Hard tissues in fish evolution: history and current issues

2018·1.3 MB·English

by  Schultze, H P

Hard tissues in fish evolution: history and current issues
by
Hans-Peter ScHultze (1)
Abstract. – A short survey of the distribution of scale characters in osteichthyans is mapped onto recently pub-
lished cladograms of gnathostomes. The recently confirmed relationship of polypterids with scanilepids places
their early ontogenetic features as advanced features within palaeonisciform actinopterygians. the pore-canal
system (which seems to hold nerves for sensing water pressure changes) of cosmoid scales appears as a singu-
lar feature of dipnoans and rhipidistians without connection to the rich vascular system in basal osteichthyans.
elasmoid scales appear many times independently within actinopterygians and sarcopterygians. elasmodine is
a homoplastic feature in osteichthyans, it is a new formation in neopterygian elasmoid scales, supposedly even
here twice independently derived in teleosts and halecomorphs.
Résumé. – les tissus durs et l’évolution des poissons : histoire et questions actuelles
© SFI
Received: 16 Nov. 2017 la distribution des caractères des écailles des ostéichtyens est retracée sur les plus récents cladogrammes des
Accepted: 13 Jan. 2018
gnathostomes. la relation de parenté récemment proposée entre polyptéridés et scanilépidés suggère un état déri-
Editor: O. Otero
vé de leurs traits ontogénétiques précoces au sein des actinoptérygiens paléonisciformes. le système de pores et
de canaux des écailles cosmoïdes (qui pourrait contenir des nerfs sensibles aux changements de la pression de
l’eau) apparait comme un caractère singulier des dipneustes et des rhipidistiens, sans relation apparente avec
le système richement vascularisé des ostéichtyens basaux. les écailles élasmoïdes sont apparues plusieurs fois
Key words
indépendamment au sein des actinoptérygiens et des sarcoptérygiens. Lʼélasmodine est un caractère homoplas-
Histology
tique chez les ostéichtyens et une formation nouvelle des écailles élasmoïdes des néoptérygiens, probablement
Scales
apparue deux fois indépendamment chez les téléostéens et les halécomorphes.
Osteichthyes
Actinopterygii
Sarcopterygii
this paper is an update of Schultze (2015) to embrace Agassiz broadly defined ganoid scales as those with a
two papers (Giles et al., 2017; Qu et al., 2017), which clarify bony base, which can be covered by an enamel layer or dif-
the position of polypterids and the concept of cosmine in ferent other hard tissues. the result was that he grouped very
early osteichthyans. In addition, I place special emphasis on different fishes under the ganoid scale category for instance:
the contribution of the French histology group since the end cephalaspids, acanthodians, actinopterygians (teleosts with
of the 1970s, especially to that of Francois J. Meunier. bony plates as the catfish Hypostoma, holosteans, chondro-
Fish scales have been a subject of interest since the steans, and palaeonisciforms), osteolepid sarcopterygians,
beginning of microscopy in the 1600s (see early history lungfish, such as Dipterus and Lepidosiren, and coelacanths.
in Baudelot, 1873 or Hase, 1907). One example is Agas- The placoid fishes included the chondrichthyans with a
siz (1833: 68-80), who used four scale types to divide and large variety of tooth shapes and tooth-like placoid scales;
describe fossil fishes in an outstanding compilation that was the placoid scales themselves were not dealt with except for
the start of paleoichthyology (Agassiz, 1833-1843). the four a denticle of a ray.
types distinguished by Agassiz were the cycloid, ctenoid, Agassiz classification based on scales did not succeed.
ganoid, and placoid scales. Already in 1841, Peters argued that a division between
cycloid scales are characterized by concentric lines (cir- cycloid and ctenoid scales does not exist; both types do
culi) and may have radial furrows in the covered anterior occur on the same fish. Müller (1845) confirmed that and
field or not. They are composed of two layers, a hard-upper introduced a classification of actinopterygians, where the
layer and a flexible lower lamellar layer. ctenoid scales teleosts are defined on two soft characters and one hard skel-
show the same structure in the covered anterior field as etal feature (Arratia, 2001, 2015). Nevertheless, the division
cycloid scales, except that the posterior margin is serrated or between cycloid and ctenoid scales appears frequently in
the posterior free part (field) is occupied by spines or articu- the literature, even though more recently Roberts (1993) has
lated cteni. Agassiz placed teleostean fishes – as we define shown that there are different kinds of ctenoid scales, which
them today – within these two scale groups. In addition, tel- appear independently as differentiation of cycloid scales in
eosts with bodies covered by bony shields were placed in the various teleost lineages. the assemblage of ganoid fishes
ganoid fishes. by Agassiz (1833-1843) was too broad and diverse and not
(1) Kansas university, Natural History Museum and Biodiversity Institute, 1345 Jayhawk Boulevard, lawrence, KS 66045, uSA.
[[email protected]]
Cybium 2018, 42(1): 29-39.
Hard tissue in fish evolution Schultze
based on a consistent characterization, so that it was disman- formed by lamellae of collagen (with the direction of the col-
tled by Müller (1845) and following authors. After Agassiz lagen fibres changing from lamella to lamella), whereas iso-
(1833-1843), scales were defined more precisely and not pedine was first defined as the basal part of rhomboid scales
used for classifications. formed of bone. Williamson (1851) had shown already that
Williamson (1849) defined ganoine as a superficial tissue round scales are built of two mineralized layers. the upper
present in rhomboid scales of actinopterygians and “cros- layer is homogeneous, whereas the less mineralized basal
sopterygians”. the term cosmine was used by Williamson layer is formed of collagen lamellae with different orienta-
(1849) and following authors (e.g. Aldinger, 1937) for den- tions. Mandl corpuscles appear in the basal layer and waves
tine. In contrast, cosmine is here defined as a combination of mineralization start at the top of the basal layer (Meunier
of tissues, enamel and dentine, with a pore canal system et al., 1978: pl. 2, fig. 8a, b).
by Ørvig (1951, 1967). Goodrich (1907, 1909) published the external layer (couche cotelée = ridged layer =
the classic histological illustrations of ganoid and cosmoid osseous layer) of the elasmoid scale of actinopterygians was
scales, dividing the ganoid scale into palaeoniscoid type interpreted as different tissues in early publications, where-
(with dentine) and lepidosteoid type (without dentine and as it is just a thin bony layer with bone cells in amiids and
with Williamson canals); he placed the ctenoid scale within primitive teleosts and without bone cells in advanced tele-
the cycloid scale as a special form of the latter. Furthermore, osts (Schultze, 1966). Schultze (1966) posited that the exter-
Aldinger (1937) published a monograph on ganoid scales, nal layer was derived from the bony basal layer (isopedine)
whereas Gross (1956) published a monograph on cosmoid of the lepidosteoid-type scale in the close relatives or in the
scales. Recently, summaries on the integumentary skeleton most primitive members of teleostei, the pholidophorids, as
have been published by Huysseune and Sire (1998), Sire et represented by Pholidophorus latiusculus (tab. I). Sire et al.
al. (2009), Meunier (2011), and Schultze (2015). (2009: 417) derived it from “odontogenetically derived tis-
sue different from the morphologically comparable (but not
homologous) osteogenetic derivative isopedine”; its position
Scale chaRacteRS on a cladogram of early teleosts (e.g. Arratia, 2001, 2013,
2017) suggests homology. Meunier and Brito (2004) had a
Round (elasmoid) scales different interpretation, deriving the external layer from a
The scale classification by Agassiz (1833) corresponds “superficial mineralized layer” in an unidentified Pholido-
roughly to a division between round scales (his cycloid and phorus scale, which occurs in no other pholidophorid, but
ctenoid scales) and rhombic or rhomboid scales (his ganoid probably in some species of the non-monophyletic “Pholido-
scales). cycloid and ctenoid scales are types of round (elas- phoriformes” (see Arratia, 2000). the external layer in the
moid) scales (Peters, 1841; Müller, 1845) unique to teleosts histological section (Meunier and Brito, 2004: fig. 3) has the
(Arratia, 2015). A second type, the amioid scale (Amiiden- same appearance as the underlying ganoine layers, and the
Rundschuppe in Schultze, 1966), appears independently external layer overlaps the underlying ganoine layer as well,
in different lineages of osteichthyans (Klaatsch, 1890; as in normal ganoid scales.
Schultze, 1977, 1996, 2015). the rhomboid scales are built the external layer is covered by the so-called limiting
by three layers (basal bone layer, dentine, and overlying layer (Schönbörner et al., 1979) in the posterior field of an
enamel) in basal osteichthyans. the participation of these elasmoid scale. the limiting layer has been compared with
layers changed within osteichthyans: the three layers of ganoine (Sire et al., 2009), but a contribution from the epi-
rhomboid scales can be replaced. that occurs in the extreme dermal cells has not been shown yet (Sire, 1988; Sire et al.,
in round scales. 2009). In addition, the attachment of Sharpey-fibre-like bun-
Bertin (1944) introduced the term elasmoid scale for dles to the limiting layer (zylberberg and Meunier, 1981)
round scales, and confused scale nomenclature by using the makes it unlikely that this layer is related to ganoine.
term isopedine instead of elasmodine for the basal layer of the basal layer of the elasmoid scale is built by lamel-
the elasmoid scale even though he showed that this layer is lae of collagen fibres, which can be mineralized secondar-
Table I. – Changes from ganoid to
elasmoid scales in actinopterygians;
“lost” = not formed; elasmodine is con-
sidered to be a new formation in both
teleostei and Halecomorphi.
30 Cybium 2018, 42(1)
Schultze Hard tissue in fish evolution
ily. there are no bone cells; nevertheless, cells (elasmocytes structure for both tissues – a prismatic imprint (enamel) on
of Meunier, 1983, 1984) occur in some elasmoid scales. the surface of cosmoid scales, which is in contrast to minute
the collagen fibres have different orientations in succes- elevations (ganoine) on ganoid scales, where the microtu-
sive lamellae (Williamson, 1851), the “twisted ‘plywood’ bercles correspond to the centre of a forming epidermal cell.
counter plaques” of Meunier (1981). Meunier described the The microtubercles were first described by Reissner (1859),
structure in different taxa; the actinistian Latimeria (Giraud then shown in peels by Schultze (1966, 1977), in thick thin
et al., 1978; Meunier and Géraudie, 1980), extant lungfishes sections by Ørvig (1967), and as an SeM (Scanning elec-
(Meunier and François, 1980; Meunier, 1980), holostean tron Microscopy) picture by ermin et al. (1971). the SeM
Amia (Meunier, 1981), and teleosts (Meunier and Géraudie, made it easy to observe the structure so that it has been used
1980; Meunier, 1984). In 1984, Meunier published an over- for species identification (Gayet and Meunier, 1986; Meu-
view of the different arrangement of fibres (the changing nier et al., 1988). the microtubercles are not always visible,
angle from lamella to lamella), which may indicate that this nevertheless they are known in Paleozoic actinopterygians,
homoplastic character varies among lineages. unfortunately, such as amblypterids (štamberg, 2016a, b) and Cheirolepis
Meunier accepted the term “isopédine” for the basal layer of (zylberberg et al., 2017). Since the early publication of Wil-
the elasmoid scale, following Bertin (1944). the term isope- liamson (1849), ganoine was considered enamel or enamel-
dine characterizes the bony basal part of ganoid scales (Pan- oid until Sire et al. (1986, 1987) and Sire (1994) demonstrat-
der, 1856; for definition see Sire et al., 2009), whereas the ed in regenerated scales of Erpetoichthys and Lepisosteus,
basal part of elasmoid scales is not ossified. Schultze (1996: respectively, that ganoine is a formation of the basal epider-
87, characterization of elasmodine) proposed the term elas- mal layer, and thus, enamel (see also Qu et al., 2015). the
modine for these packages of collagen fibres. Later on, Sire contact between the epidermis and ganoine is not as direct as
and Huysseune (2003) described the different ontogenetic in true enamel, and the growth is different in both tissues.
growth between elasmodine and isopedine. the growth is easy to recognize in ganoid scales by lami-
Sire et al. (2009) homologized the elasmodine layer with nae in the isopedine interdigitating with successive ganoine
the dentine layer of polypterid scales, which seems very layers in lepidosteoid type scales and dentine in palaeo-
unlikely, because elasmoid scales in amioid and teleostean niscoid scales. the isopedine, dentine and ganoine of each
actinopterygians derive independently from lepidosteoid layer may be slightly resorbed before the next layer is depos-
scales, which have lost the dentine. In addition, polypterids ited (Gross, 1935; Aldinger, 1937; Ørvig, 1978a, b). Resorp-
belong to a side branch of palaeonisciform actinopterygians tion lines are typical for ganoid scales contrary to cosmoid
(see below and Giles et al., 2017). elasmodine appears to be scales, where they are missing in the cosmine, occurring
a new formation in elasmoid scales. only below. the rich canal system, which carries vessels and
elasmoid scales have evolved multiple times independ- nerves to the dentine, is highly variable within palaeonisci-
ently within osteichthyans (Klaatsch, 1890; Schultze, 1977, morphs (Aldinger, 1937).
2015). Most elasmoid scales are characterized by radially cosmine is a combination of tissues and structure: a sin-
arranged structures in the covered part of the scale (amio- gle layer of enamel covers the dentine layer, which is inter-
id type), with the exception of the cycloid scale (including rupted by the pore-canal system. cosmine forms the surface
the different ctenoid scales) where circuli form the covered layer in cosmoid scales, where resorption lines are unknown,
field. except for the Westoll-lines in dipnoans. thomson (1977;
repeated by Meinke, 1984) argued that the whole surface is
Rhomboid scales resorbed and formed anew. However, I checked and re-stud-
Rhomboid scales of osteichthyans have a peg-and-socket ied the material described by thomson (1977) and found no
articulation in the vertical rows. The free field is covered by sign of resorption in the scales of Ectosteorhachis (thom-
dentine, ganoine or enamel. the cover can be reduced, and son, 1975: figs 2, 15, 23; Thomson, 1977: fig. 2) or ��eeggaa--
the bony base also forms the surface in scales and scutes of lichthys (Thomson, 1977: fig. 3). The resorption Thomson
actinopterygians, such as chondrosteans, aspidorhynchids, described (1975: fig. 23; refigured by Meinke, 1984: fig.
pycnodonts (Schultze, 1966), and silurids (with superficial 1B) corresponds to a canal opening in an osteolepid scale
hyaloine cover; Sire, 1993; Sire and Meunier, 1993; Sire et (see Gross, 1956: fig. 50A = Megalichthys) or the margin
al., 2009) and in scales of some sarcopterygians, such as pan- of a Westoll-line (see Gross, 1956: fig. 70A, B = Dipterus),
derichthyids and Glyptopomus (Jarvik, 1950; Ørvig, 1957). which thomson (1975: figs 24, 25) described for �egali-
Williamson (1849) introduced the term ganoine for the chthys. In my opinion, Ectosteorhachis is an unfit choice to
superficial enamel in ganoid and cosmoid scales. He dis- study growth of cosmine, because cosmine is developed in
tinguished ganoine from tooth enamel of mammals, but he patches and does not form a continuous surface layer. Bor-
used the term ganoine for the enamel on cosmoid scales, too. gen (1989) described reabsorbed grooves on osteolepidid
Schultze (1977: pl. 13, figs 2, 3) showed a different surface jaws, which look like postmortem or even post-fossilization
Cybium 2018, 42(1) 31
Hard tissue in fish evolution Schultze
etchings and have nothing to do with the growth process of Polypterus is considered the most primitive living actin-
these fishes. In cosmoid scales, growth can only be observed opterygian, but it is not the most primitive fossil actinop-
easily in the basal layers below the cosmine (where succes- terygian. the genus was placed close to scanilepiforms
sive odontodes occur), which can be resorbed and are cov- by Aldinger (1937) and Schultze (1968) on histological
ered by bone tissue before the cosmine layer is formed (first grounds (canal system and arrangement of bone cells around
shown by Gross, 1930: pl. IV, fig. 5; Bystrow, 1939: fig. 2B; the canals, respectively) and by Jakovlev (1973), Selezneva
repeated by Ørvig, 1957: fig. 9D; Ørvig, 1967, fig. 6 = Lac- (1985) and Sytchevskaya (1999) on morphological similari-
cognathus; by Huysseune and Sire, 1998: fig. 3A; and by ties of Evenkia with Polypterus. cloutier and Arratia (2004)
Sire et al., 2009: fig. 14A, not Glyptolepis as stated). cladogram shows Polypterus together with Acipenser and
lu et al. (2016: 7, 2017) confused cosmine and ganoine neopterygians as the sister group of Tarrasius and Guildai-
(there is no cosmine in Cheirolepis). cosmine is not a tissue, chthys, separate from palaeoniscimorphs. A similar place-
but a combination of tissues (one layer of enamel on dentine) ment appears in a new phylogenetic analysis of actinoptery-
gians that includes scanilepiforms (Giles et al., 2017). the
with a pore canal system, whereas ganoine is a tissue (a kind
two polypterid genera Polypterus and Erpetoichthys and
of enamel) and not a “composite tissue”. Resorption is nearly
the sister group Evenkia are hypothesized to be the most
always present in connection with ganoine and dentine, and
advanced scanilepiforms (Fig. 1), and the chinese Middle
rarely found in cosmine, where it occurs in the precursor of
triassic Fukangichthys appears as the most basal scanilepi-
the top cosmine layer. cosmine is limited to sarcopterygians
form in this analysis. Scanilepis occurs in the late triassic
above onychodonts and actinistians, and does not occur in
(Rhaetian), the earliest fossil polypterid in the late creta-
actinopterygians (including �eemannia).
ceous (cenomanian). thus, there is still a time gap of about
the term isopedine was created by Pander (1856) for
110 million years between the two groups, which is not
lamellar bone (= “laminar thick-layered bone tissue” after
comparable to a ghost line of about 320 million years if the
Ørvig, 1967). Isopedine forms the base of ganoid and cos-
polypterids are considered to be the most primitive actinop-
moid scales. It does not exist in that form in elasmoid scales
terygians. the youngest palaeoniscimorph with rhomboid
except in round scales of Paleozoic sarcopterygians. the
palaeoniscoid scales can be found in Pteroniscus from the
external layer, not the basal layer, of elasmoid scales in
late Jurassic, which is not related to scanilepiforms.
neopterygians is here interpreted as corresponding to the iso-
the relationship of polypterids as the most advanced
pedine of lepidosteoid-type scales (Schultze, 1966, 1996).
scanilepiforms suggests that the histological structure of
their scales represents an advanced form of the palaeonis-
coid scale type within palaeonisciforms, and the occurrence
ScaleS and PhylogenieS
of elasmodine between dentine and isopedine is an advanced
character within palaeonisciforms and not a basal character
Histological characters can and should be used in phylo-
in actinopterygians or even of osteichthyans as proposed by
genetic analyses as any other character. Proper identification
Sire et al. (2009). Scanilepis shows no indication of elasmo-
is essential for creating and interpreting cladograms, even
dine. thus, it could be said that the polypterids are another
though there may be different interpretations among authors.
group converging on elasmoid scales within scanilepiforms.
It is dangerous to construct phylogenies of characters inde-
pendently from “real” trees (Sire et al., 2009). For example,
Basal osteichthyan scales
one should not omit a character, such as acrodine occurring
In recent years, the understanding of the interrelation-
in Ligulalepis (King et al., 2017), otherwise it might place
ships of lower osteichthyans has changed grossly, based
the taxon wrongly, out of the actinopterygians in that case mainly on new finds of osteichthyans in the Lower Devonian
(long et al., 2015). and Silurian of china, which were placed initially in sarcop-
terygians or basal osteichthyans. These finds have added tre-
Polypterus and elasmodine mendously to our knowledge of early sarcopterygians and
Sire (1989) discovered elasmodine in the scales of the actinopterygians and demonstrated the problems in placing
extant Polypterus between the dentine and the basal isope- basal taxa. Some taxa previously assigned to sarcopterygians
dine. He constructed an additional palaeoniscoid type scale, (e.g. �eemannia) have been moved to actinopterygians (e.g.
the polypteroid type ganoid scale, with elasmodine lying long et al., 2015). Nevertheless, the published phylogenies
between dentine and the bony basal plate. Sire et al. (2009: do not agree (compare zhu et al., 2009, 2013 and King et al.,
fig. 16) considered the polypteroid-type ganoid scale as the 2017 with long et al., 2015 or Schultze, 2015).
basal osteoichthyan scale type and argued that elasmoid the hypothesis of relationships represented in Fig. 1 for
scales are paedomorphic structures in actinopterygians and Actinopterygii above Ligulalepis is based on Giles et al.
sarcopterygians. (2017), and for basal osteichthyans and sarcopterygians, on
32 Cybium 2018, 42(1)
Schultze Hard tissue in fish evolution
Figure 1. – Appearance of elasmoid scales within osteichthyans shown on an interrelationship scheme of Osteichthyes after Long et al.
(2015), Schultze (2015), and King et al. (2017) for the lower part and after Giles et al. (2017) for the actinopterygians above Ligulalepis.
Node A = Osteichthyes: de, dentine, i, isopedine, r, rhomboid scale; node B = de, dentine, en, enamel, i, isopedine, r, rhomboid; node
c = Sarcopterygii: el, elasmoid; node c’ = r, rhomboid, co, cosmine (dipnoi are represented by Diabolepis and their elasmoid scale by that
of Neoceratodus); node D = Actinopterygii: ga?, questionable for basal taxa, r, rhomboid; canal system of Andreolepis typical for lower
actinopterygians and osteichthyans; node D’ = a, acrodine in Ligulalepis (after Schultze, 2015: fig.13) and higher actinopterygians, ga,
ganoine, r, rhomboid (only branches with elasmoid scale are named in lower actinopterygians). Scales of Lophosteus superbus after Gross
(1968, fig. 1A), of Actinistia after Smith (1940: fig. 70, Latimeria chalumnae), Onychodontida after Andrews et al. (2006: fig. 60b, Ony-
chodus jandemarrai), of Dipnoi after Kerr (1955: fig. 4B, Neoceratodus), of Rhizodontida after Long (1989: fig. 13, Barameda decipiens),
of Tristichopterida after Jarvik (1980: fig. 138 B3, Eusthenopteron foordi), of Holoptychiidae after Ørvig (1957: fig. 13A, Holoptychius
sp.), of Sphaerolepis after Fritsch (1893: pl. 109, fig. 5), of Polypteridae after Rauther (1929: fig. 136, Erpetoichthys calabricus), of Coc-
colepis combination after Agassiz (1843: vol. 2, pl. 26, fig. 7) and Schultze (1996: fig. 4), of Eurycormus (original), of Leptolepis cory-
phaenoides (original), and of an amiid after Grande and Bemis (1998: fig. 201, Cyclurus macrocephalus).
Cybium 2018, 42(1) 33
Hard tissue in fish evolution Schultze
long et al. (2015), Schultze (2015), and King et al. (2017). tems. thus, cosmine is lacking.”). Sire et al. (2009) used, in
Histological features have only limited importance for the addition to cloutier (1996), a paper by Friedman (2007) to
placement of taxa, nevertheless characters such as cosmine argue in favour of cosmine as a basal structure in actinistians
and acrodine are considered characteristic for larger groups. where Styloichthys is interpreted as a basal actinistian. Not
Acrodine, a highly mineralized dentine cap on teeth, occurs considering that in all other trees published by colleagues
only in actinopterygians above Cheirolepis (included). (zhu and Yu, 2002; zhu et al., 2009, 2012), Styloichthys
therefore, Ligulalepis should be placed within actinoptery- appears at the base of the rhipidistians, I still cannot reconcile
gians, if one includes the presence of acrodine in Ligulalepis the position of Styloichthys in Friedman (2007). In Friedman
(Schultze, 2015; justification that the tooth is very likely of (2007) cladogram, Styloichthys appears as the sister group
Ligulalepis: see Burrow, 2002) in the data matrix. cosmine to actinistians, whereas it is closer to porolepiforms in other
is considered characteristic of sarcopterygians. thus, it was cladograms (zhu et al., 2006, 2009; long et al., 2015; King
erroneously reconstructed for �eemannia (zhu et al., 2006; et al., 2017). Styloichthys has 10 characters (Youngolepis
and see above and Schultze 2015: 16), because the genus mistakenly coded as not having an intracranial joint) in com-
was previously placed within sarcopterygians. mon with Miguashaia, but 52 with Youngolepis in Friedman
A rich canal system supplies the dentine in actinoptery- (2007). Styloichthys also lacks an extracleithrum, a typical
gians (see Aldinger, 1937: figs 22, 51 for Cheirolepis; fig. 53 bone of actinistians. consequently, and after the available
for Elonichthys; or fig. 60 for Scanilepis). Aldinger (1937: evidence, I cannot favour the hypothesis that Styloichthys
14) made the scales translucent by applying alcohol, xylene, is an actinistian, and thus an argument that actinistians pos-
anise oil or thin canada balsam, which reveals the canal sys- sessed cosmine. It appears at the present time that cosmine
tem. even thicker thin sections (a method used by Gross; he with the pore-canal system appeared first above Onycho-
did not prepare serial sections as cited by Qu et al., 2017: dontida + Actinistia within sarcopterygians – in lungfish and
1199) give a partial three-dimensional picture, in contrast to rhipidistians. A rich canal system is present in basal osteich-
petrographic thin sections (preferred by Ørvig), which are thyans, such as in Lophosteus (Gross, 1969) and in taxa here
useful in distinguishing tissues. today, the often preferred placed at the base of actinopterygians. Nevertheless, an indi-
pictures gained by the synchrotron (e.g. Qu et al., 2013, cation of a pore-canal system (which opens to the outside
2017) show the canal system beautifully in three-dimen- and might have carried organs sensing pressure changes or
sions. Nevertheless, it does not show the relationships to electroreceptors) is not evident in the taxa with a rich canal
other structures, such as dentine tubules, growth and resorp- system (for carrying vessels and nerves to the dentine and
tion lines, or different tissues. Virtual two-dimensional thin connecting to dermis above the scales). Guiyu as the sister
sections (Qu et al., 2017: fig. 2B, C) yield poor resolution of taxon of Achoania and Psarolepis (Fig. 1) suggests that these
structures that are clearly observable in a normal thin section three taxa have no cosmine because Guiyu has none.
(Qu et al., 2017: fig. 2D).
A canal system comparable to that of palaeoniscimor- Distribution of scale characters on a cladogram
phs is present in Andreolepis (Qu et al., 2017), �eeman- The cladogram in figure 1 is a composite of recently pub-
nia (zhu et al., 2006, 2010 without the reconstructed pore- lished cladograms by long et al. (2015), Schultze (2015),
canal system), Psarolepis (Qu et al., 2013, 2017, the pores and King et al. (2017) for the lower part and by Giles et al.
are arranged in rows as in actinopterygians; bulb-shaped (2017) for the actinopterygians above Ligulalepis. the scale
pore cavities and mesh canals are not present), Guiyu (zhu at the base of Osteichthyes (node A) is a rhomboid scale (r)
et al., 2009) and Achoania (zhu et al., 2001). the longitu- with an isopedine (i) basal part and dentine in the sculptures,
dinal canals follow the ridges on the surface, and the pores and enamel is missing (e.g. Lophosteus; Gross, 1969). the
open between the ridges (e.g. Andreolepis; Gross, 1968; rhomboid shape of the scales persists in actinopterygians
chen et al., 2012; and Qu et al., 2017) as in palaeoniscimor- up to basal holosteans and basal teleosts. Primitive amiids
phs (e.g. Williamson, 1849: pl. 41, fig. 8; Aldinger, 1937: (Sinamiidae) have rhomboid (lepidosteoid type) scales,
fig. 36; Schultze, 2015: fig. 16). Bulb-shaped pore cavities whereas Amioidea and caturoidea have elasmoid scales,
typical for cosmine (see Gross, 1956) are absent in any of with their basal sister group, Parasemionotiformes, hav-
these canal systems. campbell et al. (2010: figs 8A, B, 28A, ing rhomboid scales (Grande and Bemis, 1998). the most
B) figured the bulb-shaped pore cavities very clearly in the basal teleosts, the pholidophorids, have rhomboid scales
outer layer of the cosmine-covered snout of different Devo- (Arratia, 2013), as do closely related groups, such as the
nian dipnoans by micro-X-ray tomography. aspidorhynchids. thus elasmoid scales occur independently
there is no cosmine in early actinistians (zhu et al., in neopterygian groups, the amiides (halecomorphs) and
2012; miscoding of Miguashaia having cosmine in cloutier, teleosts. the advanced palaeoniscimorph taxon Coccolepis
1991, but corrected in cloutier, 1996: 242: “However, none has elasmoid scales on the flanks and rhomboid scales on
of the thin sections of Miguashaia shows the pore canal sys- the upper lobe of the heterocercal caudal tail (Hilton et al.,
34 Cybium 2018, 42(1)
Schultze Hard tissue in fish evolution
2004). Another coccolepid taxon, �orrolepis, possesses knowledge of rhomboid scales in onychodonts or actinis-
elasmoid scale in addition to ganoid scales along the lateral tians with an intermediate canal system.
line (Skrzycka, 2014). the relationship of Jurassic ccooccccoo-- true enamel in cosmine forms one single superficial
lepidae ttoo ootthheerr ppaallaaeeoonniisscciimmoorrpphhss iiss nnoott kknnoowwnn,, nneevveerrtthhee-- layer and shows hexagonal impressions of the basal epi-
less all other Jurassic and triassic Palaeoniscimorpha pos- dermal cells on its surface. the ganoine is characterized
sess rhomboid scales. there exists at least three Palaeozoic by microtubercles and forms multilayered packages within
taxa with elasmoid scales, Cryphiolepis (traquair, 1881), actinopterygians. unclear is the relationship of the enamel
Guntherichthys (Mickle, 2011), and Sphaerolepis (Fritsch, in basal osteichthyans (basal actinopterygians in Fig. 1) to
1893); their relationship to each other and to other palaeo- ganoine or true enamel. Schultze (2015) used the overlap-
niscimorphs in the carboniferous is unknown. One has to ping of the enamel as indication of ganoine. this feature can
assume that the elasmoid scales in these taxa derived from be observed in Guiyu (Qiao and zhu, 2010), a taxon with
rhomboid palaeoniscoid scales, which occur in all other Pal- actinopterygian-like rhomboid scales, and in Psarolepis (Qu
aeozoic palaeoniscimorphs. thus, elasmoid scales already et al., 2013); scales of Achoania are not known. In the actin-
occurred independently in a few palaeoniscimorph actinop- opterygians, overlapping ganoine is known in �eemannia
terygians, and this scale type became established in neop- (zhu et al., 2006).
terygians, the Halecomorphi and teleostei. the rich vascular system in the scales in basal actinop-
Within sarcopterygians, the basal rhipidistians (node terygians (Fig. 1) resembles that in ganoid scales of palaeo-
c’) have rhomboid scales, whereas rhomboid scales are niscimorph and scanilepiform actinopterygians and does not
not known in onychodonts and actinistians. Most dipnoans show characteristics of cosmoid scales of sarcopterygians.
(Diabolepis and descendants) have round scales, except Nevertheless, it cannot be excluded that this is a feature of
the most basal ones, such as Uranolophus (Denison, 1968). basal osteichthyans.
Round scales of some Devonian dipnoans (Dipterus, ��hhiinnoo�-
dipterus, and Griphognathus) possess cosmine on the free
field (Gross, 1956; Ørvig, 1969a; Schultze, 1969), whereas concluSionS
cosmine occurs on rhomboid scales only in rhipidistians,
with the exception of Heimenia (Ørvig, 1969b; Mondéjar- (1) there are two types of rhomboid scales in Osteich-
Fernández and clément, 2012), a taxon with rhombic and thyes, ganoid (palaeoniscoid and lepidosteoid types) and
round scales. In Heimenia, its rhomboid scales and round cosmoid scales. the histological structure of the polypterid
scales possess a thick base of lamellar bone covered by scale, with the occurrence of elasmodine below the dentine
a thick layer of spongy bone, dentine and a single enamel and above the isopedine, is an advanced form of the ganoid
layer (Mondéjar-Fernández and Clément, 2012: figs 8, 9). scale (palaeoniscoid type) within scanilepid palaeoniscimor-
The round scales of Devonian dipnoans have a thick bony phs.
(isopedine) base (Gross, 1956: figs 71, 75), like Heimenia (2) elasmoid scales occur independently in many line-
and other rhipidistians (Gross, 1956: figs 57, 58). Elasmoid ages of osteichthyans. elasmodine is a homoplastic charac-
scales are known in extant dipnoans (Meunier and François, ter, a new formation in each group, where it occurs. It is not
1980) and may already occur in late Paleozoic dipnoans. derived from isopedine (bony basal part of rhomboid scales)
the elasmocytes occur between the lamellae in dipterid in neopterygians, nor from dentine as Sire (1989) suggested
scales, whereas they are within the lamellae in rhipidistian by placing the polypterid scale at the base of osteichthyans
scales (Gross, 1956: figs 57, 58). The external layer is rela- (see also Sire et al., 2009). the elasmoid (round) scales in
tively thick compared to actinopterygian elasmoid scales. rhipidistians are derived independently from forms with
One can observe growth stages, as in the isopedine of the rhomboid scales.
base of rhomboid scales (Gross, 1956: fig. 71A, B). (3) Elasmodine has a ‘plywood’ structure – the fibres ori-
Round scales without cosmine are known only in ony- entation changes from lamella to lamella (detailed descrip-
chodonts and actinistians, where the structure of the elasmo- tions by Meunier, 1980, 1981, 1983, 1984).
dine is well-described for Latimeria by Giraud et al. (1978). (4) Microtubercles are characteristic for ganoine; they
the sequence in the cladogram (Fig. 1) shows that cosmine occur on the surface of ganoine, whereas true enamel shows
occurs only in rhipidistians + dipnoans. Growth stages in the the imprint of basal epidermal cells, a hexagonal design.
form of denticles (or odontodes) occur in the spongy bone (5) Ganoine is characteristic for actinopterygians; it is
below the cosmine, which may support the old hypothesis a special multilayered enamel. Its surface is covered with
that cosmine is a single event, the final cover of the scale in microtubercles. In basal actinopterygians, the ganoine over-
rhipidistians, whereas Westoll-lines indicate growth in dip- laps underlying ganoine only marginally.
noan scales. A phylogenetic connection of cosmine with the (6) cosmine occurs only in rhipidistians and dipnoans.
rich canal system in basal osteichthyans would require the Its superficial layer is true enamel with a hexagonal imprint
Cybium 2018, 42(1) 35
Hard tissue in fish evolution Schultze
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