Syst. Biol. 57(6):857–875, 2008
c Society of Systematic Biologists
Copyright ISSN: 1063-5157 print / 1076-836X online
DOI: 10.1080/10635150802559257
Phylogeny of the Beaked Whale Genus Mesoplodon (Ziphiidae: Cetacea) Revealed
by Nuclear Introns: Implications for the Evolution of Male Tusks
M EREL L. D ALEBOUT ,1 D EBBIE S TEEL,2,3 AND C. S COTT B AKER 2,3
1
School of Biological, Earth, and Environmental Sciences (BEES), University of New South Wales, Kensington, NSW 2052, Australia;
E-mail: [email protected] (M.L.D.)
2
School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New Zealand
3
Marine Mammal Institute and Department of Fisheries and Wildlife,
Oregon State University, 2030 SE Marine Science Drive, Newport, Oregon 97365, USA
Abstract.— With 14 species currently recognized, the beaked whale genus Mesoplodon (family Ziphiidae) is the most speciose
in the order Cetacea. Beaked whales are widely distributed but are rarely seen at sea due to their oceanic distribution,
deep-diving capacity, and apparent low abundance. Morphological differentiation among Mesoplodon species is relatively
limited, with the exception of tooth form in adult males. Based on scarring patterns, males appear to use their tusk-like
teeth as weapons in aggressive encounters with other males. Females are effectively toothless. We used sequences from
seven nuclear introns (3348 base pairs) to construct a robust and highly resolved phylogeny, which was then used as a
framework to test predictions from four hypotheses seeking to explain patterns of Mesoplodon tusk morphology and/or
the processes that have driven the diversification of this genus: (1) linear progression of tusk form; (2) allopatric speciation through isolation in adjacent deep-sea canyons; (3) sympatric speciation through sexual selection on tusks; and (4)
selection for species-recognition cues. Maximum-likelihood and Bayesian reconstructions confirmed the monophyly of the
genus and revealed that what were considered ancestral and derived tusk forms have in fact arisen independently on several occasions, contrary to predictions from the linear-progression hypothesis. Further, none of the three well-supported
species clades was confined to a single ocean basin, as might have been expected from the deep-sea canyon-isolation or
sexual-selection hypotheses, and some species with similar tusks have overlapping distributions, contrary to predictions
from the species-recognition hypothesis. However, the divergent tusk forms and sympatric distributions of three of the four
sister-species pairs identified suggest that sexual selection on male tusks has likely played an important role in this unique
radiation, although other forces are clearly also involved. To our knowledge, this is the first time that sexual selection has
been explicitly implicated in the radiation of a mammalian group outside terrestrial ungulates. [Cetacean; nuclear introns;
phylogeny; sexual selection; teeth; weapons.]
Evolutionary radiations involving ornaments or displays have been documented in a wide range of organisms, including Hawaiian Drosophila flies (Kaneshiro,
1983), African Great Lake cichlids (Seehausen and van
Alphen, 1999), and passerine birds (West-Eberhard,
1983). Radiations based on weapons of male-male competition are less common but also occur, though reasons why such characters might diverge in form are far
less clear (Emlen et al., 2005). Examples of radiations
of weaponry include the antlers and horns of ungulates
(Geist, 1978; Lundrigan, 1996), the claws of amphipods
and isopods (Shuster and Wade, 2003), the tusks of frogs
(Shine, 1979), and the horns of dung and rhinoceros
beetles (Eberhard, 1980; Emlen et al., 2005). In many
species, secondary sexual characters can also fulfill dual
functions (Berglund et al., 1996), as weapons in malemale competition (intra-sexual selection) and as cues for
female choice (inter-sexual selection) or species recognition (see also below). Such traits often arise through
male-male competition and serve as honest signals to
other males regarding fighting ability or dominance.
These traits may then be co-opted by females as indicators of male phenotypic quality when selecting a mate.
Conversely, males may use information from traits that
initially evolved through female choice (Berglund et al.,
1996).
With 21 species described to date, the Ziphiidae
(beaked whales) are the most speciose family in the order Cetacea after the Delphinidae (oceanic dolphins), yet
they are among the least known of mammalian groups
(Wilson, 1992). Beaked whales are deep-diving odontocetes (toothed whales) that live in the offshore waters
of all the world’s oceans except the highest latitudes of
the Arctic. They are rarely seen at sea due to their elusive habits, long dive capacity, and, for some species,
probable low abundance (Reeves et al., 2002). Most information has come from beachcast or stranded animals,
and several species are known from only a handful of
specimens.
The majority of species in this family comprise the
genus Mesoplodon (n = 14); the other five recognized
genera are monotypic or consist of antitropical species
pairs. Mesoplodon beaked whales are relatively similar
in overall appearance but differ dramatically from one
another in their tooth morphology (Mead, 1989). These
whales possess only a single pair of teeth, which vary by
species in their shape, size, and position in the lower
jaw. The tusk-like teeth develop only in adult males
and protrude outside the mouth when the jaw is closed
(Fig. 1). In females, the teeth do not develop and remain
hidden in the gum tissues, so that the animals are effectively toothless. Examination of stomach contents indicates that these whales feed primarily on deep-water
squid. The teeth do not appear to be used for feeding,
and the small amount of evidence gathered to date suggests that there is little difference in diet between males
and females (Sekiguchi et al., 1996). Instead, analysis of
scarring patterns suggests that males use their tusks as
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FIGURE 1. Adult male Gray’s beaked whales, Mesoplodon grayi, stranded in New Zealand showing distinctive tusk-like teeth and linear scars
likely caused by tooth rakes received in aggressive encounters with other males. Photocredits: G. Lento (upper), A. Glaser (lower).
weapons in intra-sexual combat, presumably to obtain
reproductive access to females (Heyning, 1984). Several
species of Mesoplodon are found in each ocean basin. On
a broad scale, these species overlap in distribution (geographic sympatry) but may be ecologically parapatric
due to differences in preferred prey (niche partitioning).
Four hypotheses have been put forward to explain
patterns of Mesoplodon tusk morphology and/or the
processes that have driven the diversification of this
genus. After first clarifying the taxonomic status of many
ziphiids (Moore, 1957, 1960, 1963, 1966), Moore (1968)
proposed a linear progression of phenetic relationships
among Mesoplodon species based primarily on the position and angle of inclination of the male tusks (Fig. 2).
In other ziphiid genera, the tusks or largest pair of
mandibular teeth are conical and occur at the apex of
the lower jaw. Moore (1968) considered Mesoplodon to
be the most derived of the extant genera, and argued
that Mesoplodon species with apical, forward-inclined
tusks were “primitive,” whereas those with backwardsinclined tusks set back from the apex of the mandible
were more derived. This hypothesis provides a clear
framework for the expected phylogenetic relationships
among the species but makes no prediction regarding
patterns of geographic distribution and provides no
mechanism to explain the process by which speciation
occurred.
The second hypothesis seeks to explain the overall
morphological similarity of beaked whales and suggests
that speciation was driven by population isolation in
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DALEBOUT ET AL.—TUSK EVOLUTION IN BEAKED WHALES
FIGURE 2. Adult male Mesoplodon beaked whale tusk morphology
(lateral views of lower jaws), arranged in a linear progression from
ancestral to derived, as perceived by Moore (1968) based on a combination of tusk position, size, and angle of inclination (hypothesis
H1-A). Other beaked whale genera have forwardly inclined tusks at
the apex of the lower jaw. Although the tusks of mature males are,
in general, accurately portrayed in these images, the potential for and
degree of intraspecific variation that may occur in these characters has
not been shown. Note that tusk coding options (Fig. 3, Table 3) were
based on quantitative data from the literature and not reliant on the
images shown here. Jaw images are labeled with three- or four-letter
species codes, scientific names, and common names. Asterisks highlight species discovered since 1968. For M. peruvianus, the circle highlights the position of the small tooth. M. traversii, a species with teeth
similar to those of M. layardii (van Helden et al. 2002), but not included
in this genetic study, is not shown.
859
deep-sea canyons (Carwardine, 1995). Beaked whales
rarely venture into shallow waters and most sightings
occur beyond the edge of the continental shelf, often associated with submarine canyons and seamounts (Barlow
et al., 2006; MacLeod et al., 2006). Therefore, populations
in different canyon systems may be largely isolated from
one another, yet would evolve in parallel to adapt to similar conditions. Under this form of allopatric speciation,
species in adjacent deep-water regions within an ocean
basin would be expected to be more closely related to
one another than to species in other ocean basins. However, the canyon-isolation hypothesis makes no predictions about tusk morphology.
The third hypothesis proposes that sexual selection
may have been an important driver of speciation and
diversification in this genus (Dalebout, 2002). This
idea is supported by the strong sexual dimorphism in
Mesoplodon tooth morphology and its presumed role
in intra-sexual competition (Heyning, 1984). Under the
sexual-selection hypothesis, directional or disruptive
selection on tooth morphology could lead to sympatric
speciation. This predicts that groups of related species
that differ in tusk morphology would co-occur in the
same ocean basin and, specifically, that sister-species
with similar distributions are likely to have highly
divergent tooth forms.
The fourth hypothesis suggests that the variation observed in the position and shape of the tusks could function as species recognition cues and therefore as a precopulatory isolating mechanism (MacLeod, 2000). Although
this hypothesis does not address the process by which
speciation initially occurred, it predicts that divergent
tooth morphologies would arise through directional selection and character displacement in areas of secondary
contact between species. This process would therefore
also result in divergent tooth morphology among species
with overlapping distributions.
Testing the predictions of these hypotheses requires a
robust phylogeny of Mesoplodon species. However, since
Moore’s (1968) pioneering morphological work, there
has been little further investigation of beaked whale
evolutionary relationships. Several large-scale studies of
cetacean phylogeny have included a handful of ziphiids
but revealed little about relationships within this family
(Arnason and Gullberg, 1996; Messenger and McGuire,
1998; Cassens et al., 2000; May-Collado and Agnarsson,
2006). All 21 known ziphiid species were recently confirmed to be genetically distinct based on mitochondrial
(mt) DNA control region and cytochrome b sequences
(Dalebout et al., 2004). To determine whether patterns
of species distinctiveness were reflected in the nuclear
genome as well, Dalebout et al. (2004) also compiled a
suite of actin intron sequences. Although higher-level
relationships were not well-resolved by the rapidly
evolving mtDNA markers due to phylogenetic noise and
saturation (see also Dalebout et al., 2002, 2003), preliminary analysis of the intron sequences indicated that a
multiple nuclear gene approach should produce a robust and highly resolved phylogeny for this remarkable
genus.
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SYSTEMATIC BIOLOGY
Here we use partial sequences from seven nuclear introns (3348 base pairs) to construct such a phylogeny
for the majority of Mesoplodon beaked whales. The resulting nuclear phylogeny was used as a framework
within which to test predictions from the four hypotheses
of speciation and tusk evolution (Fig. 3): the linearprogression hypothesis (H1) predicts that tusk morphology will follow a trend from ancestral to more derived
forms; both the deep-sea canyon-isolation (H2) and the
sexual-selection hypotheses (H3) predict that clades of
related species will occur in the same ocean basin; and
both H3 and the species-recognition hypothesis (H4)
predict that species with overlapping or adjacent distributions will have divergent tusk forms. However, H3
predicts that tusk divergence will be most pronounced
in sister-species pairs (sympatric speciation), whereas
for H4, the species involved need not necessarily be so
closely related (i.e., secondary contact).
M ATERIALS AND M ETHODS
DNA Extraction, Amplification, and Sequencing
We sampled 13 of the 14 known Mesoplodon species
and two confamilial outgroups (Ziphius cavirostris and
Tasmacetus shepherdi). Soft tissue samples were obtained
from dead, stranded animals or victims of incidental
fisheries takes (bycatch) and preserved in 70% ethanol
or 20% salt-saturated dimethyl sulphoxide (DMSO)
and stored at 4◦ C or −20◦ C prior to genetic analysis.
The missing species, M. traversii, is currently known
only from fragmentary skeletal material (van Helden
et al., 2002), which is unsuitable for amplification of
nuclear introns. DNA was extracted using standard
phenol:chloroform methods (Sambrook et al., 1989),
as modified for small samples by Baker et al. (1994).
The polymerase chain reaction (PCR) was used to amplify partial introns from seven nuclear genes: biglycan (BGN), 706 base pairs (bp); catalase (CAT), 559 bp;
rhodopsin (RHO), 166 bp; cytotoxic T-lymphocyteassociated serine esterase 3 (CTLA3), 305 bp; cholinergic receptor–nicotinic, alpha polypeptide 1 (CHRNA1),
366 bp; muscle actin (ACT), 925 bp; and major histocompatibility complex class II (DQA), 456 bp. Each of the
seven genes are found on a different chromosome in humans (Lyons et al., 1997) and are assumed to be unlinked
and independent in cetaceans. As the vast majority of
genes are unlinked (e.g., Turelli, 1984), we considered
this a reasonable assumption. See Table 1 for primer and
PCR information. PCR products were sequenced on an
ABI 377, modified ABI 373, or ABI 3700 automated sequencer (Applied Biosystems, Inc.) using BigDye Dye
Terminator Chemistry. Fragments were sequenced at
least twice in both directions for confirmation in the majority of cases. Sequences were aligned and edited manually using the program SEQUENCHER ver. 4.0 (Gene
Codes Corporation, Inc.). Alignment of intron sequences
was generally straightforward as relatively few insertions and deletions appear to have occurred since their
divergence from common ancestral sequences. Gen-
VOL. 57
Bank accession numbers for all sequences are listed in
Table 2.
Phylogenetic Analyses
Files for each of the seven introns were concatenated
to form a combined data set (COMBO, 3348 bp) using
MacClade ver. 4.07 (Maddison and Maddison, 2005). We
attempted to use the same set of individuals to generate
all sequences, but amplification problems with poorquality DNA from decomposing stranded specimens required us to create chimeric sequences in some cases
(see Appendix 1). Data on variable sites, shared-derived
(phylogenetically informative [PI]) sites, estimates of
transition/transversion ratio, and the mean divergence
among ingroup taxa for each gene were obtained using
MEGA3 (Kumar et al., 2004).
Phylogenetic analysis of individual introns and the
COMBO data set was performed using maximum
parsimony (MP), minimum evolution (ME; neighbor
joining), and maximum-likelihood (ML) methods as implemented in PAUP* 4.0b10 (Swofford 2003). To test for
conflicting signal among gene segments, an initial evaluation of the individual introns was performed with a
bootstrap support/conflict criterion of 90% (de Queiroz,
1993; Teeling et al., 2005). MP-based pairwise partition
homogeneity tests (Farris et al., 1995) with 1000 replicates were also performed. MP analyses of the COMBO
data set were conducted using random addition of taxa,
tree-bisection reconnection branch swapping, without
considering insertion-deletions (indels) as fifth characters, and a limit of 1,000,000 rearrangements. For ME
and ML analyses, the Akaike information criterion (AIC)
(Akaike, 1973; Posada and Buckley, 2004) was used to
select a K81uf+I+G model with estimated proportion of
invariable sites (Pinvar, I) = 0.7368 and gamma (G)-shape
parameter for distribution of rates (alpha) = 0.9307, using
ModelTest Online ver. 3.8 (Posada and Crandall, 1998;
Posada, 2006). For comparison, additional analyses were
run using a Bayesian information criterion (BIC)-selected
model (HKY+I [Pinvar, I = 0.8449]). For ML, starting
trees were obtained via neighbor joining. The reliability
of nodes was assessed using 500 full heuristic (MP, ML)
or 1000 neighbor-joining (ME), non-parametric bootstrap
replicates. Clades with bootstrap values ≥70% were considered robust.
Bayesian (BAY) analyses of the COMBO data set
were performed using MrBayes ver. 3.1.2 (Huelsenbeck
and Ronquist, 2001; Ronquist and Huelsenbeck, 2003).
Analyses were conducted using uniform priors, random starting trees, no phylogenetic constraints, and
four simultaneous Markov chains run for 10,000,000
generations, with trees sampled every 100 generations
and the first 250,000 generations discarded as burn-in.
The ML model for BAY analyses used two substitution
types, with rate variation across sites estimated using the
“invgamma” option, such that a proportion of the sites
is invariable (Pinvar), whereas the rate for the remaining
sites (alpha) is drawn from a gamma distribution. Each
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DALEBOUT ET AL.—TUSK EVOLUTION IN BEAKED WHALES
861
FIGURE 3. Predictions from the four hypotheses: H1, linear progression of tusk morphology; H2, deep-sea canyon isolation; H3, sexual
selection; and H4, species recognition. See text for discussion. For H1, the column highlighted in gray (A) represents the linear progression in
tusk form proposed by Moore (1968) based on a combination of tusk position, size, and angle of inclination in the jaw as shown in Figure 2.
See Table 3 for details of this and other (B through J) tusk coding options. The H1 table and terminal nodes on the H2 tree are labeled with
species codes as per Figure 2. For H2 and H3, shaded boxes and circles indicate species’ distributions: North Atlantic, white; North Pacific, gray;
Southern Hemisphere, hatched. For species found in more than one ocean basin, the main center of distribution was used, such that all species,
except M. densirostris (found in all oceans), could be assigned to a specific ocean-basin clade (i.e., equivalent to the H2+H3 “relaxed” option in
Table 5).
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SYSTEMATIC BIOLOGY
TABLE 1. Primers used for amplification of nuclear introns in beaked whales. All PCR reactions used a final concentration of 2.5 mM Mg2+ .
Tm, annealing temperature in ◦ C.
Primer name
Sequence
Primer source
Tm
BGN-F
BGN-R
5 -CTCCAAGAACCACCTGGTG-3
5 -TTCAAAGCCACTGTTCTCCAG-3
Lyons et al. (1997)
Lyons et al. (1997)
62
CAT-F
CAT-R
RHO-F
RHO-R
5 -AAAGACTGACCAGGGCATCA-3
5 -AGGGTAGTCCTTGTGAGGCC-3
5 -AGGGGAGGTCACTTTATAAGGG-3
5 -CCAGCATGGAGAACTGCC-3
5 -AAGAATTTCCCTATCCATGCTATG-3
5 -GGTTCCTGGTTTCACATCATC-3
5 -GACCATGAAGTCAGACCAGGAG-3
5 -GGAGTATGTGGTCCATCACCAT-3
Lyons et al. (1997)
Lyons et al. (1997)
55
Lyons et al. (1997)
Lyons et al. (1997)
Lyons et al. (1997)
Lyons et al. (1997)
Lyons et al. (1997)
Lyons et al. (1997)
55
5 -GGTTATCTGATGTATTCC-3
5 -CTTGTGAACTGATTACAGTCC-3
5 -CCACTACTTTAGGCAG-3
5 -TGTAAAACGACGGCCAGTCTGCCTAAAGTAGTGG-3
5 -CCGGATCCCAGTACACCCATGAATTTGATGG-3
5 -CCGGATCCCCAGTGCTCCACCTTGCAGTC-3
Palumbi and Baker (1994)
Palumbi and Baker (1994)
Palumbi and Baker, unpublished
Palumbi and Baker, unpublished
Auffray et al. (1987)
Auffray et al. (1987)
50
CTLA3-F
CTLA3-R
CHRNA1-F
CHRNA1-R
ACT3-Fa
ACT1385-Ra
ACT5-Fa
M13-ACT5-Ra
DQA1-F
DQA2-R
50
55
54
a
See Dalebout et al. (2004) for ACT primer map. ACT5-F and M13-ACT5-R are internal primers within the large fragment amplified by ACT3-F and ACT1385-R
and were used for sequencing only.
BAY run was replicated to ensure a convergence of results. Assessment of convergence was based on several
diagnostics: the average standard deviation of split frequencies (less than 0.002 at the end of a run), a plot of
generation versus log-likelihood scores (at convergence,
different independent runs are expected to sample similar likelihood values resulting in a “white noise” plot),
and all PSRF (potential scale reduction factor) scores are
equal to 1.000 (Ronquist et al., 2005). An extra-long run
(25,000,000 generations) was also conducted to ensure
that a robust convergence had been reached. Clades with
posterior probabilities of ≥0.95 were considered robust
(Rannala and Yang, 1996).
To test whether the strength of inferences of relationships among ingroup taxa was influenced by choice of
outgroups, COMBO analyses were repeated using only
one of the two available outgroups and the resulting
topologies compared. For the same purpose, an additional set of analyses (MP, ME, NJ, and BAY) was conducted using a reduced combined data set, including six
of the seven introns (3084 bp; missing CTLA3) and a third
confamilial outgroup (Hyperoodon planifrons).
Testing Alternative Hypotheses
To test predictions from the four hypotheses, tusk
forms were sorted into categories following the linear
progression proposed by Moore (1968) based on a combination of tusk position, size, and angle of inclination
(Figs. 2 and 3, H1-A), where 1 = apical; 2 = larger tusks
set some way back from apex; 3 = massive triangular tusks in middle of jaw; 4 = tusks in middle of jaw
with strong backwards inclination; and 5 = tusks raised
up on prominent arch with a forwards inclination. To
test the sensitivity of these categories, nine other coding schemes (H1-B to H1-J) based on various tusk characters assumed to be more independent (e.g., position,
size, shape, angle of inclination, on arch or not) were
also assessed (Table 3, Fig. 3). Predictions from hypotheses H1 to H3 were compared statistically under ML to
TABLE 2. The seven nuclear introns analysed for this study. The number of base pairs (bp) analyzed for each gene segment, GenBank accession
numbers, the number of variable and phylogenetically informative (PI) sites among all Mesoplodon species and among Mesoplodon and outgroup
species (n = 2), the mean pairwise genetic distances (Tamura 3-parameter model, gamma rates [alpha = 1.0]) with standard errors (SE) among
Mesoplodon species, and transition/transversion ratios (Ti/Tv) are shown.
Gene
BGN
CAT
RHO
CTLA3
CHRNA1
ACT
DQA
COMBO
Number bp
analyzed
GenBank accession
numbers
671
516
166
264
350
925
456
3348
EU447744–EU447758
EU447759–EU447773
EU476106–EU476120
EU476121–EU476135
EU476136–EU476150
EU476151–EU476165
EU476166–EU476180
No. variable sites
Mesoplodon/all
taxa
No. PI sites
Mesoplodon/all taxa
Mean pairwise
distance (SE)
Mesoplodon
Mean
Ti/Tv(SE)
Mesoplodon
27/36
10/12
4/8
10/20
8/16
37/44
18/25
114/161
6/11
3/4
0/3
4/8
0/1
5/9
9/9
27/45
0.009 (0.002)
0.004 (0.001)
0.009 (0.002)
0.008 (0.003)
0.003 (0.001)
0.008 (0.002)
0.008 (0.002)
0.007 (0.001)
2.4 (0.77)
1.1 (0.53)
0.3 (0.15)
1.0 (0.63)
0.2 (0.40)
3.4 (0.91)
2.7 (1.02)
2.0 (0.60)
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DALEBOUT ET AL.—TUSK EVOLUTION IN BEAKED WHALES
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TABLE 3. Details of Mesoplodon tusk coding options.
H1-A
H1-B
H1-C
H1-D
Linear progression
in tusk form based
on combination of
tusk position, size,
and angle of
inclination in jaw
(Moore 1968)
Tusk position—as
qualitative measurea
Tusk position—in
relation to
mandibular
symphysisb
Tusk position—as
quantitative
measurec
H1-E
Tusk size
H1-F
Tusk lengthb,d
H1-G
Tusk widthb,d
H1-H
Tusk shape
H1-I
Tusk inclination
H1-J
Tusk raised up on prominent arch
1 = apical
2 = larger tusks set some way back from apex
3 = massive triangular tusks in middle of jaw
4 = tusks in middle of jaw with strong backwards inclination
5 = tusks raised up on prominent arch and angled forwards
1 = apical
2 = intermediate distance
3 = furthest back
1 = apical
2 = between apex and posterior end of symphysis
3 = overlapping with posterior end of symphysis
4 = posterior to mandibular symphysis
1 = apical
2 = approx. 100 mm back
3 = approx. 200 mm back
4 = approx. 300 mm back
1 = small
2 = medium
3 = massive
4 = straplike
1 = less than 100 mm
2 = 100–200 mm
3 = greater than 200 mm
1 = less than 50 mm
2 = greater than 60 mm
3 = greater than 70 mm
4 = greater than 100 mm
1 = approx. conical
2 = flattened, triangular, small
3 = flattened, triangular, large
4 = straplike
1 = anterior
2 = vertical
3 = mild posterior
4 = strong posterior
1 = yes
2 = no
a
Data from Moore (1968).
Data from Mead (1989).
Data from Carwardine (1995).
d
Data from Dalebout et al. (2002).
b
c
the best phylogenetic tree using approximately unbiased
tests (AU; Shimodaira, 2002) and Shimodaira-Hasegawa
tests (SH; Shimodaira and Hasegawa, 1999), as implemented in the program CONSEL ver. 0.1i (Shimodaira
and Hasegawa, 2001). Both these tests are appropriate
for comparing both a priori and a posteriori phylogenetic
hypotheses, unlike the Kishino and Hasegawa (1989)
test. The SH test may, however, be overly conservative because the number of trees included in the confidence set
increases as the number of trees being considered increases (Strimmer and Rambaut, 2002). The AU test uses
a multi-scale bootstrap technique to remove this bias and
has been recommended for general tree selection problems (Shimodaira, 2002). Predictions from hypotheses
H3 and H4 were assessed using ML reconstructions of
ancestral states (distribution, tusk form) as implemented
in the program MESQUITE (Maddison and Maddison,
2006). We also considered using the program BayesTraits
Multistate (Pagel and Meade, 2006), but unfortunately
this application is unable to deal with polytomies. A single outgroup (Ziphius cavirostris) was used for these and
subsequent analyses (see below).
Estimation of Divergence Dates
A likelihood-ratio test was performed using PAUP* to
assess if substitution rates could be modeled as clocklike. Based on these results, PAML ver. 3.14 (Yang, 1997)
and ESTBRANCHES (Thorne et al., 1998; Kishino et al.,
2001) were used to estimate branch lengths for the
COMBO data set ML topology, using a F84+G model
with five rate categories, following the recommendations
of Rutschmann (2005). The likelihood scores obtained
were compared to check convergence. Divergence times
were then estimated using MultiDivTime (Thorne et al.,
1998), a Bayesian approach that does not assume a strict
clock and can incorporate user-provided constraints.
There are only a limited number of fossil calibration
points for beaked whales. The family arose in the early
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Miocene (∼24 million years ago [Ma]), reached the height
of its morphological diversity in the mid-Miocene, and
remained well represented in late Miocene (7 to 10 Ma;
Barnes et al., 1985; Mead, 1989). Unfortunately, the majority of ziphiid fossils lack the diagnostic characters required for attribution to extant lineages, and the few
that do possess such features have generally been obtained from geological strata that cannot be dated (e.g.,
Owen, 1870; Kellogg, 1928a, 1928b). As a result, the origin of the modern genera remains in doubt (Mead, 1989;
Fordyce, 2002). However, an estimate of 24 ± 5 Ma for
the divergence of Ziphius and Mesoplodon was provided
by a molecular investigation of phylogenetic relationships among ancient cetacean lineages (Cassens et al.,
2000—as inferred from Fig. 2; a multi-gene phylogeny
calibrated using fossil dates for the origin of the modern family Delphinidae, 11 to 13 Ma). Further, a number of specimens attributable to the Ziphius lineage have
recently been described from late Miocene deposits (approximately 10 Ma; Lambert, 2005).
We therefore explored divergence dates obtained from
several combinations of parameters that constrained
the origin of the genus Mesoplodon to 30 Ma (option A),
20 Ma (option B), and 10 Ma (option C). Two versions
of each option were run: the first using only an upper
bound (maximum age; 30, 20, and 10 Ma, respectively),
and the second using both an upper and lower bound
(±5 Ma around maximum ages used for the first).
Following recommendations in Thorne’s readme file
(http://statgen.ncsu.edu/thorne/multidivtime.html),
and using 10 Ma as one time unit, values used for
the a priori number of expected time units between
tip and root (ingroup depth; rttm), the mean of prior
distribution for rate at root node (rtrate), and the prior
for the Brownian motion parameter (nu) were as follows:
(A) 3.0, 0.001, 0.3; (B) 2.0, 0.001, 0.5; and, (C) 1.0, 0.002,
1.0. Bigtime was set to 50 Ma. After a burn-in of 100,000
generations, 1,000,000 generations of Markov chains
were sampled every 100 generations. Posteriors for each
option were computed twice (using different random
starting points) to check convergence of results.
R ESULTS
Variation in Phylogenetic Signal among Introns
The seven introns differed in their contribution to the
phylogenetic signal, as reflected in the number of sharedderived (phylogenetically informative, PI) sites (Table 2),
ranging from 0 sites (RHO and CHRNA1) to 9 sites
(DQA), with a total of 27 PI sites for the COMBO data
set. The amount of phylogenetic signal had some correlation with segment length (bp), with longer introns
generally contributing more PI sites. Pairwise genetic
distances among Mesoplodon species also varied by intron segment, suggesting some differences in the rate of
accumulation of mutations among loci. There was little resolution of relationships in the individual intron
analyses (see Appendix 2). Of the few strongly supported nodes, only one was not observed in subsequent
COMBO reconstructions (BGN, 85% bootstrap support).
VOL. 57
Partition homogeneity tests revealed low-level conflict
(P = 0.03–0.05) in phylogenetic signal between BGN and
three other introns (CTLA3, ACT, and DQA), as well as
between CTLA3 and ACT and between ACT and DQA.
Serial removal and replacement of single species from the
analyses did not affect these results, suggesting that the
conflict was locus- rather than taxon-specific. However,
none of the pairwise tests were significant after Bonferroni corrections for multiple comparisons. This overall
lack of conflict among individual introns also provides
some support for our assumption that these genes are
unlinked and independent in cetaceans.
Phylogenetic Reconstruction with Combined
Intron Data Set
In contrast to the individual intron analyses, the
COMBO data set yielded a robust, highly resolved phylogeny. Three main clades were strongly supported by
bootstrap scores (BS) and/or Bayesian posterior probabilities (BPP; Fig. 4). The same clades with similar
levels of high support were obtained when BGN was
excluded and with different combinations of outgroups.
Further support for the phylogeny was provided by
lineage-specific, shared-derived nucleotide substitutions
and deletions (synapomorphies; Table 4).
The radiation of genus Mesoplodon appears to have
begun with the divergence of the lineage leading to
Sowerby’s beaked whale, M. bidens. This was followed
by several rapid divergence events resulting in the straptoothed whale clade (M. layardii, M. bowdoini, and M.
carlhubbsi; BS MP 61/ME 73/ML 68, BPP 0.99), the Perrin’s beaked whale clade (M. hectori, M. peruvianus, M.
perrini, M. grayi, M. stejnegeri, and M. densirostris; BS
60/59/60, BPP 0.99), and the True’s beaked whale clade
(M. ginkgodens, M. mirus, and M. europaeus; BS 90/93/87,
BPP 1.00). Within the straptoothed whale clade, M. carlhubbsi and M. bowdoini were identified as likely sister
species, though this node received somewhat lower support (BS < 50/69/< 50, BPP 0.83). Within the Perrin’s
beaked whale clade, M. stejnegeri and M. densirostris and
M. peruvianus and M. perrini were identified as sister
species (BS 74/79/69, BPP 0.97, and BS 96/95/93, BPP
1.00), and within the True’s beaked whale clade, M. mirus
and M. europaeus were identified as sister species (BS
99/100/97, BPP 1.00).
Alternative Hypotheses of Evolution
AU and SH tests revealed that alternative hypotheses of relationships among Mesoplodon species predicted
from H1 to H3 were significantly less likely than the best
ML tree (P < 0.001; Table 5). Instead of following a linear progression, tusk form appears to be highly plastic,
and forms considered to be ancestral or derived under
the scheme proposed by Moore (1968) appear to have
evolved independently on a number of occasions. Similarity in tusk morphology was generally not a good indicator of relatedness, and most sister species possessed
divergent tusk forms (e.g., M. perrini and M. peruvianus).
2008
DALEBOUT ET AL.—TUSK EVOLUTION IN BEAKED WHALES
FIGURE 4. Phylogenetic relationships among Mesoplodon beaked
whale species reconstructed using maximum likelihood and an AICselected model (−ln L = 6055.03782). The same robust topology was
obtained from analyses using a BIC-selected model. Bootstrap scores
≥50% are shown above or alongside internal nodes (MP/ME/ML), and
Bayesian posterior probabilities ≥0.80 are shown below. Node E was
collapsed into a polytomy by MP, ME, and ML bootstrap analyses (i.e.,
bootstrap scores <50%) but was strongly supported by BAY analysis
(0.99). See Table 4 for distribution of shared-derived sites supporting
these nodes. <, less than 50% bootstrap score.
Further, none of the three main clades was confined to
a single ocean basin, as might be expected from H2 and
H3 (Fig. 5).
Reconstruction of ancestral states confirmed the high
plasticity of tusk morphology with all five tusk forms under H1-A estimated to be approximately equally likely
at all internal nodes (Fig. 6a, right). Similar plasticity
was observed in assessments of more independent features of tusk morphology (Fig. 6b, H1-B to H1-J). In only
one case was a specific tusk character state found to be
diagnostic for a particular clade; only members of the
straptoothed whale clade, together with the ancestral lineage M. bidens, have tusks that overlap with the posterior
end of the mandibular symphysis (H1-C, state 3). Better
resolution was obtained from the ancestral area analysis
865
(Fig. 6a, left): the straptoothed whale clade most likely
arose in the Southern Hemisphere before dispersing into
the North Pacific; the Perrin’s beaked whale clade most
likely arose in the Southern Hemisphere before dispersing into the North Pacific and beyond; and the True’s
beaked whale clade most likely arose in the North Pacific
before dispersing into the North Atlantic. It should be
recognized, however, that the ML model implemented in
MESQUITE is quite simple and, as such, caution should
be exercised in the interpretation of the estimated probabilities of these ancestral states.
Although predictions from H4 do hold in the North
Atlantic for at least some tusk coding options, this was
not the case for other ocean basins where a greater variety of species co-occur (Table 6). For example, under H1A, two pairs of species have similar tusks in the North
Pacific (state 3—M. stejnegeri, M. carlhubbsi; state 5—
M. densirostris, M. peruvianus), whereas in the Southern
Hemisphere, three pairs of species have similar tusks
(state 1—M. mirus, M. hectori; state 2—M. grayi, M. ginkgodens; state 5—M. densirostris, M. peruvianus). A similar
pattern was found with other tusk coding options—
namely, that species with tusks that are similar based
on some measures, though they may differ based on
other measures, do in fact have overlapping distributions in many cases. This finding also broadly contradicts
predictions from H3. However, sympatric sister species
nonetheless appear to represent a relatively good match
with these predictions. Three sister-species pairs overlap
in distribution: M. europaeus and M. mirus in the North
Atlantic and M. perrini and M. peruvianus and M. stejnegeri and M. densirostris, in the North Pacific. The first
two possess divergent tusks under the majority of coding
options, and although the tusks of M. stejnegeri and M.
densirostris do appear similar based on evaluation of their
position in the jaw, size, width, and overall shape (H1-B
to -E, H1-G, H1-H), they differ markedly in their length,
angle of incline, and whether or not they are raised up
on an arch (H1-F, H1-I, H1-J).
Estimated Divergence Dates
Substitution patterns in our data set did not follow a
strict molecular clock model (P < 0.01). Estimates generated using a relaxed molecular clock were in agreement
on the order and tempo at which the lineages diverged
but differed in their estimates of divergence dates, as
expected under the different parameter options. We considered option B2 (emergence of Mesoplodon between 25
and 15 Ma) to be the most likely scenario and only these
results are presented here (Fig. 5). The radiation of Mesoplodon beaked whales does not appear to have occurred
in a single burst. Instead, new lineages have continued to
arise throughout the evolutionary history of this genus.
As a result, extant lineages represent a wide range of
ages. The youngest lineages include four sister-species
pairs, for which divergence estimates range from 10.4 to
5.3 Ma. Assuming current distributions are an accurate
reflection of past distributions, the North Atlantic was
first colonized by M. bidens, followed later by members
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SYSTEMATIC BIOLOGY
TABLE 4. Summary of the distribution of sites supporting internal nodes in the phylogeny as labeled in Figure 4. All characters are singlenucleotide substitutions unless indicated otherwise. Numbers in parentheses indicate how many of these represent unique, lineage-specific,
shared-derived characters (synapomorphies)—i.e., changes that occur only once in the tree.
Node
BGN
CAT
RHO
CTLA3
CHRNA1
ACT
DQA
A
B
C
D
E
F
G
H
I
J
K
4 (4)
1 (1)
3 (3)
3 (2)
1 (1)
1 (1)
3 (3)
2 (1)
1 (0)
1 (0)
2 (0)
1a (1)
1 (0)
2 (2)
1 (1)
2 (0)
1 (1)
8 (5)
a
1 (1)
1 (0)
1 (1)
3 (2)
3 (3)
7 (4)
1 (1)
9 (8)
1 (1)
1 (1)
3 (1)
7 (3)
Total
13 (12)
4 (3)
2 (1)
1 (0)
3 (0)
3 (3)
0 (0)
1 (1)
3 (3)
4 (1)
4 (2)
38 (26)
Two-base pair deletion.
of the True’s beaked whale clade (three species), whereas
M. densirostris (Perrin’s beaked whale clade) was a relative latecomer to these waters. The North Pacific was
first colonized by two lineages from the straptooth and
True’s beaked whale clades but subsequently exploited
more widely by several members of the Perrin’s beaked
whale clade (four species). The Southern Hemisphere is
largely the domain of the straptooth and Perrin’s beaked
whale clades, but two members of the True’s beaked
whale clade have also made successful incursions into
this region. Note that although M. densirostris is one of
the youngest members of this group, it has the widest
distribution and is found in all three ocean basins.
D ISCUSSION
Radiation of the Genus Mesoplodon
Of the four hypotheses put forward to explain patterns of Mesoplodon tusk morphology and/or the processes that have driven the diversification of this genus,
only two seem to warrant further consideration—sexual
selection (H3; Dalebout, 2002) and species recognition
(H4; MacLeod, 2000). The co-occurrence of species with
similar tusks in the North Pacific and Southern Hemisphere appears to contradict predictions from the latter.
However, our coding of the tusks based on various characteristics such as position in the jaw, size, shape, and
angle of inclination is somewhat artificial. In reality, the
tusks of every species are sufficiently unique that they
can be used as diagnostic characters for species identification by researchers (e.g., Allen et al., 2001; Allen, 2007).
Further, it is also not clear how other whales perceive
these tusks. Here we have assumed that the tusks are
a visual cue. Given the echolocation abilities of beaked
whales (Johnson et al., 2004), the tusks could also provide
a unique acoustic profile. Toothed whales use the phonic
lips in their nasal passages to produce sounds that are
transmitted through the waxy melon in the forehead.
Echoes from objects such as prey or other whales are
then received via the lower jaws (Jones, 2005). The tusks
are associated with the receiving components of this system, which in whales is quite separate from the soundproducing component. Therefore, it seems unlikely that
they function as modifiers of acoustic signals, as would
TABLE 5. Approximately unbiased (AU) and Shimodaira-Hasegawa (SH) test scores comparing the best maximum likelihood (ML) tree with
alternative hypotheses. See Table 3 and Figure 3 for details of H1 tusk coding.
Difference in
ML best tree
H1-A
H1-B
H1-C
H1-D
H1-E
H1-F
H1-G
H1-H
H1-I
H1-J
H2+H3 stricta
H2+H3 relaxedb
a
−ln L
–ln L
AU P value
SH P value
6063.049
6196.247
6209.074
6162.888
6208.283
6204.027
6211.812
6215.172
6209.628
6205.718
6211.714
6212.809
6195.401
(best)
133.198
146.025
99.839
145.234
140.978
148.763
152.123
146.579
142.669
148.665
149.760
132.352
1.000
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
<0.0001
0.999
0.001
0.001
0.001
0.001
<0.0001
0.001
0.001
0.001
<0.0001
0.001
<0.0001
<0.0001
Only species found in a single ocean basin were assigned to ocean-basin clades. See Figure 5 for information on species distributions.
For species found in more than one ocean basin, the main center of distribution was used to designate ocean basin of origin, such that all species, except M.
densirostris, were assigned to ocean-basin clades.
b
2008
DALEBOUT ET AL.—TUSK EVOLUTION IN BEAKED WHALES
867
FIGURE 5. Maximum likelihood topology with estimated dates of divergence (asterisk highlights constraint node—origin of genus Mesoplodon
between 25 and 15 million years ago). Terminal nodes are labeled with species codes as per Figure 2. Tusk morphology is depicted by jaw images
adjacent to branch termini. See text for discussion of tusk category codes (T1 to T5). Shaded boxes indicate species’ distributions: North Atlantic,
white; North Pacific, gray; Southern Hemisphere, hatched. Some species occur in multiple ocean basins. Ma, million years ago; Ple, Pleistocene.
be required if they were involved in the production of
species-specific courtship calls.
The species-recognition hypothesis also assumes that
there is female choice in the selection of mates and a high
potential for mistakes. Ornaments that serve as cues for
species recognition are usually possessed by both sexes
(Andersson, 1994). Where ornaments are possessed by
only one sex, mate choice is the prerogative of the other
sex (West-Eberhard, 1983). Given that it is the adult males
who have tusks, female choice is expected to be the dominant pattern. Sex-specific recognition cues can help animals avoid mistakes in breeding with similar-looking
species in crowded ecosystems, or, as may be the case
for Mesoplodon beaked whales, if encounters with conspecifics are rare. If mistakes in mate identification did
occur, we would expect to occasionally encounter hybrids. In baleen whales, hybrids between blue and fin
whales (Balaenoptera musculus and B. physalus) have been
encountered on several occasions, whereas in toothed
whales, hybridization can occur among several dolphin
species, though this generally happens only in captivity
(see review by Bérubé and Aguilar, 1998). However, no
hybrid beaked whales have been reported to date from
morphology or genetics. Overall, the species recognition hypothesis does not therefore appear to offer sufficient explanation for the diversity and distribution of
male tusk form in Mesoplodon beaked whales, though
selection for species recognition cues could nonetheless
help maintain divergent tusk morphologies among some
sympatric species.
None of the three main Mesoplodon clades was confined to a single ocean basin, as might be expected from
strict sympatric speciation driven by sexual selection.
However, three of the four sister-species pairs have both
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SYSTEMATIC BIOLOGY
overlapping distributions and divergent tusk forms, as
predicted by this hypothesis. The only sister-species pair
that does not follow this pattern occurs in different ocean
basins (Fig. 5). These sister-species pairs are among the
youngest lineages in this genus. This pattern, as revealed
by our analyses, suggests that although sexual selection
may have played an important role in the diversification of this genus, the broad evolutionary time scale on
which this process likely occurred, together with the high
dispersal abilities of these species and the plasticity of
tusk form, may have overwritten much of the evidence.
Species evolving in sympatry through sexual selection
could subsequently disperse to new areas where they
would incur new costs for the effective exploitation of
new niches. Little is known about the diet of these whales
beyond their preference for deep-water squid (MacLeod
et al., 2003). Although the tusks are not used for feeding,
large tusks are likely to be costly to grow and maintain.
In some species, the tusks may even hinder feeding. For
example, the long strap-like teeth of M. layardii grow to
curve over the upper jaw and limit the gape to only a few
centimeters (Reeves et al., 2002). More importantly perhaps, violent male-male combat is also a costly activity
that can result in injury. Although there is no doubt that
the original function of the male tusks is as weapons, it
is not clear that all extant Mesoplodon species engage in
violent combat. The widespread occurrence of these encounters has been inferred from the heavy, highly visible
scarring accumulated by adult males, but this behavior
has never been observed (Mead et al., 1982; Heyning,
1984). Note that it is also possible that this scarring is
used by females as an indicator of male quality (Macleod,
1998). Insufficient fresh specimens have been examined
for some Mesoplodon species to determine whether they
all engage in equally violent contests. In some cases, it is
possible that male-male combat no longer occurs (e.g., M.
ginkgodens; Reeves et al., 2002), and as a result, selection
on the tusks for use as weapons may have been relaxed.
Tempo of Speciation
Due to the paucity of beaked whale fossils of known
age and with clear links to extant lineages, our estimates
of divergence dates were reliant on a single calibration
point. The window of time covered by this calibration
point, and by the different parameter scenarios explored,
FIGURE 6. (a and b) Reconstruction of ancestral states (distribution and tusk form) based on maximum likelihood. Terminal nodes are labeled
with species codes as per Figure 2. Distribution coded as per “relaxed” option in Table 5. See Table 3 for details of tusk coding options.
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DALEBOUT ET AL.—TUSK EVOLUTION IN BEAKED WHALES
FIGURE 6. (Continued)
869
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SYSTEMATIC BIOLOGY
VOL. 57
FIGURE 6. (Continued)
was very wide (30 to 5 Ma). As a result, our divergence
date estimates for Mesoplodon species have large standard
errors and should be interpreted with caution. As new
fossil beaked whales come to light and their affinities to
modern taxa are clarified (Lambert, 2005; Lambert and
Louwye, 2006), these estimates will likely require revision. It is worth noting, however, that our estimate for
the divergence of the youngest sister-species pair in this
genus (M. perrini and M. peruvianus) at 5.3 Ma is concordant with estimates from mtDNA based on the general mammalian rate of approximately 1% divergence
per million years (Dalebout, 2002).
However, investigation of the relative tempo at which
speciation occurred is not reliant on robust fossil calibrations. Speciation has clearly continued throughout the
evolution of the genus, no matter to what date its initial
emergence is constrained. This is an interesting observation in itself as radiations driven primarily by sexual
selection often seem to occur in a quick burst over a short
period of time—e.g., cichlids in the African Great Lakes
(Galis, 1998; Genner et al., 2007). This suggests that the
radiation of Mesoplodon beaked whales has perhaps not
been as rapid as would expected if it were driven by
strong, sustained sexual selection.
The potential impact of missing lineages should, however, also be considered. By necessity, we have been able
to assess only the diversity and distribution of extant
species. Many other Mesoplodon species may have fallen
by the wayside during the evolution of this group and
likely also influenced the tempo and mode of this radiation. Ghost-lineage analysis could provide some insight into the proportion of missing taxa (Teeling et al.,
2005) but unfortunately is reliant on multiple fossil calibrations, which are not available in this case.
Agreement between Molecules and Morphology
Here we have presented the first robust, highly resolved molecular phylogeny for Mesoplodon beaked
whales, one of the most speciose, yet least well-known,
of cetacean genera. This work, based on nuclear intron
sequences, complements and supports earlier studies in
which mtDNA data were used to confirm the genetic distinctiveness of all previously recognized species in this
group (Dalebout et al., 2004) and describe two additional
species (Dalebout et al., 2002; van Helden et al., 2002). To
date, there have been no explicit attempts to reconstruct
evolutionary relationships among beaked whales based
2008
871
DALEBOUT ET AL.—TUSK EVOLUTION IN BEAKED WHALES
TABLE 6. Tusk forms by ocean basin. Species codes follow Figure 2. Species distributions are as indicated in Figure 5. See Table 3 for details of
H1-A to H1-J tusk form coding options. Sister species found in the same ocean basin are indicated by “+” between species codes and character
states. M. stejnegeri (Mst) and M. densirostris (Mde—all oceans) are also sister species and co-occur in the North Pacific. M. carlhubbsi (Mca) and
M. bowdoini (Mbow) are sister species but do not overlap in distribution.
Distribution
Species
H1-A
H1-B
H1-C
H1-D
H1-E
H1-F
H1-G
H1-H
H1-I
H1-J
North Atlantic
Mbi, Meu + Mmi
North Pacific
Mca, Mgin, Mpi + Mpe, Mst
Southern Hemisphere
Mbow, Mgr, Mhe, Mlay, Mmi, Mpe
All oceans
Mde
4, 2 + 1
3, 2 + 1
3, 2 + 1
4, 2 + 1
2, 2 + 2
1, 1 + 1
1, 2 + 1
2, 2 + 1
4, 2 + 1
1, 1 + 1
3, 2, 1 + 5, 3
2, 2, 1 + 2, 2
3, 4, 1 + 4, 4
3, 3, 1 + 3, 3
3, 3, 2 + 1, 3
2, 1, 1 + 1, 2
3, 4, 1 + 1, 3
3, 3, 2 + 1, 3
2, 2, 2 + 1, 3
1, 1, 1 + 2, 1
3, 2, 1, 4, 1, 5
2, 2, 1, 3, 1, 2
3, 2, 1, 3, 1, 4
3, 3, 1, 4, 1, 3
3, 2, 2, 4, 2, 1
2, 1, 1, 3, 1, 1
3, 3, 1, 2, 1, 1
3, 3, 2, 4, 1, 1
3, 2, 1, 4, 1, 1
1, 1, 1, 1, 1, 2
5
2
4
3
3
2
3
3
1
2
on morphological features. There are several reasons for
this. First, many species in this family are rare, with several known from fewer than 30 individuals (Reeves et al.,
2002). Second, most morphological work on cetaceans
focuses on cranial characters. In beaked whales, these
features can differ strongly by sex and age class, further reducing the number of specimens available for
inter-species comparison (e.g., Mead, 1989). Third, many
species have wide geographic distributions. As a result, specimens are scattered in museum collections
throughout the world. Finally, cranial morphology in this
group appears to be relatively conserved across species,
perhaps due to ecological constraints associated with
deep-diving. Attempts to clarify the morphological distinctiveness of these species have traditionally placed
most emphasis on the male tusks and features of the
“vertex,” the elevated crest formed by the cranial bones
behind the superior nares (e.g., Moore, 1966, 1968). From
a phylogenetic perspective, it is not clear that small-scale
differences in the arrangement of the vertex bones have
any real adaptive function and, as such, can serve as
a useful character to reconstruct evolutionary relationships in this group.
Morphological assessments have, however, suggested
close relationships between several Mesoplodon species
that this study has subsequently confirmed to be sisterspecies pairs. For example, Moore (1957, 1960) proposed
a sister-species relationship between M. mirus and M.
europeaus based on cranial morphology, whereas M. carlhubbsi and M. bowdoini were initially described as the
same species (Hubbs, 1946) before further morphological analyses revealed their distinctiveness (Moore, 1963).
Interestingly, although these sister-species relationships
were supported by our nuclear intron work, mtDNA
analyses failed to resolve the close relationship between
the latter pair (although it was not strongly excluded
either; Dalebout et al., 1998, 2004). This may be due
to the relatively old age of this divergence (approximately 10.4 Ma; Fig. 5) and the accumulation of phylogenetic noise (homoplasies) by the mtDNA genome
since this time. The other sister-species pairs identified
here are all younger (approximately ≤7.4 Ma) and were
also resolved by previous mtDNA analyses (although
like most other higher-level nodes, such groupings generally received low BS scores in mtDNA reconstructions;
e.g., Dalebout et al., 2002). Cranial morphology has also
suggested a link between M. bowdoini and M. traversii
(Reyes et al., 1996; Baker, 2001), the only described Mesoplodon species not included in this study. M. traversii
is currently known from three partial skulls from the
Southern Hemisphere and its external appearance remains unknown (van Helden et al., 2002). mtDNA analyses suggest that M. traversii is likely a member of the
straptooth clade and of similar age as the other three
species (Dalebout, 2002). The position of the tusks in
M. traversii, which overlap with the posterior end of the
symphysis, also supports this conclusion. Confirmation
of this relationship will require nuclear data and fresh
tissue samples from which high-quality DNA can be extracted. Intriguingly, tusk form in M. traversii is similar to that of M. layardii (van Helden et al., 2002) even
though their skulls differ, such that M. traversii appears
to be a morphological composite of the other taxa in this
clade.
Although cranial features can be used to infer sisterspecies relationships in this family, similarity in tusk
form can be misleading given the plasticity of this feature as demonstrated by our analyses (Fig. 6a, b). The
large apical tusks of both M. hectori and M. perrini initially led researchers to assume that they represented a
single species (Mead, 1981; Mead and Baker, 1987). When
mtDNA analyses revealed the distinctiveness and nonsister-species relationship of these rare whales (Dalebout
et al., 1998, 2002), the morphological features were reevaluated. As expected from the deep mtDNA divergence (Dalebout et al., 2002)—a pattern later confirmed
by analysis of a nuclear intron (Dalebout et al., 2004)—
there are several fixed morphological differences between these taxa, although they are relatively subtle
(Dalebout et al., 2002). The phylogeny presented here
provides further confirmation of the distinctiveness of
these species (Fig. 5) and suggests that their similar tusks
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SYSTEMATIC BIOLOGY
are the result of parallel evolution and the retention or
re-emergence of ancestral character states. It is worth noting that although M. hectori and M. perrini resemble one
another in their conservative vertex morphology (Mead
and Baker, 1987), this resemblance is stronger still between M. perrini and its real sister species, M. peruvianus,
though their tusks are highly divergent.
CONCLUSIONS AND FURTHER WORK
We have tested predictions from four hypotheses regarding the evolution and diversification of a speciose
genus of whales using a robust, highly resolved molecular phylogeny. The patterns observed in three of the four
sister-species pairs identified strongly suggest that sexual selection on weaponry in the form of the male tusks,
together perhaps with selection for species recognition
cues, has played an important role in this unique radiation. To our knowledge, this is the first time that sexual
selection has been explicitly implicated in the radiation of
a mammalian group outside terrestrial ungulates. However, the extent to which sexual selection has occurred,
and the effect of other selection pressures (e.g., female
mate choice, niche separation, and diet), is difficult to ascertain due to our lack of knowledge about many aspects
of beaked whale biology. Insights into social organization, including the role of male-male combat and female
mate choice, will be difficult to obtain as most Mesoplodon
species are rarely encountered at sea and generally cannot be observed for extended periods (Reeves et al., 2002).
However, sightings of single adult males accompanying
multiple adult females suggest that these whales may
have a polygynous mating system (McSweeney et al.,
2007), a system that often does not allow for significant
female choice. Dead stranded or beachcast animals could
also provide a wealth of information about niche separation if the stomach contents are collected (MacLeod
et al., 2003). This should be done far more regularly than
is currently the case in many areas.
Robust reconstruction of relationships among the
other genera in this family will require data from a
suite of nuclear introns similar to those analyzed here
for Mesoplodon beaked whales. Previous analyses based
on two introns (ACT and DQA) failed to resolve these
relationships due to the presence of very short internode lengths at the base of the tree, suggestive of a
rapid radiation event (Dalebout, 2002). Closely related
outgroups, which could help determine the polarity of
character state changes, are also unavailable. Beaked
whales are among the oldest of cetacean lineages (Barnes
et al., 1985). The closest sister groups are the Platanistidae (river dolphins) and Physeteridae (sperm whales;
Heyning, 1997; Cassens et al., 2000), both of which have
been reduced to essentially a single extant species (a stark
contrast to the Ziphiidae). The long branches of these
sister groups may therefore be as much of a hindrance
as a help in the reconstruction of a robust phylogeny
(Felsenstein, 1978). As a result, nuclear data, including
short interspersed repeated elements (SINES; Nikaido
et al., 2001), from a range of cetacean families will likely
VOL.
57
be needed to resolve inter-generic relationships among
beaked whales.
ACKNOWLEDGMENTS
For collection and access to samples and specimens, we thank New
Zealand Department of Conservation field center staff (NZ); Kelly
Robertson, US NMFS Southwest Fisheries Science Center (SW); Bob
Reid, Scottish Agricultural College (SAC); Nick Gales, Australian
Antarctic Division (WA); Marty Haulena, the Marine Mammal Center (TMMC), California; Paul Jepson, Institute of Zoology, London
(NHMUK); John Heyning, Los Angeles County Museum of Natural
History (LAM); Charley Potter, Smithsonian Institution US National
Museum of Natural History (NE, WAM); Cath Kemper, South Australian Museum (SAM); Tadasu Yamada, National Science Museum,
Japan (TSM); and John Wang, FormosaCetus, Taiwan (TW). Abbreviations in parentheses refer to species codes in Appendix 1. We thank
Sarah Mesnick, US NMFS Southwest Fisheries Science Center, for initiating discussion regarding the role of sexual selection in the radiation
of the Ziphiidae; Robin Beck, UNSW, for assistance with phylogenetic
analyses; Vivian Ward, University of Auckland for beaked whale jaw
images; and Andrew Glaser, New Zealand Department of Conservation, and Gina Lento, University of Auckland, for use of Gray’s beaked
whale photographs. This article benefitted from comments by William
B. Sherwin, Systematic Biology Editor-in-Chief Jack Sullivan, Associate
Editor Michael Charleston, and an anonymous reviewer. Funding for
DNA sequencing was provided by grants to C.S.B. from the New
Zealand Marsden Fund, the US Marine Mammal Commission, and the
Committee for Research and Exploration of the National Geographic
Society. M.L.D. is supported by a UNSW Vice-Chancellor’s Postdoctoral Fellowship.
R EFERENCES
Akaike, H. 1973. Information theory and an extension of the maximum
likelihood principle. Pages 267–281 in Second International Symposium on Information Theory. Akademiai Kiado, Budapest.
Allen, B. M. 2007. Smithsonian Institution Marine Mammal Program
beaked whale identification guide (http://www.nmnh.si.edu/vert/
mammals/beaked whales/pages/main menu.htm). Accessed 20
June 2007.
Allen, B. M., R. E. Chapman, and J. G. Mead. 2001. Species and sex
determination of Mesoplodon and Ziphius based on mandibular measurements. Abstract, 14th Biennial Conference on the Biology of Marine Mammals. Vancouver, BC, Canada. Available from the Society
for Marine Mammalogy, PO Box 692042, Orlando, FL 32869–2042,
USA.
Andersson, M. 1994. Sexual selection. Princeton University Press,
Princeton, New Jersey.
Arnason, U., and A. Gullberg. 1996. Cytochrome b nucleotide sequences and the identification of five primary lineages of extant
cetaceans. Mol. Biol. Evol. 13:407–417.
Auffray, C., J. W. Lillie, A. J. Korman, J. M. Boss, N. Frechin, F. Guillemnot, J. Cooper, R. C. Mulligan, and J. L. Strominger. 1987. Structure
and expression of HLA-DQA and -DXA genes: Interallelic alternate
splicing of the HLA-DQA gene and functional splicing of the HLADQX gene using a retroviral vector. Immunogenetics 26:63–73.
Baker, A. N. 2001. Status, relationships and distribution of Mesoplodon
bowdoini Andrews, 1908 (Cetacea: Ziphiidae). Mar. Mammal. Sci.
17:473–493.
Baker, C. S., R. W. Slade, J. L. Bannister, R. B. Abernethy, M. T. Weinrich,
J. Lien, J. Urban, P. Corkeron, J. Calmabokidis, O. Vasquez, and S. R.
Palumbi. 1994. Hierarchical structure of mitochondrial DNA gene
flow among humpback whales Megaptera novaeangliae, world-wide.
Mol. Ecol. 3:313–327.
Barlow, J., M. Ferguson, W. F. Perrin, L. Ballance, T. Gerrodette, G. G.
Joyce, C. D. MacLeod, K. Mullin, D. L. Palka, and G. T. Waring 2006.
Abundance and densities of beaked and bottlenose whales (family
Ziphiidae). J. Cet. Res. Man. 7:263–270.
Barnes, L. G., D. P. Domning, and C. E. Ray. 1985. Status of studies on
fossil marine mammals. Mar. Mammal. Sci. 1:15–53.
2008
DALEBOUT ET AL.—TUSK EVOLUTION IN BEAKED WHALES
Berglund, A., A. Bisazza, and A. Pilastro. 1996. Armaments and ornaments: An evolutionary explanation of traits of dual utility. Biol. J.
Linn. Soc. 58:385–399.
Bérubé, M., and A. Aguilar. 1998. A new hybrid between a blue whale,
Balaenoptera musculus, and a fin whale, B. physalus: Frequency and
implications of hybridization. Mar. Mammal. Sci. 14:82–98.
Carwardine, M. 1995. Whales, dolphins and porpoises. HarperCollins,
London.
Cassens, I., S. Vicario, V. G. Waddell, H. Balchowsky, D. Van Belle, D.
Wang, F. Chen, R. S. Lal Mohan, P. C. Simões-Lopes, R. Bastida, A.
Meyer, M. J. Stanhope, and M. C. Milinkovitch. 2000. Independent
adaptation to riverine habitats allowed survival of ancient cetacean
lineages. Proc. Natl. Acad. Sci. USA 97:11343–11347.
Dalebout, M. L. 2002. Species identity, genetic diversity and molecular systematic relationships among the Ziphiidae (beaked whales).
PhD thesis, School of Biological Sciences, University of Auckland,
Auckland, New Zealand.
Dalebout, M. L., C. S. Baker, V. G. Cockcroft, J. G. Mead, and T. K.
Yamada. 2004. A comprehensive and validated molecular taxonomy
of beaked whales, family Ziphiidae. J. Hered. 95:459–473.
Dalebout, M. L., J. G. Mead, C. S. Baker, A. N. Baker, and A. L. van
Helden. 2002. A new species of beaked whale Mesoplodon perrini sp.
n. (Cetacea: Ziphiidae) discovered through phylogenetic analyses of
mitochondrial DNA sequences. Mar. Mammal. Sci. 18:577–608.
Dalebout, M. L., G. J. B. Ross, C. S. Baker, R. C. Anderson, P. B.
Best, V. G. Cockcroft, H. L. Hinsz, V. Peddemors, and R. L. Pitman.
2003. Appearance, distribution and genetic distinctiveness of Longman’s beaked whale, Indopacetus pacificus. Mar. Mammal. Sci. 19:421–
461.
Dalebout, M. L., A. van Helden, K. Van Waerebeek, and C. S.
Baker. 1998. Molecular genetic identification of southern hemisphere
beaked whales (Cetacea: Ziphiidae). Mol. Ecol. 7:687–694.
de Queiroz, K. 1993. For consensus (sometimes). Syst. Biol. 42:368–372.
Eberhard, W. G. 1980. Horned beetles. Sci. Am. 242:166–182.
Emlen, D. J., J. Marangelo, B. Ball, and C. W. Cunningham. 2005. Diversity in the weapons of sexual selection: Horn evolution in the beetle
genus Onthophagus (Coleoptera: Scarabaeidae). Evolution 59:1060–
1084.
Farris, J. S., M. Kallersjo, A. G. Kluge, and C. Bult. 1995. Testing the
significance of incongruence. Cladistics 10:315–319.
Felsenstein, J. 1978. Cases in which parsimony and compatibility methods will be positively misleading. Syst. Zool. 27:401–410.
Fordyce, R. E. 2002. Fossil record. Pages 453–471 in Encyclopedia of
marine mammals (W. F. Perrin, B. Wursig, and J. G. M. Thewissen,
eds.). Academic Press, San Diego.
Galis, F. 1998. Why are there so many cichlid species? TREE 13:1–2.
Geist, V. 1978. On weapons, combat and ecology. Pages 1–30 in Aggression, dominance, and individual spacing (L. Kramer, P. Pliner, and
T. Alloway, eds.). Plenum, New York.
Genner, M. J., O. Seehausen, D. H. Lunt, D. A. Joyce, P. W. Shaw, G.
R. Carvalho, and G. F. Turner. 2007. Age of cichlids: New dates for
ancient lake fish radiations. Mol. Biol. Evol. 24:1269–1282.
Heyning, J. E. 1984. Functional morphology involved in intraspecific
fighting of the beaked whale, Mesoplodon carlhubbsi. Can. J. Zool.
62:1645–1654.
Heyning, J. E. 1997. Sperm whale phylogeny revisited: Analysis of the
morphological evidence. Mar. Mammal. Sci. 13:596–613.
Hubbs, C. L. 1946. First records of two beaked whales, Mesoplodon bowdoini and Ziphius cavirostris from the Pacific Coast of the United States.
J. Mammal. 27:242–255.
Huelsenbeck, J. P., and F. Ronquist. 2001. MrBayes: Bayesian inference
of phylogenetic trees. Bioinformatics 17:754–755.
Johnson, M., P. Madsen, W. Zimmer, N. de Soto, and P. Tyack. 2004.
Beaked whales echolocate on prey. Proc. R. Soc. Lond. B 271:S383–
S386.
Jones, G. 2005. Echolocation. Curr. Biol. 15:R484-R488
Kaneshiro, K. Y. 1983. Sexual selection and direction of evolution in
the biosystematics of Hawaiian Drosophilidae. Ann. Rev. Entomol.
28:161–178.
Kellogg, R. 1928a. The history of whales-their adaptation to life in water
(Part I). Quart. Rev. Biol. 3:29–76.
Kellogg, R. 1928b. The history of whales-their adaptation to life in water
(Part II). Quart. Rev. Biol. 3:174–208.
873
Kishino, H., and M. Hasegawa. 1989. Evaluation of the maximum
likelihood estimate of the evolutionary tree topologies from DNA
sequence data, and branching order in Hominoidea. Mol. Evol.
29:170–179.
Kishino, H., J. L. Thorne, and W. J. Bruno. 2001. Performance of a divergence time estimation method under a probabilistic model of rate
evolution. Mol. Biol. Evol. 18:352–361.
Kumar, S., K. Tamura, and M. Nei. 2004. MEGA3: Integrated software
for molecular evolutionary genetics analysis and sequence alignment. Brief. Bioinf. 5:150–163.
Lambert, O. 2005. Systematics and phylogeny of the fossil beaked
whales Ziphirostrum du Bus, 1868 and Choneziphius Duvernoy, 1851
(Mammalia, Cetacea, Odontoceti), from the Neogene of Antwerp
(North of Belgium). Geodiversitas 27:443–497.
Lambert, O., and S. Louwye. 2006. Archeoziphius microglenoideus, a new
primitive beaked whale (Mammalia, Cetacea, Odontoceti) from the
Middle Miocene of Belgium. J. Vert. Paleo. 26:182–191.
Lundrigan, B. 1996. Morphology of horns and fighting behaviour in
the family Bovidae. J. Mammal. 77:462–475.
Lyons, L. A., T. F. Laughlin, N. G. Copeland, N. A. Jenkins, J. E.
Womack, and S. J. O’Brien. 1997. Comparative anchor tagged sequences (CATS) for integrative mapping of mammalian genomes.
Nat. Genet. 15:47–56.
MacLeod, C. D. 1998. Intraspecific scarring in odontocete cetaceans: An
indicator of male “quality” in aggressive social interactions? J. Zool.
Lond. 244:71–77.
MacLeod, C. D. 2000. Species recognition as a possible function for
variations in position and shape of the sexually dimorphic tusks of
Mesoplodon beaked whales. Evolution 54:2171–2173.
MacLeod, C. D., W. F. Perrin, R. L. Pitman, J. Barlow, L. Ballance, A.
D’Amico, T. Gerrodette, G. Joyce, K. D. Mullin, D. L. Palka, and G.
T. Waring. 2006. Known and inferred distributions of beaked whale
species (Ziphiidae: Cetacea). J. Cet. Res. Man. 7:271–286.
MacLeod, C. D., M. B. Santos, and G. J. Pierce. 2003. Review of data on
diets of beaked whales: Evidence of niche separation and geographic
segregation. J. Mar. Biol. Assoc. (UK) 83:651–665.
Maddison, W. P., and D. R. Maddison. 2005. MacClade: Analysis of
phylogeny and character evolution. Sinauer Associates, Sunderland,
Massachusetts.
Maddison, W. P., and D. R. Maddison. 2006. Mesquite: A modular system for evolutionary analysis. Version 1.12. Available at
http://mesquiteproject.org.
May-Collado, L., and I. Agnarsson. 2006. Cytochrome b and Bayesian
inference of whale phylogeny. Mol. Phylog. Evol. 38:344–354.
McSweeney, D. J., R. W. Baird, and S. D. Mahaffy. 2007. Site fidelity,
associations, and movements of Cuvier’s (Ziphius cavirostris) and
Blainville’s (Mesoplodon densirostris) beaked whales off the island of
Hawai’i. Mar. Mamm. Sci. 23:666–687.
Mead, J. G. 1981. First records of Mesoplodon hectori (Ziphiidae) from
the Northern Hemisphere and a description of the adult male. J.
Mammal. 62:430–432.
Mead, J. G. 1989. Beaked whales of the genus Mesoplodon. Pages 349–430
in Handbook of marine mammals (S. H. Ridgway and R. Harrison,
eds.). Academic Press, London.
Mead, J. G., and A. N. Baker. 1987. Notes on the rare beaked whale,
Mesoplodon hectori (Gray). J. R. Soc. N. Z. 17:303–312.
Mead, J. G., W. A. Walker, and W. J. Houck. 1982. Biological observations
on Mesoplodon carlhubbsi (Cetacea: Ziphiidae). Smiths. Contrib. Zool.
344:1–25.
Messenger, S. L., and J. A. McGuire. 1998. Morphology, molecules and
the phylogenetics of cetaceans. Syst. Biol. 47:90–124.
Moore, J. C. 1957. Differences between the beaked whales Mesoplodon
mirus and Mesoplodon gervaisi. Am. Mus. Nov. 1831:1–25.
Moore, J. C. 1960. New records of the gulf-stream beaked whale, Mesoplodon gervaisi, and some taxonomic considerations. Am. Mus. Nov.
1993:1–35.
Moore, J. C. 1963. Recognizing certain species of beaked whales of the
Pacific Ocean. Am. Mid. Nat. 70:396–428.
Moore, J. C. 1966. Diagnoses and distributions of beaked whales of the
genus Mesoplodon known from North American waters in whales,
dolphins and porpoises. Pages 32–16 in International Symposium
on Cetacean Research. University of California Press, Washington,
DC.
874
VOL. 57
SYSTEMATIC BIOLOGY
Moore, J. C. 1968. Relationships among the living genera of beaked
whales. Field. Zool. 53:209–298.
Nikaido, M., F. Matsuno, H. Hamilton, R. L. J. Brownell, Y. Cao, W.
Ding, Z. Zuoyan, A. M. Shedlock, R. E. Fordyce, M. Hasegawa, and
N. Okada. 2001. Retroposon analysis of major cetacean lineages: The
monophyly of toothed whales and the paraphyly of river dolphins.
Proc. Natl. Acad. Sci. USA 98:7384–7389.
Owen, R, 1870. Monograph on the British fossil Cetacea from the Red
Crag. The Palaeontological Society, London.
Pagel, M., and A. Meade. 2006. Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov Chain Monte
Carlo. Am. Nat. 167:808–825.
Palumbi, S. R., and C. S. Baker. 1994. Contrasting population structure
from nuclear intron sequences and mtDNA of humpback whales.
Mol. Biol. Evol. 11:426–435.
Posada, D. 2006. ModelTest Server: A web-based tool for the statistical
selection of models of nucleotide substitutions online. Nucleic Acids
Res. 34:W700–W703.
Posada, D., and T. R. Buckley. 2004. Model selection and model averaging in phylogenetics: Advantages of Akaike Information Criterion and Bayesian approaches over likelihood ratio tests. Syst. Biol.
53:793–808.
Posada, D., and K. A. Crandall. 1998. ModelTest: Testing the model of
DNA substitution. Bioinformatics Appl. Notes 14:817–818.
Rannala, B., and Z. Yang. 1996. Probability distribution of molecular
evolutionary trees: A new method of phylogenetic inference. J. Mol.
Evol. 43:304–311.
Reeves, R. R., S. S. Brent, P. J. Clapham, J. A. Powell, and P. A. Folkens.
2002. National Audubon Society guide to marine mammals of the
world. Chanticleer Press, New York.
Reyes, J. C., K. Van Waerebeek, J. C. Cárdenas, and J. L. Yañez. 1996.
Mesoplodon bahamondi sp. n. (Cetacea, Ziphiidae), a living beaked
whale from the Juan Fernandez Archipelago, Chile. Bol. Mus. Nac.
Hist. Nat. Chile 45:31–44.
Ronquist, F., and J. P. Huelsenbeck. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–
1574.
Ronquist, F., J. P. Huelsenbeck, and P. van der Mark. 2005. MrBayes 3.1
Manual. Available at http://mrbayes.scs.fsu.edu/manual.php.
Rutschmann, F. 2005. Bayesian molecular dating using PAML/
multidivtime. A step-by-step manual. University of Zurich, Switzerland. Available at http://www.plant.ch.
Sambrook, E., F. Fritsch, and T. Maniatis. 1989. Molecular cloning. Cold
Spring Harbor Press, Cold Spring Harbor, New York.
Sasaki, T., M. Nikaido, S. Wada, T. K. Yamada, Y. Cao, M. Hasegawa,
and N. Okada. 2006. Balaenoptera omurai is a newly discovered baleen
whale that represents an ancient evolutionary lineage. Mol. Phylogenet. Evol. 41:40–52.
Seehausen, O., and J. M. van Alphen. 1999. Can sympatric speciation
by disruptive sexual selection explain rapid evolution of cichlid diversity in Lake Victoria? Ecol. Lett. 2:262–271.
Sekiguchi, K., N. T. W. Klages, and P. B. Best. 1996. The diet of the straptoothed whales (Mesoplodon layardii). J. Zool. Lond. 239:453–463.
Shimodaira, H. 2002. An approximately unbiased test of phylogenetic
tree selection. Syst. Biol. 51:492–508.
Shimodaira, H., and M. Hasegawa. 1999. Multiple comparisons of loglikelihoods with applications to phylogenetic inference. Mol. Biol.
Evol. 16:1114–1116.
Shimodaira, H., and M. Hasegawa. 2001. CONSEL: For assessing the
confidence of phylogenetic tree selection. Bioinformatics 17:1246–
1247.
Shine, R. 1979. Sexual selection and sexual dimorphism in the Amphibia. Copeia 2:297–306.
Shuster, S., and M. Wade. 2003. Mating systems and strategies. Princeton University Press, Princeton, New Jersey.
Strimmer, K., and A. Rambaut. 2002. Inferring confidence sets of possibly misspecified gene trees. Proc. R. Soc. Lond. B 269:137–142.
Swofford, D. L. 2003. PAUP*. Phylogenetic analysis using parsimony
(*and other methods). Version 4. Sinauer Associates, Sunderland,
Massachusetts.
Teeling, E. C., M. S. Springer, O. Madsen, P. Bates, S. J. O’Brien, and
W. J. Murphy. 2005. A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307:580–584.
Thorne, J. L., H. Kishino, and I. S. Painter. 1998. Estimating the rate of
evolution of the rate of molecular evolution. Mol. Biol. Evol. 15:1647–
1657.
Turelli, M. 1984. Heritable genetic variation via mutation-selection balance: Lerch’s zeta meets the abdominal bristle. Theor. Popul. Biol.
25:138–193.
van Helden, A. L., A. N. Baker, M. L. Dalebout, J. C. Reyes, K. Van
Waerebeek, and C. S. Baker. 2002. Resurrection of Mesoplodon traversii
(Gray, 1874), senior synonym of M. bahamondi Reyes, Van Waerebeek,
Cárdenas and Yañez, 1995 (Cetacea: Ziphiidae). Mar. Mammal. Sci.
18:609–621.
Wada, S., M. Oishi, and T. K. Yamada. 2003. A newly discovered species
of living baleen whale. Nature 426:278–281.
West-Eberhard, M. J. 1983. Sexual selection, social competition, and
speciation. Quart. Rev. Biol. 58:155–178.
Wilson, E. O. 1992. Diversity of Life. Harvard University Press, Cambridge, Massachsetts.
Yang, Z. 1997. PAML: A program package for phylogenetic analysis by
maximum likelihood. Comp. Appl. BioSci. 13:555–556.
First submitted 21 February 2008; reviews returned 28 May 2008;
final acceptance 11 September 2008
Associate Editor: Michael Charleston
APPENDIX 1. Identification codes of specific individuals used to generate nuclear intron sequences. Gene names are listed across the top,
species names are represented by three- or four-letter codes. Mesoplodon species codes follow Figure 2. Tsh, Tasmacetus shepherdi; Zca, Ziphius
cavirostris. Different identification numbers across the same species indicate where chimeric concatenated sequences were used for phylogenetic
analysis.
Species
BGN
CAT
RHO
CTLA3
CHRNA1
ACT
Mbi
Mbow
Mca
Mde
Meu
Mgin
Mgr
Mhe
Mlay
Mmi
Mpi
Mpe
Mst
Zca
Tsh
MbiSAC13091
MbowNZ04
McaSW73
MdeNHMUK
MeuSW7444
MginNZ03
MgrNZ67
MheWA02
MlayNZ10
MmiSW4968
TMMCC75
MpeLAM95654
MstSW4962
ZcaNZ12
TshNZ01
MbiSAC13091
MbowNZ04
McaSW1563
MdeNHMUK
MeuSW7444
Mgin01TW
MgrNZ67
MheNZ02
MlayNZ08
MmiSW4972
TMMCC75
MpeLAM95654
MstSW9491
ZcaNZ12
TshNZ01
MbiSAC13091
MbowNZ04
McaSW1563
MdeNZ02
MeuSW4120
Mgin01TW
MgrNZ55
MheNZ02
MlayNZ08
MmiSW4968
TMMCC75
MpeLAM95654
MstSW9491
ZcaNZ12
TshNZ01
MbiNE3070
MbowNZ06
McaSW1563
MdeNZ02
MeuSW4120
MginNZ03
MgrNZ55
MheWA02
MlayNZ10
MmiSW4972
TMMCC75
MpeLAM95654
MstSW9491
ZcaNZ12
TshNZ01
MbiSAC13091
MbowNZ04
McaSW73
MdeNHMUK
MeuSW7444
Mgin01TW
MgrNZ55
MheNZ02
MlayNZ10
MmiSW4968
TMMCC75
MpeLAM95654
MstSW9491
ZcaNZ06
TshNZ01
MbiWAM490
MbowSAM18047
McaSW73
MdeNHMUK
MeuSW7443
MginNZ03
MgrNZ01
MheWA02
MlayNZ10
MmiSW4968
TMMCC75
MpeLAM95654
MstTSM30135
ZcaNZ06
TshNZ02
DQA
MbiSAC13091
MbowMhe01
McaSW1563
MdeNHMUK
MeuSW4120
MginNZ03
MgrNZ02
MheMgr09
MlaySAM9788
MmiSW4968
TMMCC75
MpeLAM95654
MstSW4962
ZcaNZ12
TshNZ01
2008
DALEBOUT ET AL.—TUSK EVOLUTION IN BEAKED WHALES
APPENDIX 2
Maximum likelihood analyses of individual introns. Terminal nodes
are labeled with species codes as per Figure 2. Bootstrap scores ≥50%
875
are shown. Scores in bold font indicate strongly supported nodes. Asterisk in BGN tree highlights the only strongly supported node not observed in subsequent analyses of the concatenated (COMBO) data set.