The Phylogenetic Intrarelationships of Spiny-Rayed Fishes (Acanthomorpha, Teleostei, Actinopterygii): Fossil Taxa Increase the Congruence of Morphology with Molecular Data

Abstract

Acanthomorpha (spiny-rayed fishes) is a clade of teleosts that includes more than 15, 000 extant species. Their deep phylogenetic intrarelationships, first reconstructed using morphological characters, have been extensively revised with molecular data. Moreover, the deep branches of the acanthomorph tree are still largely unresolved, with strong disagreement between studies. Here, we review the historical propositions for acanthomorph deep intrarelationships and attempt to resolve their earliest branching patterns using a new morphological data matrix compiling and revising characters from previous studies. The taxon sampling we use constitutes a first attempt to test all previous hypotheses (molecular and morphological alike) with morphological data only. Our sampling also includes Late Cretaceous fossil taxa, which yield new character state combinations that are absent in extant taxa. Analysis of the complete morphological data matrix yields a new topology that shows remarkable congruence with the well-supported molecular results. Lampridiformes (oarfishes and allies) are the sister to all other acanthomorphs. Gadiformes (cods and allies) and Zeiformes (dories) form a clade with Percopsiformes (trout-perches) and the enigmatic Polymixia (beardfish) and Stylephorus (tube-eye). Ophidiiformes (cusk-eels and allies) and Batrachoidiformes (toadfishes) are nested within Percomorpha, the clade that includes most of modern acanthomorph diversity. These results provide morphological synapomorphies and independent corroboration of clades previously only recovered from molecular data, thereby suggesting the emergence of a congruent picture of acanthomorph deep intrarelationships. Fossil taxa play a critical role in achieving this congruence, since a very different topology is found when they are excluded from the analysis.

Full text

ORIGINAL RESEARCH
published: 14 November 2016
doi: 10.3389/fevo.2016.00129
Frontiers in Ecology and Evolution | www.frontiersin.org 1November 2016 | Volume 4 | Article 129
Edited by:
Andrey Tatarenkov,
University of California, Irvine, USA
Reviewed by:
Adriana López-Arbarello,
Ludwig Maximilian University of
Munich, Germany
Guillermo Orti,
George Washington University, USA
Francesco Santini,
University of California Davis, USA
*Correspondence:
Donald Davesne
donald.davesne@earth.ox.ac.uk
†Present Address:
Donald Davesne,
Department of Earth Sciences,
University of Oxford, Oxford, UK
Specialty section:
This article was submitted to
Phylogenetics, Phylogenomics, and
Systematics,
a section of the journal
Frontiers in Ecology and Evolution
Received: 18 August 2016
Accepted: 28 October 2016
Published: 14 November 2016
Citation:
Davesne D, Gallut C, Barriel V,
Janvier P, Lecointre G and Otero O
(2016) The Phylogenetic
Intrarelationships of Spiny-Rayed
Fishes (Acanthomorpha, Teleostei,
Actinopterygii): Fossil Taxa Increase
the Congruence of Morphology with
Molecular Data.
Front. Ecol. Evol. 4:129.
doi: 10.3389/fevo.2016.00129
The Phylogenetic Intrarelationships
of Spiny-Rayed Fishes
(Acanthomorpha, Teleostei,
Actinopterygii): Fossil Taxa Increase
the Congruence of Morphology with
Molecular Data
Donald Davesne 1, 2*†, Cyril Gallut 1, Véronique Barriel 2, Philippe Janvier 2,
Guillaume Lecointre 1and Olga Otero 3
1Institut de Systématique, Évolution, Biodiversité, UMR 7205 Centre National de la Recherche Scientifique, UPMC, École
Pratique des Hautes Études, Sorbonne Universités, Muséum National d’Histoire Naturelle, Paris, France, 2Centre de
Recherche sur la Paléobiodiversité et les Paléoenvironnements, UMR 7207 Centre National de la Recherche Scientifique,
UPMC, Sorbonne Universités, Muséum National d’Histoire Naturelle, Paris, France, 3Institut de Paléoprimatologie,
Paléontologie Humaine: Évolution et Paléoenvironnements, UMR 7262 Centre National de la Recherche Scientifique,
Université de Poitiers, Poitiers, France
Acanthomorpha (spiny-rayed fishes) is a clade of teleosts that includes more than
15, 000 extant species. Their deep phylogenetic intrarelationships, first reconstructed
using morphological characters, have been extensively revised with molecular data.
Moreover, the deep branches of the acanthomorph tree are still largely unresolved, with
strong disagreement between studies. Here, we review the historical propositions for
acanthomorph deep intrarelationships and attempt to resolve their earliest branching
patterns using a new morphological data matrix compiling and revising characters
from previous studies. The taxon sampling we use constitutes a first attempt to
test all previous hypotheses (molecular and morphological alike) with morphological
data only. Our sampling also includes Late Cretaceous fossil taxa, which yield new
character state combinations that are absent in extant taxa. Analysis of the complete
morphological data matrix yields a new topology that shows remarkable congruence
with the well-supported molecular results. Lampridiformes (oarfishes and allies) are the
sister to all other acanthomorphs. Gadiformes (cods and allies) and Zeiformes (dories)
form a clade with Percopsiformes (trout-perches) and the enigmatic Polymixia (beardfish)
and Stylephorus (tube-eye). Ophidiiformes (cusk-eels and allies) and Batrachoidiformes
(toadfishes) are nested within Percomorpha, the clade that includes most of modern
acanthomorph diversity. These results provide morphological synapomorphies and
independent corroboration of clades previously only recovered from molecular data,
thereby suggesting the emergence of a congruent picture of acanthomorph deep
intrarelationships. Fossil taxa play a critical role in achieving this congruence, since a
very different topology is found when they are excluded from the analysis.
Keywords: Acanthomorpha, Teleostei, Actinopterygii, morphological phylogeny, Lampridiformes, Gadiformes,
Zeiformes, Percomorpha

Davesne et al. Intrarelationships of Spiny-Rayed Fishes
INTRODUCTION
Nearly one third of modern vertebrate diversity is contained
within Acanthomorpha, a group of teleosts (Teleostei,
Actinopterygii) collectively known as the spiny-rayed fishes
(Rosen, 1973; Nelson et al., 2016). The more than 15,000
acanthomorph species occupy every aquatic environment, with
a strong preponderance in marine ecosystems. The phenotypic
diversity of acanthomorphs is considerable: They include such
widely divergent morphotypes as seahorses (Syngnathidae),
flatfishes (Pleuronectiformes), pufferfishes (Tetraodontiformes),
flying fishes (Exocoetidae), and oarfishes (Regalecidae). Several
important model organisms such as the medaka (Oryzias latipes),
the fugu (Takifugu rubripes), and the stickleback (Gasterosteus
aculeatus) are also part of the group (Chen et al., 2004).
Deciphering acanthomorph phylogeny is then crucial for better
understanding patterns and mechanisms of diversification
in vertebrates. However, it has proven difficult to resolve, as
was pointed out in pioneering phylogenetic studies based on
morphology (Greenwood et al., 1966; Rosen, 1973; Stiassny,
1986; Patterson and Rosen, 1989; Johnson and Patterson, 1993).
Subsequent molecular phylogenetic studies have significantly
impacted acanthomorph phylogeny (Wiley et al., 2000; Miya
et al., 2001, 2003; Chen et al., 2003, 2014; Dettai and Lecointre,
2005; Li et al., 2009; Broughton, 2010; Betancur-R et al., 2013;
Grande et al., 2013; Near et al., 2013; Malmstrøm et al., 2016),
triggering the emergence of some new and increasingly stable
patterns of relationships. However, many parts of the tree
remain poorly resolved, notably for the deep intrarelationships
of acanthomorphs, corresponding to a phase of diversification
that occurred before the end-Cretaceous mass extinction event
(Patterson, 1993; Friedman, 2010).
CONTEXT OF THE STUDY
Contribution of Morphology to
Acanthomorph Phylogeny
In the late 1960s and 1970s, pioneering studies of morphological
characters began to organize acanthomorph classification with
a phylogenetic scope. Such was the case of Greenwood
et al. (1966),Rosen and Patterson (1969), and Rosen (1973),
the latter naming the clade Acanthomorpha for the first
time. Along with subsequent works by Stiassny (1986) and
Patterson and Rosen (1989), these successive studies contributed
greatly to our present knowledge of acanthomorph evolution,
notably by proposing major acanthomorph clades supported
by morphological synapomorphies. Computed phylogenetic
analyses of acanthomorphs based on taxon-by-character matrices
began to be available in the 1990s, with studies by Stiassny
and Moore (1992) and Johnson and Patterson (1993) who
proposed a comprehensive hypothesis for deep acanthomorph
intrarelationships (Figure 1A). Wiley et al. (2000) proposed
a phylogenetic analysis using combined morphological and
molecular data. Their morphological dataset is essentially based
on Johnson and Patterson’s, and their tree topology based on
anatomical data alone (Wiley et al., 2000, Figure 8A—and
not Figure 8C as stated in the article) does not contradict
the original study because of a mere lack of resolution.
Springer and Orrell (2004) explored acanthomorph relationships
through the gill-muscle characters only, yielding a different
topology that is weakly supported by their data. Mirande
(2016) analyzed a large dataset of combined molecular and
morphological data covering the diversity of actinopterygians
(including acanthomorphs). However, this work does not include
an analysis of morphological data alone; moreover, at the level
of deep acanthomorph relationships, the parsimonious tree
obtained from the analysis of molecular data alone does not differ
from the proposed final hypothesis obtained with combined data,
which suggests that morphological data did not fundamentally
influence the combined topology. Other phylogenetic analyses
using morphology alone were either based on a smaller subset
of acanthomorphs, for example Gadiformes (Endo, 2002; Grand
et al., 2014), Percopsiformes and related taxa (Murray and
Wilson, 1999) and Zeiformes (Tyler et al., 2003; Tyler and Santini,
2005), or were centered on early fossil taxa (Otero et al., 1995;
Otero and Gayet, 1996; Alvarado-Ortega and Than-Marchese,
2012; Davesne et al., 2014; Delbarre et al., 2016). Thus, to date no
morphological dataset has been capable of challenging the results
of Johnson and Patterson (1993) (Figure 1A).
Current Knowledge of Deep
Acanthomorph Intrarelationships
Since the beginning of the twenty-first century, molecular
phylogenetic studies have significantly revised acanthomorph
phylogeny, including the deep intrarelationships at the base of the
tree (Figure 1B). Acanthomorph phylogeny based on molecular
data is simultaneously: (1) significantly different from what
was proposed by the morphological data alone; (2) increasingly
stable, due the repetition of some results from one independent
study to another, and using different sets of markers; (3) still
largely unresolved because the different molecular datasets have
consistently diverged on many key points (Figure 1B).
Acanthomorph Monophyly
The taxa currently grouped under the name Acanthomorpha
were initially treated as three distinct groups (Greenwood
et al., 1966): Paracanthopterygii (see below), Atherinomorpha
(including killifishes, flying fishes, needlefishes, silversides, etc.),
and Acanthopterygii (centered on “perciforms”). These three
groups were later united in Acanthomorpha, on the basis of the
presence of true spines in dorsal, anal and sometimes pelvic fins
(Rosen, 1973). Subsequent studies corroborated acanthomorph
monophyly by adding morphological synapomorphies for
the clade (Rosen, 1985; Stiassny, 1986; Stiassny and Moore,
1992; Johnson and Patterson, 1993). Molecular data, however,
are much more ambiguous regarding the monophyly of
Acanthomorpha. While acanthomorph monophyly has
been supported by studies based on combined nuclear and
mitochondrial markers (Wiley et al., 2000; Dettai and Lecointre,
2005; Grande et al., 2013), mitochondrial genomes (Broughton,
2010), and large datasets of multiple nuclear markers (Near
et al., 2012, 2013; Betancur-R et al., 2013; Faircloth et al.,
2013; Malmstrøm et al., 2016), it has also been questioned
by studies based on mitochondrial (Colgan et al., 2000; Miya
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Davesne et al. Intrarelationships of Spiny-Rayed Fishes
FIGURE 1 | Consensus of the phylogenetic hypotheses for Acanthomorpha, summarizing previously published results. (A) Morphological hypothesis
(Patterson and Rosen, 1989; Johnson and Patterson, 1993; Olney et al., 1993). (B) Molecular hypothesis based on the latest large-scale acanthomorph datasets
(Miya et al., 2005, 2007; Broughton, 2010; Betancur-R et al., 2013; Grande et al., 2013; Near et al., 2013; Chen et al., 2014).
et al., 2001, 2003, 2005, 2007; Poulsen et al., 2013), combined
(Chen et al., 2003, 2014; Mirande, 2016) and nuclear (Li
et al., 2008; species tree of Faircloth et al., 2013) datasets. In
the latter case, Lampridiformes (opahs, oarfishes and allies;
Figure 2C), at least, form a clade with Myctophiformes (the
lanternfishes; Figure 2B), considered as the extant sister group
to acanthomorphs on the basis of morphology (Rosen, 1973;
Stiassny, 1986, 1996; Johnson, 1992). This uncertainty about
acanthomorph monophyly is probably linked to the uncertainty
about the position of Lampridiformes: They have been assigned
to almost every possible position within the acanthomorph tree
in the successive molecular studies, often associated with low
support values (Davesne et al., 2014).
Unresolved Position for Polymixiiformes and
Percopsiformes
Other acanthomorph groups also have a very variable position
from one study to another. Polymixiiformes (represented today
only by the genus Polymixia, beardfishes; Figure 2D) has been
classified in Beryciformes (Greenwood et al., 1966) and possibly
Paracanthopterygii (Rosen and Patterson, 1969). However, the
latest anatomical studies supported Polymixiiformes as an
isolated lineage (Figure 1A), sister to all other acanthomorphs
except for Lampridiformes (Stiassny and Moore, 1992; Johnson
and Patterson, 1993). Percopsiformes (trout-perches and allies;
Figures 2E,F) has been consistently supported as part of
Paracanthopterygii (see below and Figure 1A) by anatomists
(Gosline, 1963; Rosen and Patterson, 1969; Patterson and Rosen,
1989; Murray and Wilson, 1999). Mitochondrial data support
Percopsiformes and Polymixia as closely related to Gadiformes-
Zeiformes, either as sequential sister groups (Miya et al., 2003;
Broughton, 2010), or forming a clade together (Miya et al.,
2005, 2007; Dillman et al., 2011). Studies based on either
nuclear markers, or a combination of nuclear and mitochondrial
markers, have suggested different positions for these two taxa:
Either sequential sister groups to Gadiformes-Zeiformes (Dettai
and Lecointre, 2005; Grande et al., 2013; Chen et al., 2014) or
to Lampridiformes (Li et al., 2009), sister to Acanthopterygii
for Polymixia and to Gadiformes-Zeiformes for Percopsiformes
(Betancur-R et al., 2013), or forming together a clade which
is in turn sister to all other acanthomorphs (Near et al., 2013;
Malmstrøm et al., 2016). The phylogenetic position of these two
taxa is, therefore, far from being settled on the basis of current
data (Figure 1B).
Composition of Paracanthopterygii
According to its first delimitation (Greenwood et al.,
1966), Paracanthopterygii was a series of teleosts sister
to Acanthopterygii, and including Percopsiformes,
Batrachoidiformes (toadfishes; Figure 2L), Gobiesociformes
(clingfishes), Lophiiformes (anglerfishes), Gadiformes (cods,
hakes and allies; Figure 2H), Ophidiiformes (cusk-eels and allies;
Figure 2J), and Zoarcoidei (eelpouts).
Rosen and Patterson (1969) proposed a list of characters
supporting Paracanthopterygii, which they later revised
and completed (Patterson and Rosen, 1989). In their
definition, Paracanthopterygii only includes Percopsiformes,
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Davesne et al. Intrarelationships of Spiny-Rayed Fishes
FIGURE 2 | Examples of species from the taxa studied. (A) Aulopiformes, Synodus saurus, MNHN/SBMC uncataloged. (B) Myctophiformes, Myctophum
punctatum, MNHN/SBMC uncataloged. (C) Lampridiformes, Lampris guttatus, SBMC 2004-0006. (D) Polymixiiformes, Polymixia lowei, NOAA uncataloged. (E)
Percopsiformes, Aphredoderus sayanus, painting. (F) Percopsiformes, Percopsis omiscomaycus, painting. (G) Stylephoriformes, Stylephorus chordatus,
MNHN.IC.2004-1316. (H) Gadiformes, Pollachius pollachius, MNHN/SBMC uncataloged. (I) Zeiformes, Zeus faber, MNHN/SBMC uncataloged. (J) Ophidiiformes,
Cataetyx laticeps, MNHN/SBMC uncataloged. (K) Beryciformes, Hoplostethus mediterraneus, MNHN/SBMC uncataloged. (L) Batrachoidiformes, Halobatrachus
didactylus, MNHN/SBMC uncataloged. (M) Beryciformes, Sargocentron hastatum, MNHN 2013-0848. (N) Percomorpha, Dicentrarchus labrax, MNHN/SBMC
uncataloged. Abbreviations: adf, adipose fin; sdf, spinous first dorsal fin. Scale bar equals 10 mm (A,B,D–F), 50 mm (G–N), 100 mm (C). Sizes are based on
specimen measurements, or on the “common length” measure given in FishBase (D-F). Photos D. Davesne (G), courtesy of Iglésias (2014) (A,B, H–N), NOAA (D) and
Wikimedia Commons (D,E).
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Davesne et al. Intrarelationships of Spiny-Rayed Fishes
Batrachoidiformes, Lophiiformes, Gadiformes, and
Ophidiiformes (Figure 1A). This assemblage has been
controversial since its inception, and most of its constituent taxa
have been excluded from it at one point or another on the basis
of their anatomy (Gosline, 1968; Fraser, 1972; Gill, 1996; Chanet
et al., 2013; Grande et al., 2013). Moreover, molecular data have
consistently shown the polyphyly of Paracanthopterygii sensu
Patterson and Rosen (see below for details), implying that the
delimitation of the group should be comprehensively reassessed.
Gadiformes-Zeiformes Clade
Gadiformes have always been part of Paracanthopterygii since
the first definition of the group (Greenwood et al., 1966;
Rosen and Patterson, 1969; Patterson and Rosen, 1989).
Zeiformes (dories; Figure 2I) were considered as close relatives
of Tetraodontiformes (triggerfishes, pufferfishes, and allies) and
Caproidae (boarfishes) in the first detailed study of their position
amongst acanthomorphs (Rosen, 1984). Later on, studies
including a larger sampling of acanthomorph representatives
suggested that Zeiformes lies within Acanthopterygii, but outside
Percomorpha (Stiassny and Moore, 1992; Johnson and Patterson,
1993). Subsequent analyses (Tyler et al., 2003; Tyler and
Santini, 2005) provided arguments for the monophyly and
intrarelationships of Zeiformes, while once again proposing a
clade that unites them with Tetraodontiformes and Caproidae.
Since their earliest attempts at resolving acanthomorph
phylogeny, studies based on molecular datasets have suggested a
very different position for both orders (Figure 1B) by supporting
a Gadiformes-Zeiformes clade (Wiley et al., 2000; Miya et al.,
2001, 2003; Chen et al., 2003; Dettai and Lecointre, 2004,
2005). The subsequent molecular studies have also consistently
supported this clade (Li et al., 2009; Near et al., 2012, 2013;
Betancur-R et al., 2013; Grande et al., 2013; Chen et al., 2014;
Malmstrøm et al., 2016).
Despite some early claims (Wiley et al., 2000), this grouping
(or, at least, an inclusion of Zeiformes within Paracanthopterygii)
had already been anticipated by some morphologists (Gaudant,
1979; Gayet, 1980a,b; Gill, 1996). This hypothesis seems to indeed
be supported by numerous morphological characters (Borden
et al., 2013; Grande et al., 2013), but has never been formally
tested by a comprehensive morphological phylogenetic analysis.
Stylephorus Outside Lampridiformes
Stylephorus chordatus (the tube-eye; Figure 2G) is a distinctive
mesopelagic acanthomorph with an elongate body, a reduced
caudal fin, and extremely modified jaws forming a protrusible
tube-like feeding device. Several interpretations have prevailed
regarding the position of Stylephorus—including possible
affinities with “amphibians” rather than with teleosts according
to its original describer in 1791 (Pietsch, 1978)—but once the
discovery of more specimens allowed for further investigations
on its morphology, it was included in Lampridiformes (Regan,
1908, 1924; Starks, 1908). Stylephorus was classified within
the lampridiform suborder Taeniosomi (Figure 1A), alongside
Radiicephalus, Lophotidae, Trachipteridae, and Regalecidae in
subsequent works (Oelschläger, 1983; Olney, 1984; Olney et al.,
1993).
The first molecular (mitogenomic) phylogenetic analysis that
includes this species (Miya et al., 2007) proposed a different
position for Stylephorus, within the Gadiformes-Zeiformes clade
(Figure 1B). This result has been corroborated subsequently in
every other analysis of mitochondrial and nuclear markers (Near
et al., 2012, 2013; Betancur-R et al., 2013; Grande et al., 2013;
Malmstrøm et al., 2016), and by the shared loss of the immune
system’s Mx gene (Solbakken et al., 2016). This new arrangement
has also been supported (Grande et al., 2013) and opposed
(Roberts, 2012) on the basis of morphology, each time without
a comprehensive phylogenetic analysis.
The Status of Beryciformes
Beryciformes has been variably interpreted over time. Initially,
it was viewed as a paraphyletic assemblage of acanthopterygians
(Patterson, 1964; Greenwood et al., 1966). Later studies
(Johnson and Patterson, 1993; Patterson, 1993) have supported a
monophyletic Beryciformes that includes Berycidae (alfonsinos),
Trachichthyidae (roughies; Figure 2K), Holocentridae
(soldierfishes and squirrelfishes; Figure 2M), and other
related families. Stephanoberyciformes (deep sea taxa such
as ridgeheads, whalefishes, and pricklefishes) was regarded as
either an independent order (Johnson and Patterson, 1993),
or included in Beryciformes (Moore, 1993). In these studies,
Beryciformes was seen as the sister group to percomorphs
within Acanthopterygii (Figure 1A). At least one anatomical
study, using characters of the pelvic girdle, challenged the
monophyly of Beryciformes by recovering holocentrids as closer
to percomorphs than to other beryciforms (Stiassny and Moore,
1992).
Molecular studies have supported diverse arrangements
for Beryciformes (Figure 1B). They have been resolved as
monophyletic, either excluding (Wiley et al., 2000) or including
Stephanoberyciformes (Miya et al., 2001, 2005; Near et al., 2012,
2013; Grande et al., 2013), or as paraphyletic (Colgan et al., 2000;
Li et al., 2009; Betancur-R et al., 2013; Chen et al., 2014).
Ophidiiformes and Batrachoidiformes in
Percomorpha
The inclusion of Ophidiiformes and Batrachoidiformes in
Paracanthopterygii is consistently rejected by molecular studies
(Wiley et al., 2000; Miya et al., 2003, 2005; Li et al., 2009; Near
et al., 2012, 2013; Betancur-R et al., 2013; Chen et al., 2014).
According to these studies, they are included in Percomorpha,
as successive sister groups to all other percomorphs (Figure 1B).
The same studies consistently group Lophiiformes with
Tetraodontiformes instead of Batrachoidiformes (Miya et al.,
2003; Dettai and Lecointre, 2005; Yamanoue et al., 2007; Holcroft
and Wiley, 2008; Betancur-R et al., 2013; Near et al., 2013), and at
least some anatomical data also support this hypothesis (Chanet
et al., 2012, 2013).
Aims of the Study
Within the new phylogenetic framework brought by molecular
studies, it is time to revisit the large-scale acanthomorph
intrarelationships with morphological data, to address the
following issues: (1) are the morphological data adequate to
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Davesne et al. Intrarelationships of Spiny-Rayed Fishes
robustly resolve deep phylogenetic divergences; (2) are the
topologies supported by these data congruent with previous
hypotheses supported by morphological (Figure 1A), molecular
data (Figure 1B) or neither; (3) do fossil taxa have an impact on
the topology?
The sampling we use allows testing all previous phylogenetic
hypotheses, morphological as well as molecular. This was not
the case of the previous studies based on morphology, which
used a reduced subset of acanthomorph diversity, not including
some key taxa. For example, Gadiformes, Batrachoidiformes,
and Ophidiiformes were all absent from the matrix of Johnson
and Patterson (1993). Our sampling also includes fossil taxa
from the Late Cretaceous; that is, amongst the oldest known
acanthomorphs. They are expected to display character state
combinations that are absent in extant taxa. A number of
previous studies have stressed the importance of fossil taxa for
phylogenetic inference (Gauthier et al., 1988; Donoghue et al.,
1989; Cobbett et al., 2007), including in acanthomorphs (Santini
and Tyler, 2004; Davesne et al., 2014). The experimental design
of the present study permits us to estimate the influence of fossils
on the results by analyzing the dataset with and without them.
MATERIALS AND METHODS
Taxon Sampling
Our taxon sample includes 26 taxa, of which 19 are extant.
Synodus and Gymnoscopelus represent Aulopiformes
(lizardfishes; Figure 2A) and Myctophiformes (lanternfishes;
Figure 2B), respectively. Together, they represent two of
the closest extant acanthomorph relatives, according to the
morphological (Rosen, 1985; Stiassny, 1986, 1996; Johnson and
Patterson, 1993) and most molecular evidence (Broughton, 2010;
Near et al., 2012, 2013; Betancur-R et al., 2013; Grande et al.,
2013). The inclusion of a myctophiform in the analysis allows
testing the alternative hypothesis of acanthomorph polyphyly
(see above).
Our sampling of extant acanthomorphs includes at least
one representative for each of the groupings identified by both
molecular and morphological data (Figure 1). Thus, the minimal
taxonomic coverage that is needed to test the various topologies
found in the literature is included. Its focus is on the main
relationships between acanthomorph clades and some portions
of the acanthomorph tree are not covered enough to resolve their
relationships (e.g., percomorphs). Further, more detailed studies
would be needed to address these other phylogenetic questions.
Velifer,Lampris, and Regalecus represent Lampridiformes;
and Stylephorus has been included, in order to test its position
among Lampridiformes or other acanthomorphs. Polymixia
represents Polymixiiformes. Aphredoderus and Percopsis
(for Percopsiformes), Merluccius and Bregmaceros (for
Gadiformes), Halobatrachus (for Batrachoidiformes) and
Brotula (for Ophidiiformes) allow testing the composition of
the Paracanthopterygii, as defined by Patterson and Rosen
(1989). We did not include Lophiiformes, because all molecular
data and some anatomical evidence suggest a deeply nested
position within Percomorpha. Zeus and Cyttus are added in
order to test the proposed Gadiformes+Zeiformes relationship.
A trachichthyid (Hoplostethus) and a holocentrid (Sargocentron)
represent Beryciformes sensu lato. The inclusion of these both
families leaves open the possibility of recovering a paraphyletic
Beryciformes, as suggested by some studies (Stiassny and Moore,
1992; Betancur-R et al., 2013). Dicentrarchus and Lates represent
‘generalized’ representatives of Percomorpha, which do not
show extreme morphological specializations that could hinder
phylogenetic reconstruction.
The seven fossil taxa (Figure 3) have been chosen for
their potential phylogenetic positions (as suggested by previous
studies) that span the entire tree. †Ctenothrissa, from the
Cenomanian (Late Cretaceous) of England and Lebanon
(Figure 3A), was described as either a stem-acanthomorph
(Patterson, 1964) or a stem-ctenosquamate (Gaudant, 1978,
1979). The affinities of †Pycnosteroides, from the Cenomanian of
Hajula, Lebanon (Figure 3C), have been interpreted differently
depending on the authors, owing to its singular character
state combination. According to previous phylogenetic analyses,
†Pycnosteroides is a member of Lampridomorpha (Davesne
et al., 2014; Delbarre et al., 2016), alongside with †“Aipichthys”
(Figure 3B) and †Aipichthyoides (both from the Cenomanian
of Near East and England). In the present study, the character
coding for †“Aipichthys” was based on the species †“A.”
minor and †“A.”velifer, which are phylogenetically distinct
from †A. pretiosus, the type species of the genus (Delbarre
et al., 2016). †Sphenocephalus, from the Campanian (Upper
Cretaceous) of Germany, (Figure 3D) has been described as a
paracanthopterygian, closely related to at least Percopsiformes
and Gadiformes (Rosen and Patterson, 1969; Patterson and
Rosen, 1989; Murray and Wilson, 1999; Grande et al., 2013;
Davesne et al., 2014). †Omosomopsis, from the Cenomanian of
Jbel Tselfat, Morocco (Figure 3E), has been interpreted as a
polymixiiform (Patterson, 1993; Taverne, 2011), but some of its
characters suggest a close relationship to paracanthopterygians
(Otero and Gayet, 1996). †Stichocentrus, from the Cenomanian
of Hajula, Lebanon (Figure 3F), is a probable beryciform
that has been regarded as related to modern holocentrids
(Gayet, 1980c, 1982). It has been chosen amongst numerous
other, closely related coeval taxa, because it has been well-
described morphologically (Patterson, 1967; Gayet, 1980c) and
proposed as a fossil calibration point for divergence-time
analyses of acanthomorph phylogeny (Benton et al., 2015).
All the fossils in our sampling come from Late Cretaceous
deposits, more specifically from the Cenomanian (with the
exception of †Sphenocephalus, found exclusively in Campanian
deposits). In consequence, they are coeval with the oldest known
acanthomorph body fossils (Patterson, 1993).
Character Coding
The morphological characters were observed on dissections and
dry osteological preparations, or on fluid-preserved specimens
housed in public collections (Appendix 1 in Supplementary
Material). When preserved in fluid, the specimens were X-ray
tomographed (GE Phoenix v-tome-x L240, microfocus 240 kV
at the AST-RX platform, Muséum national d’Histoire naturelle,
Paris) and the skeleton was virtually reconstructed in 3D by
means of the Mimics software (version 17.0 64-bit). The list
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Davesne et al. Intrarelationships of Spiny-Rayed Fishes
FIGURE 3 | Six of the seven fossil taxa used in the analyses. (A) †Ctenothrissa signifer, NHMUK PV P47524. (B) †’Aipichthys’velifer, MNHN.F.HAK57. (C)
†Pycnosteroides levispinosus, MNHN.F.HDJ105. (D) †Sphenocephalus fissicaudus, NHMUK PV P9059. (E) †Omosomopsis simum, MNHN.F.DTS222d. (F)
†Stichocentrus liratus, MNHN.F.HDJ97. Scale bar equals 10 mm (A–D,F), 5 mm (E). Photos by D. Davesne, C. Lemzaouda, and P. Loubry.
of specimens used in the study is provided in Appendix 1 of
Supplementary Material. We coded the remaining taxa by using
data from the literature (e.g., ´
Swidnicki, 1991; Otero, 2004).
The morphological characters that we use for our phylogenetic
analyses (Appendix 2 in Supplementary Material) are mostly
compiled from previous studies (Stiassny, 1986; Patterson
and Rosen, 1989; Stiassny and Moore, 1992; Johnson and
Patterson, 1993; Otero and Gayet, 1996; Grande et al., 2013).
Almost all characters are coded from the skeleton. The
resulting data matrix (Supplementary Table 1) contains 26 taxa
and 66 characters. It is available in electronical version on
MorphoBank (O’Leary and Kaufman, 2011, 2012), project 2349
(http://morphobank.org/permalink/?P2349). There is 7.58% of
missing data, noted as “?” in the matrix. Most of them are
due to incomplete preservation of fossil taxa. 5.24% of the
character states are scored as inapplicable. They are noted
as “–” in the matrix and are mainly a consequence of
the coding strategy used for characters 2–3, 31–32, 35–36,
and 65–66. Character 24 is the only one to be parsimony-
uninformative.
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Davesne et al. Intrarelationships of Spiny-Rayed Fishes
Phylogenetic Analyses
We performed three phylogenetic analyses. Analysis 1 is a
simultaneous analysis of all 26 taxa of our sampling, Analysis
2 includes the 19 extant taxa only, and Analysis 3 includes
the seven fossil taxa only. Analysis 2 and Analysis 3 allow us
to estimate the impact of fossil taxa on the results. Character
polarity was determined by the outgroup criterion. Trees were
rooted with the aulopiform Synodus in Analyses 1 and 2, because
every morphological and molecular study to date has recovered
Aulopiformes outside of Acanthomorpha. The trees were rooted
with †Ctenothrissa (as the only fossil taxon in our dataset that
is not a crown-acanthomorph) in the third analysis. In all
analyses, every character was treated as unordered. The character
matrix was submitted to parsimony analyses using both PAUP∗
version 4.0a147 (Swofford, 2002) and TNT version 1.1 (Goloboff
et al., 2008). With PAUP∗, we performed a heuristic search with
a random addition sequence and the "TBR" branch-swapping
algorithm (10000 replicates, holding 10 trees at each step). With
TNT we performed a new technology search with the default
parameters for sectorial search, ratchet (10 iterations), drift (10
cycles) and tree-fusing, and hitting minimal tree length 100 times.
We also used TNT to run 1000 replicates of a bootstrap analysis
retaining all clades found with a frequency ≥50%, and to estimate
the Bremer support values.
RESULTS
The results of all analyses are identical whether PAUP∗or TNT
is used. The simultaneous analysis of the extant and fossil taxa
(Analysis 1) yielded one parsimonious tree, with a length of
198 steps, a consistency index (CI) of 0.419 and a retention
index (RI) of 0.684 (Figure 4). The consistency and retention
indexes of each character after this analysis are presented in the
Supplementary Table 2.
The tree shows †Ctenothrissa as a sister to Acanthomorpha,
which include three main clades: (1) a clade Lampridomorpha
(sensu Davesne et al., 2014) including †“Aipichthys,”
†Aipichthyoides,Velifer,Lampris and Regalecus, but not
†Pycnosteroides; (2) a clade (“Clade A”) that includes beryciforms
in paraphyly with Percomorpha (sensu Wiley and Johnson, 2010;
Betancur-R et al., 2014) which, in turn, includes Dicentrarchus
and Lates as sequential sister groups to Batrachoidiformes
(Halobatrachus) and Ophidiiformes (Brotula); (3) a clade (“Clade
B”) that includes †Pycnosteroides,Polymixia,†Omosomopsis,
†Sphenocephalus, and Percopsiformes as sequential sister groups
to a clade that unites Gadiformes, Zeiformes, and Stylephorus.
Lampridomorpha is sister to all remaining acanthomorphs.
Analysis 2 (extant taxa only) yielded four parsimonious
trees with a length of 166 steps, a CI of 0.482 and a RI of
0.676 (Figure 5A). It shows a largely incongruent topology:
Polymixia and Percopsiformes are sister groups to the other
acanthomorphs, including the Clade A of Analysis 1 in paraphyly
with Zeiformes, Gadiformes and “traditional” Lampridiformes
(including Stylephorus).
Analysis 3 (fossil taxa only) yielded one parsimonious
tree with a length of 43 steps, a CI of 0.791 and a RI of
0.609 (Figure 5B). The topology is entirely compatible with
that of Analysis 1, with †Pycnosteroides,†Omosomopsis, and
†Sphenocephalus grouped together and forming a clade with
†Stichocentrus, while †’Aipichthys’ and †Aipichthyoides form
another clade.
The relatively low trees’ retention indexes, bootstrap values
and Bremer supports for most clades (Figures 4,5) reflect the
relatively high level of homoplasy in the dataset. For instance,
in Analysis 1 only 15 characters (23% of the total) have a RI of
1.000, representing uniquely derived characters (Supplementary
Table 2).
DISCUSSION
Acanthomorph Intrarelationships
The three main clades recovered by Analysis 1 have been
given various names in different classifications, even when
their taxonomic content is essentially the same (Johnson and
Patterson, 1993; Wiley and Johnson, 2010; Betancur-R et al.,
2014; Nelson et al., 2016). In order to maintain clarity in the
discussion, we give the following provisional names to these
clades:
- Lampridomorpha: Lampridiformes and their extinct close
relatives (sensu Davesne et al., 2014);
- Clade A: “Beryciformes” and Percomorpha (including
Ophidiiformes and Batrachoidiformes). This clade is either
named Euacanthopterygii (Johnson and Patterson, 1993),
Acanthopterygii (Nelson et al., 2016), or Euacanthomorphacea
(Betancur-R et al., 2014);
- Clade B: Polymixiiformes, Percopsiformes, Gadiformes,
Zeiformes, Stylephorus, and their extinct close relatives. This
assemblage is alternatively named Paracanthopterygii (Grande
et al., 2013; Nelson et al., 2016) or Paracanthomorphacea
(Betancur-R et al., 2013, 2014).
These three clades are unambiguously recovered by our Analysis
1, but the support values of Clades A and B are relatively
low (Figure 4). Further anatomical work (including on “soft”
tissues) on character distribution and homology would be needed
in order to find supplementary synapomorphies for the clades
recovered by this study. Adding more representative taxa for each
acanthomorph group could also prove valuable to increase the
support of these deep relationships.
Acanthomorph Monophyly
We recovered the clade Acanthomorpha in the two analyses
that tested its monophyly (Figures 4,5A). With Analysis
1, Acanthomorpha is supported by three unambiguous
synapomorphies: The presence of unpaired and unsegmented
spines (Figures 6A,B) on the dorsal (351) and anal fins (401),
and the contact between the lateral ethmoids and the vomer (81;
Figure 6C). All three characters were previously used to define
Acanthomorpha (Stiassny, 1986; Johnson and Patterson, 1993).
†Ctenothrissa is recovered as sister to crown-acanthomorphs,
in a position that somehow reflects Patterson’s (1964) ideas
but contradicts later studies (Gaudant, 1978, 1979; Davesne
et al., 2014). This topology, while well-supported by our data,
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Davesne et al. Intrarelationships of Spiny-Rayed Fishes
FIGURE 4 | Parsimonious tree obtained from Analysis 1 (complete analysis, extant and fossil taxa). Length =198, CI =0.419, RI =0.684. Support values
are above branches: Bremer indexes (bigger font)/bootstrap values (italics). Unambiguous synapomorphies are below branches.
should be taken with caution, since the sampling of non-
acanthomorph taxa is too limited to ensure a definitive placement
of †Ctenothrissa. The four unambiguous synapomorphies of
this †Ctenothrissa +Acanthomorpha clade also characterize
acanthomorphs if fossils are not taken into account:
- The loss of the adipose fin (391), implying the independent
re-acquisition of this attribute in modern Percopsiformes
(Figure 2F);
- The anterior position of the pelvic girdle (571). A
“trend” toward an anterior migration of the pelvic fin
in acanthomorphs was already described by Greenwood
et al. (1966), and later more in details by Stiassny
and Moore (1992) and Parenti and Song (1996). More
specifically, it is redefined here as the pelvic girdle inserting
anterior to the ventral tip of the distal postcleithrum
(Figure 6B);
- Two characters that have been previously optimized as
synapomorphies of Lampridomorpha (Davesne et al., 2014):
The pelvic girdle contacts the pectoral girdle at the level of the
coracoids (582), and the hyomandibula bears only one articular
head with the cranium (171)—both of these characters undergo
numerous reversions within Acanthomorpha.
Finally, two synapomorphies are ambiguous for Acanthomorpha
because there is no data regarding their presence in
†Ctenothrissa. Nonetheless, they are unique to acanthomorphs
if only extant taxa are considered. These are the close bonding
between the dorsal limb of the posttemporal and the epioccipital
(131) and the presence of facets on the first vertebral centrum for
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Davesne et al. Intrarelationships of Spiny-Rayed Fishes
FIGURE 5 | (A) Strict consensus of the four parsimonious trees obtained from Analysis 2 (extant taxa only). Length =166, CI =0.482, RI =0.676. (B) Tree obtained
from Analysis 3 (fossil taxa only). Length =43, CI =0.791, RI =0.609. The clade names on the right refer to the results of Analysis 1 (Figure 4). Support values are
above branches: Bremer indexes (bigger font)/bootstrap values (italics). Unambiguous synapomorphies are below branches.
its articulation with exoccipital condyles (281). Both characters
were already regarded as acanthomorph synapomorphies
(Rosen, 1985; Stiassny, 1986).
With these nine synapomorphies in total, our study strongly
supports the monophyly of Acanthomorpha, in accordance with
earlier anatomical works (Stiassny and Moore, 1992; Johnson and
Patterson, 1993; Davesne et al., 2014) and with most molecular
studies based on nuclear markers (Betancur-R et al., 2013;
Faircloth et al., 2013; Near et al., 2013) and in contradistinction to
most of the molecular studies using part or all of the mitogenome
(Miya et al., 2003, 2005; Chen et al., 2014; Mirande, 2016).
Position of Lampridiformes
Analysis 1 recovered Lampridomorpha (with lampridiforms
as its only extant members) as the sister group to all other
acanthomorphs (Clade A +Clade B). This topology is usually
recovered by morphology (Johnson and Patterson, 1993; Davesne
et al., 2014) but is poorly supported by molecular data, both
within datasets (associated support values are often low) and
from one study to another. This suggests that incongruence in
the phylogenetic positions of Lampridiformes might be driven
by sampling or branch-length artifacts rather than by a strong
phylogenetic support.
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Davesne et al. Intrarelationships of Spiny-Rayed Fishes
FIGURE 6 | Examples of acanthomorph synapomorphies. (A) Relative positions of the pelvic and pectoral girdle (left), and dorsal fin (right) of a
non-acanthomorph, Myctophum nidulum, MNHN.IC.1993.2333. (B) Relative positions of the pelvic and pectoral girdle (left), dorsal fins (right), and anal fin (below) of
an acanthomorph, Dicentrarchus labrax, MNHN uncataloged. (C) Ethmoid region of an acanthomorph, Sparus aurata, MNHN uncataloged. Abbreviations: afr, anal-fin
soft rays; afsp, anal-fin spines; apt, anal pterygiophore; cl, cleithrum; co, coracoid; dfr, dorsal-fin soft rays; dfsp, dorsal-fin spines; dpcl, distal postcleithrum; dpt,
dorsal pterygiophores; leth, lateral ethmoid; meth, mesethmoid; pcfr, pectoral-fin rays; pcr, pectoral radials; pvg, pelvic girdle; pvfr, pelvic-fin rays; sc, scapula; sn,
supraneurals; vo, vomer. Scale bar equals 1 mm (A,B), 10 mm (C). C&S preparations N. K. Schnell. Photos D. Davesne and N. K. Schnell.
In the present study, two synapomorphies unambiguously
support the monophyly of (Clade A +Clade B):
- The premaxilla bears a postmaxillary process (21), which
is absent in lampridomorphs and non-acanthomorphs
(Figure 7A);
- The supraoccipital bears a spina occipitalis (161) that separates
exoccipitals medially and reaches the dorsal roof of the
foramen magnum. The spina occipitalis is absent in all
modern Lampridiformes, while the state is unknown in fossil
lampridomorphs.
Position and Status of Polymixiiformes
According to Analysis 1, Polymixia is included in Clade B,
sister to the clade formed by Percopsiformes, Gadiformes,
Stylephorus, and Zeiformes, echoing the molecular analyses that
include mitochondrial data (Miya et al., 2003, 2005; Broughton,
2010; Chen et al., 2014). Clade B also includes the fossil taxa
†Omosomopsis and †Pycnosteroides (Figure 4).
The interpretation of †Pycnosteroides varies considerably
between authors. It has been referred to as a member of
Beryciformes (Patterson, 1964; Gayet, 1980c), Polymixiiformes
(Taverne, 2011; Murray and Wilson, 2014), Acanthomorpha
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Davesne et al. Intrarelationships of Spiny-Rayed Fishes
FIGURE 7 | Examples of synapomorphies for Gadiformes +Zeiformes. (A) Left premaxillae in lateral view of (from top to bottom and left to right) Synodus
scituliceps, PB-6475; Dicentrarchus labrax, MNHN uncataloged; Merluccius gayi, PB-5124; Zeus faber, MNHN uncataloged. (B) Posterior region of the neurocranium
and anteriormost vertebrae in lateral view of Merluccius merluccius, MNHN uncataloged; Zeus faber, MNHN uncataloged. Abbreviations: alp, alveolar process of the
premaxilla; asp, ascending process of the premaxilla; boc, basioccipital; eocc, exoccipital condyle; ns1, neural spine of the first vertebra; pmp, postmaxillary process
of the premaxilla; pmpn, posterior notch on the postmaxillary process of the premaxilla; ptt, posttemporal; soc, supraoccipital; vc, vertebral centrum. Scale bar equals
10 mm. Photos D. Davesne and Osteobase (http://osteobase.mnhn.fr/).
incertae sedis possibly related to Acanthopterygii (Patterson,
1993) and Lampridomorpha (Davesne et al., 2014; Delbarre
et al., 2016). The present study contradicts all previous results by
showing †Pycnosteroides as the sister to modern representatives
of Clade B, this being supported by two unambiguous
synapomorphies: The long neural spine of the second preural
vertebra (441) and the reduction of the number of principal
caudal-fin rays to 18 (511).
†Omosomopsis has been presented as a member of
Polymixiiformes and Polymixiidae by Patterson (1993)
based on its modified anterior branchiostegals (231). On
the contrary, our analysis suggests that this character state
might be convergent between these two taxa. Indeed,
†Omosomopsis is found to be more closely related to
Percopsiformes than to Polymixia, as in the analysis by
Otero and Gayet (1996). The unambiguous synapomorphies
that support this relationship are the losses of the anterior
supramaxilla (41), of the basisphenoid (111), and of one
epural (461).
The characters that unite †Pycnosteroides,†Omosomopsis, and
Polymixia according to recent taxonomic revisions (Taverne,
2011; Murray and Wilson, 2014) are the long neural spine on
NPU2 and the 18 principal caudal rays, two character states that
are shown here to be synapomorphies of the larger Clade B. In
the light of these results, it appears that a redefinition of the
composition and synapomorphies of a putative Polymixiiformes
clade (including other early fossil taxa, not analyzed here) is
much needed.
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Davesne et al. Intrarelationships of Spiny-Rayed Fishes
Percopsiformes, Gadiformes, and Zeiformes Clade
Our analyses did not recover a clade Paracanthopterygii sensu
Patterson and Rosen (1989). In Analysis 1, Gadiformes and
Percopsiformes form a clade with Zeiformes and Stylephorus,
instead of Ophidiiformes and Batrachoidiformes, themselves
nested within Percomorpha in clade A (Figure 4).
†Sphenocephalus is recovered here as the sister to
Percopsiformes +Gadiformes +Zeiformes, echoing earlier
works (Otero and Gayet, 1996; Murray and Wilson, 1999;
Grande et al., 2013; Davesne et al., 2014). The characters
that support this relationship are the presence of a notch
in the postmaxillary process of the premaxilla (31)—the so-
called “gadoid” notch (Figure 7A), and of no more than one
supraneural bone in front of the dorsal fin (312).
Percopsiformes is sister to Gadiformes, Zeiformes, and
Stylephorus, in congruence with several molecular datasets
(Dettai and Lecointre, 2005; Broughton, 2010; Betancur-R et al.,
2013; Grande et al., 2013; Chen et al., 2014). The synapomorphies
of this clade are the absence of supramaxillae (51), the fusion of
the second ural centrum with the upper hypurals while staying
autogenous from the first ural centrum (421), and the fusion of
proximal and distal postcleithra (531). All these three characters
are convergent with Lampridiformes and Batrachoidiformes. In
addition, the monophyly of Percopsiformes is recovered here
and supported by three unambiguous synapomorphies; it was
also previously recovered with molecular data (Dillman et al.,
2011; Grande et al., 2013), but was ambiguous with morphology
(Patterson and Rosen, 1989; Murray and Wilson, 1999).
The Gadiformes +Zeiformes clade (also including
Stylephorus, see below) is supported by no less than nine
unambiguous synapomorphies, including the loss of palatine
teeth (201), the shortening of the second vertebral centrum
(301;Figure 7B)—previously used as a synapomorphy
of Ophidiiformes +Gadiformes +Batrachoidiformes +
Lophiiformes, and the close association between the first neural
spine and the neurocranium (291;Figure 7B)—previously
used as a Gadiformes +Batrachoidiformes +Lophiiformes
synapomorphy (Patterson and Rosen, 1989). Another potential
synapomorphy (not included in our study due to lacking fresh
material for dissection in many taxa) is the presence, in both
Gadiformes and Zeiformes, of intrinsic sonic muscles limited to
the anterior end of the swim bladder (Kasumyan, 2008).
Stylephorus with Gadiformes and Zeiformes
The present phylogenetic analysis of morphological characters
is the first to include Stylephorus alongside lampridiforms and
acanthomorph representatives. In agreement with all molecular
studies, Stylephorus is included within clade B alongside
Gadiformes and Zeiformes, instead of within Lampridiformes.
However, it is recovered here as sister to Zeiformes (Figure 4),
whereas molecular data suggest a closer relationship with
Gadiformes (e.g., Miya et al., 2007). This Stylephorus-Zeiformes
relationship is supported by four unambiguous synapomorphies:
The ascending processes of the premaxillae are longer than
the articular processes (11), the soft rays of the dorsal, anal
(411), and pectoral (561) fins are unbranched and there is no
contact between the quadrate and the reduced metapterygoid
(181). The latter two synapomorphies are unique for this clade,
and therefore not found in any gadiform or lampridiform. In
addition, the first vertebra of Stylephorus is much reduced and its
neural spine is closely associated with the neurocranium (291), a
Gadiformes +Zeiformes synapomorphy (Figure 7B) also absent
in Lampridiformes.
Conversely, several synapomorphies that are exclusive to
Lampridiformes are absent in Stylephorus: It lacks the frontal
vault (151), the condylar articulation between the anterior
ceratohyal and the ventral hypohyal (221;Figure 8), and its
first dorsal pterygiophore is not inserted anterior to the
first neural spine (332). It also has four autogenous pectoral
radials, instead of the three (551) that are observed in all
lampridiforms except for Veliferidae. The presence of exclusive
Gadiformes +Zeiformes synapomorphies, combined with the
absence of several exclusive lampridiform synapomorphies
(all the other ones being either ambiguously present, or
FIGURE 8 | (A) Velifer hypselopterus, MNHN.IC.1982.0025, reconstructed
from virtual tomographic data. Ventral portion of the left hyoid arch, in medial
view, reversed (anterior faces left). (B) Stylephorus chordatus,
MNHN.IC.2004.1317, reconstructed from virtual tomographic data. Ventral
portion of the left hyoid arch, in medial view, reversed (anterior faces left).
Abbreviations: achy, anterior ceratohyal; bhy-hhy, facet of the basihyal-dorsal
hypohyal articulation; chy-hhy, condyle of the anterior ceratohyal-ventral
hypohyal articulation; dhhy, dorsal hypohyal; ihy, interhyal; pchy, posterior
ceratohyal; raphhy, retro-articular process of the ventral hypohyal; vhhy, ventral
hypohyal. Scale bar equals 2 mm.
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Davesne et al. Intrarelationships of Spiny-Rayed Fishes
convergent in Stylephorus) strongly support the hypothesis
of a close relationship between Gadiformes, Zeiformes, and
Stylephorus.
Clade A: Beryciformes, Ophidiiformes, and
Batrachoidiformes
The monophyly of Clade A is supported by numerous
synapomorphies. These include the double-headed cranio-
hyomandibular articulation (170;Figure 9A), the presence of
antero-median pelvic processes (581), and a Baudelot’s ligament
inserting proximally on the basioccipital rather than on anterior
vertebrae (251). In Zeus and Velifer, a non-homologous condition
shows the ligament inserting on the exoccipitals, instead of on
the basioccipital as it is the case in members of Clade A. The
peculiar, “chain-link” articulation of the dorsal-fin spines (361),
and the asymmetric base of the pelvic spines (661,Figure 9B)
are also unique to Clade A (Mok and Chang, 1986), but
optimized ambiguously at this node due to missing data in
fossils. Finally, the pelvic-fin spine (651;Figure 9B), a diagnostic
“acanthopterygian” character according to Greenwood et al.
(1966), has an ambiguous phylogenetic history with our topology:
It could either be a synapomorphy of Clade A convergent with
†Pycnosteroides and Zeiformes, or a synapomorphy of Clade A +
Clade B (with multiple secondary losses).
Within Clade A, “beryciforms” are recovered as paraphyletic:
The holocentrid Sargocentron is more closely related to
percomorphs than to the trachichthyid Hoplostethus (Figure 4).
Indeed, Sargocentron and percomorphs share a separate, entirely
spinous anterior dorsal fin (371;Figures 2M,N)—with multiple
reversions within percomorphs, the fusion of the ural centra
together and with the upper hypurals (421, 431) and the reduction
in the number of hypurals (491).
Finally, Percomorpha includes Ophidiiformes (Brotula)
and Batrachoidiformes (Halobatrachus), congruent with every
molecular study including these taxa together. However, it should
be kept in mind that we used a very limited taxon sampling
for Percomorpha, and that expanding it might have changed
the resulting topology. Batrachoidiformes and Ophidiiformes
share several synapomorphies with the other members of Clade
A, such as the two hyomandibular heads (there is only one
in most members of Clade B, see Figure 9A), the insertion of
the Baudelot’s ligament on the basioccipital (rather than on
the exoccipitals or vertebrae), the asymmetrical pelvic spine
base (Figure 9B; the pelvic spine is present but extremely
reduced in Ophidiiformes) and—only in Batrachoidiformes—
the spinous anterior dorsal fin (Figure 2L). In addition, Brotula
possesses a supramaxilla, a basisphenoid and palatine teeth,
all lost within Clade B (see above). Our findings parallel
those of previous authors (Gosline, 1968; Fraser, 1972; Gill,
1996; Wiley and Johnson, 2010) who viewed these character
observations as potential challenges to the monophyly of
“Paracanthopterygii.”
FIGURE 9 | Examples of synapomorphies of Clade A. (A) Left hyomandibulae in medial view (anterior faces right) of (from left to right) Gadus morhua, PB-A-16;
Zeus faber, MNHN uncataloged; Dicentrarchus labrax, MNHN uncataloged; Batrachoides pacifici, PB-7005; Brotula clarkae, PB-6515. Arrows point to the head(s) of
the cranio-hyomandibular articulation. (B) Left pelvic-fin spines in anterior view of (from left to right and top to bottom) Zeus faber, MNHN uncataloged; Batrachoides
pacifici, PB-7005; Dicentrarchus labrax, MNHN uncataloged. Arrows point to the base of the pelvic spine. Scale bar equals 10 mm. Photos D. Davesne and
Osteobase (http://osteobase.mnhn.fr/).
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Davesne et al. Intrarelationships of Spiny-Rayed Fishes
Congruence with Molecular Results
Table 1 summarizes the topologies found by relevant
morphological and molecular phylogenetic analyses. It
shows that molecular analyses since 2005 have systematically
agreed on a number of points, namely the rejection of a
paracanthopterygian clade, the monophyly of a Gadiformes
+Zeiformes clade (that also includes Stylephorus) and the
inclusion of Ophidiiformes and Batrachoidiformes within
Percomorpha. All of these results are also recovered in our
Analysis 1 (Figure 4).
Only two minor conflicts remain between our topology
and this molecular “consensus”: Stylephorus is sister to
Zeiformes, instead of Gadiformes; and Ophidiiformes and
Batrachoidiformes form a clade together, instead of being
sequential sister groups with other percomorphs. However, our
percomorph sampling is much reduced and not suitable for
providing an effective test of percomorph interrelationships.
Already well-supported by their repetition from one dataset
to another, the clades found in the “molecular consensus” are
hereby corroborated by a diverse set of morphological characters
(Table 1).
Some results are not recovered in every molecular study
(Table 1), for example: The monophyly of Acanthomorpha and
the sister group relationship of Lampridiformes with other
acanthomorphs (corroborated by our results), the monophyly
of Beryciformes (not corroborated by our results), the grouping
of Percopsiformes with Gadiformes +Zeiformes and of this
ensemble with Polymixiiformes (both corroborated by our
results). However, it should be noted that these conflicting nodes
are commonly associated with comparatively low support values
(bootstrap indexes and/or posterior probabilities) in molecular
studies. Therefore, these clades are neither robust, nor repeated, a
combination that should be sufficient to not accept them directly
(Chen et al., 2003; Li and Lecointre, 2009). By contrast, the non-
monophyly of acanthomorphs is an example of relationship that
is simultaneously robust and not repeated. The Lampridiformes
+Myctophiformes clade of Miya et al. (2005) has a posterior
probability of 0.99 or 1. However, it is never repeated in analyses
based on nuclear markers only, nor in another study that used the
mitochondrial genome (Broughton, 2010). Assessing in which
way gene sampling affects phylogenetic reconstruction in this
zone of the tree should be the subject of later investigation.
The Impact of Fossil Taxa
Our Analysis 2 of extant taxa alone (Figure 5A) fails to recover
clades that are always present with molecular results, for example
a monophyletic Clade A or a Gadiformes +Zeiformes clade.
Two of the three main acanthomorph clades of Analysis 1 are
not recovered by this analysis: Clade A is paraphyletic and
includes part of Clade B and Lampridiformes, while Clade B is
polyphyletic (Polymixia and Percopsiformes are separated from
Gadiformes, Zeiformes, and Stylephorus, the latter three forming
a clade with Lampridiformes). Lampridomorpha (reduced to
extant Lampridiformes) is monophyletic, but with different
intrarelationships (Regalecus is sister to Velifer +Lampris). On
the other hand, when fossil taxa are analyzed alone (Figure 5B),
they show the same pattern of interrelationships as with
Analysis 1.
What is shown here is a possible case of “character extinction,”
where many character state combinations were present in the
earliest members of a group, but disappeared since, due to
either the extinction of the taxa that bore them, or extensive
subsequent morphological evolution. This is for example
the case in Lampridomorpha, whose extant representatives
(Lampridiformes) are both relatively less diverse (due to the
extinction of many clades at the end of the Cretaceous), and
very anatomically-distinctive compared with the oldest known
members of the clade (Delbarre et al., 2016). Omitting the early
fossil taxa from the analyses can then have an effect similar
to the “long branch attraction” that is commonly described in
molecular phylogenetics, with extant taxa artificially grouped
together on the basis of similar character state combinations, that
are recovered here as non-homologous. An example occurs with
Lampridiformes, Gadiformes, Zeiformes, and Stylephorus, that
are grouped together by numerous synapomorphies in Analysis
2, but are widely separated by fossil representatives in Analysis 1.
A similar phenomenon is observed by Davesne et al. (2014) when
fossil taxa are not included.
Our results show yet another empirical example in which
morphological phylogenetic analyses including fossil and extant
taxa achieve a higher congruence with molecular topologies
compared with analyses that include only extant taxa. Similar
results have been found previously for the deep intrarelationships
of amniotes (Gauthier et al., 1988; Donoghue et al., 1989),
arthropods (Legg et al., 2013), and annelids (Parry et al., 2016).
CONCLUSION AND PERSPECTIVES
In the present study, we provide a morphological dataset of extant
and fossil taxa that consolidates our current understanding of
the earliest stages of acanthomorph evolution. The phylogeny we
recover is consistent with topologies proposed by the multiple
molecular analyses available today (Table 1), contributing to
an integrative view of the interrelationships of this important
clade. This congruence is a strong case that morphology can
accurately resolve deep phylogenetic relationships. Through this
first attempt at covering acanthomorph diversity, we show that
even well-known morphological characters can bring valuable
support to enduring phylogenetic questions as long as a relevant
coverage of the topology (including fossil taxa) is provided. A
good example of this is our strong support of a clade including
Gadiformes and Zeiformes, permitted by including both taxa in
an analysis of morphological characters for the first time.
Analyses of morphological characters in fossil and extant
taxa should continue to be performed, even when molecular
data are available, due to their key role in: (1) corroborating
the molecular results with independent character sets, which
increases the reliability of the repeated clades (Grande, 1994;
Miyamoto and Fitch, 1995; Chen et al., 2003); (2) providing
a framework for the evolution of morphological characters;
(3) integrating taxon and character evolution in deep time, by
explicitly supporting phylogenetic positions for fossil taxa that
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Davesne et al. Intrarelationships of Spiny-Rayed Fishes
TABLE 1 | Summary of the main studies presented in this article, and associated phylogenetic hypotheses.
Stiassny and
Moore, 1992
Johnson and
Patterson, 1993
Patterson and
Rosen, 1989
Wiley et al., 2000 Miya et al.,
2005/2007
Broughton, 2010
Clades tested Morphology
(pelvic girdle only)
Morphology Morphology Morphology +1 mitoch.
+1 nuclear rDNAs
Complete
mitogenomes
Protein-coding
mitochondrial genes
Acanthomorpha Yes Yes Outgroups
absent
Yes No Yes
Clade A +Clade B Ambiguous Yes La. absent Yes Yes (La. outside
Acanthomorpha)
Yes
La. +Pe. +Ga. +Ze. No–Ga. absent No–Ga. absent La., Ze. absent No No No
La. +Clade A Ambiguous No La. absent No No No
Po. +Pe. +Ga. +Ze.
(Clade B)
No–Ga. absent No–Ga. absent No No Yes Yes
Po. +Pe. Ambiguous No No No Yes No
Pe. +Ga. +Ze. No–Ga. absent No–Ga. absent Ze. absent No No Yes
Pe. +Ga. +Op. +Ba. Assumed yes Assumed yes Yes No No No
Ga. +Ze. Ga. absent Ga. absent Ze. absent Yes Yes Yes
Stylephorus +Ga. +
Ze.
Stylephorus and
Ga. absent
Stylephorus and
Ga. absent
Stylephorus and
Ze. absent
Stylephorus absent Yes (2007 only) Stylephorus absent
Clade A No Yes Assumed yes Yes Yes Yes
Ze. +Clade A Yes Yes Assumed yes No No No
Beryciformes No Yes Absent No Yes Yes
Op. in Percomorpha Assumed no Assumed no No Yes Yes Yes
Ba. in Percomorpha Assumed no Assumed no No Yes Yes Ba. absent
Li et al., 2009 Grande et al., 2013 Near et al., 2013 Betancur-R et al.,
2013
Chen et al., 2014
Clades tested 4 nuclear markers 4 nuclear/3 mitoch. markers 10 nuclear
markers
20 nuclear markers 6 nuclear/3
mitochondrial markers
Acanthomorpha Ambiguous yes Yes Yes No with RY-coding/
yes without
Clade A +Clade B No Yes (using parsimony) No No No
La. +Pe. +Ga. +Ze. Yes +Po. No No Yes No with RY-coding/
yes without
La. +Clade A No Yes (using likelihood) Yes No No
Po. +Pe. +Ga. +Ze. (Clade B) Yes +La. Yes No No Yes
Po. +Pe. No No Yes No No
Pe. +Ga. +Ze. No Yes No Yes Yes
Pe. +Ga. +Op. +Ba. No No No No No
Ga. +Ze. Yes Yes Yes Yes Yes
Stylephorus +Ga. +Ze. Stylephorus
absent
Yes Yes Yes Stylephorus absent
Clade A Yes Yes Yes Yes Yes
Ze. +Clade A No No No No No
Beryciformes No Yes Yes No No
Op. in Percomorpha Yes Yes Yes Yes Yes
Ba. in Percomorpha Yes Yes Yes Yes Yes
Molecular “consensus” Present analysis–complete Present analysis–no fossils
Clades tested Morphology Morphology
Acanthomorpha Ambiguous Yes Yes
Clade A +Clade B Ambiguous Yes No
La. +Pe. +Ga. +Ze. Ambiguous No No
La. +Clade A Ambiguous No No
(Continued)
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Davesne et al. Intrarelationships of Spiny-Rayed Fishes
TABLE 1 | Continued
Molecular “consensus” Present analysis–complete Present analysis–no fossils
Po. +Pe. +Ga. +Ze. (Clade B) Ambiguous Yes No
Po. +Pe. Ambiguous No Ambiguous
Pe. +Ga. +Ze. Ambiguous Yes No
Pe. +Ga. +Op. +Ba. No No No
Ga. +Ze. Yes Yes No
Stylephorus +Ga. +Ze. Yes Yes No
Clade A Yes Yes No
Ze. +Clade A No No No
Beryciformes Ambiguous No No
Op. in Percomorpha Yes Yes No
Ba. in Percomorpha Yes Yes No
Ba., Batrachoidiformes; Ga., Gadiformes; La., Lampridiformes; Op., Ophidiiformes; Pe., Percopsiformes; Po., Polymixiiformes; Ze., Zeiformes.
could be subsequently used for divergence time analyses—either
directly or as calibration points (Benton and Donoghue, 2007;
Parham et al., 2012; Sauquet, 2013).
A more generalized and fruitful dialogue between morphology
and molecular data is needed in phylogenetics. Molecular
analyses may provide a broad and detailed phylogenetic
framework, but maintaining a lively research program in
morphology is still necessary in order to provide independent
evidence to the molecular phylogenies and, more generally, to
understand the history of the relationships between forms and
functions in an evolutionary context (Giribet, 2015; Lee and Palci,
2015).
AUTHOR CONTRIBUTIONS
Designed the study: DD, CG, PJ, GL, and OO. Designed the
character list: DD, VB, and OO. Performed the analyses: DD and
CG. Wrote the paper: DD, CG, and OO. Reviewed, corrected, and
approved the final version of the manuscript: DD, CG, VB, PJ, GL,
and OO.
ACKNOWLEDGMENTS
The authors would like to thank the collection managers that
allowed access to the specimens under their care: Philippe
Béarez, Gaël Clément, Claude Ferrara, Zora Gabsi, Patrice
Pruvost (MNHN), Emma Bernard, Zerina Johanson, James
Maclaine, Martha Richter (NHMUK), Markus A. Krag (ZMUC),
Radford Arrindell (AMNH), and Rivka Rabinovich (HUJ). We
also sincerely thank the following for fruitful discussion on
morphological characters and their coding: Ralf Britz (NHMUK),
Giorgio Carnevale (Università degli Studi di Torino), Bruno
Chanet (MNHN), Matt Friedman (University of Oxford),
G. David Johnson (National Museum of Natural History,
Smithsonian Institution), and Nalani Schnell (MNHN). CT-
scan data was acquired at the AST-RX platform (UMS 2700
OMSI, Muséum national d’Histoire naturelle) with the help
of Miguel García-Sanz. Iconography was kindly provided by
Samuel Iglésias, Christian Lemzaouda, Philippe Loubry, and
Nalani Schnell (MNHN), as well as by Philippe Béarez and
the Osteobase team (http://osteobase.mnhn.fr/). Roger Close
(University of Oxford) is warmly thanked for reviewing the
English of the manuscript. DD was supported financially by the
ATM “Formes possibles, formes réalisées” (MNHN) and by the
Natural Environment Research Council, grant no. NE/J022632/1
(to Matt Friedman, University of Oxford).
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: http://journal.frontiersin.org/article/10.3389/fevo.
2016.00129/full#supplementary-material
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Conflict of Interest Statement: The authors declare that the research was
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