J. Mt. Sci. (2023) 20(1): 129-140 e-mail: jms@imde.ac.cn http://jms.imde.ac.

cn
https://doi.org/10.1007/s11629-021-7184-6

Original Article

Historical relationships of the Mesoamerican highlands, with emphasis on

tropical montane cloud forests: a temporal cladistic biogeographical

analysis

CASTRO-TORREBLANCA Marisol1,2 https://orcid.org/0000-0001-5486-9420; e-mail: balam_mampar@hotmail.com

ESPINOSA David2 https://orcid.org/0000-0002-9938-4686; e-mail: despinos@unam.mx

BUENO-HERNÁNDEZ Alfredo2 https://orcid.org/0000-0003-4663-9937; e-mail: abueno@unam.mx

LUNA-VEGA Isolda3* https://orcid.org/0000-0002-7243-9018; e-mail: luna.isolda@gmail.com

*Corresponding author

1 Biological Sciences Graduate Program, Coordination of Graduate Studies, National Autonomous University of Mexico,
University City, Coyoacán 04510 Mexico City, Mexico
2 Comparative Biology and Biodiversity Research Unit, Facultad de Estudios Superiores Zaragoza, National
Autonomous University of Mexico, Av. Batalla del 5 de mayo s/n, Col. Ejército de Oriente 09230 Mexico City, Mexico
3 Laboratory of Biogeography and Systematics, Department of Evolutionary Biology, Faculty of Sciences, National
Autonomous University of Mexico, University City, Coyoacán 04510 Mexico City, Mexico

Citation: Castro-Torreblanca M, Espinosa D, Bueno-Hernández A, Luna-Vega I (2023) Historical relationships of the

Mesoamerican highlands, with emphasis on tropical montane cloud forests: a temporal cladistic biogeographical analysis.
Journal of Mountain Science 20(1). https://doi.org/10.1007/s11629-021-7184-6

© Science Press, Institute of Mountain Hazards and Environment, CAS and Springer-Verlag GmbH Germany, part of Springer Nature 2023

Abstract: The historical relationships of nine areas
of endemism of the tropical montane cloud forests
(TMCFs) were analysed based on a temporal cladistic
biogeographical approach. Three cladistic
biogeographical analyses were conducted based on 29
cladograms of terrestrial taxa by partitioning them
into three time-slices, namely, Miocene, Pliocene, and
Pleistocene. The results showed different area
relationships over time. For the Miocene and Pliocene
time slices, the Isthmus of Tehuantepec acted as a
geographic barrier that fragmented the TMCFs into
two portions: west of the Isthmus and east of the
Isthmus. In the case of the Pleistocene, the TMCFs
were broken into two portions, one related to the
Neotropical region and the other to the Nearctic
region. Furthermore, the analyses allowed us to detect
the influences of different geological and
Received: 24-Oct-2021
Revised: 12-Oct-2022
Accepted: 13-Dec-2022
paleoclimatological events on the distribution of the
TMCFs over time. Therefore, the TMCFs current
distribution might have been driven by geological
events during the Miocene-Pliocene, whereas climatic
fluctuations have the highest impact during the
Pleistocene.
Keywords: Dispersal; Evolutionary biogeography;
Paralogy free subtree analysis; Vicariance
1 Introduction
Cladistic biogeography is an approach to
historical biogeography that analyses the distribution
of biodiversity through patterns of relationships
between areas of endemism, based on the
phylogenetic relationships of the taxa that inhabit
them (Contreras-Medina et al. 2007; Crisci and

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Morrone 1992; Espinosa and Llorente 1993). This
approach combines the biogeographical ideas
formulated by Croizat (1958, 1964) and Hennig's
phylogenetic systematics (1966). The fundamentals of
cladistic biogeography indicate that the congruence
between taxonomic cladograms transformed into
areagrams can help elucidate the fragmentation
sequence of the studied areas and propose hypotheses
of relationships between the areas of endemism
(Contreras-Medina 2006; Morrone 1997).
Cladistic biogeographic hypotheses can show
relationships between areas that could seem different
or even contradictory because the biogeographic areas
and the biotas harbored have complex and reticulated
histories. These hypotheses can be associated with a
given time interval and do not represent atemporal
general hypotheses (Nihei 2008). Donoghue and
Moore (2003) suggested that in the absence of
temporal information, the search for area
relationships may be susceptible to pseudo-
congruence or pseudo-incongruence (Cecca et al.
2011). Pseudo-congruence occurs when the area
cladograms of different taxa show the same area
relationships, even though the taxa diversified at
different times. Pseudo-incongruence occurs when
different area cladograms conflict with each other, but
the age of the taxa analyzed indicates that they
diversified in response to the same events. Distinct
lineages and clades may have different temporal
histories associated with particular historical events.
The relative importance of each of such events can
only be segregated if we can estimate the time of
diversification of the analyzed lineages and separate
them according to time-slicing (Cecca et al. 2011;
Upchurch et al. 2002). In cladistic biogeography,
time-slicing is defined as the partitioning analysis of
taxa under a temporal sequence, where each
stratigraphical interval is known as a time-slice (Cecca
et al. 2011). Time-slicing has been applied in recent
cladistic biogeographic studies to analyze endemic
areas of North American deserts (Gámez et al. 2017)
and to discern the biotic affinities of the Mexican
Transition Zone (Corral-Rosas and Morrone 2017).
The Mesoamerican highlands include several
distinct mountain ranges in Mexico and Central
America. The Mesoamerican mountain ranges is a
region that is currently recognized as a biodiversity
hotspot at a global scale (Myers, Mittermeier et al.
2000) characterized by its high levels of
diversification and endemism (Flores-Villela 1993).
130
The Mesoamerican mountain ranges include the
Sierra Madre Occidental and Sierra Madre Oriental,
both of which extend from north to south in the
western and eastern side of Mexico, respectively; the
Trans-Mexican Volcanic Belt, which runs from east to
west through central Mexico; the Sierra Madre del Sur
along the south-western coast of Mexico; the
highlands complex in central Oaxaca, Mexico; the
mountains in Chiapas, Mexico and north-western
Central America and the Talamanca Cordillera
including the Talamanca highlands and the volcanic
ranges of the northwest and central Costa Rica
(Marshall 2007) (Fig. 1).
Tropical montane cloud forests (TMCFs) within
the Mesoamerican highlands are recognized
worldwide because of their extraordinary biodiversity,
which is severely threatened (Aldrich et al. 2000;
CONABIO 2010; Rojas-Soto et al. 2012). The
Mesoamerican TMCFs exhibit a significant
geographical disjunction, separating forest patches
and the mountain range systems. The fragmented
pattern of these TMCFs represents an ideal system
model for studying evolutionary biogeography (Luna-
Vega et al. 1999; Sullivan et al. 2000).
The historical relationships of the Mesoamerican
highlands are still under investigation (Flores-Villela
and Goyenechea 2001). Therefore, there are no
explicit hypotheses regarding the biogeographical
relationships of the TMCFs endemic areas. Previous
studies have shown a close relationship between
vascular plants (Luna-Vega et al. 2001) and birdlife
(Sánchez-González et al. 2008) of the Sierra Madre
del Sur and the Sierra Madre Oriental and those of the
TMCFs of Central America. However, these
hypotheses about the relationships among the TMCFs
are based on a distributional pattern among taxa.
Therefore, corroboration through a cladistic
biogeography analysis is required, which involves
comparing area cladograms derived from taxonomic
cladograms (Morrone 2004) of endemic or
characteristic taxa to the TMCFs to propose historical
relationships hypotheses among areas of endemism
for TMCFs.
Integrating molecular phylogenetic data into a
cladistic biogeographic framework for different time-
slices may be helpful to empirically assess the area's
relationship over time (Gámez et al. 2017). Likewise,
analyzing the cenocrons separately by time-slices may
have consequences in determining the
biogeographical affinities of the areas (Corral-Rosas

Fig. 1 Endemic areas analyzed are the main Mesoamerican mountain ranges where tropical montane cloud forests
occur.
and Morrone 2017). Therefore, our purpose was to
formulate cladistic biogeographic hypotheses among
areas of the Mesoamerican highlands with an
emphasis on TMCFs areas of endemism based on the
phylogenetic hypotheses of sympatric taxa over three
time-slices (Miocene, Pliocene, and Pleistocene), and
to contrast the obtained results with the hypotheses of
areas' relationships generated in previous studies.
This study could contribute to the knowledge about
the evolution of Mesoamerican TMCFs, one of the
world's most diversified biotic hotspots.
2 Materials and Methods
2.1 Study areas
We analyzed nine areas previously recognized by
Arriaga et al. (1997), Espinosa et al. (2000), and
Morrone (2019) as endemism areas. The analyzed
areas are the main Mesoamerican mountain ranges
where TMCFs occur from moderate to high elevations
in each mountain range (Halffter 2017; Luna-Vega et
al. 1999, 2001; Sánchez-González et al. 2008). In
addition, we included two more areas of endemism:
J. Mt. Sci. (2023) 20(1): 129-140
the Sierra de Los Tuxtlas and the Talamanca
Cordillera (Fig. 1), previously recognized by Flores-
Villela and Goyenechea (2001), which contain taxa
with a distribution shared with the Chiapas Highlands
in Mexico and Guatemala. Based on a previous
regionalization proposed by Luna-Vega et al. (2004)
of the Sierra Madre Oriental, as well as recent studies
where different taxonomic groups with distribution in
the TMCFs show different levels of divergence in their
lineages (Grünwald et al. 2015; Mota-Vargas et al.
2017; Parra-Olea et al. 2005; Vallejo and González-
Cózatl 2012). Because of this, we decided to divide
this mountain range into two areas for analysis: the
northern Sierra Madre Oriental and the southern
Sierra Madre Oriental. The areas considered as units
in the present study (Fig. 1) are the following:
- Northern Sierra Madre Oriental (nSME): north-
eastern Mexico, the TMCFs are located in the southwest
and north-central Tamaulipas and northeast of Nuevo
León (Gual-Díaz and González-Medrano 2014).
- Southern Sierra Madre Oriental (sSME): east-
central Mexico, the TMCFs are located in a narrow
strip from Xilitla in the SE of San Luis Potosí to the
Santo Domingo River Canyon in the north of Oaxaca
(Gual-Díaz and González-Medrano 2014).
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- Sierra Madre Occidental (SMOcc): western Mexico,
the TMCFs in this area have a fragmented distribution
composed of small fragments, mainly in Sinaloa.
- Trans-Mexican Volcanic Belt (TVB): central
Mexico, extending between Jalisco and Veracruz,
virtually cutting Mexico into northern and southern
halves (Marshall and Liebherr 2000).
- Oaxacan Highlands (OH): north-eastern part
of the Mexican state of Oaxaca, including the
mountain ranges: Sierra de Juárez, Nudo de
Zempoaltépetl, and Sierra Mazateca. Some authors
have recognized that this area may be a part of the
Sierra Madre del Sur (Cervantes-Zamora 1990) or the
southernmost portion of the Sierra Madre Oriental
(Morrone 2017).
- Sierra Madre del Sur (SMS): south-central
Mexico includes the mountains of Guerrero and
Oaxaca, limited by the Trans-Mexican Volcanic Belt in
the north and the Isthmus of Tehuantepec and the
Sierra de Juárez in the east. The TMCFs have a
fragmented distribution in the Mexican states of
Michoacán, Guerrero and Oaxaca (Gual-Díaz and
González-Medrano 2014).
- Sierra de Los Tuxtlas (TUX): in the southeast
of the Mexican state of Veracruz, it includes the Sierra
de Santa Marta and Los Tuxtlas. This area was
considered a biogeographic province by Escalante et
al. (1993), a biogeographic sub-province by Espinosa
et al. (2008), and a biotic district by Morrone (2014).
- Chiapas Highlands (CHI): mountainous areas
in southern Mexico, Guatemala, Honduras, El
Salvador, and Nicaragua, ranging from 500 to 2000
m. The TMCFs in this area are found in patches in the
mountainous massifs of Chiapas, continuing into the
Nicaraguan Depression (Kappelle and Brown 2001;
Marshall 2007; Rovito and Parra-Olea 2016).
- Talamanca Cordillera (TAL): extends from
northern Costa Rica through western Panama (Savage
1966). The TMCFs occur between elevations of 500 to
3500 m. They are in the Guanacaste cordillera, Tilarán,
Central Volcanic, and Talamanca (Kappelle 2001).
2.2 Analyzed taxa
We analyzed the geographic distribution and
phylogenetic relationships of 29 terrestrial taxa,
including genera and species of mammals, birds,
reptiles, amphibians, and plants (Table 1). They were

Table 1 Taxa analysed and classified according to the time slices to which they belong, with references.
Time-slice Group Taxon References
Chiropterotriton García-Castillo et al. 2017
Miocene Amphibians Sarcohyla Caviedes-Solis et al. 2018
(23-5.3 Myr) Thorius Rovito et al. 2013
Birds Lampornis García-Moreno et al. 2006
Plants Quercus (section Quercus) Hipp et al. 2018
Aquiloeurycea Sandoval-Comte et al. 2017
Amphibians Ishtmura Sandoval-Comte et al. 2017
Pliocene Ishtmura belli Bryson et al. 2018
(5.3-2.5 Myr) Reptiles Crotalus intermedius Bryson et al. 2011
Birds Dendrortyx Tsai et al. 2019
Cryptotis Guevara and Cervantes 2014
Mammals
Habromys León-Paniagua et al. 2007
Plants Moussonia deppeana Ornelas and González 2014
Atropoides Castoe et al. 2009
Reptiles
Xenosaurus Nieto-Montes de Oca et al. 2017
Aphelocoma unicolor Venkatraman et al. 2019
Arremon brunneinucha Moreno-Contreras et al. 2020
Aulacorhynchus Bonaccorso et al. 2011
Chlorospingus ophthalmicus Bonaccorso et al. 2008
Birds
Cyanolyca Bonaccorso 2009
Pleistocene
Dendrortyx macroura Tsai et al. 2019
(2.5-0.1 Myr)
Lepidocolaptes affinis Arbeláez-Cortés et al. 2010
Myioborus miniatus Pérez-Emán et al. 2010
Glaucomys volans Kerhoulas and Arbogast 2010
Hadleyomys Almendra et al. 2018
Megadontomys Vallejo and González-Cózatl 2012
Mammals
Microtus Crawford et al. 2011
Peromyscus aztecus Sullivan et al. 2000
Reithrodontomys sumichrasti Hardy et al. 2013

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chosen because phylogenetic hypotheses were
available for them. Their species are primarily
exclusive, endemic to, or characteristic of the TMCFs
and their distributional ranges correspond to the
analyzed areas. We selected those taxa that inhabit at
least three of the areas of endemism described above.
Although other potential taxa with published
phylogenetic analyses could be considered, some of
them and their species do not chiefly inhabit humid
montane forests, so their inclusion may obscure the
real biogeographical patterns. Some taxa analyzed
here have been considered in previous cladistic
biogeographical studies because their endemism areas
cover the distributional pattern of montane cloud
forests (Corral-Rosas and Morrone 2017; León-
Paniagua and Morrone 2009). Therefore, some
historical relationships between the areas could be
concordant with these studies. Then, we assigned
each taxon to a given time slice using its estimated
minimum age of divergence. Finally, we used the
phylogenetic data of the basal node of each cladogram
to define the minimum age of each taxon. We
considered this age as relative, as a reference for
allocation to specific time slices, which are: Miocene
(23-5.3 Myr), Pliocene (5.3-2.5 Myr), and Pleistocene
(2.5-0.1 Myr).
2.3 Cladistic biogeographical analysis
Parsimony analysis of paralogy-free subtrees was
applied (Contreras-Medina et al. 2007; Morrone
2009; Nelson and Ladiges 1996) to obtain general
area cladograms representing hypotheses of the
biogeographical history of the analyzed taxa and the
areas where their distributional areas. It comprises
the following four basic steps: (1) for each taxon–area
cladogram, we eliminated the duplicated areas or
node-redundant and obtained the subtrees; (2)
components are identified on each subtree; (3) a data
matrix is built, scoring '1' for presence and '0' for the
absence of components in the analyzed areas; and (4)
parsimony analysis of the data matrix is undertaken
to identify the general area cladogram (Fig. 2).
Of the initial 29 taxon-area cladograms, we
identified 32 paralogy-free subtrees and 86
informative components were extracted from them
(Appendix 1). According to the minimum age of each
taxon, we constructed three data matrices, each one
corresponding to successive time-slices: Miocene
J. Mt. Sci. (2023) 20(1): 129-140
time-slice, Miocene + Pliocene time slice, and
Miocene + Pliocene + Pleistocene time slice (Table 1).
To obtain the general area cladograms, we
analyzed the matrices using NONA (Goloboff 1999)
through WINCLADA (Nixon 2002) by applying multiple
tree bisections and reconnections (TBR). In addition,
we included a hypothetical area coded with all 0s to
root the cladograms.
3 Results
We obtained three most parsimonious general
area cladograms (GAC) by analyzing the three matrices
corresponding to three time-slices (Fig. 3); for the
Miocene with ten steps, a consistency index of 0.80
and a retention index of 0.84; for the Pliocene time-
slice with 57 steps, a consistency index of 0.57 and a
retention index of 0.53; finally, for the Pleistocene
time-slice with 162 steps, a consistency index of 0.53
and a retention index of 0.59.
The general area cladograms obtained for the
Miocene time-slice (23-5.3 Myr) showed the following
sequence: Sierra de los Tuxtlas (TUX), Sierra Madre
Occidental (SMOcc), northern Sierra Madre Oriental
(nSME), Chiapas highlands (CHI)-Talamanca
Cordillera (TAL), Trans-Mexican Volcanic Belt (TVB),
southern Sierra Madre Oriental (sSME), Sierra Madre
del Sur (SMS)-Oaxacan highlands (OH) (Fig. 3a).
The general area cladogram for the Pliocene time-
slice (5.3-2.5 Myr) (Fig. 3b) presented a dichotomy
between an east clade and a west clade separated by
the Tehuantepec Isthmus. The west clade showed the
following sequence: Sierra de los Tuxtlas (TUX),
Fig. 2 Paralogy-free subtree analysis. (a) Taxonomic
cladogram; (b) Taxon-area cladograms with paralogous
nodes; (c) Identify the paralogy-free subtrees; (d)
Represent the nodes of all the paralogy-free subtrees in a
component or three-item matrix; (e) the general area
cladograms.
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Some area relationships

shown matched in all the
general area cladograms for
each time slice. For example,
the close relationship
between the southern Sierra
Madre Oriental (sSME),
Sierra Madre del Sur (SMS),
and the Oaxacan highlands
(OH) is maintained
throughout the general area
cladograms of the three-
time slices. In addition, the
Talamanca Cordillera (TAL)
and Chiapas Highlands (CHI)
are shown as sister areas in
the Miocene and Pliocene
time-slices (Fig. 3).
Geological events of the
main geological features of
Mesoamerica that might be
correlated to the general
area cladograms obtained
for the different time slices
(Fig. 3) are as follows:

3.1 Early-Late-Miocene
time slice (23-5.3 Myr)

Fig. 3 General area cladograms obtained, and corresponding maps. (a) Miocene Important geological
time-slice, (b) Pliocene time-slice, and (c) Pleistocene time-slice. Areas: Northern events occurred over this
Sierra Madre Oriental (nSME); Southern Sierra Madre Oriental (sSME); Sierra Madre
Occidental (SMOcc); Trans-Mexican Volcanic Belt (TVB); Oaxacan Highlands (OH); period with consequences
Sierra Madre del Sur (SMS); Chiapas Highlands (CHI). for the lowland biota of
central Mexico: (1) Late
Chiapas highlands (CHI)-Talamancan Cordillera (TAL). uplift of the Sierra Madre Occidental at the western
The east clade showed the following sequence: part of central Mexico (~22-20 Myr) developing an
northern Sierra Madre Oriental (nSME), Trans- extensive rain shadow and promoting the formation
Mexican Volcanic Belt (TVB), southern Sierra Madre of thorn scrub lowlands on the side of the mountain
Oriental (sSME), Sierra Madre del Sur (SMS)-Oaxacan opposite to the wind (Chihuahuan Desert). (2)
highlands (OH). Formation episodes of the Trans-Mexican Volcanic
The general area cladogram for the Pleistocene Belt during the Early to Mid-Miocene (19-8 Ma). This
time-slice (2.5-0.01 Myr) (Fig. 3c) showed two clades: included the formation fo low elevation volcanoes,
in one clade, the Sierra Madre Occidental (sMOcc) and beginning in the east and proceeding westward over
the Trans-Mexican Volcanic Belt (TVB) are shown as the east part. The Trans-Mexican Volcanic Belt
sister areas. The other clade showed the following developed during 19 Ma, along four episodes of
sequence: northern Sierra Madre Oriental (nSME), volcanism that affected the area asynchronously;
Talamanca Cordillera (TAL), Sierra de los Tuxtlas orogenia: Miocene-Pliocene (east) and Pleistocene-
(TUX), Chiapas highlands (CHI), southern Sierra Quaternary (west). (3) The main tectonic events that
Madre Oriental (sSME), and Sierra Madre del Sur formed the Sierra de Los Tuxtlas occurred during the
(SMS)-Oaxacan highlands (OH). late Miocene (Ferrari et al. 2012; Gámez et al. 2017;

134

Mastretta-Yanes et al. 2015). (4) The region between
CHI and SMS suffered a partial down-dropping
during the late Miocene to early Pliocene, leading to
the destruction of what is thought to have been a
highland corridor spanning the current Ishtmus of
Tehuantepec (Barrier et al. 1998). (5) Existence of a
marine gap between the Chortis and Lower Central
American highlands during the Miocene and the
majority of the Pliocene. The Nicaragua Depression
separates two highland masses, The Chortis block
highlands (Honduras and Nicaragua) to the north and
the Lower Central American highlands of Costa Rica
and Panama (Marshall 2007; Rogers et al. 2002).
Alternatively, Kirby and MacFadden (2005) have
suggested that a narrow landmass connected modern-
day Honduras and Costa Rica during this time.
3.2 Pliocene time slice (5.3-2.5 Myr)
During the Late Pliocene, the Trans-Mexican
Volcanic Belt underwent magmatic episodes at
different points along the current eastern and western
portions, continuing the formation of the mountain
range (Ferrari et al. 2012). The Isthmus of
Tehuantepec is a narrow (ca. 200 km) lowland strip of
land between the sierras of Oaxaca and Central
America, extending along a fault zone and formed as
the result of subsidence associated with tectonic
extension in the late Miocene to Pliocene (Barrier et al.
1998). Final formation of the Chiapas highlands
associated with tectonic activity at the triple plate
junction at the Isthmus of Tehuantepec. Geological
reconstructions pointed to a Pliocene (3-4 Myr)
closure of the Isthmus of Panama (Coates and
Obando 1996). However, recent geological and
geochemical evidence suggests a much earlier near-
closure of the Isthmus of Panama in the Miocene
around 15 Mys and even the tectonic collision
between the Panama arc and South America began
23-25 Myr (Farris et al. 2011).
3.3 Pleistocene time slice (2.4-0.01 Myr)
The main magmatic episodes of the Trans-
Mexican Volcanic Belt were the closing of the
mountain range over central Mexico (Ferrari el at.
2011), forming the current geographical arrangement
of Mexico. The latest eruptions of the San Martín
Pajapan and Santa Marta volcanoes occurred between
2.4-1.0 million years ago. The last tectonic event was
J. Mt. Sci. (2023) 20(1): 129-140
the definitive land connection between Middle and
South America. Climatic cycles began in the late
Pliocene and extended through the Pleistocene.
4 Discussion
The implementation of cladistic biogeography
analyses by time slices in an additive synchronous
manner allowed us to infer the area relationships
among TMCFs and determine their biogeographic
affinities. Some of these relationships were identified
in previous studies with different taxa and
biogeographic methods. For example, Luna-Vega et al.
(1999) proposed a preliminary hypothesis for area
relationships when analyzing 24 localities of the
Mexican TMCFs that correspond to five Mexican
floristic provinces sensu Rzedowski (1978). They
found that the areas located in the Sierra Madre
Oriental, the Sierra Madre del Sur, and the Trans-
Mexican Volcanic Belt have a close relationship.
These relationships are similar to our results for the
Miocene time slice.
Our CGA results for the Mioceno and Pliocene
time-slices showed that the Isthmus of Tehuantepec
acted as a geographic barrier that fragmented the
TMCFs into two portions: west of the Isthmus and
east of the Isthmus. We suggest that this disjunction
gradually occurred during the Pliocene (5.3-2.5 Myr)
because the Trans-Mexican Volcanic Belt formed at
different ages. As a result, the TMCFs located at the
west of the Isthmus had a greater biogeographic
affinity to the Nearctic region. Our statement is
supported by the fact that northern biotic elements of
more recent penetration in the MTZ could not
penetrate southwards as they found lowlands because
the Isthmus of Tehuantepec was already established
(Halffter 2017). The Isthmus of Tehuantepec has been
considered in several biogeographic studies as a
physiographic and ecological barrier that split the
biota between the Chiapas Highlands and the rest of
Mexico (Arellano et al. 2005; Barrier et al. 1998;
Carleton et al. 2002; León-Paniagua et al. 2007;
Sullivan et al. 2000).
Molecular analyses have shown a congruence
between the values of genetic divergence among the
mountain faunas (e.g., Campylopterus, Cryptotis,
Glaucomys, Papogeomys, Habromys, Peromyscus
aztecus, Reithrodontomys, among others) at both
sides of the Isthmus of Tehuantepec (Arellano et al.
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2005; Edwards and Bradley 2002; León-Paniagua et
al. 2007; Esteva et al. 2010; Ornelas et al. 2013;
Rovito et al. 2015; Sullivan et al. 1997, 2000). Thus,
our results suggest that the Isthmus of Tehuantepec
does not always act as a biogeographic barrier
(Pleistocene).
The Pleistocene GAC that resulted from our
analysis, which shows a clade composed of forest from
eastern and southern Mexico to Central America (Fig.
3C), closely agrees with the area relationships
obtained by Sánchez-González et al. (2008) from the
distribution patterns of Neotropical humid montane
forests' avifauna. They obtained a Mesoamerican
clade consisting of the endemic avifauna of the humid
montane forests of the Sierra Madre del Sur, northern
and southern Sierra Madre Oriental, and Oaxacan
and Chiapas Highlands. This clade includes the
Isthmus of Tehuantepec, widely recognized as a
crucial vicariant event that modeled the
Mesoamerican biota's diversity (Morrone and
Márquez 2001; Prance 1982).
Likewise, the dichotomy shown in the Pleistocene
GAC suggests that these forests are well-differentiated
into two regions: the TMCFs that belong to the Sierra
Madre Occidental and the Trans-Mexican Volcanic
Belt with an affinity to the Nearctic region and the
TMCFs that correspond to the rest of Mesoamerica
with an affinity to the Neotropical region. This
relationship pattern is consistent with previous
cladistic biogeography studies of the ZTM (Corral-
Rosas and Morrone 2017; Marshall and Liebherr
2000; Miguez-Gutiérrez et al. 2013), where a strong
relationship between the Sierra Madre Occidental and
the Trans-Mexican Volcanic Belt is evident. Likewise,
once the geographical connection between
Mesoamerica and South America had been
established, around 2.6 Myr, the Great American
Biotic Interchange triggered (Webb 2006), and the
elements of the Neotropical fauna in their movement
northwards encountered geographical barriers such
as the Trans-Mexican Volcanic Belt and continued
northwards along the coastal plains (Halffter 2017).
Considering all the biogeographical relationships
in our study, we suggest that the current distribution
of TMCFs was the product of vicariant and dispersal
events associated with geological events. Geology
transformed physiography and therefore became a
climate modifier. Later, climate cycles during the
Quaternary Period promoted recent evolutionary
processes (Cevallos-Ferriz et al. 2012; Rahbek et al.
136
2019a). According to the simulations of the last glacial
maximum (LGM) and the paleo-data available for
Mesoamerica during the Quaternary Period's
glaciations (Caballero et al. 2010; Graham 1999; Still
et al. 1999), climate changes promoted expansion
cycles of the Neotropical biotas to which species that
has previously adapted to the TMCFs responded by
expanding their distribution to the lowlands during
the glacial periods. During subsequent interglacial
periods, the distribution of TMCFs contracted,
promoting isolation, the divergence of lineages, and
biotic differentiation between TMCFs areas (Ornelas et
al. 2013).
The fossil record shows that cold-temperate
affinity taxa extended to lower elevations during the
Last Glacial Maximum (20 kya) and then contracted
to higher elevations as conditions began to warm
during the Holocene (Lozano-García et al. 2005;
Ortega-Rosas et al. 2008). Changes in precipitation
also occurred, a factor that was particularly important
for cloud forest species (Ramírez-Barahona and
Eguiarte 2013). An example of this is the current
distribution patterns of various plant taxa such as
Fagus, Liquidambar, and Acer, as well as animal taxa
such as the rodents Microtus, Peromyscus, and
Heteromys (Ceballos et al. 2010) distributed in the
mountainous areas of the eastern United States, the
Sierra Madre Oriental, and the Chiapas Highlands,
continuing through to Guatemala.
Glacial periods generally expanded the
distribution ranges of TMCFs species, while warmer
interglacial periods resulted in population
fragmentation, differentiation, and possible
speciation within mountain ranges. The combination
of events and the interactive processes of dispersal
and displacement, niche evolution, persistence, and
extinction promoted the geographical isolation of
populations (Nevado et al. 2018; Rahbek et al. 2019b)
and, therefore, the spatial patterns of biodiversity.
Our study provides empirical evidence on the
biogeographical relationships of Mesoamerican
TMCFs over time. The current distribution pattern of
these forests can be explained by geological events
that modified the landscape and, consequently, the
climatic conditions of the areas during the Miocene-
Pliocene (Ferrari et al. 2012). Likewise, the direct
interactions between the global climate cycles and the
complex topography of mountainous areas that
caused variations in scenopoetic conditions eventually
promoted the expansion-contraction of TMCFs areas

during the Pleistocene-Holocene (Graham 1999;
Ornelas et al. 2013; Rahbek et al. 2019b).
There are different views on whether TMCFs are
considered to be a natural biogeographic unit. The
distributional congruence of different plant genera
(Luna-Vega et al. 2001) and birds (Sánchez-González
et al. 2008) that are characteristic of these forests
suggests that they could adequately constitute a
biogeographic unit since the widespread distribution
of habitat-dependent taxa is evidence of common
history (Chapman 1926). A recent study led by
Rahbek et al. (2019b) assumes that, as an island, each
mountainous region can be viewed as a biogeographic
unit in itself, with in situ extinction and speciation
processes playing a pivotal role in building the
regional species assemblage. Likewise, the
phylogenetic information obtained from various taxa
shows a geographical structure of the Mesoamerican
and South American clades.
5 Conclusions
To conclude, the incorporation of the temporal
dimension in this study allowed, in practice, a
comprehensive and congruent analysis of space, time,
and form. This temporal dimension makes it possible
to address the dynamics of the biogeographical
relationships between the areas of endemism over
time and formulate robust biogeographical
hypotheses. The results of our analysis show that the
TMCFs of the eastern and south-eastern sides of
Mexico, and the Sierra Madre del Sur to the
Talamanca Cordillera, are characterized by the same
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M. Castro-Torreblanca thanks the Programa de
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