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Endemic African mammals shake the phylogenetic tree

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The order Insectivora, including living taxa (lipotyphlans) and archaic fossil forms, is central to the question of higher-level relationships among placental mammals. Beginning with Huxley, it has been argued that insectivores retain many primitive features and are closer to the ancestral stock of mammals than are other living groups. Nevertheless, cladistic analysis suggests that living insectivores, at least, are united by derived anatomical features. Here we analyse DNA sequences from three mitochondrial genes and two nuclear genes to examine relationships of insectivores to other mammals. The representative insectivores are not monophyletic in any of our analyses. Rather, golden moles are included in a clade that contains hyraxes, manatees, elephants, elephant shrews and aardvarks. Members of this group are of presumed African origin. This implies that there was an extensive African radiation from a single common ancestor that gave rise to ecologically divergent adaptive types. 12S ribosomal RNA transversions suggest that the base of this radiation occurred during Africa's window of isolation in the Cretaceous period before land connections were developed with Europe in the early Cenozoic era.
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Endemic African mammals
shake the phylogenetic tree
Mark S. Springer*, Gregory C. Cleven*, Ole Madsen
,
Wilfried W. de Jong
†‡
, Victor G. Waddell§,
Heather M. Amrine* & Michael J. Stanhope§
* Department of Biology, University of California, Riverside, California 92521,
USA
Department of Biochemistry, University of Nijmegen, PO Box 9101,
6500 HB Nijmegen, The Netherlands
Institute for Systematics and Population Biology, University of Amsterdam, PO
Box 94766, 1090GT Amsterdam, The Netherlands
§ Biology and Biochemistry, Queens University, 97 Lisburn Road,
Belfast BT9 07BL, UK
.........................................................................................................................
The order Insectivora, including living taxa (lipotyphlans) and
archaic fossil forms, is central to the question of higher-level
relationships among placental mammals
1
. Beginning with
Huxley
2
, it has been argued that insectivores retain many primi-
tive features and are closer to the ancestral stock of mammals than
are other living groups
3
. Nevertheless, cladistic analysis suggests
that living insectivores, at least, are united by derived anatomical
features
4
. Here we analyse DNA sequences from three mito-
chondrial genes and two nuclear genes to examine relationships
of insectivores to other mammals. The representative insectivores
are not monophyletic in any of our analyses. Rather, golden moles
are included in a clade that contains hyraxes, manatees, elephants,
elephant shrews and aardvarks. Members of this group are of
presumed African origin
5,6
. This implies that there was an exten-
sive African radiation from a single common ancestor that gave
rise to ecologically divergent adaptive types. 12S ribosomal RNA
transversions suggest that the base of this radiation occurred
during Africa’s window of isolation in the Cretaceous period
before land connections were developed with Europe in the
early Cenozoic era.
Relationships among orders of placental mammals have proved
difficult to resolve
1
. To extend the available mitochondrial (mt)
sequences, a 2.6-kilobase (kb) segment containing the 12S rRNA,
valine transfer RNA, and 16S rRNA genes was sequenced for nine
taxa to generate a data set that is representative of 12 of the 18
placental orders and all three insectivore suborders
4
. Phylogenetic
analyses provide strong support for well-established mammalian
clades such as carnivores, hominoids, and Cetacea plus Artiodactyla
(Fig. 1a). In agreement with other molecular studies
7–10
that
included an assortment of taxa, most interordinal associations are
not resolved at bootstrap values .75%. However, the mtDNA data
do provide strong support for the association of the two paen-
ungulates (hyrax, manatee) together, and of these with elephant
shrews, aardvarks and golden moles (Fig. 1a and Table 1). The
association of hyraxes with proboscideans and sirenians was sug-
gested by Cope
11
. A competing hypothesis is an association of
hyraxes with perissodactyls
12
. Our results agree with earlier
protein
13,14
and DNA studies
7–10
supporting Cope’s paenungulate
hypothesis. In addition to bootstrap support, T-PTP
15
and Kishino
Hasegawa
16
tests also support paenungulate monophyly (Table 2).
Anatomical data provide some evidence that aardvarks and/or
elephant shrews may be related to paenungulates
17,18
but suggest
other hypotheses as well: for example, six osteological features are
putative synapomorphies uniting elephant shrews with lagomorphs
and rodents
19
. All the available sequence data, including amino-acid
sequences
13,14
, DNA sequences for three nuclear genes
8–10
, and the
present mitochondrial genes, support an association of aardvarks
and elephant shrews with paenungulates. What is most unexpected
is that golden moles, a family of insectivores, are also part of this
clade. 12S rRNA sequences earlier suggested an association of
golden moles with paenungulates, but did not provide convincing
bootstrap support for this hypothesis
7
. Our expanded data set
demonstrates that insectivores are not monophyletic (Table 2)
Table 1 Bootstrap support for select clades based on different methods
Clade
Paenungulata Paenungulata þ aardvark
þ elephant shrew
þgolden mole
Mitochondrial DNA
Parsimony 99 95
Transversion parsimony 64 90
Minimum evolution
TamuraNei I 100 92
TamuraNei II 100 78
Logdet 99 90
Maximum likelihood 100 100
vWF
Parsimony
All positions 49 99
1st and 2nd positions 24 65
3rd positions 51 93
Transversion parsimony 30 95
Minimum evolution
TamuraNei I 37 99
TamuraNei II 30 99
Logdet 43 97
Maximum likelihood 78 100
A2AB
Parsimony
All sites 71 88
1st and 2nd positions 49 81
3rd positions 31 67
Transversion parsimony 71 54
Minimum evolution
TamuraNei I 83 84
TamuraNei II 28 25
Logdet 79 78
Maximum likelihood 81 89
.............................................................................................................................................................................
Only two of the three paenungulate orders were represented among the mitochondrial and
A2AB sequences. TamuraNei
27
I and II distances were calculated by using an equal-rates
assumption and a gamma-distribution of rates, respectively.
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Figure 1 Majority-rule parsimony bootstrap trees based on mitochondrial (a),
vWF (b), and A2AB (c) sequences. Bootstrap values and decay indices,
respectively, are above and below branches. The minimum-length tree (3,836
steps; consistency index, 0.430) for the mitochondrial data is 4, 7, 43 and 66 steps
shorter than trees that constrain shrew þ hedgehog, rodent monophyly, insecti-
vore monophyly, and hyrax þ horse, respectively. Insectivore monophyly and a
hyrax-perissodactyl association require 29 and 64 additional steps, respectively,
in comparison to five minimum-length vWF trees (2,401 steps; consistency index,
0.511). Insectivore monophyly requires 26 additional steps in comparison to the
shortest A2AB tree (1,469 steps; consistency index, 0.730).
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and that golden moles, elephant shrews, aardvarks and paenungu-
lates are part of the same clade.
To corroborate these findings, we obtained sequences from exon
28 of the von Willebrand factor (vWF) gene for golden mole,
hedgehog and pangolin. Adding these to the existing vWF data
set
9
, we found high bootstrap support for the inclusion of golden
moles with paenungulates, elephant shrews and aardvarks (Fig. 1b
and Table 1). Sequences from the a-2B adrenergic receptor gene
(A2AB) also support the association of golden moles with paenun-
gulates, elephant shrews and aardvarks (Fig. 1c and Table 1).
Parsimony and maximum-likelihood trees supporting the paenun-
gulategolden moleaardvarkelephant shrew clade are signifi-
cantly better than the best trees that constrain insectivore
monophyly (Table 2).
This expanded clade, which includes five placental orders plus
golden moles, has not been previously hypothesized on the basis of
morphological or molecular data. Elephants, sirenians, hyraxes,
golden moles, aardvarks and elephant shrews show a variety of
ecological and morphological specializations and it is not surprising
that morphology has not elucidated their common ancestry, now
evident from DNA sequences. It is notable that all six of these groups
are of probably African origin or, in the case of the aquatic sirenians,
from along the margins of the former Tethys Sea
5,6,13
. In two cases
(golden moles and elephant shrews), geographic distribution has
been restricted to Africa for the complete temporal range of these
taxa
5
. Thus geographic evidence adds to the molecular data in
support of this African origin’ clade. The radiation of the African
clade parallels endemic radiations of other vertebrate taxa on
Southern Hemisphere continents during the breakup of Gondwana-
land; for example, marsupials and passerine birds in Australia
20
, and
marsupials, edentates and notoungulates in South America
5
.
Paenungulate orders diverged from each other 51 to 59 million
years (Myr) ago, as deduced from 12S rRNA transversions (Table 3).
Deeper in the African clade, average divergence times between
paenungulates and other lineages range from 67 to 80 Myr. The
mean divergence time between taxa in the African clade and the
other 13 orders of placental mammals is ,91 Myr. These divergence
times support the hypothesis that many eutherian orders arose
before the extinction of dinosaurs at the end of the Cretaceous
21
and
imply that conventional views on the origins of the African mammal
fauna
5
are incorrect. Africa’s window of isolation extended from the
Late Cretaceous, when Africa became separated from South Amer-
ica, to the early Cenozoic, when tenuous connections developed
between northern Africa and Europe. The window of isolation
extended from at least 80 Myr (ref. 20), if not earlier, until the early
Cenozoic. The traditional view is that condylarths, prosimian
primates and creodont carnivores reached Africa from the north
after the docking of Africa with Europe
5
. From the condylarth stock,
groups such as proboscideans and sirenians ostensibly originated in
Africa. Other elements of the African mammal fauna, including
perissodactyls, artiodactyls, insectivores and living carnivore
families, presumably arrived in the Neogene with the establishment
of the Arabian Peninsula. Evidence for an extensive African clade,
including taxa with divergence times as old as 80 Myr, is inconsistent
with this view. The ancestor of the African clade probably resided in
Africa before the window of isolation and did not arrive from the
north in the early Cenozoic. The role of geographic isolation and
continental break-up in the early diversification of placental mam-
mals is potentially more important than previously recognized.
M
. . . . . .. .. .. .. . . . . . . . . .. .. . . . . . . . . . . .. .. . . . . . . . . .. .. . . . . . . . . . . .. .. .. .. . . . . . . .. .. .. . . . . . . .. . . .. .. . . . . . . . . . . .. .. . . . . . . . . .. ..
Methods
Amplification and sequencing. 12S rRNA and tRNA genes were amplified
and sequenced as described
22
. 16S rRNA genes were amplified using primers for
valine-tRNA (for example, 59-tacaccyaraagatttca-39) and leucine-tRNA (for
example, 59-agaggrtttgaacctctg-39) and sequenced. Accession numbers for the
new mitochondrial sequences (Echymipera kalubu (bandicoot); Dromiciops
gliroides (monito del monte); Sorex palustris (shrew); Manis sp. (pangolin);
Amblysomus hottentotus (golden mole); Procavia capensis (hyrax); Trichechus
manatus (manatee); Orcyteropus afer (aardvark); Elephantulus rufescens
(elephant shrew)) are U97335U97343. 12S rRNA sequences for several of
these taxa have been deposited in GenBank (M95108 (golden mole), U61073
(monito del monte), U61079 (pangolin), U61083 (manatee), U61084 (hyrax)).
Accession numbers for additional mitochondrial sequences are as follows: cow
(J01394); blue whale (X72204); fin whale (X61145); horse (X79547); cat
(U20753) harbour seal (X63726); grey seal (X72004); human (J01415); gorilla
(D38114); orang-utan (D38115); guinea-pig (L35585); hedgehog (X88898); rat
(X14848); mouse (J01420); opossum (Z29573); platypus (U33498; X83427).
Exon 28 of the vWF gene was amplified and sequenced as described
9
. Accession
numbers for Manis sp., Erinaceus europaeus (hedgehog), and Amblysomus
hottentotus vWF sequences are U97534U97536. Additional vWF sequences
are from ref. 9. Part of the single-copy, intronless A2AB gene was amplified
using the primers A2ABFOR (59-asccctactcngtgcaggcnacng-39) and A2ABREV
(59-ctgttgcagtagccdatccaraaraaraaytg-39). PCR products were cloned into a T/
A cloning vector (Promega) and both strands were sequenced for at least two
clones using the Thermo Sequenase fluorescent-labelled primer cycle sequen-
cing kit (Amersham). Accession numbers for the new A2AB sequences (Elephas
maximus (elephant); Orycteropus afer (aardvark); Macroscelides proboscideus
(elephant shrew); Amblysomus hottentotus (golden mole); Procavia capensis
(hyrax); Erinaceus europaeus (hedgehog); Talpa europaea (mole)) are Y12520–
Y12526. Additional a-2 adrenergic sequences are M34041 (human); M32061
(rat); (L00974) (mouse), and U25722U25724 (guinea-pig).
Sequence alignment and phylogenetic analysis. Sequences were aligned
using CLUSTAL W (ref. 23). rRNA alignments were modified in view of
secondary structure
24,25
. Ambiguous regions were omitted from subsequent
analyses
26
; this resulted in 2,152, 1,261 and 1,132 nucleotide positions,
respectively, for the mt, vWF and A2AB genes. The mt, vWF and A2AB data
sets contain 810, 497 and 393 informative sites, respectively. Phylogenetic
analyses (parsimony, minimum evolution with TamuraNei
27
and Logdet
28
distances, maximum likelihood under the HKY85 (ref. 29) model) were
conducted with PAUP 4.0d52-54, written by D. L. Swofford. The mitochondrial
tree was rooted using platypus and marsupial sequences. The vWF tree was
rooted with the sloth
7
; alternatively, rooting with either hedgehog or rodents
supports the African’ clade and contradicts insectivore monophyly. For the
A2AB tree, sequences with the suffix B are from the A2AB subfamily.
GuineaPigA and GuineaPigC sequences are from other subfamilies in the a-2
adrenergic receptor family and were used as outgroups. Bootstrap analyses used
full heuristic searches with 500 replications for parsimony and minimum
Table 2 Significance levels of T-PTP and KishinoHasegawa tests
Constraint Mitochondrial DNA vWF A2AB
T-PTP KH-P KH-L T-PTP KH-P KH-L T-PTP KH-P KH-L
Perissodactyls þ hyracoids 0.01 0.00110.0022 ,0.0001 0.00 ,0.0001 ,0.0001 MT MT MT
Insectivore monophyly 0.05 ,0.0001 0.0001 0.01 0.0311 0.0477 0.00 0.00020.0067 0.0001
...................................................................................................................................................................................................................................................................................................................................................................
In each case, trees with constraints were compared against either minimum length (T-PTP, KH-P) or highest likelihood (KH-L) trees. T-PTP tests were based on 100 permutations. KH-P,
Kishino–Hasegawa test with parsimony; KH-L, KishinoHasegawa test with maximum likelihood; MT, missing taxa.
Table 3 Divergence times (Myr) based on 12S rRNA transversions
Divergence event N Mean Standard
deviation
Standard
error
Among Paenungulates 3 54.8 4.2 2.4
Paenungulates to golden mole 3 67.1 8.7 5.0
Paenungulates to aardvark 3 74.0 12.0 6.9
Paenungulates to elephant shrew 3 79.9 9.9 5.7
African clade to other 13 orders 78 91.1 15.5 1.6
.............................................................................................................................................................................
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evolution and 100 replications for maximum likelihood. Shape parameters for
the gamma distribution were estimated from minimum length trees
26
and were
0.32 (mtDNA), 0.59 (vWF) and 0.52 (A2AB).
Divergence times. 12S rRNA transversions accumulated linearly as far back as
the eutherianmetatherian split
24
. Nine independent cladogenic events were
selected based on 12S rRNA sequence availability and paleostratigraphic
data
10,24,30
(for example, Rattus to Mus (14 Myr); Sus to Tayassu (45 Myr);
ruminants to Cetacea (60 Myr); Erinaceus to Metatheria (130 Myr)). Relative
rates were calculated in reference to xenarthrans. TamuraNei transversion
distances (transversions only) were adjusted for relative rate differences
30
against the xenarthran standard. Rate-adjusted estimates of sequence diver-
gence were regressed against paleostratigraphic divergence estimates for each of
the nine calibration points (origin forced through zero; r
2
¼ 0:97;
P ¼ 0:0000002). The resulting equation ðdivergence time ðin MyrÞ ¼ sequence
divergence=0:00063Þ was used to estimate interordinal divergence times after
making similar adjustments for relative rates. Additional details will be
presented elsewhere (M.S., manuscript in preparation).
Received 23 December 1996; accepted 18 April 1997.
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Hypothermia in foraging
king penguins
Y. Handrich*, R. M. Bevan
, J.-B. Charrassin*,
P. J. Butler
, K. Pu
¨
tz
, A. J. Woakes
,
J. Lage* & Y. Le Maho*
* Centre d’Ecologie et Physiologie Energe
´
tiques, Centre National de la Recherche
Scientifique, 23 rue Becquerel, 67087 Strasbourg cedex 2, France
School of Biological Sciences, University of Birmingham, Edgbaston,
Birmingham B15 2TT, UK
Abteilung Meereszoologie, Institut fu
¨
r Meereskunde, Du
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sternbrooker Weg 20,
D-24105 Kiel, Germany
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The ability to dive for long periods increases with body size
1
, but
relative to the best human divers, marine birds and mammals of
similar or even smaller size are outstanding performers. Most
trained human divers can reach a little over 100 m in a single-
breath dive lasting for 4 min (ref. 2), but king and emperor
penguins (weighing about 12 and 30 kg, respectively) can dive to
depths of 304 and 534 m for as long as 7.5 and 15.8 min, respec-
tively
35
. On the basis of their assumed metabolic rates, up to half
of the dive durations were believed to exceed the aerobic dive
limit, which is the time of submergence before all the oxygen
stored in the body has been used up
4,6,7
. But in penguins and many
diving mammals
7,8
, the short surface intervals between dives are
not consistent with the recovery times associated with a switch to
anaerobic metabolism
4
. We show here that the abdominal tem-
perature of king penguins may fall to as low as 11 8C during
sustained deep diving. As these temperatures may be 10 to 20 8C
below stomach temperature, cold ingested food cannot be the only
cause of abdominal cooling. Thus, the slower metabolism of
cooler tissues resulting from physiological adjustments associated
with diving per se, could at least partly explain why penguins and
possibly marine mammals can dive for such long durations.
King penguins are pelagic predators. To obtain food for their
chicks, the parents forage at sea up to the subantarctic or polar
frontal zones, 3001,000 km away from their breeding colony
9,10
.
They essentially rely on myctophid fish, of which most are captured
in daytime at 150300 m depths
11
. As sea temperatures there are
4 8C or lower, their stomachs are cooled by ingested prey
12,13
. In
freely foraging king penguins, which normally have a body tem-
perature of 38 8C on land, stomach temperatures as low as 19 8C
have been reported
11,14
. There is a 24 8C fall in body temperature
during free diving activity in seals
15,16
and birds
1719
and it has been
suggested that a slight reduction in body temperature during diving
might enhance aerobic diving time
6,15,17,18
. The cold food that
antarctic animals eat could contribute to this hypothermia
14,2022
,
or the aerobic dive limit (ADL) of penguins might be prolonged by a
process of temperature-induced metabolic suppression that is
independent of stomach cooling.
To investigate these possibilities, the separate influences of feed-
ing and diving on the abdominal temperatures of foraging animals
have to be determined. It is important to obtain simultaneous
measurements of the temperatures inside and outside the stomach
while the animals are freely diving, so that the extent of the
temperature changes in relation to diving and feeding activity
during the course of a foraging trip can be found. We therefore
implanted three data loggers into each of 12 free-ranging king
penguins (see Methods). The data loggers (Fig. 1) measured the
temperature of each bird at the top (T
abtop
) and bottom (T
abbot
) of
the abdomen, as well as inside the stomach (T
stom
). Hydrostatic
pressure was also recorded to monitor the diving behaviour. Both
the upper-abdominal and stomach loggers measured the full range
of temperatures; the lower-abdominal device recorded temperatures

Supplementary resources (19)

... These retroposons were then used for phylogenetic inferences. The results confirmed the results of previous molecular systematics studies that supported the monophyly of Afrotheria and Paenungulata (elephants, sirenians, and hyraxes) [76], with four and five retroposon insertions, respectively. We also characterized a retroposon insertion that supported the monophyly of aardvarks and African insectivores (tenrecs and golden of river dolphins is also demonstrated, with no inconsistency in SINE insertion patterns. ...
... Although the SINE method has been well credited after its success in the inference of cetacean phylogeny, the "wet" experiments faced technical difficulties with respect to elucidating the internal phylogeny of Afrotherian mammals. A molecular phylogenetic analysis that integrated multiple nuclear gene sequences revealed that mammals that are widely distributed in Africa (elephants, sirenians, hyraxes, aardvarks, tenrecs, golden moles, and elephant shrews) form a monophyletic group, which came to be called the Superorder "Afrotheria" [76]. However, the monophyly of Afrotheria was not accepted by most of the paleontological and anatomical studies [77]. ...
... These retroposons were then used for phylogenetic inferences. The results confirmed the results of previous molecular systematics studies that supported the monophyly of Afrotheria and Paenungulata (elephants, sirenians, and hyraxes) [76], with four and five retroposon insertions, respectively. We also characterized a retroposon insertion that supported the monophyly of aardvarks and African insectivores (tenrecs and golden moles) and a sister relationship with the elephant shrew, both of which were not evident based on previous molecular phylogenetic analyses ( Figure 5). ...
Article
Full-text available
Currently, the insertions of SINEs (and other retrotransposed elements) are regarded as one of the most reliable synapomorphies in molecular systematics. The methodological mainstream of molecular systematics is the calculation of nucleotide (or amino acid) sequence divergences under a suitable substitution model. In contrast, SINE insertion analysis does not require any complex model because SINE insertions are unidirectional and irreversible. This straightforward methodology was named the “SINE method,” which resolved various taxonomic issues that could not be settled by sequence comparison alone. The SINE method has challenged several traditional hypotheses proposed based on the fossil record and anatomy, prompting constructive discussions in the Evo/Devo era. Here, we review our pioneering SINE studies on salmon, cichlids, cetaceans, Afrotherian mammals, and birds. We emphasize the power of the SINE method in detecting incomplete lineage sorting by tracing the genealogy of specific genomic loci with minimal noise. Finally, in the context of the whole-genome era, we discuss how the SINE method can be applied to further our understanding of the tree of life.
... Cooper et al. 2014). More recently, Tethytheria and additional placental groups were recovered within the clade Afrotheria (Springer et al. 1997(Springer et al. , 2015Murphy et al. 2001aMurphy et al. , b, 2021, a group that includes Afrosoricida (e.g. tenrecs, golden moles), Macroscelidea (elephant shrews), Tubulidentata (aardvarks), Proboscidea (elephants), Sirenia, and Hyracoidea (hyraxes). ...
Chapter
Sirenians represent a striking group of quadruped mammals that are adapted to marine life. There are four extant species of sirenians (three sea cows and the dugong) but the fossil record, which extends from the early Eocene, shows a much richer diversity, and global distribution. Sirenians belong to the crown-group Sirenia and their closest extinct relatives belong to Pan-Sirenia. Sirenia is nested within Tethytheria, along with elephants and desmostylids, and Tethytheria belongs to the larger mammalian clade Afrotheria. The paleoneurology of Pan-Sirenia and Sirenia is based on anatomical descriptions of approximately two dozen natural and digital cranial endocasts and a couple of bony labyrinth endocasts. Sirenian brains are characterized by lissencephalic cerebral hemispheres, reduced olfactory system, reduction in the optic nerves, presence of a large trigeminal nerve and associated components, and thick meninges of the central nervous system. In contrast to other modern paenungulates, which include the gyrencephalic and large-brained elephants, sirenians have lissencephalic brains whose components are linearly arranged, and small relative brain sizes (EQs). Future work is needed to further incorporate the anatomical diversity of sirenian cranial endocasts into phylogenetic character matrices and to increase our knowledge about the inner ear evolution of the group.
... Boreoeutheria is polyphyletic with equally weighted characters and paraphyletic with implied weighting. These results are inconsistent with the evolutionary scenario proposed by the authors, which requires the assumption that Boreoeutheria and Afrotheria are natural groups, as supported by molecular evidence (e.g., Springer et al. 1997, Murphy et al. 2001Song et al. 2012). We therefore conducted a new analysis, using the same data matrix and searching options (implied weighting, k = 3) but forcing the monophyly of both Boreoeutheria and Afrotheria. ...
Article
Full-text available
The debate regarding the evolutionary relationships of the extinct South American native ungulates (SANUs) to the major placental clades Afrotheria and Boreoeutheria is exciting and has profound implications for our understanding of their early diversification and paleobiogeography. Although this controversy has not yet proven resolvable using morphological evidence, paleoproteomic and ancient DNA analyses support that at least some SANUs (i.e., Litopterna and Notoungulata) are members of Boreoeutheria, closely related to Perissodactyla (the Panperissodactyla hypothesis). Here we present a critical assessment of a recently published morphology-based study that claims that: (1) some SANUs (i.e., Notoungulata, Astrapotheria, Pyrotheria, and Xenungulata) represent a monophyletic supraordinal group, the Sudamericungulata, closely related to the Afrotherian hyracoids; and (2) the remaining SANUs (i.e., Litopterna and Didolodontidae, placed in a separate taxon, Panameridiungulata) are boreoeutherian in origin. Because this proposal (hereafter, the Sudamericungulata - Panameridiungulata or S-P hypothesis) is based on an incongruously reduced sample of boreoeutherians (including only a single perissodactyl) and inadequate character sampling restricted to dental and mandibular traits, it cannot be regarded as a satisfactory test of SANU relationships. Moreover, the S-P hypothesis fails to recover monophyletic Boreoeutheria and/or Afrotheria, making it incompatible with all well-established hypotheses of placental diversification. We find that the introduction of molecular constraints forcing the monophyly of Boreoeutheria and Afrotheria produces new trees, all recovering Sudamericungulata and Panameridiungulata nested within Boreoeutheria. These results are consistent with our analyses using a corrected version of the S-P matrix. Although we acknowledge that boreoeutherian affinities have still not been conclusively demonstrated for all nominal SANUs, it is beyond argument that any further credible testing must be based on much more exhaustive surveys than are currently available.
... The polyphyletic origins of Wagner's Insectivora were recognized by morphologists who removed menotyphlan insectivores from this group and placed them in the orders Dermoptera, Macroscelidea, and Scandentia [51,52]. However, morphologists continued to support the monophyly of Lipotyphla (solenodons, moles, shrews, hedgehogs, tenrecs, golden moles) [51,[53][54][55] until this group was shown to be polyphyletic based on molecular data and divided into Afrosoricida and Eulipotyphla [56][57][58][59]. Even with the general acceptance of lipotyphlan polyphyly, cladistic analyses of morphology-only data sets have continued to support the monophyly of this clade [31]. ...
Article
Full-text available
Pseudoextinction analyses, which simulate extinction in extant taxa, use molecular phylogenetics to assess the accuracy of morphological phylogenetics. Previous pseudoextinction analyses have shown a failure of morphological phylogenetics to place some individual placental orders in the correct superordinal clade. Recent work suggests that the inclusion of hypothetical ancestors of extant placental clades, estimated by ancestral state reconstructions of morphological characters, may increase the accuracy of morphological phylogenetic analyses. However, these studies reconstructed direct hypothetical ancestors for each extant taxon based on a well-corroborated molecular phylogeny, which is not possible for extinct taxa that lack molecular data. It remains to be determined if pseudoextinct taxa, and by proxy extinct taxa, can be accurately placed when their immediate hypothetical ancestors are unknown. To investigate this, we employed molecular scaffolds with the largest available morphological data set for placental mammals. Each placental order was sequentially treated as pseudoextinct by exempting it from the molecular scaffold and recoding soft morphological characters as missing for all its constituent species. For each pseudoextinct data set, we omitted the pseudoextinct taxon and performed a parsimony ancestral state reconstruction to obtain hypothetical predicted ancestors. Each pseudoextinct order was then evaluated in seven parsimony analyses that employed combinations of fossil taxa, hypothetical predicted ancestors, and a molecular scaffold. In treatments that included fossils, hypothetical predicted ancestors, and a molecular scaffold, only 8 of 19 pseudoextinct placental orders (42%) retained the same interordinal placement as on the molecular scaffold. In treatments that included hypothetical predicted ancestors but not fossils or a scaffold, only four placental orders (21%) were recovered in positions that are congruent with the scaffold. These results indicate that hypothetical predicted ancestors do not increase the accuracy of pseudoextinct taxon placement when the immediate hypothetical ancestor of the taxon is unknown. Hypothetical predicted ancestors are not a panacea for morphological phylogenetics.
... The silhouettes of mammals are out of scale. a molecular phylogenetic "revolution, " which started with the recognition of a lineage of African endemic mammals (Springer et al., 1997). Later, it was formally proposed as Afrotheria (Stanhope et al., 1998), breaking up the traditional Ungulata, since Afrotheria took four of their lineages (Proboscidea, Sirenia, Hyracoidea, and Tubulidentata; Springer et al., 2004). ...
Article
Full-text available
The South American native ungulates (SANUs) are usually overlooked in Eutherian phylogenetic studies. In the rare studies where they were included, the diversity of SANUs was underrated, keeping their evolutionary history poorly known. Some authors recognized the SANUs as a monophyletic lineage and formally named it Meridiungulata. Here, we recognized and defined a new supraordinal lineage of Eutheria, the Sudamericungulata, after performing morphological phylogenetic analyses including all lineages of SANUs and Eutheria. The SANUs resulted as non-monophyletic; thus, Meridiungulata is not a natural group; Litopterna and “Didolodontidae” are Panameriungulata and closer to Laurasiatheria than to other “Meridiungulata” (Astrapotheria, Notoungulata, Pyrotheria, and Xenungulata). The other “Meridiungulata” is grouped in the Sudamericungulata, as a new monophyletic lineage of Afrotheria Paenungulata, and shared a common ancestor with Hyracoidea. The divergence between the African and South American lineages is estimated to Early Paleocene, and their interrelationships support the Atlantogea biogeographic model. Shortly afterward, the Sudamericungulata explosively diversified in its four lineages. Confronting the Sudamericungulata evolutionary patterns and the Cenozoic natural events (such as tectonics and climatic and environmental changes, among others) helps to unveil a new chapter in the evolution of Gondwanan Eutheria, as well as the natural history of South America during the Cenozoic.
... Sengis or elephant-shrews (order Macroscelidea) are part of an ancient radiation of African mammals, the Afrotheria, which also includes elephants, sea cows, hyraxes, aardvark, golden moles, and tenrecs (Springer et al. 1997;Stanhope et al. 1998). The single extant family in this order, Macroscelididae, includes 20 recognized species in two sub-families: the soft-furred sengis (Macroscelidinae), with 15 species within four genera (Macroscelides, Elephantulus, Petrosaltator and Petrodromus), and the 'giant' sengis (Rhynchocyoninae) with a single genus (Rhynchocyon) and five species (Corbet & Hanks 1968;Rovero et al. 2008;Dumbacher et al. 2014Dumbacher et al. , 2016Carlen et al. 2017). ...
Article
A new subspecies of giant sengi or elephant-shrew, first documented in 2008, is described from northern coastal Kenya. All five currently described species and most known subspecies of Rhynchocyon are compared to this new lineage. Molecular analyses using mitochondrial and nuclear markers from the single DNA sample available for the new lineage show differences from other forms and reveal a close relationship with the allopatric golden-rumped sengi R. chrysopygus (0.43% divergence at the 12S mitochondrial locus). This level of 12S divergence is similar to that between other subspecies pairs within Rhynchocyon. Based on three voucher specimens and 843 images from camera traps, the new lineage is similar to R. chrysopygus in the rufous-maroon sides and shoulders but is distinguished by the lack of the golden rump, the presence of jet-black distal rump and thighs, dark dorsal line, and a pronounced nuchal crest of hairs. Though it also shows superficial pelage similarities to two Tanzania species, R. udzungwensis and the dark coastal form of R. cirnei macrurus, the new form has differences in pelage coloration that are clearly diagnosable from all other taxa. This new lineage has an allopatric distribution to all known Rhynchocyon taxa, with the closest congener being R. chrysopygus located 140 km apart. We estimate a potential range size for the new taxon of ~1980 km2 in the Boni and Dodori National Reserves with habitat consisting of mixed thickets and dry forests. Because of its close genetic relationship with R. chrysopygus, its allopatric distribution, and divergent coloration, the new subspecies is designated Rhynchocyon chrysopygus mandelai. The previously described populations of R. chrysopygus from southern coastal Kenya are now designated R. chrysopygus chrysopygus. As the current severe political insecurity in the area threatens the new taxon, we hope that its description will help establish immediate conservation priorities and action for the subspecies and its habitat.
Chapter
This second volume completes the unique survey of North American Tertiary mammals, and covers all the remaining taxa not contained in Volume 1. It provides a complete listing of mammalian diversity over time and space, and evaluates the effect of biogeography and climatic change on evolutionary patterns and faunal transitions, with the distribution in time and space of each taxon laid out in a standardized format. It contains six summary chapters that integrate systematic and biogeographic information for higher taxa, and provides a detailed account of the patterns of occurrence for different species at hundreds of different fossil localities, with the inclusion of many more localities than were contained in the first volume. With over thirty chapters, each written by leading authorities, and an addendum that updates the occurrence and systematics of all of the groups covered in Volume 1, this will be a valuable reference for paleontologists and zoologists.
Chapter
This second volume completes the unique survey of North American Tertiary mammals, and covers all the remaining taxa not contained in Volume 1. It provides a complete listing of mammalian diversity over time and space, and evaluates the effect of biogeography and climatic change on evolutionary patterns and faunal transitions, with the distribution in time and space of each taxon laid out in a standardized format. It contains six summary chapters that integrate systematic and biogeographic information for higher taxa, and provides a detailed account of the patterns of occurrence for different species at hundreds of different fossil localities, with the inclusion of many more localities than were contained in the first volume. With over thirty chapters, each written by leading authorities, and an addendum that updates the occurrence and systematics of all of the groups covered in Volume 1, this will be a valuable reference for paleontologists and zoologists.
Article
Elephants and sea cows and tenrecs; hyraxes and aardvarks and sengis and golden moles. What do these very divergent and different looking mammals have in common? They are each other’s closest living relatives, and all belong to the placental mammal clade Afrotheria (‘African beasts’), which is one of the four major clades of placental mammals along with Xenarthra (anteaters, sloths, armadillos), Euarchontoglires (e.g. rodents, rabbits, primates), and Laurasiatheria (e.g. bats, carnivorans, odd-toed and even-toed ungulates) (Figure 1). Unlike many animal groups that were recognized and named long ago based on anatomical features, the Afrotheria emerged as a natural clade only in the 1990s when molecular techniques were applied to the problem of placental mammal classification. The recognition of Afrotheria represents a triumph of molecular phylogenetics and brings together a fantastically diverse assemblage of placental mammals with widely disparate ecological and morphological adaptations. Although Afrotheria was not previously proposed based on studies of anatomical characters, additional support for the monophyly of this clade comes from geography and the fossil record. Specifically, the six extant orders in Afrotheria share with each other early fossil representatives that are known from Africa or along the margins of the ancient Tethys Sea, hence Afrotheria.
Article
The Afrotheria clade includes a large group of extant mammals, and the aardvark (Orycteropus afer) is the only representative of the order Tubulidentata in it. Here, we studied the morphological nature of the orbital region, eye tunics, upper and lower eyelids, superficial gland of the third eyelid, the third eyelid, deep gland of the third eyelid, and lacrimal gland in post‐mortem specimens obtained from three captive aardvarks, two young and one adult. The obtained samples were analyzed using macroscopic, histological, and histochemical methods. We observed choroidal tapetum lucidum fibrosum in all specimens, which was typical for aardvarks. The superficial gland of the third eyelid was a compound multilobar tubular branched gland of a mucous nature. The deep gland of the third eyelid produced a serous secretion. The seromucous secretion was typical for the lacrimal gland. We compared the morphological data of the O. afer skull with that from other endemic African mammals in the Afrotheria clade. We found that other authors provided different anatomical names for some bones and foramina located within the orbit. The types and function of eyelid glands, as well as eyeball glands of aardvarks, can primarily be connected with their habitat. Our study may constitute an introduction to the ontogenesis of individual eyeball glands in aardvarks. This article is protected by copyright. All rights reserved.
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Full-text available
RAPID shifts in climate during the last glacial are now well documented, particularly from the oxygen isotope records of the two Greenland ice cores GRIP1,2 and GISP23. In the GRIP record1,2 these climate events are also seen during the preceding (Eemian) interglacial which may be an analogue for the future climate, warmed by the greenhouse effect. But these shifts are not found in the Eemian section of the GISP2 core3, casting doubt on whether the rapid shifts in the GRIP oxygen isotope record really do represent a climate signal. Here we present magnetic susceptibility, pollen and organic carbon records from maar lake deposits in the Massif Central, France. These data provide an independent record of past climate and we find that they correlate well with the ice-core records during the last glacial. During the Eemian, two rapid cooling events seen in our record also correlate with those seen in the GRIP ice core, supporting the idea that rapid climate change did occur in the Eemian interglacial and demonstrating that it extended to continental Europe.
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Full-text available
A 5-yr simulation of the last glacial maximum using the UGAMP GCM is presented. It has a full seasonal cycle, T42 resolution, and interactive land surface and sea ice. Boundary conditions of SST, sea ice extent and land ice elevation are taken from the CLIMAP dataset and orbital parameters and carbon dioxide concentration are adjusted. It is compared with a 10-yr simulation of present-day climate using the same model.The results are analyzed in terms of processes leading to the maintenance of the atmospheric circulation and temperature structure, midlatitude transient behavior, precipitation, and eventually accumulation of ice over the glaciers. The model responds in a similar manner to previous studies in global mean statistics but differs in its treatment of regional climates. Changes in sea ice and orography are equally important in determining the positions of the upper-level jets. The Atlantic jet and storm track in particular are much stronger than in the present-day simulation, and the associated distribution of precipitation and snowfall changes accordingly. Both major ice sheets are maintained by snowfall at the center and ablation at the edges at a reasonable rate through the annual cycle.The results with a full seasonal cycle are compared to perpetual integrations by the authors and found to be very similar in most measures.
Chapter
The mammals seem ideally suited for taxonomy. As the eminent Theodore Gill wrote in 1873, “it takes no penetrating acumen to recognize man, the monkeys, the bats, the typical ruminants, and the typical cetaceans as distinct forms existent in nature” (Gill, 1873). This clarity of vision, however, does not extend to the question of relationships among the major mammalian groups. Although there is nearly unanimous agreement on the tripartite division of mammals into monotremes, marsupials, and eutherians, agreement generally stops at this point. The majority of living mammals, the eutherians or “placentals,” are often presented as a series of some 15 ordinal-level taxa without reference to a hierarchic classification. Similarly, the phylogenetic history of eutherians is commonly depicted as a bushlike radiation sprouting from mysterious roots at the end of the Mesozoic.
Article
The Age Calibration Program, CALIB, published in 1986 and amended in 1987 is here amended anew. The program is available on a floppy disk in this publication. The new calibration data set covers nearly 22 000 Cal yr (approx 18 400 14C yr) and represents a 6 yr timescale calibration effort by several laboratories. The data are described and the program outlined. -K.Clayton