., D. subtentaculata, D. sicula, and P.
felina) was obtained from the literature (Table S3). The environmental
niche of each species was modelled using the software Maxent 3.4.0
(Phillips et al., 2017; Phillips & Dudík, 2008) with information about
six non- correlated hydro- environmental variables extracted from the
HydroATLAS database (Linke et al., 2019) (Table S4). In the case of
D. subtentaculata, we inferred an additional model including the ob-
tained potential distribution of D. sicula and P. felina as variables to
analyse the impact of these species on the distribution of D. subten-
taculata. Finally, we used ENMTools v1.3 (Warren et al., 2010) to as-
sess the degree of niche overlap between D. subtentataculata and the
other two species in the Iberian Peninsula by calculating Schoener's
D statistic (where 0 indicates completely different niches and 1 indi-
cates an identical niche) (Schoener, 1968). We also used ENMTools to
perform identity tests to see whether the obtained D metrics were
significantly different from those assuming no niche differentiation.
3 | RESULTS
3.1 | Phylogenetic relationships
The sequences of the six molecular markers used in the present
study comprised a total aligned length of 5439 characters with no
significant levels of substitution saturation (Table S5). The phyl oge-
netic trees obtained using MrBayes, RaxML, and IQ- TREE for the
two datasets showed the same topology (Figure 2; Figures S1– S3).
As expected, the Western Mediterranean species formed a highly
supported monophyletic group (Western clade) in relation to the
Eastern Mediterranean species (Eastern clade) (Figure 2). The
Western clade was split into clade A (D. gonocephala, D. etrusca and
D. liguriensis) and clade B (the remaining western species). Clade
B was divided into a clade corresponding to the Sardinian species
D. hepta and D. benazzii (clade B1), and another clade, including
the species from Africa (D. tubqalis and Dugesia sp. 1), the Balearic
Islands (D. corbata and D. aurea) and the Iberian Peninsula (D. vila-
farrei and D. subtentaculata) (clade B2). The first species to diverge
within clade B2 was D. tubqalis, followed by Dugesia sp. 1 from
Morocco. The two species from Mallorca (D. aurea and D. corbata)
constituted a monophyletic clade with a sister group relationship
with D. vilafarrei and D. subtentaculata. Most of these clades were
highly supported independent of the method used, except for clade
B, which received low support in all methods, and the group con-
stituted by D. subtentaculata and D. vilafarrei, which showed low
support values with the likelihood methods (Figure 2).
3.2 | Divergence time estimation
The topology of the time- calibrated trees obtained with BEAST for
both datasets was identical to that obtained with MrBayes, RaxML
and IQ- TREE (Figure 2; Figures S1- S3). The mean age estimates and
confidence intervals of the nodes were highly similar between the
two datasets (Table S6). Th e only no de markedly different bet ween
the two datasets corresponded to the split within D. subtentaculata
(node 12), and it was inferred as being double the timing of Dataset
1 in Dataset 2 (0.82 and 1.69 Mya, respectively). For the remaining
node s, we referred to the ages est imates of Dataset 2, as it incl ude s
the most divergent Cox1 haplotype of D. subtentaculata, and thus
provides a better representation of the species' genetic diversity.
The split between the Western and Eastern clades was inferred
at a mean age of 25.85 Mya. Within the Western clade, clades A
and B split at around 23.09 Mya, whereas the divergence between
clade B1 and clade B2 dated back to 20.52 Mya. The first split
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LERIA et al .
within clade B2 (divergence between D. tubqalis and the remain-
ing species within this clade) occurred at approximately 15.02 Mya.
Subsequently, the divergence between Dugesia sp. 1 from Morocco
and the group including D. corbata, D. aurea, D. vilafarrei and D. sub-
tentaculata was estimated to have occurred at around 12.67 Mya.
The clade, including the species from Mallorca (D. corbata and D.
aurea), began to diverge from the ancestors of D. vilafarrei and D.
subtentaculata at around 10.91 Mya. Finally, the divergence of D.
corbata and D. aurea dated back to 8.03 Mya, slightly after the split
between D. vilafarrei and D. subtentaculata, which was inferred to
have occurred at around 9.47 Mya.
3.3 | Ancestral range estimation
The results obtained with BioGeoBEARS for the two datasets were
nearly identical, and both indicated that the DEC model best fit-
ted our data (Table S7). These analyses also indicated that there
were no significant differences between the performances of
models DEC and DEC + j (p- value of 1 in the likelihood ratio test).
The resulting ancestral range estimation under the DEC model for
Dataset 2 is shown in Figure 3 (all values mentioned below refer to
this dataset). All the estimated ranges of node 2 (ancestor of the
We s tern clad e) in c luded Eur ope plu s the Bal ear ic Isl and s, the C orso-
Sardinian Archipelago, the Betic region, the Riff region and/or the
Iber ian Pen insula. Among the se infe rred ances tra l ran ges, the range
showing the highest probability was that constituted by Europe,
the Balearic Islands and the Corso- Sardinian Archipelago (approxi-
mately 20%), while the probabilities of the remaining area combina-
tions accounted for <10% each. Subsequently, the estimated range
of node 3 (ancestor of clade A) corresponded to Europe (61.1%),
Europe plus the Iberian Peninsula (13.1%) and the last two regions
plus the Corso- Sardinian Archipelago (10.6%). The latter mentioned
range was the most probable for node 4 (54.9%), followed by the
Corso- Sardinian Archipelago plus the Iberian Peninsula (30.2%), or
plus Europe (10.5%). Different from nodes 2, 3 and 4, the inferred
range of node 5 (ancestor of clade B) was limited to two possible
area combinations outside continental Europe: the Balearic Islands
plus the Corso- Sardinian Archipelago and the Riff (48.5%), and
the Balearic Islands plus the Corso- Sardinian Archipelago and the
Betics (47.9%). The estimated range of node 6 (ancestor of cla de B1)
was exclusively the Corso- Sardinian Archipelago (99.9%), whereas
the estimated range of node 7 (ancestor of clade B2) was the region
constituted by the Balearic Islands, the Betics and the Riff (96.1%).
FIGURE 2 Time- calibrated phylogeny of Dugesia from the Western Mediterranean obtained with BEAST based on six molecular markers.
Summarisation method: maximum credibility. Node bars correspond to the 95% high posterior density intervals of the time estimates
(yellow: dataset 1; blue: dataset 2). Values over the nodes correspond to mean time estimates in million years ago obtained in dataset 2.
Right values at nodes correspond to the numbering used in Table S6. Coloured dots at nodes indicate the support values obtained in the
different phylogenetic analyses (PP: posterior probability; BT: bootstrap). CP (MAT): calibration point used in the BEAST analysis. Boxes and
letters on the right indicate the main clades. Scale bar represents time in million years. Letters A– S in brackets indicate the distribution of
each species (A: Africa, Ba: Balearic Islands, Be: Betics, E: Europe, G: Greece, I: Iberian Peninsula, R: Riff and S: Corso- Sardinian Archipelago).
Photograph: Dugesia subtentaculata from the Iberian Peninsula (0.7 cm in length)
D. gonocephala (E)
D. etrusca (EIS)
D. liguriensis (EIS)
D. benazzii (S)
D. tubqalis (A)
Dugesia sp. 1 (R)
D. aurea (Ba)
D. corbata (Ba)
D. vilafarrei (Be)
D. subtentaculata (AR)
D. improvisa (G)
D. damoae (G)
Dugesia sp. 2 (G)
D. aenigma (G)
D. hepta (S)
D. aurea (Ba)
D. corbata (Ba)
D. vilafarrei (Be)
D. subtentaculata (BeI)
D. cretica (G)
25.8
20.44
10.42
8.24
7.94
1.69
9.47
10.91
8.03
12.67
15.02
20.52
23.09
17.22
4.77
30 25 20 15 10 50
Million years
CP (MAT)
A
B
B1
B2
0,82
9
35
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
PP = 1
BT = 100
PP ≤ 0.95
BT ≤ 70
0.99 ≥ PP > 0.95
99 ≥ BT > 70
BEASTMrBayes
RaxML
IQ-TREE
6
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LERIA et al.
This lat ter- mentioned region was also estimated as the most proba-
ble range for node 8 (97%). In the case of node 9, alt hough the range
constituted by the Balearic Islands, the Betics and the Riff was es-
timated to be the most probable one (78.7%), the range constituted
by the Bal earic Isl ands, the Betics and Af rica showed 9.8% probab il-
ity. Finally, while the ancestor of D. aurea and D. corbata (node 10)
was estimated with a high probability as within the Balearic Islands
(99.6%), the ancestor of D. vilafarrei and D. subtentaculata (node 11)
was inferred to be from the Betic– Riff region (58.14%) or in other
areas, including the Betic region and different regions of Africa and
the Iberian Peninsula. A similar range reconstruction was found for
the ancestor of D. subtentaculata (node 12), which included many
area combinations of the Iberian Peninsula and the Betics plus dif-
fe rent re g ions of Africa . The de t a iled pe rcentag e probab i liti e s of the
reconstructed ancestral ranges of all nodes are shown in Table S8.
3.4 | Environmental niche modelling
The environmental niche models for D. subtentaculata, D. sicula and P.
felina from the Iberian Peninsula yielded AUC values higher than 0.8
with both the training and testing data (Table S9). This indicated that
the model had a high predictive power for all of the species distribu-
tion cases. The mean output pictures of the Maxent model showed
that the habitat suitability of D. subtentaculata was at its maximum
along the northern coast of the Iberian Peninsula (Figure. S4). In
contrast to D. subtentaculata, the habitat suitability for D. sicula was
high in different regions of the Mediterranean coast on the Iberian
Peninsula, whereas habitat suitability of P. felina was at its maximum
along th e Pyrenees and in certain regions on the norther n co ast of the
Iberian Peninsula (Figure S4).
In the case of D. subtentaculata, the contributions from envi-
ronmental variables to the model were roughly balanced; the high-
est was associated with land cover (23.9%), followed by the slope
(17.9%), natural water discharge of the river (16.5%), temperature
(15.5%), lithology (14.5%) and then precipitation (11.8%). The most
suitable environmental conditions for this species were as follows:
rivers with a low natural water discharge (mean annual less than 200
m3 per second) running on sedimentary rocks either within broad-
leaved deciduous tree cover or sparse herbaceous/shrub cover on
terrain slopes of approximately 15°, with a mean annual temperature
of approximately 13°C, and a relatively high precipitation regime
(mean annual around 1200 mm) (Figure 4).
For the species D. sicula and P. felina, the slope was the environ-
mental variable contributing the most to their distribution models
(29.1% and 48.5%, respectively), whereas the remaining variables
showed different percentage contributions to the model depending
on the species (Table S10). The most suitable environmental condi-
tions for these species are shown in Figure 4.
The distribution model inferred for D. subtentaculata, including
the obtained potential distribution of D. sicula and P. felina as addi-
tional variables, also yielded high AUC values for both the training
and testing data (0.932 ± 0.017 and 0.890 ± 0.043, respectively). In
this analysis, the potential distribution of P. felina was the variable
that contributed the most to the model (36.6%), whereas the po-
tential distribution of D. sicula was a variable that contributed the
least (3.9%). The analysis also showed that the habitat suitability of
D. subtentaculata was at its maximum when the habitat suitability of
P. felina ranged from 0.5 to 0.9 and when the habitat suitability of D.
sicula was either close to 0 or around 0.6 (Figure S5).
Schoener's D niche overlapping statistics were 0.4533 between
D. subtentaculata- D. sicula, and 0.5485 between D. subtentaculata- P.
felina, indicating a certain degree of niche overlap between the two
species pairs, particularly between D. subtentaculata and P. felina.
However, the results of the identity tests showed that both D val-
ues were significantly different than the ones obtained assuming no
niche differentiation (p- values lower than 0.001).
4 | DISCUSSION
We propose a novel phylogenetic scheme for Dugesia from the
Western Mediterranean and exclude the possible impact of intrain-
dividual genetic diversity on the divergence time estimates of the
genus. Based on this information, we provided a biogeographical
FIGURE 3 Ancestral ranges of Dugesia from the Western
Mediterranean estimated with BioGeoBEARS (model DEC) on
the BEAST time- calibrated phylogeny. Letters A– S indicate
the different geographical ranges included in the analysis. Pie
charts at nodes represent the estimated relative probability of
the different ancestral ranges of the lineages, with each colour
denoting a different geographical range (see Table S8 for detailed
probabilities). Numbers at nodes are used to refer to each node in
the text. Scale bar represents time in million years
05101520
(S) D. benazzi
i
(S) D. hepta
(R) Dugesia sp. (1)
(AKR) D. subtentaculata
(BeI) D. subtentaculata
(Be) D. vilafarre
i
(Ba) D. corbata
(Ba) D. aurea
(A) D. tubqali
s
(E) D. gonocephala
(EIS) D. liguriensi
s
(EIS) D. etrusca
(G) Outgroup
IS
EIS
AIK
BeIR
ABeI
AIR
EI
Ba
BaBeS
BaRS
BaES
BaBeR
BaBeE
BaER
S
BeES
ERS
ES
BeKR
ABeK
BeR
ABeR
ABe
E
25
EIS
EIS
ES
BaBeR
BaBeR
ABaBe
ABeR
3
5
6
7
8
9
10
11
12
4
A
B
B1
B2
2
BeIR
K: Kabylies
R: Riff
S: Corso-Sardinian Archipelago
A: Africa
Ba: Balearic Islands
Be: Betics
E: Europe
G: Greece
I: Iberian Peninsula
|
7
LERIA et al .
scenario for Dugesia based on the interplay of microplate tecton-
ics, abiotic environmental factors and species interactions. This
work contributes to our understanding of how different factors
interact to shape species diversity and distribution over time.
4.1 | Impact of high intraindividual genetic
diversity on divergence time estimations
The dating of evolutionary events, such as the timing of species di-
vergence, relies on the production of calibrated phylogenies that are
sensitive to the genetic sequences used to build them. High levels
of intraindividual genetic diversity have not only been detected
in different Dugesia species (Dols- Serrate et al., 2020; Lázaro &
Riutort, 2013; Leria et al., 2019), but also in several groups of plants
and corals (Gill, 1986; Schweinsberg et al., 2015), and these are the
result of accumulated somatic mutations during long periods of
asexual reproduction. Our results showed that the effect of select-
ing one or another intraindividual haplotype on the estimated diver-
gence ages was restricted to the species that showed intraindividual
genetic diversity, whereas it had no effect on the age estimates for
the rest of the species. These results highlight the importance of
considering intraindividual genetic diversity when working with
asexual organisms at the species level. However, it has no impact in
our conclusions regarding the biogeographical history of the genus
Dugesia that we elucidate in the following subsections.
4.2 | Novel phylogenetic relationships within
Dugesia from the Western Mediterranean
Our phylogenetic analysis of the Western Mediterranean Dugesia
species suggests a new evolutionary scenario for this group. A sin-
gle similar previous analysis (Lázaro et al., 2009) placed D. subten-
taculata sensu lato (presently divided into D. aurea, D. corbata, D.
vilafarrei and D. subtentaculata sensu stricto; Leria et al., 2020) as
sister to the rest of the western species. In contrast, we propose
that the clade constituted by these four species is a derived group
within Western Mediterranean Dugesia, which is sister to the en-
demic species from northern Africa (viz., D. tubqalis and the putative
new species Dugesia sp. 1 from Morocco) and together constitute a
clade with the two endemic species from Corsica and Sardinia (viz.,
FIGURE 4 Relative effect of different hydro- environmental variables on the potential distribution of the species D. subtentaculata, D.
sicula and P. felina in the Iberian Peninsula, obtained with Maxent. Y- axis: habitat suitability (from 0 to 1); X- axis: variation range of each
variable. For the variables corresponding to the Land cover and the Lithology, only those categories showing habitat suitability higher than
0.5 have been represented
Broadleaved deciduous tree cover
Needle-leaved evergreen tree cover
Mixed tree cover
Shrub cover
Sparse herbaceous or sparse shrub cover
Cultivated and managed areas
Mosaic cropland/shrub/herbaceous cove
r
Natural and artifical lakes
Artificial surfaces and associated areas
BV: Basic volcanic rocks
SS: Siliciclastic sedimentary rocks
BP: Basic plutonic rocks
MS: Mixed sedimentary rocks
CS: Carbonate sedimentary rocks
Lithology
0
0.1
0.2
0.4
0.3
0.5
0.6
0.7
0.8
0.9
1
BP IVBV LSS MS MTCS
MT: Metamorphic rocks
IV: Intermediate volcanic rocks
L: Lakes
Herbaceous cover
US
US: Unconsolidated sediments
Temperature (ºC)
04 810121618
0
0.1
0.2
0.4
0.3
0.5
0.6
0.7
0.8
0.9
1
26 14 20 24 6810 12 14 16
0
0.1
0.2
0.4
0.3
0.5
0.6
0.7
0.8
0.9
1
Precipitation (mm x100)
18
Dugesia subtentaculata
Dugesia sicula
Polycelis felina
Land cover
0
0.1
0.2
0.4
0.3
0.5
0.6
0.7
0.8
0.9
1
0510 15 20 25 30 35
0
0.1
0.2
0.4
0.3
0.5
0.6
0.7
0.8
0.9
1
Slope (º)
0300
0
0.1
0.2
0.4
0.3
0.5
0.6
0.7
0.8
0.9
1
Natural discharge (m³/s)
20
06
00100400 500 700
8
|
LERIA et al.
D. hepta and D. benazzii) (clade B). In our phylogeny, the first split
within Western Mediterranean Dugesia corresponds to the separa-
tion of the species D. gonocephala, D. liguriensis and D. etrusca (Clade
A) and clade B described above. This new and better re solved phylo-
genetic scenario results from the addition of four molecular markers
into the analysis, the increased taxon sampling and the selection of
a more closely related outgroup that helped avoid systematic errors
(Graham et al., 2002). Nevertheless, a node remains in our tree with
low statistical support; it groups the species D. hepta and D. benazzii
with the rest of the species in clade B and could result from rapid
diversification between these groups. The other relationships that
we determined, such as those within clade A or the phylogenetic re-
lationships obtained between the species that were previously sub-
sumed within D. subtentaculata, agreed with the findings of previous
studies (Lázaro et al., 2009; Leria et al., 2020).
4.3 | Microplate tectonics played an important role
in Western Mediterranean Dugesia diversification
Our results indicate that the palaeogeographical events in the
Western Mediterranean during the Oligocene– Miocene period were
key to shaping the biogeographical history of Dugesia in this region
(Figure 5). Our ancestral range estimation analysis indicated that the
ancestor of the Dugesia Western clade was situated in southwestern
Europe at around 30 Mya. This result agrees with that of a recent
study of the biogeographical history of the entire genus Dugesia
(Solà et al., 2022), which places the arrival of this ancestral lineage to
Europe from Africa during this period through a connection existing
between the land masses that today constitute the Italian Peninsula
and Tunisia (Hinsbergen et al., 2020). The orogeny of the Alps and the
Pyrenees had been ongoing for 30 million years (Dèzes et al., 2004);
as the habitat suitability of Dugesia likely decreases on steep slopes,
we thus hypothesise that both mountain ranges acted as porous
barriers to the expansion of Dugesia from the Italian Peninsula. In
particular, the Alps likely restricted the northward expansion of this
ancestral lineage to Central Europe, and the Pyrenees limited its
entry to the Iberian Peninsula. This situation likely channelled the
dispersion of this Dugesia lineage bet ween th e two mounta in ranges,
which is an area constituting part of the landmass that resulted in the
first Mediterranean microplate (Figure 5b).
The initial detachment of the first microplate from the continent
(approximately 25 Mya) likely resulted in the first diversification
event within the Western Mediterranean Dugesia, where the ances-
tor of the species D. gonocephala, D. etrusca and D. liguriensis (which
remained on the continent) was isolated from the ancestor of the
species presently distributed in the Western Mediterranean Islands,
Northern Africa and the Iberian Peninsula (which remained on the
microplate) (Figure 5c). This event has also been proposed as a driver
of the diversification between the Iberian and Corso- Sardinian spe-
cies within the genera of freshwater arthropods Stenasellus and
Tyrrhenoleuctra (Fochetti et al., 2009; Ketmaier et al., 2003). In the
subsequent fragmentation of the microplate at around 21 Mya, the
ancestor of D. hepta and D. benazzi would have been isolated on the
microplate corresponding to Corsica, Sardinia and Calabria, while
the ancestor of the other species would have remained on the por-
tion of the landmass including the Balearic Islands, the Betic region
and the Riff (Figure 5d), that later collided with Northern Africa at
approximately 15 Mya. The short time span between microplate de-
tachment from the continent and its first fragmentation (4 My) may
explain the lack of resolution found in this part of the tree. The col-
lision between the rest of the microplate and northern Africa would
have facilitated the dispersion of some of the Dugesia lineages to
this region, and this would have given rise to at least two Moroccan
species that are present in our tree (Figure 5e). A similar dispersion
event from the Betic– Rif f plate to norther n Africa has also been sug-
gested for lizards of the genus Psammodromus (Mendes et al., 2017 ).
Additionally, pre- Messinian dispersions between the Iberian
Peninsula and Northern Africa have been proposed for Cyprinid
fish (Levy et al., 2009), which reinforces the hypothesis that land
bridges between these regions were accompanied by freshwater
connections.
Finally, the fragmentation of the Balearic– Betic– Riff microplate
appears to have occurred in two consecutive steps, and this drove
the diversification of the species that remained in this region. In the
first step, this microplate would have fragmented into the Riff re-
gion and the Balearic– Betic region at around 12 Mya, and this would
have isolated the ancestors of the two Moroccan species (that would
have dispersed to the Riff region during the contact period) from the
ancestors of D. aurea, D. corbata, D. vilafarrei and D. subtentaculata
(that would have remained in the Balearic– Betic region) (Figure 5f).
The second and final split of this microplate at around 10 Mya prob-
ably isolated the ancestor of D. aurea and D. corbata in the Balearic
Islands, whereas the ancestor of D. vilafarrei and D. subtentaculata
would have remained in the Betic region that became part of the
Iberian Peninsula (Figure 5g).
Although our results are in general agreement with Rosenbaum's
palaeogeographical model for microplate tectonics, the final result
disagrees. Rosenbaum's model suggests that the Balearic Islands
were isolated from the other plate fragments at around 25– 21 Mya,
while our results point to a connection between the Balearic Islands
and the Betic region until 10 Mya. The biogeographical importance
of the connection between the Balearic Islands and the Betics was
proposed by Colom (1978). Importantly, this connection until 10
Mya has already been proposed in other phylogeographical stud-
ies (Bidegaray- Batista & Arnedo, 2 011; Chueca et al., 2015), and it
agrees with alternative tectonic models that suggest the union of
the Balearic Islands to the Betic– Riff microplate lasted until the early
Tortonian (at around 11 Mya) or that different periods of connec-
tion existed between these two microplates until this period (Dèzes
et al., 2004; Schettino & Turco, 2011; Hinsbergen et al., 2020).
Finally, although the Sardinian populations of D. etrusca and
D. liguriensis were not included in the present study, our results
provide insights into their biogeographical history. These species
could have dispersed to the microplate corresponding to Corsica–
Sardinia– Calabria when this landmass came into contact with the
|
9
LERIA et al .
Italian Peninsula (from 18 Mya until the opening of the Tyrrhenian
Sea at around 10– 6 Mya) (Rosenbaum et al., 20 02), and this is
a biogeographical pattern that has been proposed for different
taxa (Bidegaray- Batista & Arnedo, 2011 ; Carranza et al., 2008).
Alternatively, both species could have dispersed more recently from
the continent to the island during any of the land connection peri-
ods that occurred during the Messinian Salinity Crisis or during the
low sea level events that occurred until the Pleistocene (Ketmaier
& Caccone, 2013), as suggested for other groups (Fromhage
et al., 2004; Novo et al., 2015). These recent periods of land connec-
tion may also explain the dispersion of some D. benazzii populations
between Corsica and Sardinia. Recent analyses have shown that D.
benazzii may represent a species complex (Dols- Serrate et al., 2020)
with an intricate biogeographical history. In summary, further stud-
ies, including the insular populations of these species, are necessary
to provide more information about the biogeographical history of
the Corso- Sardinian Archipelago.
4.4 | Abiotic environmental factors define Dugesia
distribution after major diversification events
The present study is the first to use specific hydro- environmental
variables to model the distribution of freshwater planarian species.
Our results show that the type of land cover, the slope of the terrain
and the natural water discharge of the river likely played major roles
in driving Dugesia distributions. The slope of the terrain has previ-
ously been identified as a key factor in explaining the distribution
of the freshwater planarian species Crenobia alpina in Wales (Lock &
Reynoldson, 1976). Similarly, the current velocity (which is directly
FIGURE 5 Biogeographical history of Dugesia from the Western Mediterranean region proposed in the present study. (a) Schematic
representation of the phylogenetic relationships between Dugesia species under a temporal framework. Letters A– S in brackets indicate the
current distribution of each species (A: Africa, Ba: Balearic Islands, Be: Betics, E: Europe, I: Iberian Peninsula, R: Riff and S: Corso- Sardinian
Archipelago). (b– h) Palaeogeographical reconstructions based on Dèzes et al. (2004), Rosenbaum et al. (2002), Schettino and Turco (2011).
Framed numbers from 1 to 13 indicate the geographical location and temporal framework of each Dugesia lineage. Dark grey in pictures
(b– h): main orogenic regions
10 Mya
30 Mya
25 Mya 21 Mya 15 Mya
12 Mya
D. gonocephala (E)
D. etrusca (EIS)
D. liguriensis (EIS)
D. benazzii (S)
D. hepta (S)
D. tubqalis (A)
Dugesia sp. (R)
D. aurea (Ba)
D. corbata (Ba)
D. vilafarrei (Be)
D. subtentaculata (BeI)
D. subtentaculata (AR)
Outgroup
1
2
3
4
5
6
7
8
9
10
11
13
(a)
(b)
(c) (d) (e)
(f) (g) (h)
25 20 15 10 50
Million years
12
1
2
35
4
1’6 Mya
6
7
8
9
10
11
13
12
10
|
LERIA et al.
related to the terrain slope) has also been reported as an important
factor driving the distribution of different freshwater planarian spe-
cies in several springs of the Pyrenees (Roca et al., 1992), including
Dugesia species, although the authors suggested that slope was not
a determinant in explaining the occurrence of Dugesia in the ana-
lysed springs.
The natural water discharge of the river may represent an im-
portant abiotic factor in the distribution of freshwater planarians,
as it influences several key aquatic processes, such as the level of
dissolved oxygen, sediment transport and deposition, the water
quality, and the habitat type (Bunn & Arthington, 2002; M. Warren
et al., 2015). Finally, although the type of land cover may not ap-
pear to be an a priori determinant for a freshwater species, we
found that it was the most important variable that explains the
distribution of D. subtentaculata on the Iberian Peninsula. This dis-
covery implies that major historic changes in the vegetation and
habitat characteristics within the Western Mediterranean may
have played important roles in the biogeographical history of the
group.
After the final split of the microplates described above at approx-
imately 10 Mya, global temperatures began to cool, and Western
Mediterranean vegetation shifted gradually from evergreen forests
to mixed and deciduous tree cover (Jiménez- Moreno et al., 2010 ).
This shift from subtropical to temperate forests was probably fa-
vourable for the Dugesia lineages inhabiting continental Europe
and the western Mediterranean islands at that time, potentially
resulting in their geographical expansion. However, in the case of
Mallorca, posterior events (such as eustatic sea movements during
the Pleistocene; Dumitru et al., 2021) may have resulted in losses of
diversity and distributional range. This explains why only two en-
demic species remain on the islan d (D. aurea and D. corbata); they are
genetically highly differentiated, and each species is restricted to a
single locality.
In contrast to the aforementioned Dugesia lineages found in
southern Europe and the western Mediterranean islands after the
split of the microplates, lineages that had arrived in North Africa
from the Betic– Riff microplate (viz., the ancestors of D. tubqalis
and Dugesia sp. 1 from Morocco) encountered a gradual desertifi-
cation scenario that began in around the Miocene/Pliocene period
(Micheels et al., 2009). These unfavourable environmental condi-
tions probably restricted the geographical distribution of the lin-
eages to the forested areas of the region, and it explains why these
two species are presently endemic from the Atlas and the Riff,
which are the two most humid eco- regions of north- western Africa
(Rankou et al., 2013).
Interestingly, some D. subtentaculata populations are also pres-
ent in the Atlas and Riff regions. According to our results, the di-
vergence between the Iberian and the north African populations of
this species dates to 1.6 Mya, which indicates that the colonisation
of Africa from the Iberian Peninsula possibly happened during some
of the low sea level periods that occurred during the Pleistocene
(Figure 5h) (Clark et al., 2009). Although there is an extensive ev-
idence of species exchange between Africa and Iberia during this
period (Fernández- Mazuecos & Vargas, 2011; Gibert et al., 2003;
Kaliontzopoulou et al., 2011; Pleguezuelos et al., 20 08; Straus, 2001),
most such examples are of terrestrial vertebrates that likely crossed
the strait of Gibraltar via rafting. As Dugesia species require the
continuity of freshwater bodies for survival and dispersal, this indi-
cates that some freshwater connections may have existed between
these regions during the Last Glacial Maximum; for example, by river
plumes (Gibert et al., 2003).
Although the glacial periods of the Pleistocene may have en-
abled the increased distribution of some Dugesia species (such as the
African colonisation of D. subtentaculata), the associated permafrost
soil extensions likely reduced the diversity and distribution of the
Dugesia lineages found in continental Europe. This scenario explains
why most Western Mediterranean Dugesia species diversity is pres-
ently found in southern Europe. In contrast, continental Europe is
only occupied by genetically similar populations of D. gonocephala
(Lázaro et al., 2009), which likely expanded northward from south-
ern regions or from microrefugia in central Europe after the glaci-
ations ended. It has been proposed that a similar situation shaped
the present genetic diversity and distribution of the freshwater
planarian species, Schmidtea polychroa, S. lugubris and S. nova (Leria
et al., 2018; Pongratz et al., 2003), in addition to the current biogeo-
graphical pattern of many other European species (Hewitt, 2000).
4.5 | Interspecific competition and human
habitat transformation as potential Dugesia
distribution drivers
Environmental niche overlap between species can indicate interspe-
cific competition. In this sense, our results show a certain degree of
overlap between D. subtentaculata and P. felina and D. sicula, particu-
larly between D. subtentaculata and P. felina. Therefore, the distribu-
tion dynamics of the Dugesia li neage s arri vin g fro m Africa to Western
Europe at around 30 Mya were likely influenced by the freshwater
planarian species that were already found on the European conti-
nent, such as the genus Polycelis or Schmidtea (Lázaro et al., 2011;
Leria et al., 2018). In the case of D. subtentaculata and P. felina, both
species may be currently competing, or past interspecific competi-
tion may have resulted in niche differentiation associated with cer-
tain environmental characteristics that have not been evaluated in
the present study, such as trophic, circadian or microhabitat differ-
entiation (Afonso & Eterovick, 2007; Boddington & Mettrick, 1974 ;
Lombardo et al., 2011), and these allowed the two species to coexist
in several localities.
Unlike P. felina, and refuting our initial hypothesis, our results
imply that D. sicula may not be presently competing with D. sub-
tentaculata in the Iberian Peninsula, as their niches only overlap in
limited regions on the eastern coast, and the potential distribution
of D. sicula does not influence the distribution of D. subtentaculata.
However, our analyses show that D. sicula not only presents high
suitability for cultivated and managed areas, but it is also widely tol-
erant of different water discharge regimes, which may help to explain
|
11
LERIA et al .
its recent colonisation across the Mediterranean region that is likely
driven by human trade activities (Lázaro & Riutort, 2013). Therefore,
the replacement of different D. subtentaculata populations from the
southern and eastern coasts of the Iberian Peninsula by D. sicula may
have been driven by changes in the characteristics of the freshwa-
ter environments due to human activities, such as agriculture, live-
stock rearing and urbanisation, rather than by direct competition
between the species. For instance, unlike D. subtentaculata, D. sicula
is more frequently found in canalised rivers, wells, plant nurseries
and fountains within urban parks (Lázaro & Riutort, 2013). In the
southern regions of Europe, the environment is being increasingly
transformed from natural habitats to areas managed by humans,
and the consequences of human- driven climate changes in these
regions are contributing to extreme climate characteristics in the
Mediterranean region, such as severe droughts and sudden heavy
storms. We, therefore, tentatively predict the favoured expansion
of D. sicula in this part of the Mediterranean region, as there is a re-
duction in suitable habitats for the autochthonous Dugesia species.
ACKNOWLEDGEMENTS
We are grateful to Eduard Solà for the cession of several Dugesia se-
quences, to Neftalí Sillero and Márcia Barbosa for their advice on the
ni che mo dell ing an alys e s and to Álva ro Alons o, Bla nca Oli vet , Car olin a
Noreña, David Fuses, Eduard Filella, Francisco Monjo, Joan Ferrer
Riu, José María Martín Durán, Josep Morando Milà, Maria del Mar de
Miguel Bonet, Mette Handberg- Thorsager, Tania López and Xavi Coll
for providing information on different localities of Polycelis felina from
the Iberian Peninsula. All contributors gave their permission to carry
out this work. No collection permits were needed. This research was
supported by the Ministerio de Economía y Competitividad (projects
CGL2015– 63527 and PGC2018- 093924- B- 100) from Spain. This
research was also supported by BES- 2012- 057645 Grant from the
Ministerio de Ciencia e Innovación (to Laia Leria).
DATA AVA ILAB ILITY STATE MEN T
All sequences have been deposited in GenBank. The alignments are
available in DRYAD database: https://doi.org/10.5061/dryad.c866t
1g80.
ORCID
Marta Riutort https://orcid.org/0000-0002-2134-7674
Miquel Vila- Farré https://orcid.org/0000-0002-2553-2842
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BIOSKETCH
Laia Leria obtained her PhD in 2019, focused on understanding
the processes shaping freshwater planarians' genetic diversity.
This manuscript represents an expanded version of her the-
sis work. She and the other authors collaborate on questions
on planarian diversity at the Universitat de Barcelona (MR re-
search team web page: www.ub.edu/geisan) and the Max Planck
Institute for Multidisciplinary Sciences (MV departmental web
page: https://www.mpinat.mpg.de/64008 3/mique l- vila- farre).
Author contributions: LL, MVF and MR did the initial study de-
sign. LL processed and analysed the data and wrote the manu-
script with input from all authors. RR and XF contributed to
interpreting the results of the biogeographical analyses. All au-
thors read and approved the final manuscript. Authors declare
no conflict of interest.
SUPPORTING INFORMATION
Additional supporting information may be found in the online
version of the article at the publisher’s website.
How to cite this article: Leria, L., Riutort, M., Romero, R.,
Ferrer, X. & Vila- Farré, M. (2022). Microplate tectonics and
environmental factors as distribution drivers in Western
Mediterranean freshwater planarians. Journal of
Biogeography, 00, 1–13. https://doi.org/10.1111/jbi.14373
