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Review TRENDS in Ecology and Evolution Vol.not known No.not known Month 0000
Phylogenetics series
Deciphering relationships among the orders of pla- groups. Thus, reconstructing their phylogeny can serve as
cental mammals remains an important problem in a model for research on other organisms.
evolutionary biology and has implications for under- Here, we highlight that, in spite of the ongoing debate,
standing patterns of morphological character evolution, the congruence of most recent molecular evidence is
reconstructing the ancestral placental genome, and striking and consensus is approaching rapidly. Progress
evaluating the role of plate tectonics and dispersal in has been achieved by using larger and more diverse
the biogeographic history of this group. Until recently, molecular datasets, increasing taxon sampling to sub-
both molecular and morphological studies provided divide long branches, and using LIKELIHOOD (see Glos-
only a limited and questionable resolution of placental sary) methods of phylogeny reconstruction that explicitly
relationships. Studies based on larger and more diverse model the nucleotide substitution process and are less
molecular datasets, and using an array of methodo- susceptible to problems of STATISTICAL INCONSISTENCY
logical approaches, are now converging on a stable tree than are methods such as MAXIMUM PARSIMONY [2]. In
topology with four major groups of placental mammals. addition, results of phylogenetic analyses that rely on
The emerging tree has revealed numerous instances of nucleotide or amino acid substitutions are now comple-
convergent evolution and suggests a role for plate mented by rare genomic changes (RGCs; Box 1) that
constitute genetic markers of common descent. The major
tectonics in the early evolutionary history of placental
molecular finding is that the 18 placental orders are
mammals. The reconstruction of mammalian phylo-
divided into four clades, of which three were never
geny illustrates both the pitfalls and the powers of
suspected based on morphology. Here, we discuss the
molecular systematics.
reliability of the new tree, discuss reasons for earlier
discrepancies, highlight the remaining problems and
Are we, humans, more closely related to mice or to cows
offer a prospectus on future studies.
and dogs? A long history of debate surrounds this and
other questions pertaining to relationships among the
The growth of molecular consensus
orders of placental mammals. Difficulties in reconstruct- Until the advent of molecular approaches, mammalian
ing relationships among the orders have been attributed to phylogeny was necessarily the domain of morphology and
a rapid radiation following the Cretaceous – Tertiary paleontology. Since Darwin, the study of placental mam-
boundary [1]. Even if we consult the recent literature, mal relationships has seen episodic development and has
we find that the relationship of primates to other placental culminated in a morphological tree that remains promi-
orders is the subject of fierce debate. There are many nent in the current literature ([3– 5]; Figure 1a). Vari-
contradictory hypotheses about placental mammal ations of this tree largely conform to the topology of ordinal
relationships, both between and among molecules and relationships proposed by Novacek [6], which evolved from
morphology. Yet, it is clear that knowing the actual pattern the mammalian classifications of Gregory in 1910,
of mammalian phylogeny is very important, not only Simpson in 1945, and McKenna in 1975. The major
because it reveals our own genealogy, but also because this characteristics of this tree are that Xenarthra
family tree provides the framework to interpret the (e.g. armadillos, anteaters) are the most basal placental
evolution of morphological, physiological, behavioral, group, and that most of the remaining orders are grouped
and genomic features that characterize different mamma- into three generally accepted clades: (i) UNGULATA ,
lian taxa. Understanding placental mammal phylogeny is (ii) ARCHONTA , and (iii) ANAGALIDA . This topology deviates
also a crucial prerequisite for unraveling the biogeogra- in essential aspects from the currently emerging molecu-
phical history of this group. Mammals are better known lar tree, which recognizes three novel superordinal clades:
from morphological and molecular data than are all other AFROTHERIA , LAURASIATHERIA and EUARCHONTOGLIRES ,
the latter two of which are SISTER GROUPS [i.e. BOR-
Corresponding author: Mark S. Springer (mark.springer@ucr.edu). EOEUTHERIA ; Figure 1b].
www.sciencedirect.com 0169-5347/$ - see front matter q 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2004.05.006
ARTICLE IN PRESS TREE 298
2 Review TRENDS in Ecology and Evolution Vol.not known No.not known Month 0000
Review TRENDS in Ecology and Evolution Vol.not known No.not known Month 0000 3
(a) (b)
LHLGKPGHRSYALSPQQALGPEGVKAAAVATLSPHTVIQTTHSASEPLP Whale AGTGATGAAATGTTAACTTCTAACGACTTACGT
LHLGKPGHRSYALSPQQALGPEGVKAAAVATLSPHTVIQTTHSASEPLP Alpaca/Llama AGCGACGAAATGTTACCTTCTGATGACTCACAT
LHLGKPGHRSYALSPQQALGPESVKAAAVATLSPHTVIQTTHSASEPLP Horse AGTGAGGAAATGTTAACTTCTGATGACTCATGT
LHLGKPGHRSYALSPQQALGPEGVKAAAVATLSPHTVIQTTHSASEPLP Pangolin AGTGATGAAATGTTAACTTCTGATGATCCATGT
LHLGKPGHRSYALSPQQALGPEGVKAAAVATLSPHTVIQTTHSASEPLP Cat AGTGATGAAATGTTAACTTCTGATGACTCACCA
LHLGKPGHRSYALSPQQALGPDGVKAATVATLSPHTVIQTTHSASEPLP Bat CGTGATGAAATATTAACTTCTGATGTCTCACCT
LHLGKAGHRAYALSPQQALGPEGVKAAAVATLSPHTVIQTTHSASEALP Shrew AGTGATGATGTATTATCTTCTGATGATTTCCAT
LHLGKPGHRSYALSP-------------------HTVIQTTHSASEPLP Human AGTGATGAACTGTTAGGTTCTGATGACTCACAT
LHLGKPGHRSYALSP-------------------HTVIQTTHSASEPLP Flying lemur AGTGATGAAATTTTAGCTTCTGATGACTCACGT
LPLGKPGHRSYALSP-------------------HTVTQATHSASEPLP Tree shrew AGTGATGAAATGTTAACTTCTAACGACTCACAT
LHLGRPGHRSYALSP-------------------HTVIQTTPSASEPLP Rabbit/Hare AGTAATGAAATGTTAACTCCTGATGACTCACTT
LHLGKPGHRSYALSP-------------------HTVIQTTHSASEPLP Mouse ACTGGTGAAATGTTAACTTCTGACAGCGCATCT
LHLGKPGHRAYALSPQQALGPEGVK-AAVATLSPHTVXQTPHSASEPLP Anteater AGTGATGACATATTGACTTCTAATGACTCATGC
LHVGKTSHRSYGLSPQQALGPEGVK-AAVATLSPHSVIQTTHSASEPLP Sea cow AGTGATGGCCTG---------GATGACTTGCAT
LHLGKASHRSYALSPQQALGPEGVK-AAVATLSPHSVIQTTHSASEPLP Elephant AGTGACGGCCTG---------GATGTCTTAAAT
LHLGKASHRSYALSPQQALGPEGVK-AAVATLSPHSVIQTPHSASEPLP Hyrax AGTGACAACCTA---------AGTGATTCACCT
LHLGKAGHRSYALSPQQALGPEGVK-AAVTTLSPHTVIQTTHNASEPLP Aardvark AGTGATGGCCTG---------GATGGCTCACAT
LHLGKAGHRSYALSPQQALAPDGVK-AAVATLSPHTVIQTSHNASEPLP Elephant shrew AGCGGTGGCCTG---------GATGGCTGCCAT
LHLGKAXHRSYALSPQQALGPEGVK-AAVATLSPHTVIQTTHNASEPLP Golden mole AGTGATGGCCTG---------GATGAGTCACAT
LHLGKAGHRSYALSPQQALGPEGVK-AAVATLSPHTVIQTTHNASEPLP Tenrec AGCCACGGCCTG---------GGTGACTCTCGC
LHLGKPSHRSYALSPQQALGPEGVK-ATVATLSPHTVIQTTHSASDPLP Opossum AGTAATGTCATTTTAGTCTCTGATTACTCCTCT
TRENDS in Ecology & Evolution
Figure I. Examples of rare genomic changes (RGCs) that support the major clades of placental mammals include (a) an 18 amino-acid deletion (relative to outgroup) in
the SCA1 protein for Euarchontoglires [61] and (b) a 9-bp deletion in the BRCA1 gene (breast and ovarian cancer susceptibility gene 1) for Afrotheria [19]. Color-coding
for higher-level taxa is as follows: black, Marsupialia; red, Afrotheria; green, Xenarthra; blue, Euarchontoglires; and orange, Laurasiatheria.
membrane structures provide additional support for this lemurs). Glires is a bastion of morphological trees;
hypothesis [31]. Within Euarchontoglires, there is a Euarchonta differs from the morphological Archonta
fundamental split between GLIRES (rodents þ lago- hypothesis by removing bats from this clade. The
morphs) and Euarchonta (primates þ tree shrews þ flying molecular exclusion of bats from Archonta requires
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ARTICLE IN PRESS TREE 298
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Afrotheria
Rodentia Tubulidentata
Anagalida
Lagomorpha Proboscidea
Macroscelidea Hyracoidea
Scandentia Sirenia
Xenarthra
Archonta
Primates Xenarthra
Dermoptera Dermoptera
Euarchontoglires
Chiroptera Scandentia
Pholidota Primates
Carnivora Lagomorpha
Tubulidentata Rodentia
Cetacea Eulipotyphla
Artiodactyla Carnivora
Ungulata
Laurasiatheria
Perissodactyla Pholidota
Hyracoidea Perissodactyla
Proboscidea Cetartiodactyla
Sirenia Chiroptera
Figure 1. The prevailing morphological tree (a) and the emerging molecular tree (b) of the placental orders. (a) Morphology generally places Xenarthra (sloths, anteaters
and armadillos) as basal, and most of the remaining orders into three well-established clades: Ungulata (thought to be derived from CONDYLARTH ancestors, Archonta and
Anagalida. The depicted tree is from Shoshani and McKenna [3]. The tree obtained by Liu et al. [4] is identical, apart from placing cetaceans as sister group to the perisso-
dactyl-paenungulate clade. The tree of Novacek ([6]; http://tolweb.org/tree?group ¼ Eutheria&contgroup ¼ Mammalia) places Pholidota (pangolins) as basal sister to
Xenarthra, makes Primates and Scandentia (tree shrews) sister groups, and collapses several clades (black dotted lines). Novacek [5] subsequently collapses some further
clades (gray dotted lines), which increases reconciliation with the molecular tree. (b) The molecular tree recognizes four major clades: Afrotheria, Xenarthra, Laurasiatheria
and Euarchontoglires, of which the latter two are joined into Boreoeutheria. The presented placental ordinal topology is according to Murphy et al. [21]. Placing Marsupialia
as sister to Placentalia is based on Phillips and Penny [54] and references therein. Clades indicated by solid lines are, with rare exceptions, supported independently by all
other molecular data and analyses [24 –29]. Notable exceptions are the strong tendency of mitochondrial protein sequences to place hedgehogs and rodents as basal in the
tree [14]. Colors distinguish the four basal placental clades in the molecular tree.
convergent evolution of features related to volancy in bats separate hippos from other Suiformes (e.g. pigs) [10]. In
and flying lemurs, but eliminates the need to postulate the Eulipotyphla, shrews and hedgehogs group to the exclu-
loss of archontan ankle specializations in bats [32]. sion of moles [25,34]. This result contrasts with morpho-
Complete mtDNA analyses recently placed flying lemurs logical hypotheses that favor either moles þ shrews to
within primates and render the latter PARAPHYLETIC [14]. the exclusion of hedgehogs or moles þ hedgehogs to the
However, SINE and LINE insertions [33] and analyses of exclusion of shrews. In Rodentia, molecular data suggest a
nuclear genes [21,24] recover traditional primate MONO- novel mouse-related clade that includes murids (mice and
PHYLY. Within Laurasiatheria, Eulipotyphla (e.g. moles, rats), dipodids (jerboas), castorids (beavers), geomyids
shrews, hedgehogs) is the probable sister-taxon to the (pocket gophers), heteromyids (pocket mice), anomalurids
remaining orders. The emerging molecular support for a (scaly-tailed flying squirrels), and pedetids (springhares)
sister-group relationship between carnivores and pango- [35]. This group had never been proposed based on
lins includes concatenated nuclear sequences [21], mito- morphological and paleontological data. Within Chirop-
chondrial protein sequences [14] and an RGC (Box 1). tera (bats), both nuclear and mitochondrial sequences
Morphologically, carnivores and pangolins are unique favor microbat paraphyly, which has profound impli-
among living placental mammals in possessing an osseous cations for understanding the origins of laryngeal echolo-
tentorium that separates the cerebral and cerebellar cation (Box 2).
compartments of the cranium [3].
Molecular data are also resolving relationships within The deployment of morphological character evolution
orders, sometimes with unexpected results. In addition to Darwin [36] recognized that ANALOGICAL or adaptive
nesting whales within Artiodactyla, molecular data characters would be almost valueless to the systematist
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Review TRENDS in Ecology and Evolution Vol.not known No.not known Month 0000 5
Figure I. Relationships among the major bat lineages. (a) Traditional bat monophyly coupled with a sister-group relationship between the suborders Megachiroptera
and Microchiroptera. (b) Bat diphyly, with a sister-group relationship between megabats and primates. (c) Microbat paraphyly, with a sister-group relationship
between megabats and the rhinolophoid microbat families Hipposideridae (Old World leaf-nosed bats), Rhinolophidae (horseshoe bats), Megadermatidae (false vam-
pire bats) and Rhinopomatidae (mouse-tailed bats) [27,69,70]. Silhouettes in (a) and (b) indicate originations of flight. Black and gray silhouettes in (c) indicate alternate
scenarios for the evolution of laryngeal echolocation.
and would conceal rather than reveal true blood relation- (e.g. bones in wrist are dorsoventrally compressed and
ship. Deciphering between HOMOLOGOUS (revealing) char- serially arranged) [37]. Concealing characters have sup-
acters, which trace back to a common ancestor, and ported clades such as Edentata (xenarthrans þ pangolins),
analogous (concealing) characters, which have similar Lipotyphla, Ungulata, and Volitantia (bats þ flying lemurs).
functions but evolved separately in different groups For example, the dissociation of xenarthrans and pangolins
(e.g. bird wings and bat wings), requires independent lines on the molecular tree (Figure 1b) suggests that suppression
of evidence. Among marsupial and placental mammals, of tooth development and poorly developed (or absent)
there are numerous examples of taxa that are ecological enamel are features that evolved independently in these two
analogs, including volant forms (sugar gliders versus flying groups. Similarly, flying lemurs share numerous anatomical
squirrels), FOSSORIAL forms with specializations for digging features with bats including a humeropatagialis muscle
(marsupial mole versus African golden moles), ant-termite extending from the humerus to the patagium (i.e. flight
eating forms (Australian numbat versus South American membrane) and extensions of the patagium between the
anteater), and carnivores of various sizes (thylacine versus fingers [38]. With the deployment of bats in Laurasiatheria
wolf, marsupial sabertooth versus placental sabertooth). In and flying lemurs in Euarchontoglires, shared features of
these examples, independent adaptation to similar con- Volitantia must be interpreted as analogous characters that
ditions was revealed through other lines of evidence such as evolved independently in the two orders. Overall, the
fundamental differences in reproductive anatomy. Unfortu- splintering of numerous morphological groups across the
nately, deciphering between homologous and analogous four major clades suggests that there have been extensive
characters is less obvious in comparisons of anatomical parallel adaptive radiations among placental mammals
features among placental mammals. [19,39]. These resemblances are perhaps most striking for
In light of the molecular tree in Figure 1b, it is clear that taxa in Afrotheria and Laurasiatheria (Figure 2), but also
both revealing and concealing characters have impacted extend to Xenarthra (e.g. anteaters have external features
morphological trees of the orders of placental mammals. that parallel both pangolins and aardvarks) and Euarch-
Revealing characters include those that support Glires ontoglires (e.g. flying lemurs share features with bats). With
(e.g. loss of upper and lower first incisor) and Paenungulata the identification of HOMOPLASTIC features in different
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6 Review TRENDS in Ecology and Evolution Vol.not known No.not known Month 0000
Minority views
The emerging consensus for placental ordinal relation-
ships (Figure 1b), with its four major clades that are
supported by overwhelming sequence evidence and RGCs,
is not without critics [4,14,44]. Arnason et al.’s [14] mtDNA
analysis suggests that hedgehogs are dissociated from
other core insectivores, such as shrews and moles, and
were the earliest offshoot of the placental tree. Arnason
et al. [14] also find that rodents, Glires, Euarchontoglires,
Figure 2. Parallel morphological radiations in Afrotheria and Laurasiatheria illus- and Boreoeutheria are all paraphyletic taxa. However, Lin
trate homoplasy in external morphology. (a) African golden mole (Chrysochlori- et al. [27] found that mtDNA trees recover the same four
nae) and (b) Old World mole (Talpinae); (c) Malagasy hedgehog (Tenrecinae) and
(d) common hedgehog (Erinaceinae); (e) shrew tenrec (Oryzorictinae; Microgale
clades as nuclear genes when outgroup taxa are removed.
thomasi; Copyright Link Olson) and (f) common shrew (Soricinae); (g) manatee Peculiar features of rooted mtDNA trees can result from
(Trichechidae) and (h) dolphin (Delphininae); (i) aardvark (Orycteropodidae) and (j) inadequate models of sequence evolution [27,28] and/or
pangolin (Maninae).
unbalanced taxon sampling [28,29]. In particular, some
marsupials have unusual nucleotide compositions and
mammalian taxa, new questions arise, such as whether the there have been changes in the mutational process in both
underlying genetic architecture responsible for these hedgehogs and murid rodents relative to most other
changes involves the same or different genes. placental mammal mitochondrial genomes [27]. These
changes violate the assumptions of most methods of
The root of the placental tree and other remaining phylogeny reconstruction. For example, general time
problems reversible models of nucleotide substitution assume that
With the proposal of and strong support for the four major base composition remains the same in different lineages.
clades of placental mammals, as well as Boreoeutheria Other analyses suggest that protein-coding regions of the
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ARTICLE IN PRESS TREE 298
Review TRENDS in Ecology and Evolution Vol.not known No.not known Month 0000 7
mitochondrial genome lack sufficient power to resolve the are placed within crown-group PLACENTALIA . There are
placental radiation [45]. also extinct eutherians from the Mesozoic, some predating
Some analyses of nuclear sequences have also recovered the origin of crown-group Placentalia [48], whereas others
rodents at or near the base of the placental radiation, might be included within Placentalia [42,49]. It is now
sometimes as a paraphyletic taxon [42,44]. These studies, fundamentally important to re-examine the phylogenetic
which typically have poor taxon sampling among rodents placement of these extinct taxa in the context of the
and/or result from maximum parsimony analyses, are emerging molecular phylogeny for living taxa, with
reminiscent of the guinea pig is not a rodent hypothesis, its division of placental orders into distinct groups
which was emphatically rejected by some morphologists with southern (Xenarthra, Afrotheria) and northern
[46]. Confronted by the morphologists’ challenge to (Euarchontoglires, Laurasiatheria) hemisphere origins.
increase taxon sampling in the molecular studies, recent Total evidence with maximum parsimony has been the
studies with nuclear genes that have subdivided rodent method of choice for combined molecular and morpho-
branches provide compelling support for rodent mono- logical datasets [42,50]. New approaches include Bayesian
phyly [20,35] and underscore the importance of adequate methods, which allow molecular and morphological data to
taxon sampling [47] in phylogeny reconstruction. Taxon have their own evolutionary models [51,52]. The Lewis
sampling that breaks up long branches becomes especially [52] model for morphological characters can potentially
important with certain phylogenetic methods, such as take advantage of autapomorphies (i.e. uniquely derived
maximum parsimony, to mitigate against the potential characters) that are traditionally omitted from morpho-
effects of long-branch attraction. Long-branch attraction logical character matrices because they are uninformative
can occur when parallel/convergent substitutions on long under the maximum-parsimony criterion. One potential
branches outnumber homologous substitutions on short difficulty with combined analyses is that they fail to
interior branches. The potential pitfalls of long-branch address the weighting problem posed by including mol-
attraction with maximum parsimony were exposed in an ecular and morphological data in the same data matrix.
analysis of DNA sequences from exon 11 of the breast and Another alternative is to impose molecular scaffolds with
ovarian cancer susceptibility gene 1 (BRCA1) [19]. morphological data. Molecular scaffolds are topological
constraints derived from previous molecular analyses that
Conclusions and future challenges constrain the topology for living taxa, but not for fossil
After more than a century, we are now in the final stages of taxa. Sánchez-Villagra et al. [53] recently employed mol-
resolving the interordinal tree for living placental mam- ecular scaffolds with morphological data to investigate
mals. Morphology and molecules agree on the monophyly the phylogenetic placement of the giant, extinct rodent
of 16 out of 18 placental orders, whereas molecular Phoberomys. Given the prevalence of morphological
analyses nest whales within Artiodactyla (e.g. cows, convergence suggested by trees from molecular data,
pigs, hippos) and make Lipotyphla (e.g. hedgehogs, the challenge of placing fossil taxa is sure to lead to
moles, shrews, golden moles) DIPHYLETIC . Above the reassessments of morphological characters and new
ordinal level, analyses of molecular data corroborate the methods of phylogenetic analysis.
morphology-based Glires and Paenungulata hypotheses,
as well as a variation of Archonta, dubbed Euarchonta Acknowledgements
[18], which includes primates, tree shrews and flying We thank Michael Novacek, Peter Waddell, and an anonymous reviewer
lemurs. Other morphological superordinal hypotheses are for constructive comments about this article. This work was supported by
no longer viable in the face of robust molecular support for NSF (M.S.S.) and the Training and Mobility of Researchers (TMR)
program of the European Commission (M.J.S. and W.W.d.J.).
Afrotheria, Euarchontoglires and Laurasiatheria. With
independent lines of support for Euarchontoglires, we are
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