Species delimitation and
integrative taxonomy of the Reithrodontomys mexicanus (Rodentia:
Cricetidae) cryptic complex
Daily Martínez-Borrego1, Elizabeth
Arellano1*, Francisco X.
González-Cózatl1, Sandra M.
Ospina-Garcés2, Duke S. Rogers3
1Centro de
Investigación en Biodiversidad y Conservación, Universidad Autónoma del
Estado de Morelos, México.
2Centro de Investigaciones Tropicales, Universidad
Veracruzana, México.
3Department of Biology and Monte L Bean Life Science
Museum, Brigham Young University, USA.
*Corresponding author: elisabet@uaem.mx
Running title: Integrative
taxonomy of the R. mexicanus complex
ABSTRACT
Species boundaries are difficult to establish in groups with very
similar morphology. As an alternative, it has been suggested to
integrate multiple sources of data to clarify taxonomic problems in taxa
where cryptic speciation processes have been reported. This is the case
of the harvest mouse Reithrodontomys mexicanus , which has a
problematic taxonomy history as it is considered a complex species.
Here, we evaluate the cryptic diversity of R. mexicanus using an
integrative taxonomy approach in order to detect candidate lineages at
the species-level. The molecular analysis used one mitochondrial (cytb)
and two nuclear (Fgb-I7 and IRBP) genes. Species hypotheses were
suggested based on three molecular delimitation methods (mPTP, bGMYC,
and STACEY), and cytb genetic distances values. Skull and environmental
space differences between the delimited species were also tested to
complement the discrimination of candidate species. Based on the
consensus across the delimitation methods and genetic distance values,
four species were proposed, which were mostly supported by morphometric
and ecological data: R. mexicanus clade I, R. mexicanusclade IIA, R. mexicanus clade IIIA, and R. mexicanus clade
IIIB. In addition, the evolutionary relationships between the species
that comprise the R. mexicanus group were discussed from a
phylogenetic approach. Our findings present important taxonomic
implications for Reithrodontomys , as the number of known species
for this genus increases. Furthermore, we highlight the importance of
the use of multiple sources of data in systematic studies to establish
robust delimitations between species considered taxonomically complex.
Keywords: Cricetidae, rodents, cryptic speciation, molecular
delimitation, multiples lines of evidence
INTRODUCTION
A continuing challenge in systematics is the determination of which
species concept is most appropriate for proposing and delimiting
species. Most species have been described using morphological traits
(Mayden 1997), but an increasing
number of studies are reporting new species using molecular data (see
Jörger and Schrödl 2013).
Controversy around species concepts is largely due to the different
nature of the information upon which different concepts are based (de
Queiroz 2007). For example, the Phylogenetic Species Concept (Cracraft
1989) tends to be used when genetic data are analyzed, while studies
focusing on reproductive isolation tend to prefer the Biological Species
Concept (Mayr 1942). Bradley and Baker (2001) proposed delimiting mammal
species using the Genetic Species Concept, specifically using genetic
distances estimated from the mitochondrial gene Cytochrome b (cytb;
Baker and Bradley 2006). In an attempt to eliminate the species problem,
de Queiroz (1998; 2005; 2007) proposed the General Lineage Species
Concept (GLC). This unified concept uses different species properties,
considering elements of the most accepted concepts, and integrates
multiple lines of evidence to establish boundaries between species.
Therefore, any criteria identifying a separately evolving metapopulation
lineage are considered relevant to identify species (de Queiroz 2005).
This multisource approach is known as integrative taxonomy (Dayrat 2005)
and has been widely recommended in systematic studies (see Padial et al.
2010; Sangster 2018).
Molecular data have been crucial for studying cryptic species in
rodents; they allow both the determination of the number of entities
comprising a species complex and the delimitation of those entities
(D’Elía et al. 2019; and references therein). Using an integrative
taxonomy approach, species phylogenetic hypotheses in rodents have been
corroborated by other data sources such as morphology, ethology,
biogeography, and ecology (e.g., Almendra et al. 2018; Rivera et al.
2018; Onditi et al. 2021). Thus, the congruence among several lines of
evidence indicates robust species hypotheses (Dayrat 2005; Padial et al.
2010).
Reithrodontomys mexicanus (Saussure, 1860) is a cricetid rodent
with a discontinuous geographic distribution from Mexico to northwestern
South America (Hooper 1952; Hall 1981). Their populations occupy a
variety of habitats including humid pine-oak forests, cloud forests, and
lowland deciduous forests, and they can generally be found in an
altitude range from around 1,000 to 3,800 m. Recent changes in its
taxonomy have been proposed due to divergent lineages detected using
different genetic loci and craniodental characteristics (summarized in
Martínez-Borrego et al. 2020). Arellano et al. (2005), employing
information from the cytb gene, identified three well-differentiated
clades for this species. Based on those findings, they recommended
elevating R. cherrii to the species level and proposed the
existence of an undescribed species distributed in the Sierra Madre
Oriental and northern Oaxaca, Mexico (Arellano et al. 2005). Using
mitochondrial and nuclear genes, Miller and Engstrom (2008) also
suggested that R. mexicanus constitutes a cryptic species
complex, while Gardner and Carleton (2009) proposed the former R.
m. garichensis as a species of the R. mexicanus group based on
craniodental differences compared to the remaining Central American
species of the subgenus Aporodon .
Thus, as a species complex, R. mexicanus sensu lato needs to be
reevaluated from a taxonomic point of view. We hypothesize that each of
the divergent lineages within R. mexicanus constitutes valid
species given their significant genetic, morphological, and ecological
differences. Here, our goal is to assess the cryptic diversity of this
species based on Arellano et al. (2005) suggestion that it is composed
of at least two species. Putative species will be delimited in
accordance with the GLC under an integrative taxonomy approach.
MATERIALS AND METHODS