ORIGINAL PAPER

Contrasting Phylogenetic and Diversity Patterns in Octodontoid
Rodents and a New Definition of the Family Abrocomidae

Diego H. Verzi1 & A. Itatí Olivares1 & Cecilia C. Morgan1
& Alicia Álvarez2

# Springer Science+Business Media New York 2015

Abstract Octodontoidea is the most species-rich clade
among hystricomorph rodents. Based on a combined parsimo-
ny analysis of morphological and molecular data of extinct
and extant species, we analyze the history of South
American octodontoids and propose ages of divergence older
than interpreted so far. Early Abrocomidae are recognized for
the first time, and a new definition of the family is provided.
Traditionally accepted fossil-based times of origin for the
southern clades are reinterpreted as later stages of differentia-
tion markedly uncoupled from the origin, differentiation im-
plying specializations for open environments as shown in a
morphospace of skull variation. Origin of crown groups is also
strongly uncoupled from origin of clades as a consequence of
extinction of deep lineages. In the resulting diversity pattern of
modern southern clades of octodontoids, the combination of
greater disparity, less content of evolutionary history, and low-
er taxonomic diversity, compared to their northern counter-
parts, appears at first counterintuitive. We propose that prima-
ry components of diversity derived from evolutionary trans-
formation or anagenesis, on the one hand, and from cladogen-
esis and extinction, on the other, should not be considered
associated, or at least not necessarily. Certain patterns of

relationships between these distinct components could be
driven by environmental dynamics. Like environments,
octodontoid diversity would have been more stable in north-
ern South America, whereas in the south, both strong adaptive
change and extinction would have been triggered by emerging
derived environments.

Keywords Rodentia . South AmericanOctodontoidea .

Abrocomidae . Phylogeny . Divergence times . Diversity
patterns

Introduction

Octodontoidea is the most diverse clade among both New
World and Old World hystricomorph rodents (Woods and
Kilpatrick 2005). In the recent South American fauna, it in-
cludes small to middle sized rat-like rodents of the families
Abrocomidae, Echimyidae (including Myocastor, sometimes
included in a family of its own), and Octodontidae (including
Ctenomyinae) (Upham and Patterson 2012; Patton et al.
2015). The sister families Echimyidae and Octodontidae com-
prise more than 60 % of the extant species of South American
Hystricomorpha (caviomorphs), and have the richest fossil
record of the suborder (McKenna and Bell 1997). Echimyids
have arboreal (tree rats, bamboo rats) or terrestrial to fossorial
lifestyles (spiny rats), and they inhabit Amazonian, coastal,
and Andean tropical forests in northern South America, and
occasionally more open, xeric habitats in the Cerrado and
Caatinga (Eisenberg and Redford 1999; Emmons and Feer
1999; Bonvicino et al. 2008; Emmons et al. 2015); the semi-
aquatic coypu Myocastor is an exceptional, large-sized repre-
sentative widely distributed in southern South America.
Octodontids are terrestrial to fossorial (degus, rock rats, visca-
cha rats) and subterranean rodents (coruros, tuco-tucos)

Electronic supplementary material The online version of this article
(doi:10.1007/s10914-015-9301-1) contains supplementary material,
which is available to authorized users.

* Diego H. Verzi
dverzi@fcnym.unlp.edu.ar

1 CONICET. Sección Mastozoología, Museo de La Plata, Paseo del
Bosque S/N°, B1900FWA La Plata, Argentina

2 CONICET. División Mastozoología, Museo Argentino de Ciencias
Naturales ‘Bernardino Rivadavia’, Av. Ángel Gallardo 470,
C1405DJR Buenos Aires, Argentina

J Mammal Evol
DOI 10.1007/s10914-015-9301-1

http://dx.doi.org/10.1007/s10914-015-9301-1
http://crossmark.crossref.org/dialog/?doi=10.1007/s10914-015-9301-1&domain=pdf


endemic to mesic and arid biomes of southern South America
(Redford and Eisenberg 1992; Ojeda et al. 2013). The living
abrocomids make up a less diversified clade, sister to
echimyids-octodontids (Upham and Patterson 2012, in press).
They comprise nine (or perhaps ten) living species classified
in two genera, with terrestrial, scansorial (Abrocoma, chinchil-
la rats), and arboreal habits (Cuscomys, arboreal chinchilla-
rats), and distributed in southern South America through the
central Andes, in cloud forests, mesic environments, and Puna
and Monte deserts (Glanz and Anderson 1990; Emmons
1999; Braun and Mares 2002; Taraborelli et al. 2011; Patton
and Emmons 2015).

The fossil record of octodontoids is at least as early as late
Oligocene (Wood and Patterson 1959; Patterson and Wood
1982; Vucetich et al. 2014) or may possibly reach even the
middle-late Eocene (Frailey and Campbell 2004; Campbell
et al. 2004; Antoine et al. 2012: 1323). The phylogenetic
position of the ancient, pre-late Miocene representatives of
this strongly diversified clade is controversial. The difficulties
in interpreting early fossils arise firstly from the fact that they
are usually poorly preserved. Even beyond this, a conceptual
issue also creates controversy; ancient fossils may share few
apomorphies with modern species even within restricted
clades (see Briggs and Fortey 2005). The adoption of different
criteria regarding the significance of this issue shapes the sys-
tematic, phylogenetic, and chronological delimitation of line-
ages, resulting in differing classification proposals for
suprageneric taxa. Thus, there has been some consensus in
assigning many of the early octodontoids to Echimyidae
(e.g., Patterson and Wood 1982; Vucetich and Verzi 1991;
Carvalho and Salles 2004), partly because the living species
of this family have a conservative molar morphology that is at
least superficially similar to that of ancient octodontoids (Reig
1986); in contrast, Abrocomidae and Octodontidae are fre-
quently thought to have originated during the late Miocene,
based on the first appearances during this lapse of species with
hypsodont molars characteristic of their extant representatives
(Simpson 1945; Vucetich et al. 1999; Arnal and Pérez 2013).
Whereas in the case of Octodontidae alternative proposals
exist that consider this family to be a group as old as the
Echimyidae (Winge 1941; Wood and Patterson 1959;
Patterson and Wood 1982), the Abrocomidae had not been
until now recognized in the pre-late Miocene fossil record.
The first ancient abrocomid, preceding the modern (late
Miocene to Recent) †Protabrocoma and Abrocoma, has been
recognized quite recently among fossils largely assigned to the
conservative family Echimyidae (Verzi et al. 2014).

In this work we present results of a phylogenetic analysis of
a comprehensive sample of South American extinct and extant
octodontoid rodents, and revisit the evolutionary history of the
Octodontoidea. In addition, we provide a new definition of the
family Abrocomidae. First, we analyze the phylogenetic rela-
tionships of a wide sample of living and extinct octodontoids

on the basis of morphological and molecular evidence. The
topologies and datings obtained from these analyses are used
to delimit both taxonomically and temporally the major
octodontoid clades, in agreement with the recognition of
stages of origin and differentiation of these clades. We review
the phylogenetic diversity and morphological variation
encompassed by each clade to assess how cladogenesis, ex-
tinction, and anagenesis play a part in establishing evolution-
ary patterns. We revise the hypothesis that southern
octodontoids present differentiation stages uncoupled from
the origin of clades (i.e., modernization; Verzi et al. 2014,
2015), and analyze possible causes of the occurrence of this
pattern in the context of the palaeoclimatic history of the con-
tinent. We discuss the importance of the environment as a
factor linking the diversity resulting from cladogenesis and
extinction with that arisen from evolutionary transformation
or anagenesis.

Materials and Methods

Phylogeny and Divergence Times

Phylogenetic relationships of extinct and extant octodontoids
were examined through a combined parsimony analysis based
on a dataset of 77 morphological characters (50
craniomandibular and 27 dental from 2252 specimens exam-
ined) and four marker sequences obtained from GenBank
(Online Resources 1 and 2): growth hormone receptor
(GHR, 814 bp; 189 parsimony-informative sites), recombina-
tion activating gene 1 (RAG1, 1072 bp; 89 parsimony-
informative sites), von Willebrand factor (vWF, 1173 bp;
203 parsimony-informative sites), and mitochondrial subunit
12S (12S rRNA, 979 bp; 323 parsimony-informative sites)
genes. The matrix of morphological characters was built fol-
lowing essentially Verzi et al. (2014), and new primary ho-
mologies were recorded, including a new proposal for homol-
ogies of lower molar crests. Genes were selected following
Upham and Patterson (2012). Gene sequences were aligned
using BioEdit 7.2.0 (Hall 1999) with the default values of gap
opening and gap extension. The dataset of morphological
traits was concatenated with the genes sequences, and extinct
taxa were coded as missing for all molecular characters. This
matrix contained a total of 72 taxa and 4216 characters
(Online Resource 1); the sample of South American
octodontoids included 36 of the 53 extinct genera and 28 of
the 33 living genera; Erethizon (Erethizontoidea), Cavia,
Cuniculus, Dasyprocta, Hydrochoerus (Cavioidea), and
Chinchilla (Chinchilloidea) were included as outgroups. The
parsimony analysis was conducted treating gaps as missing
data in TNT 1.1 (Goloboff et al. 2008a, 2008b). The heuristic
search consisted in 10,000 replicates of a Wagner tree with
random addition sequence of taxa and followed by TBR

J Mammal Evol



branch swapping. In addition, we performed an extra round of
TBR on the optimal trees to increase the chance of finding all
minimum-length topologies (Bertelli and Giannini 2005).
Zero-length branches were collapsed if they lacked support
under any of the most parsimonious reconstructions
(Coddington and Scharff 1994). The age of taxa for which
no molecular datings were available was estimated through
the modified Stratigraphic Manhattan Measure (MSM*, Pol
and Norell 2001), which allows integration of phylogeny with
temporal information from the fossil record.

Phylogenetic relationships and molecular dating of diver-
gence times among living octodontoid genera were estimated
through Bayesian inference methods implemented in BEAST
2.1.3 (Bouckaert et al. 2014). The four-gene matrix was ana-
lyzed considering each gene as a partition, so model parame-
ters were estimated independently. The software jModelTest
2.1.5 (Darriba et al. 2012) was employed to determine the
most appropriate model of sequence evolution for each gene;
the best-fit model selected for all genes was general time-
reversible plus among-site rate variation (GTR+G). The anal-
yses were performed using Markov chain Monte Carlo
(MCMC) simulations for 300,000,000 generations and a sam-
ple frequency of 5000. We ran two independent runs. We used
a relaxed molecular clock model, which allows substitution
rates to vary across branches according to an uncorrelated
lognormal distribution (Drummond et al. 2006; Drummond
and Rambaut 2007). The tree prior was set as Yule process.
Convergence in the analyses was determined using the pro-
gram Tracer 1.6 (Bouckaert et al. 2014). We computed the
maximum credibility tree in TreeAnnotator 2.1.2 (Bouckaert
et al. 2014), and the first 6000 sampled trees were excluded.
Seven fossil calibrations were selected for the divergence
analyses, with the selected extinct taxa located on the tree
according to the results of the parsimony analysis (Online
Resource 3). All calibrations were set as minimum dates (the
most reliable date for the oldest levels bearing the indicative
fossil; Benton and Donoghue 2007) using lognormal priors,
which allows considering a soft bound for maximum dates.
Calibrated nodes were constrained as monophyletic.

Morphological and Phylogenetic Diversity

We analyzed the shape variation of the skull in lateral view,
which allows capturing shape changes in the orbit, rostrum,
auditory bulla, and cranial vault. We used a sample of 174
specimens belonging to 44 species of 29 genera of the families
Abrocomidae, Echimyidae, and Octodontidae (Verzi et al.
2015). This dataset included three sufficiently complete skull
remains of the extinct †Eucelophorus chapalmalensis,
†Actenomys priscus, and †Prospaniomys priscus. Two-
dimensional coordinates were captured on digital images of
the skull in left lateral view; for specimens where this side was
damaged, the reflected image of the right side was used. A set

of 20 landmarks and 19 semi-landmarks was chosen to cap-
ture skull morphology in detail (Online Resource 4). The x, y
coordinates of landmarks and semi-landmarks were digitized
using tpsDig version 2.12 (Rohlf 2008). Semi-landmarks were
slid by means of the minimum Procrustes distance criterion
(Bookstein et al. 2002; Perez et al. 2006) using tpsRelw 1.49
(Rohlf 2010). The resulting aligned Procrustes coordinates
were averaged by genus and the consensus configurations
were analyzed by Principal Components Analysis (PCA, also
known as Relative Warps Analysis) in the software MorphoJ
1.05d (Klingenberg 2011). Shape changes were pictured by
means of transformation grids. In order to visualize the phy-
logenetic relationships between the taxa included in this
morphospace, the phylogeny obtained by Bayesian analysis
was mapped onto the bivariate plot of the first two PC using
the software MorphoJ 1.05d (Klingenberg 2011), which re-
constructs the values for ancestral nodes by squared-change
parsimony (Maddison 1991). Disparity was calculated after
Foote (1993) from the landmark data of aligned specimens
(i.e., the configurations that result after sliding semi-land-
marks), using the Procrustes distance from the mean specimen
(centroid) of each group to the average of all the groups as the
distance metric. Disparity values and confidence intervals
were calculated using the DisparityBox 7.14a module of the
IMP714 package (Sheets 2012).

Phylogenetic diversity (PD), expressed as the total length
of all the branches of the tree or a particular clade, was used as
an estimate of evolutionary history contained in each familial
clade (Purvis et al. 2000; von Euler 2001; Erwin 2008); PD
was measured in units of time, i.e., million years (Ma), using
the Total Branch Length estimate (TBL) of the Caper package
for R version 0.5.2 (Omer et al. 2013) on the tree obtained by
Bayesian analysis.

Morphology of Lower Molars and Nomenclature
of Crests

We revisited the lower molar morphology of octodontoids and
generated a new interpretation for the homologies of crests
(Figs. 1, 2 and 3). We do not intend to impart greater impor-
tance to the phylogenetic information provided by molars, but
consider it a necessary task because this issue is far yet from a
consensus (see Patterson andWood 1982; Carvalho and Salles
2004; Frailey and Campbell 2004; Candela and Rasia 2012;
Antoine et al. 2012).

Candela and Rasia (2012) exhaustively revised the crest
homologies in octodontoids, especially Echimyidae, and on
this basis Candela (2015) discussed the dental characters used
in Verzi et al.’s (2014) phylogenetic analysis. In their proposal,
efforts are put on detecting relationships between dental crests
and cusps, a core criterion for determining homologies of
lophs and lophids in rodent molars (Wood and Wilson 1936;

J Mammal Evol



Marivaux et al. 2004). However, in most octodontoids the
detection of cusps is not easy. Butler (1985) proposed that
the molar morphology of caviomorphs is at an evolutionary
grade in which the occlusal surface is a flattened grinding area
adjusted to a single chewing movement, a simplification of the
two-phase chewing of cuspidate molars. More recent findings
have shown the existence of cuspidate patterns in early
caviomorphs (Frailey and Campbell 2004; Antoine et al.

2012), at least in juvenile stages (see e.g., Vucetich and
Verzi 1996; Vucetich and Kramarz 2003; Vucetich and
Vieytes 2006). In any case, Butler’s proposal seems to be the
rule for modern octodontoids (from the late Miocene on) and
even for adult individuals of earlier species.

Beyond their usefulness as landmarks, cusps and crests are
structures that function, and thus undergo changes in position,
size, or timing of development (Butler 1985; Frailey and

Fig. 1 Occlusal morphology of left Dp4-m2 (a,b,e,g,h), Dp4-m1 (c, f, i-
l), m1-2 (m, p, q), m1 (o), and m2 (d, n), with corresponding schematic
illustrations of crest homologies indicated by prime symbols. aHoplomys
gymnurus USP 2001; b and i Proechimys cuvieri UFRJ MN 20313; c
Lonchothrix emiliae MN-UFRJ 4856; d Proechimys roberti MVZ
197578; eMesomys hispidusMVZ 190653; f Trinomys dimidiatusUFRJ
MN 62275; g Trinomys elegans UFRJ MN 43842; h Proechimys
poliopus MLP 22.II.00.7, j Myocastor coypus MLP 20.XII.89.3; k
†Acarechimys minutus MPM-PV 4223; l †Acarechimys minutus MPM-
PV 4193; m †Acaremys (†Sciamys principalis) MLP 15–349; n

†Platypittamys brachyodon (modified from Wood 1949: fig. 3d); o
†Acaremys (including †Sciamys) MLP 84-III-8-83; p †Acaremys (includ-
ing †Sciamys) MLP 84-III-8-43; q Aconaemys porteri UACH 2255
(inverted right molars in b, d, e, f, h, k, p and q). Interpretation of crest
homologies according to Candela and Rasia (2012) and Candela (2015) is
shown in a and c. Schematic illustrations show the interpretation used
here. Abbreviations: Hld hypolophid; Med I metalophulid I; Med II
metalophulid II; Msd mesolophid; Neo neolophid; Psd posterolophid.
Not to scale

J Mammal Evol



Campbell 2004: 98; Lazzari et al. 2015). Therefore, the search
for possible correspondences between structures in molars
must take into account that these are dynamic. At least in
octodontoids, recognition of homologies requires interpreting
changes in the relationships between crests and cusps (or the
areas presumably occupied by the latter) or just between
crests; many of these changes are recurrent and may be
tracked with reasonable confidence.

Figure 1a’ and c’ show the interpretation followed here for the
pentalophodont pattern of the Echimyidae Hoplomys gymnurus
and the more simplified Lonchothrix emiliae, respectively, com-
paredwith the proposal of Candela andRasia (2012) for the same
taxa (Fig. 1a and c, respectively). Candela and Rasia (2012)
interpreted the second and third crests of the pentalophodont
molars as neolophid and metalophulid II, respectively (Fig. 1a),
while in Lonchothrix the second crest is identified as
metalophulid II (Fig. 1c). Their interpretation stems from priori-
tizing the assumed connection of ‘metalophulid II’ with the pre-
sumptive location of the metaconid. This proposal has a series of

difficulties. First, it offers different interpretations for the same
structures depending on whether they are recognized in premo-
lars or molars. Second, penta- and tetralophodonty are assumed
to be fixed, static morphologies without transitional stages be-
tween them. In addition, what Candela and Rasia (2012)
interpreted as metaconid is not always solely this cusp, but in
many cases represents an enlarged area formed by early ontoge-
netic fusion of crests (e.g., Acarechimys minutus, Fig. 1k, l;
Sallamys, Fig. 2a-c; Protadelphomys, Fig. 2h-k). As a result,
these authors offered different interpretations for morphologies
that are essentially identical, such as those of Dp4 vs m1-2 of
Hoplomys (Fig. 1a).

We think that pentalophodonty, tetralophodonty,
trilophodonty (and even more simplified morphologies) should
not be interpreted as static patterns but as part of different trans-
formation pathways that include transitional morphologies
(Figs. 1, 2 and 3). In this sense, the morphology of lophate
deciduous premolars is more stable than that of m1 and m2,
the latter showing more frequent reduction and fusion of crests

Fig. 2 Occlusal morphology of left lower molars, with corresponding
schematic illustrations of crest homologies indicated by prime symbols. a
Dp4-m1 of †Sallamys quispea (based on Shockey et al. 2009: fig. 5); b
m1 of †Sallamys pascuali UATF-V 5010; c m2 of †Sallamys pascuali
UATF-V 5009c; d m2 of †Willidewu estepariusMPEF 5031; e Dp4-m1
of †Willidewu estepariusMPEF 5024; fm2 of †Chasichimys bonaerense
GUNLPam 5068; g Dp4-m2 of †Chasichimys scagliai MMP 481-M

(holotype); h m1 of †Protadelphomys sp. MMP 949-M; i m1-2 of
†Protadelphomys latusMPEF 90–166; jm1-2 of †Protadelphomys latus
MPEF 90-391-4; k m1-2 of †Protadelphomys latus MPEF 90-391-1
(inverted right molars in a, b, e, f, h, i, k). Schematic illustrations show
the interpretation used here. Abbreviations: Hld hypolophid; Med I
metalophulid I; Med II metalophulid II; Msd mesolophid; Psd
posterolophid. Not to scale

J Mammal Evol



at both ontogenetic and evolutionary scales (Frailey and
Campbell 2004; Antoine et al. 2012; see Renvoisé and
Montuire 2015). Taking this into account, and the fact that de-
ciduous premolars and unreplaced molars share an embryologi-
cal origin (see Luckett 1985: 233), the morphology of Dp4 may
be useful to understand that of molars (Carvalho and Salles
2004). In Figs. 1, 2 and 3 it can be seen that the anterior portion
of the molar becomes simplified by crest fusion and reduction
(with the exception of Hoplomys, Fig. 1a). The transformation
pathway in Fig. 1a-j shows how the root of metalophulid II
becomes fused or even submerged into metalophulid I; subse-
quently, the origin of the mesolophid changes progressively by
uniting to the root of metalophulid II (Fig. 1b-g). This gives rise
to ‘crest C’ proposed by Carvalho and Salles (2004), with whose
recognition we strongly agree beyond the different interpretation
of its composition (see Fig. 1d and Carvalho and Salles 2004:
Fig. 6). The disappearance of the fossettid that separates this
mixed-origin crest from metalophulid I originates an anterior
crest simple in appearance but with a composite origin involving
the three above mentioned lophids (Fig. 1g and h). In the molars
of Figs. 1k-o and 2,metalophulid II originates close to the lingual
margin of metalophulid I. In Fig. 1k-o the mesolophid is a crest
whose distal end joins metalophulid II or the distal thickening of
the first crest corresponding to this lophid. The disappearance of
the resulting anterior fossettids leads to the formation of an ante-
rior lobe that is simple in appearance but of composite origin
(Fig. 1m, p, q). Figure 2 shows molars in which the mesolophid
is reduced to a short crest (Fig. 2h-h’) or a little spur (even absent
in some specimens). This spur was considered as the
metalophulid II by Verzi et al. (2014), but later examination of
unpublished material corresponding to †Protadelphomys sp.

(Fig. 2h-h’) in comparison with †Sallamys quispea (Fig. 2a-a’)
led us to revise this interpretation. In †S. quispea it is possible to
track the identity of the above mentioned crests fromDp4 to m1;
in m1, the short metalophulid II and mesolophid are aligned into
a short anteroposterior stretch, as if driven by pressure exerted
from behind on the anterior wall of the hypoflexid in a morphol-
ogy such as that of the Dp4. In these genera, the first lophid
becomes simple but its origin is also composite (Fig. 2b-b’, c-
c’, i-k), as is also the case in †Willidewu and †Chasichimys
(Fig. 2d-e and f-g, respectively).

Figure 3 shows another pattern, in whichmetalophulid II, as a
complete or reduced crest, originates in the posterior protoconid
area and the mesolophid is absent (a short-lived relic of the
mesolophid was detected in the m1-2 of †Caviocricetus MLP
99-XII-10-1/3, MPEF 5076, Fig. 3d-d’; and †Protacaremys
MPEF 5673 and 5652, Fig. 3a-a’; it is also present in
†Dudumus MACN- Pv CH 2040, see Arnal et al. 2014:
Fig. 3c). If metalophulid II remains separated, metalophulid I
does not have any evidence of being a composite crest.

On the basis of available evidence, we have not been able to
track a route of simplification for the trilophodont molar config-
uration of ‘eumysopines,’ ‘echimyines,’ ‘dactylomyines,’ or
abrocomids.

Results

Phylogeny

The combined parsimony analysis of morphological and mo-
lecular data resulted in a single most parsimonious tree 3,572

Fig. 3 Occlusal morphology of
left lower molars, with
corresponding schematic
illustrations of crest homologies
indicated by prime symbols. a
Dp4-m1 of †Protacaremys prior
MPEF 5652; b Dp4-m1 of
†Protacaremys priorMPEF
7557; c Dp4-m1 of
†Prospaniomys priscusMPEF
6447; d m2 of †Caviocricetus
lucasi MPEF 5076; e m1 of
†Deseadomys arambourgiMLP
93-XI-21-5 (inverted right molars
in a, c, d). Schematic illustrations
show the interpretation used here.
Abbreviations: Hld hypolophid;
Med I metalophulid I; Med II
metalophulid II;Msdmesolophid;
Psd posterolophid. Not to scale

J Mammal Evol



steps long (CI=0.56, RI=0.59), which shows the existence of
three main clades within Octodontoidea (Fig. 4). Most nodes
are poorly supported, but show essentially little character con-
flict (high relative Bremer support values).

The clade at node A clusters the traditionally recognized
Abrocomidae, i.e., euhypsodont representatives from late
Miocene to Recent, with late Oligocene to middle Miocene
genera previously assigned to other taxa of Octodontoidea
(Fig. 5; Appendix). Morphological characters supporting this
clade were the anteriorly oriented proximal portion of the
nasolacrimal canal (character state 14–1; Fig. 6), the morphol-
ogy of the lateral margin of the pterygoid fossa, on a
level with its medial margin and extending posteriorly
(character state 35–1), and the position of the anterior
margin of the coronoid apophysis, which is lateral and
ventral with respect to the alveolar margin of the mo-
lars (character state 50–1; Fig. 7). Within this clade, two
subclades were recovered. The first (node E) comprises the
extinct †Caviocricetus-†Dudumus and †Protacaremys-
†BProtacaremys^ denisae-†Prospaniomys-†Deseadomys.
These taxa share the morphology of the origin of the masse-
teric crest, which is ventrally deflected from the notch for the
tendon of the medial masseter muscle (character state 46–2),
and the morphology of the anterior lobe of Dp4 (un-
known in †Deseadomys; character-state 62–2; Fig. 3).
†Caviocricetus and †Dudumus share the morphology
and orientation of the mesolophule on DP4 (character
state 53–1) and M1 (character state 56–1) (Verzi et al. 2014:
Fig. 7a; Arnal et al. 2014: Fig. 4), while †Protacaremys-†BP.^
denisae-†Prospaniomys-†Deseadomys are clustered by the
morphology of the anterior side of metalophulid I and the
protoconid area, the latter presenting an anterior concavity
and a sharp labial end (character state 64–1; Fig. 3). The sec-
ond subclade (node F) includes the extant chinchilla rats
Cuscomys, Abrocoma bennettii, and Abrocoma cinerea com-
plex as well as the extinct †Protabrocoma and †Spaniomys,
and is supported by the shortened lower incisor (character
state 51–1) and the shape of the contour of the hypolophid
(character state 68–1). In modern abrocomids, the lower inci-
sor is extremely short (character state 51–2).

The clade at node B groups the living Octodontidae and
Echimyidae with late Oligocene (late Eocene-early Oligocene
considering †Eodelphomys) - Pleistocene fossils. They share
the metalophulid II of m1-2 originating from the metalophulid
I (character state 65–1; Figs. 1 and 2).

The clade at node C groups the living Octodontidae with late
Oligocene to Pliocene genera (Fig. 5; Appendix). Members of
this clade share the ventral deflection of the masseteric crest
posterior to the notch for the medial masseter muscle tendon
(character state 46–1; Verzi et al. 2014: Fig. 4) and the Dp4with
an anterior rounded lobe (character state 62–1; Figs. 1k, l and
2a, g). Within this group, two major subclades include the tra-
ditionally recognized living and extinct Octodontinae and

Ctenomyinae. The former (node G) includes crown
octodontines and late Oligocene to late Miocene fossils,
which share the mesolophule of M1 with its labial
end joined to the medial wall of the metacone area
(character state 56–1; Fig. 8a, c). The ‘acaremyids’
†Galileomys, †Platypittamys, and †Acaremys (including
†Sciamys) are part of the lineage that leads to extant
octodontines, with which they share the early formation of a
complex lobe anterior to the hypo- and posterolophid in the
lower molars (character-state 67–1; Fig. 1m-q); in living
octodontids this may be seen in early ontogeny (Aconaemys
FMNH 50752, 50754; UACH 2255, Fig. 1q). The grouping of
†Acaremys (including †Sciamys) with traditional octodontines
is supported by the para- and metaflexus closing markedly
earlier than the mesoflexus, the parafossette generally smaller
andmore short-lived than the metafossette (character state 60–
1; Fig. 8b-f) . †Plesiacarechimys + †Acarechimys
minutissimus-†Neophanomys form a clade external to
‘acaremyids’- extant octodontines; these three genera share a
short and posteriorly oriented mesolophule in DP4 and M1
(character states 53–1 and 55–1, respectively; Fig. 8a). The
upper early Miocene †Acarechimys minutus forms a three-
way polytomy with the mentioned clades (Fig. 4).

The clade Ctenomyinae (node H), sister to Octodontinae, is
supported by the foramen into the nasolacrimal canal opening on
the margin of the sphenopalatine fissure, oriented posteriorly
toward the fissure and not visible laterally (character state 12–
1; Fig. 9a-c), the auditory bulla extended posteriorly to the level
of the root of the paroccipital process (character state 45–1; Verzi
et al. 2014: Fig. 6), and the fusion of the mesolophule and
posteroloph+metaloph into a lobe in molars with presence of
paraflexus/fossette and mesoflexus (character state 58–1;
Fig. 8g-k). The late Miocene †Chasicomys and †Chasichimys
are part of the lineage that leads to the modern, euhypsodont
ctenomyines, and the late Oligocene to early Miocene
†Sallamys+†Protadelphomys-†Willidewu are sister to the latter.

The clade at node D comprises the extant Echimyidae and
some of the extinct genera traditionally assigned to this family
(Fig. 5; Appendix). It is diagnosed by the lacrimal foramen
opening into the maxilla (character state 10–1; Fig. 6e), the
presence of a continuous rim (without a suture) formed by
the maxilla around the foramen into the nasolacrimal canal
(character state 11–1), the lateral process of the supraoccipital
extending ventrally below the level of the mastoid process
(character state 39–1; Verzi et al. 2014: Fig. 3), and the rotated
distal portion of the paroccipital process that results in the
posterolateral or posterior orientation of its external margin
(character state 42–1; Verzi et al. 2014: Fig. 3). As in previous
analyses, two major subclades are recovered within
Echimyidae. The first of these (node I) comprises the terrestrial
spiny rats Thrichomys-†Pampamys-†Eumysops and
Hoplomys-Proechimys+the semiaquatic coypu Myocastor,
and a group of arboreal genera comprising spiny tree-rats

J Mammal Evol



Mesomys-Lonchothrix+brush-tailed rat Isothrix and
echimyines-dactylomyines. The middle Miocene
†Maruchito clusters with extant echimyines, while
the late Eocene-early Oligocene †Eodelphomys and the late
O l i g o c e n e t o e a r l y M i o c e n e a d e l p h omy i n e s
†Adelphomys-†Paradelphomys-†Stichomys-†Xylechimys
cluster with the dactylomyines. The second subclade (node J)
includes the extant terrestrial spiny rat Trinomys and the fos-
sorial Carterodon, Clyomys, and Euryzygomatomys
(euryzygomatomyines sensu Emmons 2005), as well as the
extinct †Theridomysops and †Dicolpomys.

Paleontological Datings

The age and phylogenetic relationships of fossil octodontoids
suggest a minimum late Oligocene age for the divergence

between the main octodontoid clades (Fig. 10), i.e.,
abrocomids, crown echimyids, and the major octodontid lin-
eages. Indeed, based on the evidence of †Eodelphomys, some
of these splits may have occurred earlier; however, we pur-
posely excluded †Eodelphomys from our date estimations ow-
ing to a lack of consensus regarding its proposed Eocene age
(Frailey and Campbell 2004; MacFadden 2006; Antoine et al.
2012; Woodburne et al. 2014). The initial branching of differ-
entiated, euhypsodont abrocomids, octodontines, and
ctenomyines is recorded during the late Miocene, modern
octodontines and especially abrocomids starting to diversify
slightly earlier than modern ctenomyines. The desert-adapted
octodontines and Abrocoma are first recorded at least as early
as the latest Pliocene-early Pleistocene (Fig. 10). Also during
the Pliocene, a recent branching event within ctenomyines
gave rise to the lineage leading to the extant Ctenomys.

Fig. 4 Most parsimonious tree of
a combined analysis of
morphological and molecular
data. Values of absolute/relative
Bremer support are given above
branches. A to J, nodes mentioned
in the text

J Mammal Evol



Molecular Dating of Divergences

A time-scaled phylogeny for Octodontoidea was obtained
through a relaxed molecular clock Bayesian analysis, setting
seven fossil calibrations (Online Resource 3) based on
Contamana and Tinguiririca rodents, and topology of the com-
bined tree here obtained. The nodes of the inferred phylogeny
were supported by >72 % posterior clade probabilities (PB),
except for the nodes Dactylomys-Olallamys (64 % PB),
Myocastor-Hoplomys-Proechimys (65 % PB) and Echimys/
…/Mesomys (57 % PB).

The estimated age obtained for the divergence between
Octodontoidea and Chinchilloidea is 41.7 Ma (95 % CI:
39.0–45.1 Ma). Within octodontoids, the initial divergence
that separated abrocomids from echimyids-octodontids is dat-
ed at 34.1 Ma (95 % CI: 31.2–37.1 Ma), while the echimyids/
octodontids split is estimated at 29.5 Ma (95 % CI: 27.3–
32.0 Ma). The beginning of the diversification of crown
echimyids, corresponding to the separation between their
two major clades, is estimated to have occurred at 24.1 Ma
(95 % CI: 22.2–26.3 Ma). The divergence octodontines/
ctenomyines within octodontids is dated at 25.9 Ma (95 %

CI: 25.0–27.4 Ma). Splits giving rise to genus-level lineages
within the major clades are older in echimyids than in
octodontids, with the only exception of Clyomys-
Euryzygomatomys (Online Resource 3).

Cranial Shape Variation and Disparity

Figure 11 shows the skull shape variation of living octodontoid
genera and the extinct †Prospaniomys, †Actenomys, and
†Eucelophorus (see Materials and methods) as represented in
the morphospace of the first two axes of a PCA of Procrustes
coordinates. These first two principal components (PC) ex-
plained 61.53 % of the variation. Shape changes along PC1
(36.06 % of the variation) involved mainly the size of the audi-
tory bulla (larger toward positive values), and to a lesser extent,
the size of the orbit (smaller toward positive values). Along PC2
(25.47 % of the variation), the main changes involved rostrum
shape (more elongated and procumbent toward positive values)
and relative expansion of the cranial vault (higher vault toward
negative values). As in a previous analysis (Verzi et al. 2015), the
echimyids, and especially the forest-dwelling genera, occupied a
comparatively restricted area, with most taxa having negative

Fig. 5 General morphology of
the skull (a, b, e, f, i, j) and
mandible (c, d, g, h, k, l) of
selected genera of the three
families of Octodontoidea: a
†Prospaniomys priscusMACN-
Pv CH1913; b and d Cuscomys
ashaninka MUSM 12715; c
†Prospaniomys sp. MPEF 5039;
e †Eumysops gracilis MMP 410-
M; f and h Thrichomys sp. MMP
150; g †E. gracilisMMP 798-M;
i †Pithanotomys chapalmalensis
MMP 2132-M; j and l Aconaemys
sagei MLP 17.II.92.8; k
†Pithanotomys chapalmalensis
MMP 650-S

J Mammal Evol



PC1 values and negative or near-zero PC2 values; Myocastor
was an exception, with a positive PC2 score. Octodontids were
widely spread over much of the remaining morphospace, and
included taxa with extreme values for both PC1 (the desert-

adapted Tympanoctomys and Pipanacoctomys, with
hypertrophied auditory bullae) and PC2 (the specialized subter-
ranean †Eucelophorus, with procumbent rostrum). Abrocomids
showed greater spread than the forest-dwelling echimyids along

Fig. 6 Morphology of the orbital
region: a Abrocoma sp. (cinerea
complex) MLP 2038; b
†Prospaniomys priscusMMP
952-M; c †Spaniomys riparius
MACN-A 4184; d Octodontomys
gliroidesMLP 25.XI.98.1
(erroneously assigned to Octomys
in Verzi et al. 2014: fig. 2a); e
Thrichomys sp. MMP
150-USB542. Dotted line in
photographs shows orientation of
the nasolacrimal canal.
Abbreviations: ef ethmoidal
foramen; f frontal; j jugal; lf
lacrimal foramen; m maxilla; nl
foramen into nasolacrimal canal;
ol orbital portion of lacrimal; sf
sphenopalatine fissure

Fig. 7 Dorsolateral view of right hemimandible of abrocomids: a
Thrichomys laurentius MN-UFRJ 42483; b Abrocoma bennettii MLP
2273; c †Prospaniomys priscus MPEF 7572 (inverted left

hemimandible). Abbreviations: ca coronoid apophysis; nm, notch for
the tendon of medial masseter muscle

J Mammal Evol



Fig. 8 Occlusal morphology of left upper molars. aM1 of †Acarechimys
minutissimus MPEF 5065; b M1 of †Acaremys (including †Sciamys)
MLP 15–122; c M1 of †Acaremys (including †Sciamys) MLP 15–197
(?); d M2 of Octodontomys gliroides MLP 12.VII.88.10; e M2 of
Aconaemys sagei FMNH 50754; f M1-2 of Aconaemys porteri UACH
2255; g M1-2 of †Protadelphomys latus CFG 9; h M1-2 of †Sallamys
pascuali UATF-V 5013; i M1-2 of †Sallamys pascuali UATF-V 5010; j

M1 of †Willidewu esteparius MLP 90-II-13; k M1-2 of †Chasicomys
octodontiforme MLP 55-IV-28-2 (from Pascual 1967; currently
missing) (inverted right molars in c, d, e, f, h, i, j, k). Arrows indicate
parafossette and/or metafossette. Abbreviations: Al anteroloph; Mel
metaloph; Mf mesoflexus / mesofossette; Msul mesolophule; Mtf
metaflexus/metafossette; Pf paraflexus/parafossette; Prl protoloph; Psl
posteroloph. Not to scale

Fig. 9 Morphology of foramen into nasolacrimal canal: a
†Protadelphomys latus field N° CF 025; b †Actenomys priscus MLP
field N° H-1; c Ctenomys maulinus MLP 1.X.01.4; d Octomys mimax

IMCN 024. Abbreviations: f frontal; j jugal; ia incisive alveolus; m max-
illa; M1a-M3a alveolus of M1, M2 or M3, respectively; nl foramen into
nasolacrimal canal; sf sphenopalatine fissure

J Mammal Evol



PC1. The extantCuscomys andAbrocoma had positive scores on
both PCs (near zero for †Prospaniomys). †Prospaniomys was
located close to mesic octodontids Aconaemys, Octodon, and

Spalacopus (see Álvarez and Arnal 2015), whereas the arid-
adaptedAbrocoma sp. (cinerea complex) was nearer to the desert
octodontids.

Fig. 10 Most parsimonious tree of octodontoids showing the temporal
ranges of genera. Occlusal figures of the left m1 or m2 are illustrated next
to the corresponding genus (when two figures are presented, the one to the
right is ontogenetically more derived). Times of origin (t1), morphological
differentiation (t2), and initial diversification of crown-group (t3) are indicated;
t1 denotes the origin of lineages leading to abrocomids (t1a), echimyids and
octodontids (t1b), and octodontines and ctenomyines (t1c); the differentiation
stage (t2) is represented by the acquisition of euhypsodont molars (black
occlusal figures). Dark grey background denotes differentiation times of the
southern octodontoid clades (Chasicoan-Huayquerian), and the subsequent
record of arid-adapted and desert-specialists among modern abrocomids and
octodontines (Marplatan). We use informal names for echimyid subfamilies

pending a review of their taxonomic status. Timescale after Gradstein et al.
(2008); South American LandMammal Ages boundaries after Madden et al.
(1997), Zárate (2005), Folguera and Zárate (2009), Ré et al. (2010), Perkins
et al. (2012), Deschamps et al. (2013), Dunn et al. (2013), Fernicola et al.
(2014); isotopic curve after Zachos et al. (2008); global palaeoclimatic events
after Vrba et al. (1995), Denton (1999), Zachos et al. (2001), Verzi and
Quintana (2005), Tripati et al. (2009), and Pound et al. (2012). Abbreviations:
Adelph adelphomyines; Bon Bonaerian; Cha Chapadmalalan; Chs
Chasicoan; Col Colhuehuapian; Coll Colloncuran; Dacty dactylomyines;
Des Deseadan; Ens Ensenadan; Hua Huayquerian; Lav Laventan; Mar
Marplatan; May Mayoan; Myo myocastorines; Mon Montehermosan; San
Santacrucian

J Mammal Evol



Similarly to previous results (Verzi et al. 2015), and as antic-
ipated by the relative dispersion of families in the morphospace,
the values of the disparity index (Foote’s F) calculated from this
shape variation were markedly higher for octodontids than for
echimyids. The disparity of abrocomids was intermediate, al-
though also higher than that of echimyids. Table 1 presents these
values along with those for phylogenetic diversity (PD) and tax-
onomic diversity at generic level (TD). Among the families an-
alyzed, echimyids presented the lowest F values combined with
markedly higher values of PD and TD.

Discussion

Delimitation of Higher Taxa

The clade at node A of Fig. 4 is recognized here as the family
Abrocomidae. We include therein genera that were previously
assigned to other octodontoid lineages, or considered to have

uncertain affinities, along with the modern euhypsodont rep-
resentatives (Appendix). Until the present, no fossil
octodontoid with rooted molars had been assigned to this

Fig. 11 Phylogenetic tree superimposed onto the plot of octodontoid
genera in the morphospace defined by the first two principal
components (PCs). The positions of internal nodes are reconstructed by
squared-change parsimony using the tree topology obtained. Outline di-
agrams show shape change of the skull associated with each PC (arrows)

from the consensus (solid lines and circles) to positive or negative scores.
Maps show current distribution of the familial clades after Patton et al.
(2015). Illustrated skulls not to scale. Empty circles, landmarks; solid
circles, semilandmarks

Table 1 Generic richness (TD), phylogenetic diversity (PD), and
disparity (F) of analyzed familial clades calculated from living / living+
extinct genera included in the PCA; (t) total of living genera according to
Woods and Kilpatrick (2005) and Emmons (2005)

Clade TD (t) PD F

Echimyidae 16 (22) 267 0.0039

Abrocomidae 2 (2) / 3 36 / 56 0.0055 / 0.0080

Octodontidae 8 (9) / 10 97 / 109 0.0077 / 0.011

PD is used as an estimate of evolutionary history contained in each fa-
milial clade, and is expressed as the sum of branch lengths connecting all
species within the clade (million years as obtained from the relaxed mo-
lecular clock Bayesian analysis, plus MSM* estimates for Cuscomys and
fossils; MSM* value for Carterodon is here considered zero in accor-
dance with paleontological results)

J Mammal Evol



family and the early record of abrocomids was restricted to
modern representatives belonging to the late Miocene genus
†Protabrocoma (including †BAbrocoma^ antiqua ;
Appendix). †Deseadomys, †Protacaremys, †Prospaniomys,
and †Spaniomyswere considered echimyids in the exhaustive
reviews of Wood and Patterson (1959) and Patterson and
Wood (1982) (see also Patterson and Pascual 1968). Arnal
and Kramarz (2011) interpreted †Prospaniomys as an early
offshoot of the Octodontidae lineage. Recent phylogenetic
analyses showed that these genera, like †Caviocricetus and
†Dudumus, could represent basal octodontoids not directly
related to the origin of either Echimyidae or Octodontidae
(Vucetich et al. 2014; Arnal et al. 2014; Arnal and Vucetich
2015). Alternatively, Verzi et al. (2014) included †Spaniomys
within Abrocomidae. The results obtained here expand and
support this alternative proposal through interpretation of the
above mentioned pre-late Miocene octodontoids with rooted
molars as ancient abrocomids.

The arrangement of the clades defined by nodes C and D is
similar to the ones previously interpreted by us as
Octodontidae and Echimyidae, respectively (Verzi et al.
2014, 2015), with the exception of the position of
†Caviocricetus (previously included in Octodontidae) and
†Deseadomys arambourgi (previously included in
Echimyidae; cf. Fig. 4 and Verzi et al. 2014: Fig. 1). The name
Octodontidae for node C and Octodontinae and Ctenomyinae
for the subclades at nodes G and H, respectively (Fig. 4) are
maintained here as in our previous proposal (Verzi et al. 2014,
2015). Nevertheless, we consider that a family-level assign-
ment for these two subclades (Woods and Kilpatrick 2005;
Patton et al. 2015) could be a suitable alternative given their
extended history as independent lineages. Both Ctenomyinae
and Octodontinae cluster traditional (euhypsodont) representa-
tives of each subfamily along with genera that were previously
classified as Echimyidae, as Octodontoidea with uncertain af-
finities, or as stem Octodontoidea (Appendix). In this arrange-
ment, Octodontinae includes the ‘acaremyids’ †Platypittamys
and †Acaremys (including †Sciamys) as inWood and Patterson
(1959; see also Winge 1941:190), as well as the more recently
described ‘acaremyid’ †Galileomys (Vucetich and Kramarz
2003) and the taxa †Plesiacarechimys, †Acarechimys minutus,
and †Acarechimys minutissimus. The topology of living
Octodontinae is consistent with previous molecular phyloge-
nies (Gallardo and Kirsch 2001; Honeycutt et al. 2003; Opazo
2005; Upham and Patterson 2012), and only the position of the
mountain degu Octodontomys was unstable (cf. Fig. 4 and
Online Resource 3; see also Upham and Patterson 2012:
Figs. 3 and 4). Results by Arnal and Vucetich (2015) and
Arnal et al. (2014) recovered the acaremyids and
†Plesiacarechimys as more closely related to †Dudumus and
†Caviocricetus, while Octodontidae was interpreted as a group
more recently diverged from Echimyidae (see also Vucetich
and Kramarz 2003; Frailey and Campbell 2004).

The relationship of †Sallamys+†Protadelphomys-†Willidewu
with modern Ctenomyinae is here supported by two novel syn-
apomorphies, one in the skull and another in the upper molars.
This result markedly differs from those obtained by Vucetich
et al. (2014), Arnal and Vucetich (2015), and Candela’s (2015)
reinterpretation of our previous analysis (Verzi et al. 2014).

Node D corresponds to Echimyidae in terms of the living
fauna (Emmons et al. 2015), but excludes some of the late
Oligocene to middle Miocene taxa previously referred to this
family (Fig. 4; Appendix). The relationships among
echimyids are mostly in agreement with previous molecular
(Galewski et al. 2005; Upham and Patterson 2012, in press;
Upham et al. 2013; Fabre et al. 2013, 2014; Loss et al. 2014),
morphological (Emmons 2005; Olivares et al. 2012; Candela
and Rasia 2012; Verzi et al. 2014), and combined phylogenies
(Olivares and Verzi 2014; Verzi et al. 2015). Although with
some differences, especially in the arrangement of the arboreal
genera, these results are consistent in recovering two major
subclades, one formed by the terrestrial spiny rat Trinomys
plus the fossorial genera, and the other, by terrestrial and ar-
boreal spiny rats, and the semiaquatic coypu (although see
Candela and Rasia 2012). This information, together with re-
cent phylogenies that have included the Caribbean
capromyids (Fabre et al. 2014; Upham and Patterson in
press) suggest the need for a profound revision of the status
of Echimyidae subfamilies (see Olivares and Verzi 2014;
Emmons et al. 2015).

Differences between the results obtained here and
those from other recent phylogenetic analyses of fossil
octodontoids (Arnal and Pérez 2013; Arnal et al. 2014;
Vucetich et al. 2014; Arnal and Vucetich 2015) could
be due in large part to the disparate representation of
living species in the samples considered. Arnal and
Pérez (2013: 129) interpreted Octodontidae as a group
of modern (late Miocene) origin derived from an alleg-
edly paraphyletic grouping BEchimyidae^ represented by
†Eumysops and †Stichomys; the octodontid Octomys
mimax was the only living species included in this anal-
ysis. In later proposals that included the living
echimyids Echimys and Kannabateomys, Arnal and
Vucetich (2015) and Arnal et al. (2014) supported the
grouping of †Eumysops and †Stichomys with this family, and
considered Echimyidae as sister to Octodontidae. In these
proposals, the interpretation of †Caviocricetus, †Dudumus,
†Deseadomys, †Prospaniomys, and †Protacaremys as part
of a temporally extended and diverse stem Octodontoidea
does not consider the Abrocomidae among the lineages of
Octodontoidea; in that context, these genera actually represent
stem members of Echimyidae-Octodontidae (rather than of
Octodontoidea), which is equivalent to the position of
Abrocomidae among living taxa (Upham and Patterson
2012; Fabre et al. 2013). Another possible source of discrep-
ancies with alternative proposals lies in the differential use of

J Mammal Evol



craniomandibular and dental characters (cf. Carvalho and
Salles 2004; Arnal et al. 2014: appendix 2; Verzi et al. 2014:
SOM1; Online Resource 1 in this work).

The Reinterpretation of Lower Molar Morphology

Interpreting the patterns of simplification of lophate lower
molars from the frequently more complete and stable mor-
phology of the Dp4 provides a result equivalent to the propos-
al of Lavocat for the posterior crests of upper molars (Lavocat
1974: 58–59, Fig. 1; 1976; see also Vucetich and Verzi 1994:
Fig. 3; Antoine et al. 2012: supplementary data). This fresh
outlook on the patterns of change of lower molars leads to the
recognition of a mesolophid in octodontoids and even
caviomorphs (but see Patterson and Wood 1982; Marivaux
et al. 2004; Frailey and Campbell 2004; Candela and Rasia
2012). By extension of this approach, the lower molars of the
earliest caviomorphs from Contamana †Cachiyacuy and
†Canaanimys would already show reduction of anterior
crests, and the second crest would more likely be the
mesolophid than the metalophulid II as originally interpreted
(Antoine et al. 2012). If this were the case, the implied loss of
metalophulid II supposes that a route of transformation of the
lower molars (different from those detected among
octodontoids) was already established quite early on.

Timescale of Evolutionary Stages in Major Clades

Underlying the alternative proposals for the phylogenetic re-
lationships of octodontoids, there are important differences
regarding the interpretation of the time of origin of living
higher taxa. The first records of modern Abrocomidae, with
euhypsodont molars whose morphology is similar to that of
the living forms, have been interpreted as evidence of a late
Miocene origin of this family (e.g., Reig 1986; Vucetich et al.
1999; Arnal and Pérez 2013). The interpretation of the origin
of Octodontidae, and especially Ctenomyinae (or
Ctenomyidae), has followed a similar path. As an exception,
Winge (1941) and Wood and Patterson (1959) proposed an
older origin for octodontines, but no similar hypothesis was
ever proposed for Abrocomidae or Ctenomyinae (although
see Landry 1957: 51). We think that the use of dental mor-
phology as key source of primary homologies in the fossil
record has created a bias toward the above mentioned accep-
tance of a modern origin for Abrocomidae and Octodontidae,
and has simultaneously promoted the inclusion of early
octodontoids within Echimyidae, a family whose extant spe-
cies retain lophate, rooted molars (Appendix; Fig. 10).

Three successive stages can be recognized in the evolution-
ary history of any clade, referred to as t1, t2, and t3 by Hennig
(1965: Fig. 4): t1, its origin by separation from its sister clade;
t2, its morphological differentiation by acquisition of the
apomorphies that characterize its extant members; t3, the

origin of the last common ancestor of these living representa-
tives. The time when a clade splits from its sister clade (t1) and
that of acquisition of its main diagnostic apomorphies (t2) are
often decoupled, resulting in the existence of stem members
that have split before t2 and share few Bnon-key^ apomorphies
with their corresponding crown-group (Steiper and Young
2008). However, the difficulty of separating the earliest repre-
sentatives of two diverging lineages does not negate the va-
lidity of the branching point as the origin of the resulting
clades (Briggs and Fortey 2005: 100). Thus, the interpretation
of the origin of a group on the basis of the recognition of the
main diagnostic characters present in its living representatives
should be assumed to be the product of an operational restric-
tion rather than the reflection of an actual pattern; efforts fo-
cused on the recognition of plesiomorphic basal stems are
indispensable to interpret the deep history of a lineage.
Following this last criterion, we use a total-clade definition
(i.e., including stems and crown members; Briggs and
Fortey 2005) for the familial and subfamilial clades (Figs. 4
and 10).

Abrocomids with modern dental morphology like the one
that characterizes living species are recognized in the fossil
record since the late Miocene (Fig. 10). Although with chro-
nological differences, octodontines and ctenomyines also ac-
quire their modern dental characters during the late Miocene,
thus implying strong uncoupling between the stages of origin
and morphological differentiation in these three clades. This
differentiation stage coincides with the time of origin of the
crown group in octodontines, whereas it takes place before the
origin of the crown group in ctenomyines (Verzi et al. 2014).
Based on the position of †Protabrocoma as sister of the living
abrocomid genera, the stage of modernization is also earlier
than the origin of the crown group in this family (see also
datings of the Abrocoma-Cuscomys split in Upham and
Patterson in press).

The molecular clock analysis, using a restricted sample of
living species (Online Resource 3), suggests divergence times
mostly older than interpreted so far (Leite and Patton 2002;
Honeycutt et al. 2003; Galewski et al. 2005; Opazo 2005;
Rowe et al. 2010; Upham and Patterson 2012, in press;
Fabre et al. 2013, 2014; Upham et al. 2013; Voloch et al.
2013). According to these results, the origin of octodontoids
would have taken place during the middle Eocene, near the
time represented by the most ancient South American rodent
fauna (fromYahuarango Formation, Contamana, Peru) as sug-
gested by Antoine et al. (2012) and Arnal et al. (2014). The
divergence between the lineage that led to abrocomids and the
common ancestor of echimyids-octodontids would have oc-
curred near the Eocene-Oligocene boundary, while the origin
of the echimyid and octodontid lineages is early Oligocene in
age. The initial diversification of the respective crown-groups
of octodontids and echimyids would have taken place during
the late Oligocene. It is noteworthy that the lineages leading to

J Mammal Evol



minor living clades of echimyids, i.e., echimyines,
dactylomyines, arboreal spiny-rats, and spiny rats including
Myocastor, would have branched off as early as the late
Oligocene-early Miocene. Moreover, most of the divergences
between echimyid lineages leading to living genera are mark-
edly older than expected, as anticipated by Lara et al. (1996:
410) and Da Silva and Patton (1998), and supported by recent
results (Upham and Patterson 2012, in press; Upham et al.
2013; Fabre et al. 2013, 2014). These divergences are in gen-
eral markedly older than the ones that separate the lineages
leading to living octodontid genera.

Phylogenetic and Diversity Patterns as the Outcome
of Differential Responses to Palaeoenvironmental
Changes

As mentioned, the stage of differentiation is strongly
decoupled from the origin in the southern octodontoid clades,
i.e., octodontines, ctenomyines, and abrocomids. This is in
clear contrast with the phylogenetic structure of echimyids
(Fig. 10) in which a stage of modernization distinct from the
origin of the clade is not recognizable in any of their major
subclades. These distinctly different evolutionary patterns
would have resulted from different responses to Cenozoic
environmental changes (Pascual 1967; Verzi 2002; Verzi
et al. 2014, 2015). A deepening of the global Cenozoic
cooling and drying trend (Denton 1999; Zachos et al. 2001;
Tripati et al. 2009), partially combined with local diastrophism
corresponding to Andean orogeny, gave rise to increasingly
open and arid biomes in southern South America since the late
Miocene (Pascual and Ortiz Jaureguizar 1990; Palazzesi and
Barreda 2007; Le Roux 2012; Quattrocchio et al. 2013;
Palazzesi et al. 2014). The stages of southern differentiation
in abrocomids, octodontines, and ctenomyines show a
hierarchy that follows that of these paleoenvironmental
changes. The appearance of euhypsodont lineages, and
extinction of those with primitive molars, marks the
beginning of the stage of modernization of these clades
during the late Miocene. The subsequent appearance in
the fossil record of arid-adapted and desert-specialists
among hypsodont abrocomids and octodontines coin-
cides with a profound global cooling and drying event
around 2.5 Ma, near the Plio-Pleistocene boundary
(Fig. 5; Verzi 2001; Verzi and Quintana 2005 and ref-
erences therein). As a result of this pattern, modern
southern octodontoids show wide morphological disparity in-
volving specializations to arid and desert habitats
(Abrocoma, Pipanacoctomys, Tympanoctomys) and the
subterranean ecotope (Spalacopus, Ctenomys, and the
extreme †Eucelophorus) (Table 1, Fig. 11).

In contrast to this pattern, echimyids went extinct in the
southern part of their geographical range during the late
Miocene-Pleistocene (with the exception of the peculiar

Myocastor). Given that the presence of echimyids in southern
South America has always represented an impoverished mar-
ginal sample of its astonishing diversity in the northern trop-
ical areas, it suggests that the evolutionary response to
paleoenvironmental changes by this clade would have been
fidelity to their original habitats (Verzi et al. 2014, 2015).
Because taxa which track Boriginal^ habitats (in this case at
least as a passive response, i.e., through local extinction) are
expected to be morphologically more conservative than those
that adapt to new environments (Raia et al. 2012), this could
explain the morphological similarity detected among ancient-
ly diverged lineages of echimyids (Table 1 and Fig. 11) and
the related absence of differentiation stages as perceptible
events decoupled from the origin of the clade.

The phylogenetic structure of southern abrocomids,
octodontines, and ctenomyines also differs markedly from that
of echimyids with regards to the topology of the origin of the
crown group (t3) in relation to that of the corresponding clade
(t1, Fig. 10). In the southern clades, the initial diversification
of the respective crown-groups is strongly uncoupled from the
origin of the clades. In echimyids, in contrast, the origin of the
crown-group of the family or of its two major subclades is not
uncoupled from the origin of the respective clades, not even in
the case of the larger subclade (comprising terrestrial, arbore-
al, and semiaquatic representatives) that includes early fossils.
The decoupling between t1 and t3 observed in southern
octodontoids is the result of the phylogenetic structure of ex-
tinction. In these groups, as opposed to echimyids, extinction
eliminated deep clades bringing about a marked loss of evo-
lutionary history (cf. Fig. 10 and Erwin 2008: Fig. 1); since the
late Miocene onwards, extinction affected some of the
euhypsodont genera and all the lineages with rooted molars
(Vucetich and Verzi 1999). As a result, living abrocomids and
octodontids are restricted to only late-diverged, euhypsodont
representatives.

The question remains why the modernization of
octodontoids took place latest among southern caviomorphs,
given that chinchilloids were already becoming differentiated
in the early Oligocene (see Bertrand et al. 2012) and cavioids
in the earlyMiocene (Pérez and Pol 2012); even, octodontoids
are unique among living South American hystricomorphs in
retaining a rat-like appearance (i.e., a body plan without major
modifications; e.g., Redford and Eisenberg 1992: pl. 17;
Eisenberg and Redford 1999: pl. 13).

Environmental Dynamics as a Diversity-Driving Factor

The understanding of biological diversity is a central goal in
evolutionary and ecological theories. The processes and fac-
tors that generate and control species richness, and its patterns
of spatial and temporal distribution, are among the most
revisited (e.g., Wiens and Donoghue 2004; Jablonski et al.
2006; Weir and Schluter 2007; Mittelbach et al. 2007;

J Mammal Evol



Benton 2009; Buckley et al. 2010; Rull 2011; Davies et al.
2011; Rabosky et al. 2012). A positive correlation of species
richness with morphological diversity (e.g., Ricklefs 2004), as
expected in certain ecological and evolutionary scenarios
(Eldredge and Gould 1972; Eldredge 1996; Schluter
2000), or with phylogenetic and functional diversity
(the latter being a proxy for morphological diversity)
is not the rule. Cladogenetic richness (from populations
to species) seems not be linearly related with evolution-
ary dynamics of other components of diversity. On the
contrary, there is a growing body of evidence of the
uncoupling between these components (e.g., Fortey et al.
1996; Adams et al. 2009; Safi et al. 2011; Blankers et al.
2013; Ruta et al. 2013).

Given that evolutionary transformation, i.e., anagenesis un-
derlying adaptation, requires cohesion of the evolving
lineage (Futuyma 1987) rather than the contingent per-
turbation of such cohesion that underlies cladogenesis
and extinction, adaptation and changes in cladogenetic
richness (as two primary components of diversity)
should not be expected to be coupled, or at least not
necessarily (see Szalay 1999: 52).

As described above, the distinctive evolutionary patterns of
the southern and northern octodontoid clades include, in the
former, both morphological transformation implied in the ad-
aptation to derived emerging environments, and extinction of
deep lineages causing strong loss of evolutionary history (see
von Euler 2001; Erwin 2008). As a result, the living southern
clades show greater disparity as well as less content of evolu-
tionary history and lower taxonomic diversity, which could be
considered at first as a counterintuitive pattern. We consider
that such a pattern is channelled by environmental dynamics.
Rainforests occurred in South America up to high latitudes
during the Eocene (Burnham and Johnson 2004), and whereas
the long-term global Cenozoic cooling (Denton 1999; Zachos
et al. 2001, 2008) caused their retraction toward lower lati-
tudes (Barreda and Palazzesi 2007; Quattrocchio et al. 2013;
Palazzesi et al. 2014), their current condition in northern
South America has remained essentially stable throughout
the Cenozoic (Colinvaux and De Oliveira 2001).
Conversely, in the south of the continent, the deepening
Tertiary cooling and drying trend combined with local dias-
trophism gave rise to the development of new, derived open
biomes (Pascual and Ortiz Jaureguizar 1990; Palazzesi and
Barreda 2007; Barreda and Palazzesi 2007; Le Roux 2012;
Quattrocchio et al. 2013; Palazzesi et al. 2014). As in the case
of the environments, the dynamics of octodontoid diversity
would have been more stable in the tropical habitats of north-
ern South America. Meanwhile, both strong adaptation and
extinction are expected evolutionary responses to changes
generating new environments in the south. These differential
dynamics of diversity probably occurred during much of the
Tertiary, before the late Miocene, but the exploration of this

issue is hindered by the fragmentary nature of the fossil re-
cord, especially in northern South America (MacFadden
2006; Antoine et al. 2013). Beyond this, we consider that such
dynamics are not necessarily linked to latitude, but to the
stability vs. mutability of environments on a temporal scale
(Sheldon 1996; Verzi et al. 2015).

The importance of the environment to catalyze and channel
evolutionary change has been thoroughly stated by Vrba for
the fossil record in a rich body of theory (Vrba 1992,
1995, 2004, 2005). In this proposal, coordination be-
tween the diversity resulting from cladogenesis, extinc-
tion and distribution drift, and evolutionary transforma-
tion (represented in Vrba’s proposal by a heterochronic
change axis; see Vrba 2004, 2005) is given essentially
by the environment. However, both in this theoretical
paleontological context, as in ecological approaches,
the contribution of the anagenetic component has re-
ceived relatively little attention (Verzi et al. 2015). In
this sense, as part of the efforts aimed at understanding
the history of biological diversity, it is necessary to
analyze evolutionary transformation in its environmental
context along with cladogenesis and extinction (Sheldon
1996).

The evolutionary stages of a clade provide information
regarding the dynamics of cladogenetic and anagenetic com-
ponents of diversity. The times of origin of a clade and of its
crown-group represent cladogenesis and extinction, i.e.,
changes in diversity irrespective of transformation or
anagenesis; in contrast, the lapse between the time of
origin of a clade and its differentiation stage implies
evolutionary transformation in lineages (in this case,
morphological change) a priori irrespective of cladoge-
netic diversification. Fossils provide key information on
these stages, which highlights the involvement of pale-
ontology to macroevolutionary interpretations.

Acknowledgments We thank the curators for granting access to mate-
rials under their care; B. Patterson (Field Museum of Natural History,
USA) and N. Upham (McMaster University, Canada) for sharing infor-
mation from an unpublished manuscript; J. Zachos (University of Cali-
fornia, Santa Cruz, USA) for allowing use of his original isotope dataset;
D. Pol (Museo Paleontológico Egidio Feruglio, Argentina) for providing
the TNT script for MSM*; B. Patterson, V. Pacheco (Museo de Historia
Natural, Peru), A. Feijó (Universidade Federal da Paraíba, Brazil), N.
Hurtado and G. D’Elía (Universidad Austral de Chile), M. Pérez (Museo
Paleontológico Egidio Feruglio, Argentina), and J. Tarquini (Museo de
La Plata, Argentina) for kindly providing photographs of specimens. B.
Patterson and G. D’Elía allowed the use of unpublished photographs of
Aconaemys; V. Pacheco allowed the use of unpublished photographs of
the holotype of Cuscomys ashaninka. F. Ballejo (Universidad Nacional
de La Plata, Argentina) made the pencil drawings. Detailed critical com-
ments from two anonymous reviewers greatly improved this article. We
are grateful to J.R.Wible for his detailed editorial work. This research was
supported by Agencia Nacional de Promoción Científica y Tecnológica
PICT 2012–1150 and Consejo Nacional de Investigaciones Científicas y
Técnicas PIP 0270 grants.

J Mammal Evol



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.

J Mammal Evol



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