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ISSN 10623590, Biology Bulletin, 2014, Vol. 41, No. 9, pp. 801–816. © Pleiades Publishing, Inc., 2014.
Original Russian Text © A.O. Averianov, A.V. Lopatin, 2014, published in Zoologicheskii Zhurnal, 2014, vol. 93, No. 7, pp. 798–813.
801
INTRODUCTION
Already in the 12th edition of the
System of Nature
by C. Linnaeus, eight orders of mammals were divided
into three informal supraordinal groups: Unguiculata,
Ungulata, and Mutica (Linnaeus, 1766). This system
included a total of 40 genera of mammals, most of
which correspond to the families in the current classi
fication. Linnaeus united all known marsupials into the
genus
Didelphis
of the order Bestiae. Monotreme mam
mals were discovered in the late 18th century, and in the
early 19th century they were sometimes classified with
birds (Lamarck, 1809). A.M. Blainville (1839–1864)
was the first who divided mammals into placentals
(“Monodelphia”), marsupials (“Didelphia”), and
monotremes (“Ornithodelphia”). Among the first
evolutionary classification, the system proposed by
Thomas Huxley should be noted, who divided mam
mals by the level of their organization into Hypotheria
(hypothetical ancestors), Prototheria (monotremes),
Metatheria (marsupials), and Eutheria (placentals)
(Huxley, 1880). A characteristic feature of many classifi
cations of the late 19th century is the division of mam
mals into two subclasses—Prototheria (monotremes)
and Eutheria (marsupial and placentals) (Gill, 1872;
Cope, 1898). The evolutionary highlevel systematics
of placental mammals has received the greatest devel
opment in the first half and the middle of the 20th cen
tury in the works of the New York school of mammal
ogists (Gregory, 1910; Osborn, 1910; Simpson, 1945).
In the second half of the 20th century, representatives
of the same school proposed the first classifications of
Eutheria based on the cladistic principles (McKenna,
1975; Novacek, 1982, 1986, 1993; Novacek and Wyss,
1986; McKenna and Bell, 1997; Shoshani and McK
enna, 1998). The rapid development of molecular
phylogenetics in the late 20th and early 21st centuries
gave a new impetus to the studies of the phylogenetic
relationships between the orders of placental mam
mals (Springer et al., 1997; Madsen et al., 2001; Mur
phy et al., 2001, 2001a; Meredith et al., 2011; O’Leary
et al., 2013).
In this paper, we consider the most important
advances in the highlevel systematics of placental
mammals over the past decade.
THE ORIGIN OF PLACENTAL MAMMALS
According to the latest report (Wilson and Reeder,
2005), there are 1135 genera and 5080 species of mod
ern placental mammals, and these numbers are con
stantly increasing (Reeder et al., 2007; Ceballos and
Ehrlich, 2009). All modern placental mammals, their
nearest common ancestor, and extinct descendants of
this ancestor form the crown clade Placentalia (Fig. 1).
The crown clade Placentalia with the extinct side
branches, which are phylogenetically closer to the crown
placentals than to the crown marsupials (Fig. 1), form a
common (total) clade Eutheria, or PanPlacentalia
HighLevel Systematics of Placental Mammals:
Current Status of the Problem
A. O. Averianov
a, c
and A. V. Lopatin
b
a
Zoological Institute, Russian Academy of Sciences, St. Petersburg, 199034 Russia
b
Geological Faculty, St. Petersburg State University, St. Petersburg, 199034 Russia
c
Borissiak Paleontological Institute, Russian Academy of Sciences, Moscow, 117997 Russia
email: dzharakuduk@mail.ru, alopat@paleo.ru
Received March 19, 2013
Abstract
—According to molecular data, the modern clades of placental mammals can be grouped into four
supraordinal taxa (Xenarthra, Afrotheria, Euarchontoglires, and Laurasiatheria) whose phylogenetic interre
lationships have been interpreted inconsistently. Among these taxa, the group Afrotheria has no morpholog
ical support. Within this group, there are orders that are clearly related to “condylarthrans” (“afroungulates”)
and to insectivores (“afrosoricids”). The radiation of placental mammals (the crown clade Placentalia)
started before the K/T boundary on the northern continents. Laurasiatheria are likely to be the oldest clade
of placentals: the diversification of Lipotyphla and Euungulata started ~80 Mya (Campanian) and ~70 Mya
(Maastrichtian), respectively. It is shown that the fossil record is the only reliable method to test the phyloge
netic hypotheses based on the material of the molecular and morphological studies of recent taxa.
Keywords
: mammals, placentals, phylogeny, systematics
DOI:
10.1134/S1062359014090039
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BIOLOGY BULLETIN Vol. 41 No. 9 2014
AVERIANOV, LOPATIN
(Queiroz, 2007). A sister group to Eutheria is Met
atheria (or PanMarsupialia), together with which
they form the clade Theria. Recently, †
Prokennalestes
,
†
Murtoilestes
, and †
Eomaia
from the Early Creta
ceous of Eastern Asia were considered as the most
ancient representatives of Eutheria (Kielan
Jaworowska and Dashzeveg, 1989; Averianov and
Skutschas, 2001; Ji et al., 2002). †
Juramaia
from the
middle or, more likely, the Late Jurassic of China was
recently described as the oldest member of Eutheria
(Luo et al., 2011). However, the assignment of this
taxon to Eutheria is unconvincing. By the absence of
molarized P5, it corresponds to the level of the stem
therian †
Pappotherium
from the Early Cretaceous of
North America (Averianov et al., 2010). Of these gen
era, only †
Eomaia
was included in the last phyloge
netic analysis (O’Leary et al., 2013), which was found
to be a sister taxon for the Theria.
The Cenozoic Era is often called the era of mam
mals, which replaced the Mesozoic Era of reptiles. In
this regard, the time of origin of modern orders of
mammals is of particular interest. To this end, the
question arises as to whether the explosive radiation of
mammals in the Early Cenozoic was a consequence of
the extinction of dinosaurs and other reptiles, which
“emptied” many ecological niches, especially in the
largesize class? Or does the evolution of placentals
have a long history, not yet known to us? For most of
the 20th century, it was generally believed that the
modern orders of placental animals originated in the
Cretaceous Period (Matthew, 1943; Simpson, 1945).
However, fossil records confirming this idea were
almost absent, except for the finding of three genera of
“insectivores” of the Late Cretaceous of Mongolia
(†
Deltatheridium
, †
Deltatheroides
, and †
Zalambdal
estes
) (Gregory and Simpson, 1926, 1926a; Simpson,
1928). Later, another three genera of Cretaceous
“insectivores” of Mongolia were found (Kielan
Jaworowska, 1969, 1975). The finding of a primate in
the Late Cretaceous of North America was also
reported (Van Valen and Sloan, 1965), but this speci
men, most likely, come from the Paleocene deposits
(Buckley, 1997; Clemens, 2004). Currently, genera
†
Deltatheridium
and
†
Deltatheroides
are classified into
Placentalia
to Marsupialia
PanPlacentalia
(=Eutheria)
B
b
CA
a
Fig. 1.
Main groups distinguished in the placental cladogram: (
a
) the common ancestor of Theria (Metatheria + Eutheria);
(A) paraphyletic group combining the extinct stem taxa (shown in gray in panel A); (B) crown group (clade) Placentalia, com
bining all modern placentals, their closest common ancestor (
b
), and all extinct descendants of this common ancestor (shown in
gray on panel B); (C) general (total) group PanPlacentalia, or Eutheria, combining the crown group Placentalia and stem Pla
centalia (modified from de Queiroz, 2007).
BIOLOGY BULLETIN Vol. 41 No. 9 2014
HIGHLEVEL SYSTEMATICS OF PLACENTAL MAMMALS 803
PanMarsupialia (Rougier et al., 1998). The finding of
new fauna of Late Cretaceous mammals in Central
Asia, which were dominated by Eutheria (Archibald
and Averianov, 2005), gave a new impetus to the search
for Cretaceous ancestors of modern orders of placen
tals. It was hypothesized that the Cretaceous
†Zheles
tidae
together with ungulates form the clade Ungu
latomorpha (Archibald, 1996; Nesov et al., 1998). In
addition, Cretaceous
†Zalambdalestidae
, known from
Central Asia and Mongolia, were considered as
belonging to the crown group Glires (Archibald et al.,
2001).
Archibald and Deutschman (2001) proposed three
models of possible diversification of mammals near
the CretaceousTertiary (K/T) boundary (Fig. 2):
(1) The “Explosive” model, which postulates that
the modern orders of placental mammals (crown
groups) and their supraordinal groups uniting the
crown groups and extinct stem taxa emerged after the
K/T boundary.
(2) The “Long Fuse” model, according to which
the crown groups occurred after the K/T boundary,
whereas the stem taxa of supraordinal groups existed
before the K/T boundary.
(3) The “Fast Fuse” model, according to which the
crown groups and stem taxa of supraordinal groups
emerged before the K/T boundary.
Here, “fuse” means the process of diversification of
stem branches before the emergence of the crown
group (Cooper and Fortey, 1998). Statistical analysis
of the fossil record of mammals in North America
favors the explosive model (Foote et al., 1999;
Archibald and Deutschman, 2001). However, the
majority of molecular studies dates the emergence of
the major groups of mammals to a significantly earlier
time, approximately in the middle of the Cretaceous
period, which corresponds to the “fast fuse” model
(Springer, 1997; Kumar and Hedges, 1998; Bromham
et al., 1999; Murphy et al., 2001b; Arnason and Janke,
2002; Belov et al., 2002; Huchon et al., 2002;
Archibald, 2003; Hasegawa et al., 2003; Springer et al.,
2003, 2005; BinindaEmonds et al., 2007; Meredith
et al., 2011; Goswami, 2012).
New fossil findings of Eutheria in the Late Creta
ceous of Mongolia and Central Asia and the analysis of
a large amount of morphological data have convinc
ingly shown that
†Zhelestidae, †Asioryctitheria
, and
†Zalambdalestidae
do not belong to the crown clade
Placentalia (Novacek et al., 1997; Horovitz, 2000,
2003; Wible et al., 2004, 2007, 2009; Archibald and
Averianov, 2006, 2012). In particular, the study of the
petrosal bones of zhelestids showed a very primitive
organization of their structures associated with the
middle ear and the absence of synapomorphies with
modern ungulates, which allows rejecting the Ungu
latomorpha concept (Ekdale et al., 2004; Ekdale and
Rowe, 2011).
K/T
K/T
K/T
(a)
(b)
(c)
а
b
а
b
а
b
Fig. 2.
Three models of radiation of placental mammals near
the Cretaceous–Paleogene (K/T) boundary. (a) “Explosive”
model: modern orders of Placentalia (
b
,crown groups) and
their supraordinal groups combining the crown groups and
the extinct stem taxa (
a
), emerged after the K/T boundary.
(b) “Long fuse” model: crown groups emerged after the
K/T boundary, the stem taxa of supraordinal groups
existed before the K/T boundary. (c) “Fast fuse” model:
crown groups and stem taxa of supraordinal groups
emerged before the K/T boundary (modified by Springer
et al., 2003).
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BIOLOGY BULLETIN Vol. 41 No. 9 2014
AVERIANOV, LOPATIN
The recently published phylogeny of Eutheria is
based on comparison of the molecular data and the
analysis of an unprecedented number (4541) of mor
phological traits (O’Leary et al., 2013). The authors of
this study unequivocally support the explosive model
of Placentalia radiation after the K/T boundary. How
ever, this conclusion is an artifact determined by the
sample of fossil taxa, because these authors deliber
ately ignored all the findings that were not consistent
with their hypothesis. These findings include
†
Protun
gulatum
(PanEuungulata), known from unambigu
ously Cretaceous deposits (Archibald et al., 2011) and
†
Gypsonictops
(†Leptictida
, which were classified with
Afrotheria by O’Leary et al., 2013) from the Late Cre
taceous of North America.
†
Kharmerungulatum
from
the Late Cretaceous of India can also be classified with
ungulates (Prasad et al., 2007; Goswami et al., 2011).
The elucidation of the origin of Placentalia is sig
nificantly hampered by the fact that members of this
clade penetrated North America, where the geological
record of Cretaceous–Paleogene mammals is most
complete, relatively late, in the Campanian, approxi
mately 83 Mya. Most likely, the initial stages of the
evolution of the modern orders of mammals occurred
in the coastal lowlands of Asia, where the fauna of the
second half of the Late Cretaceous is still very poorly
studied.
SUPRAORDINAL GROUPS OF PLACENTALIA
The vast majority of modern molecular studies dis
tinguishe four supraordinal groups of placentals:
Afrotheria, Xenarthra, Euarchontoglires, and Laur
asiatheria (Fig. 3). The last two superorders are com
bined into the clade Boreutheria, whose monophyly
does not cause any objections. Debates are caused by
the phylogenetic relationships of Boreutheria,
Afrotheria, and Xenarthra, which are described using
three alternative hypotheses (Fig. 4):
(1) The Exafroplacentalia (or Notolegia) hypothe
sis, according to which Afrotheria is a sister group to
other placentals (Xenarthra + Boreutheria) (Madsen
et al., 2001; Murphy et al., 2001, 2001a, 2004;
AmrineMadsen et al., 2003; Springer et al., 2003,
2004; Beck et al., 2006; Asher, 2007; Nikolaev et al.,
2007; Meredith et al., 2011);
(2) The Epitheria hypothesis, postulating Xenar
thra as a sister group to other placentals (Afrotheria +
Boreutheria) (McKenna, 1975; Novacek and Wyss,
Xenarthra
Tubulidentata
Afrosoricida
Macroscelidea
Sirenia
Hyracoidea
Proboscidea
Scandentia
Primates
Dermoptera
Rodentia
Lipotyphla
Chiroptera
Cetartiodactyla
Perissodactyla
Pholidota
Carnivora
Lagomorpha
FERAE
EUUNGULATA
GLIRES
EUARCHONTA
AFROTHERIA
SCROTIFERA
LAURASIATHERIA
BOREUTHERIA
EUARCHONTOGLIRES
Fig. 3.
Phylogenetic relationships of modern orders of mammals and supraordinal groups according to the molecular data.
BIOLOGY BULLETIN Vol. 41 No. 9 2014
HIGHLEVEL SYSTEMATICS OF PLACENTAL MAMMALS 805
1986; Shoshani and McKenna, 1998; Kriegs et al.,
2006; O’Leary et al., 2013);
(3) The Atlantogenata hypothesis, according to
which Afrotheria and Xenarthra form a monophyletic
group that is a sister group to other placentals
(Boreutheria) (Waddell et al., 1999;
Hallstr
ö
m
et al.,
2007; Murphy et al., 2007; Waters et al., 2007; Wild
man et al., 2007; Arnason et al., 2008; Prasad et al.,
2008; Schneider and Cannarozzi, 2009; Song et al.,
2012; Zoller and Schneider, 2013).
According to the studies devoted to the analysis of
transposons, Boreutheira, Afrotheria, and Xenarthra
constitute a soft polytomy, and it is assumed that the
diversification of these clades occurred almost simul
taneously (Churakov et al., 2009; Nishihara et al.,
2009).
AFROTHERIA
Clade Afrotheria includes modern orders Afrosori
cida (tenrecs and golden moles), Macroscelidea (ele
phantshrews), Tubulidentata (aardvarks), Hyra
coidea (hyraxes), Sirenia (sirens), and Proboscidea
(proboscideans). This group of orders of placentals
was first recognized by molecular methods (Springer
et al., 1997, 1999, 2004; Stanhope et al., 1998a, 1998b;
van Dijk et al., 2001; Madsen et al., 2001; Murphy
et al., 2001; Malia et al., 2002). Subclades Tethytheria
(
†Desmostylia
, Sirenia, and Proboscidea) and Pae
nungulata (Hyracoidea,
†Embrithopoda
, and
Tethytheria) have morphological support (Domning
et al., 1986; Novacek and Wyss, 1986; Rasmussen et
al., 1990; Asher et al., 2003; Gheerbrant et al., 2005).
Madagascar Pleistocene endemic
†
Plesiorycteropus
,
classified into a special order
†Bibymalagasia
(MacPhee, 1994), may belong to aardvarks (Asher et
al., 2003). The search for morphological synapomor
phies common to all Afrotheria did not give conclusive
results (
S
á
nchez
Villagra et al., 2007; Asher and Leh
mann, 2008). At the same time, there is convincing
morphological evidence of the similarity of Tenre
coidea and Chrysochloridae with the Laurasian Lipo
typhla (Asher, 1999; Whidden, 2002; Lopatin, 2006).
In recent years, an increasing amount of fossil evi
dence of the heterogeneity of Afrotheria and their
relationships with the Laurasian mammals has
appears. The oldest representatives of Macroscelidea
from the Eocene of Africa exhibit an obvious morpho
logical similarity with the “condylarthrans”
†Lou
isinidae
and
†Apheliscidae
of the Paleocene and early
Eocene of Europe and North America (Hartenberger,
1986; Simons et al., 1991; Tabuce et al., 2001, 2012;
Zack et al., 2005, 2005a; Penkrot et al., 2008; Hooker
and Russell, 2012). The relationship with condylar
thrans is also evidenced by the data on the most
ancient Proboscidea from the late Paleocene and early
Eocene of North Africa (Gheerbrant, 2009; Gheer
brant et al., 2001, 2002, 2005a, 2005b).
†
“Phenacol
ophidae” (
†Embrithopoda?
) from the late Paleocene
of East Asia and
†Anthracobunidae
from the Eocene
of the IndoPakistan region are the most close to the
ancestors of Proboscidea (Gheerbrant et al., 2005a).
The oldest sirenians are known from the early
Eocene of the Caribbean Sea Region and North
Africa; the African origin of this group is more feasible
(Domning, 2001; Benoit et al., 2013). The extinct
aquatic
†Desmostylia
are known only from the Oli
gocene and Miocene of the North Pacific (Domning
et al., 1986). The ancestors of Desmostylia were prob
ably phylogenetically closer to the proboscideans than
to the sirenians (Gheerbrant et al., 2005).
The archaic hyrax
†
Microhyrax
from the early and
middle Eocene of Algeria shows a combination of
primitive and advanced features in the structure of the
teeth and postcranial skeleton, which make it close to
the condylarthrans (Tabuce et al., 2006, 2007).
New records of the oldest tenrecs and golden moles
of the Eocene and Oligocene of North Africa are
regarded as evidence of the origin of “afrosoricids”
from archaic insectivores (Lopatin, 2006) or from the
insectivorelike
†Pantolesta
, which are close to
†
Todral e s tes
of the late Paleocene of Morocco
(Seiffert and Simons, 2000; Seiffert et al., 2007;
Seiffert, 2010).
Thus, Afrotheria has no morphological support. In
this group, orders phylogenetically related to “condy
larthrans” (“afroungulates”), on the one hand, and
insectivores, on the other (“afrosoricids”), can be
clearly distinguished.
Xenarthra
Xenarthra
Afrotheria
Laurasiatheria
Euarchontoglires
Laurasiatheria
Euarchontoglires
Afrotheria
Xenarthra
Afrotheria
Laurasiatheria
Euarchontoglires
Exafroplacentalia
Epitheria
Atlantogenata
Fig. 4.
Three main hypotheses about the phylogenetic rela
tionships of superorders of Placentalia.
806
BIOLOGY BULLETIN Vol. 41 No. 9 2014
AVERIANOV, LOPATIN
XENARTHRA
Group Xenarthra combines armadillos, sloths, and
anteaters distributed in South and Central America.
Sloths and anteaters form a monophyletic group
(Pilosa), which is a sister group to armadillos (Cingu
lata). In different classifications, these groups have an
order or a suborder rank. In studies of the 19th and
early 20th centuries, xenarthrans were often combined
with pangolins and aardvarks in the group Edentata,
which is characterized by the adaptations to a burrow
ing lifestyle and a tooth system modified to varying
degrees (Flower, 1883). In xenarthrans, teeth are
absent (anteaters) or greatly simplified and completely
devoid of enamel (armadillos and sloths) (
Vizca
í
no,
2009
). The absence of the enamel crown significantly
complicates the elucidation of relationships of xenar
thrans, because the structure of molars has many phy
logenetically significant traits. The extinct orders
†Palaeanadonta, †Taeniodonta, †Gondwanatheria
,
and
†Ernanodonta
were also classified into Edentata
(Gregory, 1910; Matthew, 1918; Wortman, 1918; Sim
pson, 1945; Szalay, 1977; Ding, 1987; Mones, 1987).
More rarely, xenarthrans were combined only with
pangolins into the group Paratheria (Thomas, 1887;
Novacek, 1986).
According to the molecular data, Xenarthra is a sis
ter group to Boreutheria (Exafroplacentalia hypothe
sis) or Afrotheria (Atlantogenata hypothesis), whereas
the majority of authors of morphological studies favor
the Epitheria hypothesis, which places xenarthrans at
the base of the placental tree (see above).
The oldest known representative of Xenarthra is the
armadillo
†
Riostegotherium
from the late Paleocene
(57–59 Mya) of Brazil (Bergqvist et al., 2004). The
oldest findings of unidentifiable Pilosa are known
from the late Eocene of Antarctica (Rose et al., 2005).
The phylogenetic position of
†
Eurotamandua
from the
middle Eocene of Germany, which resembles the
modern tetradigitate anteater (
Tam andua
), is inter
preted ambiguously: a representative of Pilosa,
†Palaeanodonta
, or Pholidota, a sister taxon to Pilosa,
or a special order
†Afredentata
(Storch, 1981; Storch
and Habersetzer, 1991; Gaudin and Branham, 1998;
Szalay and Schrenk, 1998; Rose, 1999a; Rose et al.,
2005). Most likely, this taxon belongs to Pholidota
(Rose et al., 2005).
EUARCHONTOGLIRES
This clade includes two groups long recognized by
morphologists: Euarchonta and Glires. The original
concept of Archonta included orders Menotyphla
(Scandentia + Macroscelidea), Dermoptera, Chi
roptera, and Primates (Gregory, 1910). The version of
this concept that excludes Macroscelidea from
Archonta is more widespread (McKenna, 1975; Sza
lay, 1977; Novacek and Wyss, 1986). Group Volitantia
(Dermoptera + Chiroptera), recognized by some
authors (Novacek and Wyss, 1986; Wible and
Novacek, 1988; Novacek, 1992; Szalay and Lucas,
1993, 1996; Shoshani and McKenna, 1998), is based
on the homoplasias associated with the adaptation for
flight (Silcox et al., 2005). According to the molecular
data, Chiroptera belong to the clade Laurasiatheria
(see below). The clade including Scandentia, Der
moptera, and Primates is supported by the majority of
modern molecular analyses (Adkins and Honeycutt,
1991; Liu et al., 2001; Murphy et al., 2001, 2001a;
Springer et al., 2003, 2004). Since it differs in compo
sition from Archonta, it was called Euarchonta (Wad
dell et al., 1999b; Asher and Helgen, 2010). Among
euarchontans, primates and dermopterans are sister
taxa (clade Primatomorpha); the origin of this clade is
estimated at 86.2 Mya, whereas the origin of Euar
chonta dates to 87.9 Mya (
Jane ka
et al., 2007).
The oldest tree shrews, almost indistinguishable
from the modern forms, are known from the middle
Eocene of China (Tong, 1988). Modern dermopterans
(Cynocephalidae) are limited in their distribution to
Indochina and the Sunda Islands. The fossilized flying
lemur
†
Dermotherium
is known from the Eocene and
Oligocene of Indochina and Pakistan (Ducrocq et al.,
1992; Marivaux et al., 2006). The extinct
†Plagi
omenidae
of the Paleocene and Eocene of North
America is a sister taxon to the Cynocephalidae (Sil
cox et al., 2005; Bloch et al., 2007; Ni et al., 2010).
The total clade Primates includes the crown clade
Euprimates (Strepsirrhini + Haplorrhini) and the
stem taxa combined in the group
†Plesiadapiformes
or
†Plesiadapoidea
(Rose, 2006; Silcox et al., 2005;
Bloch et al., 2007). According to one of the hypothe
ses, Dermoptera is a branch of these
†Plesiadapi
formes
(Beard, 1990, 1993; Kay et al., 1990; Kay et al.,
1992; Ni et al., 2010). According to an alternative
hypothesis, Dermoptera is a sister group to Primates
(Bloch and Boyer, 2002; Silcox, 2003; Bloch and Sil
cox, 2006; Silcox et al., 2009). Both hypotheses are
consistent with the molecular data on the phyloge
netic proximity of dermopterans and primates (
Jan
eka
et al., 2007). The oldest primate is the plesiadapi
form
†
Purgatorius
from the early Paleocene of North
America (Van Valen and Sloan, 1965; Clemens, 1974,
2004; Buckley, 1997; Fox and Scott, 2011).
Clade Glires includes the modern orders Rodentia
(rodents) and Lagomorpha (lagomorphs), character
ized by the development of the anterior pair of con
stantly growing “gnawing” incisors in the upper and
lower jaw, in which the enamel covers only the ante
riorlabial side of the crown. Rodents include almost
half of the modern species of placental mammals. In
the 19th century, lagomorphs were regarded as a sub
order of rodents (Duplicidentata). Beginning with the
work of Gidley (1912), they have been given the rank
of an independent order. The phylogenetic relation
ships of rodents and lagomorphs with different groups
of mammals were interpreted in a very wide range
c
^
c
^
BIOLOGY BULLETIN Vol. 41 No. 9 2014
HIGHLEVEL SYSTEMATICS OF PLACENTAL MAMMALS 807
(Meng and Wyss, 2005). In this regard, the Anagalida
concept, combining Lagomorpha, Rodentia, Mac
roscelidea, Cretaceous
†Zalambdalestidae
, and
Paleo gene
†Anagalidae
, should be noted (Szalay and
McKenna, 1971; Novacek, 1986). According to
another hypothesis, Glires include Lagomorpha,
Rodentia, and
†Zalambdalestidae
(Archibald et al.,
2001). Data from most modern molecular studies sup
port the monophyly of Glires (Eizirik et al., 2001;
Madsen et al., 2001; Murphy et al., 2001, 2001a;
Huchon et al., 2002; Springer et al., 2003). The mono
phyly of Glires is also confirmed by the new fossil find
ings of the stem taxa of rodents and lagomorphs, filling
the morphological gap between the crown clades
(Meng et al., 2003; Meng, 2004; Asher et al., 2005).
LAURASIATHERIA
This clade combines the largest number of modern
orders (Fig. 3). The most primitive branch of laurasi
atherians is Lipotyphla (insectivores); this name
should not be replaced by Eulipotyphla (Archibald,
2003; Asher and Helgen, 2010). For Lipotyphla, a sis
ter taxon is the extinct order
†Leptictida
, known
mainly from the Paleogene of North America,
Europe, and Asia (Novacek, 1977, 1986; Rose,
1999a). The relationship between
†
Leptictis
and ele
phantshrews in a recent study (O’Leary et al., 2013)
can be explained by the purely external similarity of
these mammals, similarly adapted to ricochet run.
The
†
Gypsonictops
from the Late Cretaceous (Campa
nian and Maastrichtian) of North America is the old
est leptictid (Lillegraven, 1969; Clemens, 1973; Fox,
1977; Novacek, 1977; KielanJaworowska et al.,
2004). Thus, the crown groups of Laurasiatheria and,
respectively, Placentalia emerged at least in the early
Campanian (83 Mya), 17 million years before the Cre
taceous–Paleogene boundary, contrary to O’Leary
et al. (2013). Interestingly, the time of diversification
of the Caribbean Solenodontidae from the common
trunk of insectivores is estimated at a similar time
(76 Mya) (Roca et al., 2004).
The remaining orders of laurasiatherians are com
bined into the clade Scrotifera, representatives of
which are characterized by the presence of a scrotum,
which develops apparently in parallel in primates
(Waddell et al., 1999b). Scrotifera is divided into three
branches: Chiroptera, Euungulata (Perissodactyla +
Cetartiodactyla), and Ferae (Carnivora + Pholidota).
Bats (Chiroptera) are the second (after rodents)
largest modern order of placentals. Bats are clearly
divided into two large groups: the fruiteating bats
(Megachiroptera) and the true bats (Microchi
roptera), feeding primarily on insects, which they
catch by means of echolocation. It was hypothesized
that the fruit bats are a sister group to primates and that
they acquired the ability to fly independently of bats
(Pettigrew, 1986; Pettigrew et al., 1989). However, the
majority of molecular and morphological studies sup
port the monophyly of Chiroptera (Mindell et al.,
1991; Simmons, 1994; Teeling et al., 2000). The oldest
bats are known from the early Eocene; they appear in
the fossil record at the same time in all continents
except Antarctica (Jepsen, 1966; Hand et al., 1994;
Simmons and Geisler, 1998; Gunnell et al., 2003;
Gunnell and Simmons, 2005; Simmons, 2005; Teje
dor et al., 2005; Smith et al., 2007; Simmons et al.,
2008; Tabuce et al., 2009).
Clade Euungulata (Perissodactyla + Cetartiodac
tyla) is supported by the molecular data (Waddell
et al., 1999a; Zhou et al., 2012). The oldest represen
tative of Euungulata is
†
Protungulatum
from the Late
Cretaceous (Maastrichtian) and Paleocene of North
America (Archibald, 1982; KielanJaworowska et al.,
2004; Archibald et al., 2011). Thus, Euungulata is the
second clade of laurasiatherians, whose radiation
began before the Cretaceous–Paleogene boundary,
contrary to O’Leary et al. (2013). A sister group to
Perissodactyla may be the extinct “condylarthran”
group
†Phenacodonta
of the Paleocene–Eocene of
North America (Hooker, 2005).
The molecular data strongly suggest the relation
ship of cetaceans with Artiodactyla, particularly Hip
popotamidae (Gatesy et al., 1996; Waddell et al.,
1999b; Madsen et al., 2001; Murphy et al., 2001,
2001b; AmrineMadsen et al., 2003; Springer et al.,
2003, 2004, 2005; Theodor, 2004; Price et al., 2005;
Agnarsson and MayCollado, 2008; Springer et al.,
2011; Zhou et al., 2011, 2012; Hassanin et al., 2012;
Nery et al., 2012). This hypothesis is supported by the
fact that the Eocene cetaceans retained the paraxonic
hind limb and by other morphological data (Gingerich
et al., 1990, 2001; Luckett and Hong, 1998; Gatesy
et al., 1999; Gatesy and O’Leary, 2001; Geisler and
Uhen, 2003, 2005; O’Leary and Gatesy, 2008). Cur
rently, Cetacea is the only placental order whose early
stages of evolution are well traced on the basis of fossil
evidence (Gatesy et al., 2013).
The last clade of laurasiatherians (Ferae) combines
two modern orders: carnivores (Carnivora) and
pangolins, or scaly anteaters (Pholidota). This group is
supported by the molecular data (Czelusniak et al.,
1990; Honeycutt and Adkins, 1993; Madsen et al.,
2001; Murphy et al., 2001; Delsuc et al., 2002;
AmrineMadsen et al., 2003). The morphological
support for this clade is weak (Rose et al., 2005). A sis
ter taxon to pangolins is the extinct order
†Palaean
odonta (=†Ernanodonta)
from the Paleogene of
North America, Europe, and Asia (Simpson, 1931;
Emry, 1970; Ding, 1987; Gheerbrant et al., 2005b;
Kondrashov and Agadjanian, 2012). Ancient
pangolins are known from the Eocene of Asia and
Europe; in the Oligocene, they penetrated into North
America (Emry, 1970, 2004; Storch, 1978; Horovitz
et al., 2005; Gaudin et al., 2006).
The crown clade Carnivora with the stem taxa
(
†Viverravidae
and †“Miacidae”) form the total clade
Carnivoramorpha, a sister group to which is the
808
BIOLOGY BULLETIN Vol. 41 No. 9 2014
AVERIANOV, LOPATIN
extinct order
†Creodonta
(Flynn and WesleyHunt,
2005; WesleyHunt and Flynn, 2005). The oldest find
ings of Carnivoramorpha are known from the early
Paleocene of North America (Fox and Youzwyshyn,
1994; Fox et al., 2010). Carnivores and creodonts
could have originated from the genus
†
Cimolestes
from
the late Cretaceous (Maastrichtian) and Paleocene of
North America (Lillegraven, 1969; Clemens, 1973).
In this case, the diversification of this clade could have
begun before the Cretaceous–Paleogene boundary.
The development of molecular systematics in the
late 20th century gave rise to the hope that this
approach will help reconstruct the phylogenetic rela
tionships of all organisms. However, the first experi
ments in genosystematics, based mainly on the mito
chondrial genome, small samples of taxa, and inade
quate statistical models, often lead to unexpected
“interesting” results. For example, articles in very rep
utable journals tried to convince us that the guinea pig
is not a rodent, that rabbits are most close to primates,
and that monotremes and marsupials form a sister
group (Graur et al., 1991, 1996; D’Erchia et al., 1996;
Janke et al., 1996, 2002; Penny and Hasegawa, 1997).
Currently, molecular highlevel systematics of mam
mals has entered a phase of maturity: in one recent
study in this field, as many as 35000 base pairs in
26 genes of 164 species are analyzed (Meredith et al.,
2011). The belief of genosystematics that their method
is the only appropriate method to reconstruct the phy
logeny remains unchanged (Springer et al., 2007).
Unfortunately, this view does not reflect the reality.
The main disadvantage in the molecular approach is
the limited sample of modern taxa whose genome can
be studied. Modern orders of mammals account for
only 40% of their total number. Except for several cur
rently thriving orders (Rodentia, Chiroptera, Lipo
typhla, and Cetartiodactyla), the diversity of mam
mals has been steadily declining, in some groups cata
strophically. At the generic level, the modern diversity
of Xenarthra and Perissodactyla is only 6 and 2.5%,
respectively, of the past diversity, which is still not
known completely (McKenna and Bell, 1997). It
would be very naive to believe that it is possible to con
struct an adequate mammalian phylogeny based on
this very small and random sample. In addition, there
are as yet unsolved methodological problems in
molecular systematics associated with different evolu
tionary patterns in different genes and drawing up
“long branches” in parsimony analysis (Wagele, 1999;
Bergsten, 2005; O’Connor et al., 2010). In morpho
logical phylogenetics, the main difficulty is the prob
lem of convergence and parallelisms. They manifest
themselves very clearly in the groups specialized to a
particular lifestyle, which requires a significant or even
a radical rearrangement of the morphological organi
zation. In mammals, parallelisms are the cause of a
great morphological similarity, which is not due to a
common origin, e.g., in digging Xenarthra and Pholi
dota and flying Chiroptera and planning Dermoptera
(Rose et al., 2005; Silcox et al., 2005). Another prob
lem is the fact that ancestral characteristics in modern
mammals are strongly modified as a result of morpho
logical divergence, which significantly complicates the
elucidation of relationships between orders. The last
problem is currently solved almost exclusively by
molecular phylogenetics. The most reliable criterion
for testing phylogenetic hypotheses obtained in recent
material by molecular or morphological methods is
the fossil record. The adequacy of a phylogenetic
hypothesis can be postulated only when the molecular
clades are confirmed by the direct fossil evidence, as in
the case of cetaceans (Gatesy et al., 2013).
ACKNOWLEDGMENTS
We are grateful to A.V. Bochkov (Zoological Insti
tute) for reading the manuscript and comments. This
study was supported by the Russian Foundation for
Basic Research (project nos. 130401401 and 1304
00525).
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