Molecules consolidate

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Phylogenetics series
Molecules consolidate the placental
mammal tree
Mark S. Springer
1
, Michael J. Stanhope
2
, Ole Madsen
3
and Wilfried W. de Jong
3
1
Department of Biology, University of California, Riverside, CA 92521, USA
2
Bioinformatics, GlaxoSmithKline, Collegeville, PA 19426, USA
3
Department of Biochemistry, University of Nijmegen, 6500 HB Nijmegen, the Netherlands
Deciphering relationships among the orders of pla-
cental mammals remains an important problem in
evolutionary biology and has implications for under-
standing patterns of morphological character evolution,
reconstructing the ancestral placental genome, and
evaluating the role of plate tectonics and dispersal in
the biogeographic history of this group. Until recently,
both molecular and morphological studies provided
only a limited and questionable resolution of placental
relationships. Studies based on larger and more diverse
molecular datasets, and using an array of methodo-
logical approaches, are now converging on a stable tree
topology with four major groups of placental mammals.
The emerging tree has revealed numerous instances of
convergent evolution and suggests a role for plate
tectonics in the early evolutionary history of placental
mammals. The reconstruction of mammalian phylo-
geny illustrates both the pitfalls and the powers of
molecular systematics.
groups. Thus, reconstructing their phylogeny can serve as
a model for research on other organisms.
Here, we highlight that, in spite of the ongoing debate,
the congruence of most recent molecular evidence is
striking and consensus is approaching rapidly. Progress
has been achieved by using larger and more diverse
molecular datasets, increasing taxon sampling to sub-
divide long branches, and using
LIKELIHOOD
(see Glos-
sary) methods of phylogeny reconstruction that explicitly
model the nucleotide substitution process and are less
susceptible to problems of
STATISTICAL INCONSISTENCY
than are methods such as
MAXIMUM PARSIMONY
[2]
.In
addition, results of phylogenetic analyses that rely on
nucleotide or amino acid substitutions are now comple-
mented by rare genomic changes (RGCs;
Box 1
)that
constitute genetic markers of common descent. The major
molecular finding is that the 18 placental orders are
divided into four clades, of which three were never
suspected based on morphology. Here, we discuss the
reliability of the new tree, discuss reasons for earlier
discrepancies, highlight the remaining problems and
offer a prospectus on future studies.
Are we, humans, more closely related to mice or to cows
and dogs? A long history of debate surrounds this and
other questions pertaining to relationships among the
orders of placental mammals. Difficulties in reconstruct-
ing relationships among the orders have been attributed to
a rapid radiation following the Cretaceous–Tertiary
boundary
[1]
. Even if we consult the recent literature,
we find that the relationship of primates to other placental
orders is the subject of fierce debate. There are many
contradictory hypotheses about placental mammal
relationships, both between and among molecules and
morphology. Yet, it is clear that knowing the actual pattern
of mammalian phylogeny is very important, not only
because it reveals our own genealogy, but also because this
family tree provides the framework to interpret the
evolution of morphological, physiological, behavioral,
and genomic features that characterize different mamma-
lian taxa. Understanding placental mammal phylogeny is
also a crucial prerequisite for unraveling the biogeogra-
phical history of this group. Mammals are better known
from morphological and molecular data than are all other
The growth of molecular consensus
Until the advent of molecular approaches, mammalian
phylogeny was necessarily the domain of morphology and
paleontology. Since Darwin, the study of placental mam-
mal relationships has seen episodic development and has
culminated in a morphological tree that remains promi-
nent in the current literature (
[3–5]
;
Figure 1a
). Vari-
ations of this tree largely conform to the topology of ordinal
relationships proposed by Novacek
[6]
, which evolved from
the mammalian classifications of Gregory in 1910,
Simpson in 1945, and McKenna in 1975. The major
characteristics of this tree are that Xenarthra
(e.g. armadillos, anteaters) are the most basal placental
group, and that most of the remaining orders are grouped
into three generally accepted clades: (i)
UNGULATA
,
(ii)
ARCHONTA
, and (iii)
ANAGALIDA
. This topology deviates
in essential aspects from the currently emerging molecu-
lar tree, which recognizes three novel superordinal clades:
AFROTHERIA
,
LAURASIATHERIA
and
EUARCHONTOGLIRES
,
the latter two of which are
SISTER GROUPS
[i.e.
BOR-
EOEUTHERIA
;
Figure 1b
].
Corresponding author: Mark S. Springer (mark.springer@ucr.edu).
0169-5347/$ - see front matter
q
2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2004.05.006
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ungulates, and placed them with aardvarks in what
later became the Afrotheria.
As sequences for complete mitochondrial genomes
became available, molecular studies of interordinal
relationships were dominated by these data. This led to
various unorthodox proposals, some of which have now
been well corroborated, notably the sister-group relation-
ship of whales to hippos
[8]
and the grouping of bats closer
to ungulates rather than to primates
[9]
. Indeed, all
subsequent sequence data
[10]
, as well as SINE inser-
tions
[11]
and a cladistic analysis of morphological charac-
ters
[12]
, support an artiodactyl ancestry for Cetacea,
whereas bats became firmly nested within Laurasiatheria
(
Figure 1b
). The proposals that the guinea pig is not a
rodent
[13]
, that hedgehog or rodents are the oldest
placental offshoots
[14]
, and that the egg-laying mono-
tremes are the sister-group of marsupials
[15]
were strongly
advocated based on mitochondrial DNA (mtDNA) data
and still persist. These hypotheses have provoked much
discussion about the reliability of deeper phylogenetic
inference from mitochondrial data
[16]
, but are now
contradicted by both morphological and other molecular
evidence supporting rodent monophyly (including guinea
pigs), a more nested position for hedgehogs within the
placental tree, and a sister group relationship between
placentals and marsupials (
Figure 1
). The use of PCR also
made the comparative sequencing of nuclear genes
feasible. In general, phylogenetic analyses of nuclear
gene segments (i) led to poorly resolved and unstable
topologies; and (ii) showed that single genes can give
misleading topologies. However, analyses of individual
nuclear genes agree with more recent molecular studies in
supporting the whale-hippo clade, Paenungulata and
Afrotheria, including enlarging the latter clade to also
include elephant shrews, golden moles and tenrecs
[17]
.
A shortcoming of most molecular studies from the 1980s
and 1990s was incomplete and unbalanced taxon sampling
that was also mostly based on relatively short segments of
single genes. Nevertheless, by combining evidence from
various separate analyses, a division of all placentals into
the four currently recognized major clades (
Figure 1b
) was
first proposed by Waddell et al.
[18]
. Solid support for these
superordinal groups has come from independent studies
that concatenated DNA sequences from many different
nuclear genes, including representatives of all extant
placental orders
[19–25]
. Subsequently, additional sup-
port for the four major clades has emerged fromanalyses of
the complete set of mitochondrial tRNA and rRNA gene
sequences
[26]
. Analyses of mitochondrial protein-coding
sequences have returned mixed results, but reconciliation
with nuclear trees is reached when methods that mitigate
against known phylogeny reconstruction problems are
employed
[27,28]
and/or taxon sampling is improved
[29]
.
Beyond sequence analyses, the four major clades are
forcefully corroborated by RGCs (
Box 1
).
Considerable resolution within the four major groups
has also been achieved. Within Afrotheria, molecular
phylogenies support Paenungulata, which also appears in
several morphological classifications
[30]
. A novel molecu-
lar result is a sister-group relationship between ele-
phant shrews and golden moles þ tenrecs
[21,25]
. Fetal
Glossary
Afrotheria: the molecular superordinal hypothesis that includes the orders
Proboscidea (elephants), Sirenia (manatees and dugongs), Hyracoidea
(hyraxes), Tubulidentata (aardvarks), Afrosoricida (golden moles and tenrecs)
and Macroscelidea (elephant shrews).
Anagalida: the morphology-based superordinal hypothesis that includes
Rodentia (e.g. rats, mice and guinea pigs), Lagomorpha (rabbits, hares and
pikas) and Macroscelidea (elephant shrews).
Archonta: the morphology-based superordinal hypothesis that includes
Chiroptera (bats), Dermoptera (flying lemurs), Primates (e.g. humans, apes
and monkeys) and Scandentia (tree shrews).
Analogy: characters that have similar functions, but that evolved indepen-
dently in different groups and are not descended from a common ancestral
precursor character.
Atlantogenata: the molecular superordinal hypothesis that includes the order
Xenarthra (sloths, armadillos and anteaters) and the superordinal group
Afrotheria.
Boreoeutheria:
the molecular superordinal hypothesis that
includes the
superordinal groups Euarchontoglires and Laurasiatheria.
Condylarth: an extinct group of primitive hoofed mammals.
Diphyletic: a group with two separate origins. For example, Edentata is
diphyletic on the molecular tree because xenarthrans and pangolins have
separate origins and do not share a common ancestor with each other to the
exclusion of other placental mammals.
Euarchontoglires: the molecular superordinal hypothesis that includes the
orders Rodentia (e.g. rats, mice and guinea pigs), Lagomorpha (rabbits, hares
and pikas), Scandenta (tree shrews), Dermoptera (flying lemurs) and Primates
(e.g. humans, apes and monkeys).
Eutheria: a stem group that includes Placentalia plus extinct mammalian taxa
that are outside of Placentalia but more closely related to placentals than to
marsupials.
Fossorial: a term that is used to describe animals that are adapted to digging,
such as moles and golden moles.
Glires: the morphology-based superordinal hypothesis that includes Rodentia
(e.g. rats, mice, guinea pigs) and Lagomorpha (rabbits, hares, pikas).
Homology: characters are homologous if they trace back to a common
ancestral precursor character.
Homoplasy: molecular or morphological similarities that evolved indepen-
dently in different lineages and were not inherited from a common ancestor.
Laurasiatheria: themolecular superordinal hypothesis that includes the orders
Eulipotyphla (hedgehogs, moles and shrews), Chiroptera (bats), Perissodac-
tyla (horses, tapirs, and rhinos), Cetartiodactyla (e.g. camels, pigs, cows,
hippos, whales and porpoises), Carnivora (e.g. dogs, bears and cats) and
Pholidota (pangolins).
Maximum likelihood: in phylogenetics, the maximum likelihood estimate of
the phylogeny is the hypothesis (e.g. evolutionary tree) that gives the highest
probability of observing the data (e.g. nucleotide sequences).
Maximum parsimony: a phylogeny reconstruction method that searches for
one or more trees that minimize the number of evolutionary changes that are
required to explain the observed differences among taxa included in the study.
Monophyletic: a group that
includes a common ancestor and all
its
descendants.
Paenungulata: the morphology-based superordinal hypothesis that includes
the orders Hyracoidea (hyraxes), Sirenia (manatees and dugongs) and
Proboscidea (elephants).
Paraphyletic: a group that includes a common ancestor but only a fraction of
its descendants.
Placentalia: a crown group that includes the most recent common ancestor of
all placental mammal and all the descendants, living and extinct, of this
common ancestor.
Sister groups: taxa that are each other’s closest relatives.
Statistical inconsistency: in phylogenetics, methods are consistent when they
converge on the correct answer given enough data. Conversely, inconsistent
methods will converge on an incorrect answer given enough data.
Ungulata: the morphology-based superordinal hypothesis that includes the
orders Hyracoidea (hyraxes), Sirenia (manatees and dugongs), Proboscidea
(elephants), Perissodactyla (horses, tapirs and rhinos), Artiodactyla (e.g.
camels, pigs, cows, pigs), Cetacea (e.g. whales and porpoises) and, variably,
Tubulidentata (aardvarks).
Some conspicuous features of the present molecular
tree emerged during the 1980s, when comparative
sequencing was performed on proteins such as hemo-
globins, myoglobin, aA-crystallin, cytochrome c and
ribonuclease
[7]
. In spite of the limited ordinal represen-
tation, these protein sequences separated
PAENUNGULATES
(e.g. elephants, hyraxes, dugongs)
from the other
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Box 1. Rare genomic changes in mammalian phylogenetics
Rare genomic changes (RGCs) include events such as insertions or
deletions (indels), retrotransposon integrations, diagnostic amino acid
signatures, changes in gene order or genome organization, gene
duplications, and genetic code changes [55,56]. RGCs have become
increasingly important in systematics and complement phylogenetic
analyses of primary sequence data. It has been argued that they
constitute excellent markers of common descent (synapomorphies or
shared derived characters) because homoplasy and secondary loss are
less likely than for single nucleotide substitutions. RGCs can serve as
arbiters in cases where primary sequences generate conflicting or
inconclusive results. Table I lists important RGCs that have contributed
to our understanding of higher-level placental phylogenetics. Figure I
illustrates deletions that support Euarchontoglires and Afrotheria. In
spite of their usefulness in higher-level systematics, RGCs are not
immune to homoplasy and other problems and must be interpreted
with caution [57]. Waddell et al. [22] provide a statistical framework for
testing alternate hypotheses using SINE data that explicitly addresses
the gene tree/species tree problem.
Table I. Important rare genomic changes (RGCs) in placental mammal systematics
RGC
a
Clade supported
Refs
79–82 amino-acid deletion in aligned APOB sequences
Afrotheria
[24]
Chromosomal rearrangements
b
Afrotheria
[58]
AfroSINEs
c
Paenungulata
[59]
3 amino-acid deletion in
a
A-crystallin protein
Xenarthra
[60]
6-bp deletion in PRNP
Euarchontoglires
[57,61]
18 amino-acid deletion in SCA1 protein alignment
Euarchontoglires
[57,61]
MLT1A0 element insertions
d
Euarchontoglires [62]
10-bp deletion in aligned sequences for the 5
0
untranslated region of the PLCB4 gene Laurasiatheria [63]
363-bp deletion in aligned APOB sequences Carnivora
þ
Pholidota [24]
SINE insertions Hippopotamidae
þ
Cetacea [11,22]
LINE1 insertion between exons 40 and 41 of the COLIA2 gene Primates [33]
FLAM integration between exons 5 and 6 of the HBX2 gene Primates [33]
Presence of Alu SINEs Primates [33]
a
Abbreviations: APOB, apolipoprotein B; COLIA2, collagen type I
a
2; FLAM, free left Alu monomer; HBX2, homeobox gene 2; LINE, long interspersed nuclear element;
PLCB4, phosphoinositide-specific phospholipase-C
b
4; PRNP, prion protein; SCA1, spinocerebellar ataxia type 1; SINE, short interspersed nuclear element.
b
Fronicke et al. [58] identified two chromosomal rearrangements that link the representative afrotherians (African elephant and aardvark) that were investigated: first, a
syntenic association of human chromosomes 5 and 21, and, second, a syntenic association of human chromosomes 1 and 19.
c
AfroSINEs are a novel family of short interspersednuclear elements that are distributedexclusively amongafrotherian taxa [59]. This distribution supports themonophyly
of Afrotheria. TheHSP (Hyracoidea, Sirenia, Proboscidea) subfamily of AfroSINES contains a 45-bpdeletion in themiddle regionof the SINE and is unique to paenungulate
taxa.
d
Three LINE insertions havebeendetected in rodents andprimates, but not in carnivores, artiodactyls, or non-mammalianvertebrates that havebeenexamined [62]. These
putative RGCs for Euarchontoglires remain to be investigated in additional taxa.
(a)
(b)
LHLGKPGHRSYALSPQQALGPEGVKAAAVATLSPHTVIQTTHSASEPLP
Whale
Alpaca/Llama
Horse
Pangolin
Cat
Bat
Shrew
Human
Flying lemur
Tree shrew
Rabbit/Hare
Mouse
Anteater
Sea cow
Elephant
Hyrax
Aardvark
Elephant shrew
Golden mole
Tenrec
Opossum
AGTGATGAAATGTTAACTTCTAACGACTTACGT
LHLGKPGHRSYALSPQQALGPEGVKAAAVATLSPHTVIQTTHSASEPLP
AGCGACGAAATGTTACCTTCTGATGACTCACAT
LHLGKPGHRSYALSPQQALGPESVKAAAVATLSPHTVIQTTHSASEPLP
AGTGAGGAAATGTTAACTTCTGATGACTCATGT
LHLGKPGHRSYALSPQQALGPEGVKAAAVATLSPHTVIQTTHSASEPLP
AGTGATGAAATGTTAACTTCTGATGATCCATGT
LHLGKPGHRSYALSPQQALGPEGVKAAAVATLSPHTVIQTTHSASEPLP
AGTGATGAAATGTTAACTTCTGATGACTCACCA
LHLGKPGHRSYALSPQQALGPDGVKAATVATLSPHTVIQTTHSASEPLP
CGTGATGAAATATTAACTTCTGATGTCTCACCT
LHLGKAGHRAYALSPQQALGPEGVKAAAVATLSPHTVIQTTHSASEALP
AGTGATGATGTATTATCTTCTGATGATTTCCAT
LHLGKPGHRSYALSP-------------------HTVIQTTHSASEPLP
AGTGATGAACTGTTAGGTTCTGATGACTCACAT
LHLGKPGHRSYALSP-------------------HTVIQTTHSASEPLP
AGTGATGAAATTTTAGCTTCTGATGACTCACGT
LPLGKPGHRSYALSP-------------------HTVTQATHSASEPLP
AGTGATGAAATGTTAACTTCTAACGACTCACAT
LHLGRPGHRSYALSP-------------------HTVIQTTPSASEPLP
AGTAATGAAATGTTAACTCCTGATGACTCACTT
LHLGKPGHRSYALSP-------------------HTVIQTTHSASEPLP
ACTGGTGAAATGTTAACTTCTGACAGCGCATCT
LHLGKPGHRAYALSPQQALGPEGVK-AAVATLSPHTVXQTPHSASEPLP
AGTGATGACATATTGACTTCTAATGACTCATGC
LHVGKTSHRSYGLSPQQALGPEGVK-AAVATLSPHSVIQTTHSASEPLP
AGTGATGGCCTG---------GATGACTTGCAT
LHLGKASHRSYALSPQQALGPEGVK-AAVATLSPHSVIQTTHSASEPLP
AGTGACGGCCTG---------GATGTCTTAAAT
LHLGKASHRSYALSPQQALGPEGVK-AAVATLSPHSVIQTPHSASEPLP
AGTGACAACCTA---------AGTGATTCACCT
LHLGKAGHRSYALSPQQALGPEGVK-AAVTTLSPHTVIQTTHNASEPLP
AGTGATGGCCTG---------GATGGCTCACAT
LHLGKAGHRSYALSPQQALAPDGVK-AAVATLSPHTVIQTSHNASEPLP
AGCGGTGGCCTG---------GATGGCTGCCAT
LHLGKAXHRSYALSPQQALGPEGVK-AAVATLSPHTVIQTTHNASEPLP
AGTGATGGCCTG---------GATGAGTCACAT
LHLGKAGHRSYALSPQQALGPEGVK-AAVATLSPHTVIQTTHNASEPLP
AGCCACGGCCTG---------GGTGACTCTCGC
LHLGKPSHRSYALSPQQALGPEGVK-ATVATLSPHTVIQTTHSASDPLP
AGTAATGTCATTTTAGTCTCTGATTACTCCTCT
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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
hypothesis
[31]
. Within Euarchontoglires, there is a
fundamental split between
GLIRES
(rodents þ lago-
morphs) and Euarchonta (primates þ tree shrews þ flying
lemurs). Glires is a bastion of morphological trees;
Euarchonta differs from the morphological Archonta
hypothesis by removing bats from this clade. The
molecular exclusion of bats from Archonta requires
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(a)
(b)
Monotremata
Monotremata
Marsupialia
Marsupialia
Xenarthra
Afrosoricida
Insectivora
Macroscelidea
Rodentia
Tubulidentata
Lagomorpha
Proboscidea
Macroscelidea
Hyracoidea
Scandentia
Sirenia
Primates
Xenarthra
Dermoptera
Dermoptera
Chiroptera
Scandentia
Pholidota
Primates
Carnivora
Lagomorpha
Tubulidentata
Rodentia
Cetacea
Artiodactyla
Eulipotyphla
Carnivora
Perissodactyla
Pholidota
Hyracoidea
Perissodactyla
Proboscidea
Cetartiodactyla
Sirenia
Chiroptera
TRENDS in Ecology & Evolution
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]
;
) 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
and flying lemurs, but eliminates the need to postulate the
loss of archontan ankle specializations in bats
[32]
.
Complete mtDNA analyses recently placed flying lemurs
within primates and render the latter
PARAPHYLETIC
[14]
.
However, SINE and LINE insertions
[33]
and analyses of
nuclear genes
[21,24]
recover traditional primate
MONO-
PHYLY
. Within Laurasiatheria, Eulipotyphla (e.g. moles,
shrews, hedgehogs) is the probable sister-taxon to the
remaining orders. The emerging molecular support for a
sister-group relationship between carnivores and pango-
lins includes concatenated nuclear sequences
[21]
, mito-
chondrial protein sequences
[14]
and an RGC (
Box 1
).
Morphologically, carnivores and pangolins are unique
among living placental mammals in possessing an osseous
tentorium that separates the cerebral and cerebellar
compartments of the cranium
[3]
.
Molecular data are also resolving relationships within
orders, sometimes with unexpected results. In addition to
nesting whales within Artiodactyla, molecular data
separate hippos from other Suiformes (e.g. pigs)
[10]
.In
Eulipotyphla, shrews and hedgehogs group to the exclu-
sion of moles
[25,34]
. This result contrasts with morpho-
logical hypotheses that favor either moles þ shrews to
the exclusion of hedgehogs or moles þ hedgehogs to the
exclusion of shrews. In Rodentia, molecular data suggest a
novel mouse-related clade that includes murids (mice and
rats), dipodids (jerboas), castorids (beavers), geomyids
(pocket gophers), heteromyids (pocket mice), anomalurids
(scaly-tailed flying squirrels), and pedetids (springhares)
[35]
. This group had never been proposed based on
morphological and paleontological data. Within Chirop-
tera (bats), both nuclear and mitochondrial sequences
favor microbat paraphyly, which has profound impli-
cations for understanding the origins of laryngeal echolo-
cation (
Box 2
).
The deployment of morphological character evolution
Darwin
[36]
recognized that
ANALOGICAL
or adaptive
characters would be almost valueless to the systematist
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Box 2. Bat relationships and the evolution of flight and echolocation
Bats (order Chiroptera) have traditionally been viewed as a mono-
phyletic order and members of the superordinal clade Archonta, which
also includes flying lemurs, tree shrews and primates. Bats are the only
mammals with the capacity for powered flight. Bat monophyly implies
homology of the flight apparatus and a single origin for mammalian
flight (Figure Ia).
Chiroptera is divided into the suborders Microchiroptera (microbats)
and Megachiroptera (megabats). Microbats are generally smaller than
megabats and are characterized by complex laryngeal echolocation
systems that transmit, receive and process ultrasonic calls. Megabats,
commonly known as Old World fruitbats, have enhanced visual acuity
and do not echolocate, with the exception of a few forms that use a
different type of echolocation based on tongue-clicks.
In the 1980s, Smith and Madkour [64] suggested that megabats were
more closely related to primates than to microbats based on
morphological characteristics of the penis. This hypothesis implied
that bats were diphyletic and that flight had evolved independently in
microbats and megabats (Figure Ib). Pettigrew and colleagues [65]
provided additional support for the ’flying primate’ hypothesis by
showing that primates and megabats share retino-tectal pathways
from the eye to the cortex. Subsequently, both morphological and
molecular data falsified the bat diphyly hypothesis and supported
traditional bat monophyly [66,67]. Nevertheless, surprising results
from molecular studies were the dissociation of bats from Archonta
[9] and the nesting of megabats within Microchiroptera (Figure Ic).
Microbat paraphyly mandates either dual origins of laryngeal
echolocation in rhinolophoid and yangochiropteran microbats or
a single origin in the common ancestor of bats followed by loss of
this feature in the common ancestor of megabats. In analyses with
living taxa only, these possibilities are equally parsimonious.
Molecular scaffold analyses based on morphological data for living
bat families plus fossil bat genera from the early Eocene favor a
single origin of laryngeal echolocation with subsequent loss in the
ancestor of megabats [68].
(a)
(b)
(c)
Microbats
Megabats
Rhinolophoid microbats
Megabats
Primates
Megabats
Other placentals
Microbats
Yangochiropteran microbats
TRENDS in Ecology & Evolution
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-
ship. Deciphering between
HOMOLOGOUS
(revealing) char-
acters, which trace back to a common ancestor, and
analogous (concealing) characters, which have similar
functions but evolved separately in different groups
(e.g. bird wings and bat wings), requires independent lines
of evidence. Among marsupial and placental mammals,
there are numerous examples of taxa that are ecological
analogs, including volant forms (sugar gliders versus flying
squirrels),
FOSSORIAL
forms with specializations for digging
(marsupial mole versus African golden moles), ant-termite
eating forms (Australian numbat versus South American
anteater), and carnivores of various sizes (thylacine versus
wolf, marsupial sabertooth versus placental sabertooth). In
these examples, independent adaptation to similar con-
ditions was revealed through other lines of evidence such as
fundamental differences in reproductive anatomy. Unfortu-
nately, deciphering between homologous and analogous
characters is less obvious in comparisons of anatomical
features among placental mammals.
In light of the molecular tree in
Figure 1b
, it is clear that
both revealing and concealing characters have impacted
morphological trees of the orders of placental mammals.
Revealing characters include those that support Glires
(e.g. loss of upper and lower first incisor) and Paenungulata
(e.g. bones in wrist are dorsoventrally compressed and
serially arranged)
[37]
. Concealing characters have sup-
ported clades such as Edentata (xenarthrans þ pangolins),
Lipotyphla,Ungulata, andVolitantia (bats þ flying lemurs).
For example, the dissociation of xenarthrans and pangolins
on the molecular tree (
Figure 1b
) suggests that suppression
of tooth development and poorly developed (or absent)
enamel are features that evolved independently in these two
groups. Similarly, flying lemurs sharenumerous anatomical
features with bats including a humeropatagialis muscle
extending from the humerus to the patagium (i.e. flight
membrane) and extensions of the patagium between the
fingers
[38]
. With the deployment of bats in Laurasiatheria
and flying lemurs in Euarchontoglires, shared features of
Volitantiamust be interpreted as analogous characters that
evolved independently in the two orders. Overall, the
splintering of numerous morphological groups across the
four major clades suggests that there have been extensive
parallel adaptive radiations among placental mammals
[19,39]
. These resemblances are perhaps most striking for
taxa in Afrotheria and Laurasiatheria (
Figure 2
), but also
extend to Xenarthra (e.g. anteaters have external features
that parallel both pangolins and aardvarks) and Euarch-
ontoglires (e.g. flying lemurs share featureswith bats).With
the identification of
HOMOPLASTIC
features in different
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