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Received: 15 September 2017    Accepted: 29 January 2018

DOI: 10.1111/faf.12275

ORIGINAL ARTICLE

Body size evolution and habitat colonization across 100 million

years (Late Jurassic–Paleocene) of the actinopterygian
evolutionary history

Guillaume Guinot  | Lionel Cavin

Department of Geology and

Palaeontology, Natural History Museum of
Geneva, Geneva, Switzerland
Correspondence/Present address
Guillaume Guinot, present address: Institut
des Sciences de l’Évolution de Montpellier
(ISEM), CNRS, IRD, EPHE, Université de
Montpellier, Montpellier Cedex 05, France.
Email: guillaume.guinot@umontpellier.fr
Funding information
Schweizerischer Nationalfonds zur
Förderung der Wissenschaftlichen
Forschung, Grant/Award Number: 200021-
140827
Abstract
Fishes are characterized by their capacity to occupy all aquatic environments and by
their amazing range of size and morphology. While it is known that habitat influenced
the diversity dynamics of fish clades, studies on environmental colonization events
through the evolutionary history of ray-­finned fishes have yielded conflicting results
as to the origin of modern clades and preferential directions of shifts. The effects of
habitat over morphological evolution such as body size remain poorly known in ver-
tebrates. However, body size evolution is more frequently addressed in terms of vari-
ation through time and numerous studies have demonstrated that successive taxa
within a clade tend to increase in size through time (Cope’s or Depéret’s rule). We use
phylogenetic comparative methods on a genus-­level actinopterygian super-­tree
based on extant and fossil data covering the Late Jurassic-­Paleogene interval. Results
indicate marine ancestry for freshwater lineages and a dominance of colonizations
from marine clades towards other habitats. Similar trends in environment occupancy
among different ray-­finned clades are explored. Three main trends affecting non-­
closely-­related clades are recognized: (i) the freshwater invaders, (ii) the predomi-
nantly marine dwellers and (iii) the environmentally labile fishes. Habitat effects on
body size evolution are not statistically supported, but most actinopterygian sub-
clades originate from small-­sized ancestors and tend to increase in size in the course
of their evolutionary history. This trend is clear for lineages restricted for long peri-
ods of time in the same environments, either marine or freshwater, but it is not ob-
served in environmentally labile fish lineages.

KEYWORDS
Actinopterygii, ancestral state reconstruction, Cope’s rule, environmental shifts, marine and
freshwaters, phylogenetic comparative methods

Fish and Fisheries. 2018;1–21. © 2018 John Wiley & Sons Ltd |  1
wileyonlinelibrary.com/journal/faf  
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2       GUINOT and CAVIN

1 |  I NTRO D U C TI O N

1 INTRODUCTION 2
Ray-­f inned fishes (Actinopterygii) are the most successful clade of
2 MATERIAL AND METHODS 3
aquatic vertebrates in terms of both taxic diversity and ecologi-
cal adaptations. This group colonized all existing aquatic environ- 2.1 Phylogenetic framework 3

ments in marine, freshwater and brackish realms and achieved a 2.2 Ancestral habitat reconstruction 3
large array of body sizes and morphologies, mirroring their high 2.3 Ancestral body length reconstruction 4
adaptive morphological disparity. This large range of modes of life 2.4 Modelling body length evolution 4
and environmental distribution makes ray-­f inned fishes a good 3 RESULTS 4
model to address evolutionary processes associated with habitat 3.1 Habitat shifts 4
colonizations and to changes in body size within clades (Albert & 3.2 Shifts in body length and environment 6
Johnson, 2012; Clarke, Lloyd, & Friedman, 2016; Romano et al.,
3.3 
Effect of environment on body length 10
2016; Sallan & Galimberti, 2015). Marine and freshwater realms evolution
differ in physiochemical features that may result in different adap- 4 DISCUSSION 10
tive response among organisms. Transfers between salt waters 4.1 Evolutionary histories of specific clades 10
and freshwaters (and vice versa) imply deep physiological adap-
4.1.1 Freshwater invaders 10
tations, in particular in osmotic regulation, adaptation to varia-
4.1.2 Predominantly marine dwellers 12
tions in temperature and oxygenation. Environmental transfer is
4.1.3 Environmentally labile fishes 13
a rare event when observed at the scale of the animal Kingdom
4.2 General trends in environment occupancy 15
(Lee & Bell, 1999), but this phenomenon happened repetitively
4.3 Body size evolution and Cope’s rule 16
in some specific clades, in particular in ray-­f inned fish groups.
Molecular studies have addressed this issue by mapping environ- 5 CONCLUSIONS 18

mental transfers on phylogenies of some wandering fish clades, ACKNOWLEDGEMENTS 18

such as the clupeiforms (Bloom & Lovejoy, 2014) and the menidiins
(Bloom, Weir, Piller, & Lovejoy, 2013). In other studies, a single
transfer from marine to freshwater environments was detected,
as in the terapontids (Davis, Unmack, Pusey, Johnson, & Pearson,
2012). However, these molecular studies are exclusively based on
living taxa and overlook a great part of the evolutionary history of
these clades provided by fossil data. Large-­s cale analyses of habi-
tat colonizations in actinopterygians are scarce and produced con-
flicting results. Carrete Vega and Wiens (2012) analysed habitat
shifts across the actinopterygian tree and found a freshwater an-
cestry for all extant marine clades as well as absence of different
diversification rates between habitats. However, this study was
largely based on extant taxa, which probably biased the signal. A
recent analysis of actinopterygian habitat colonization and diver-
sification rates showed that including fossil data resulted in an op-
posite pattern where freshwater clades originate from a marine
ancestry (Betancur-­R , Ortí, & Pyron, 2015). The authors further
demonstrated that this signal was deleted by extinctions over the
course of evolution as they found higher turnover rates in marine
clades, which is in agreement with observation of the fossil record
(Guinot & Cavin, 2015, 2016).
Ecological adaptations and body size impact the evolutionary
history of clades (Sibly & Brown, 2007), but the effects of hab-
itat over body size evolution remain poorly known. To date, the
effect of habitat on body size evolution has been addressed for
phytoplankton groups where marine species show larger sizes
than non-­marine ­species, probably in response to different chem-
ical and physical properties of habitats (Litchman, Klausmeier,
& Yoshiyama, 2009; Nakov, Theriot, & Alverson, 2014; Roselli &
Basset, 2015). Yet, the effect of habitat on size remains uncertain
ORCID 18
REFERENCES 18
SUPPORTING INFORMATION 21
within vertebrates and clades encompassing large taxic diversities in
different habitat are scarce. Today, the majority of largest-­sized ray-­
finned fishes live in freshwater environments such as the Mekong
giant catfish (Pangasianodon gigas, Pangasiidae) and the Arapaima
(Arapaima gigas, Heterotidinae) or in mixed environments like the
alligator gar (Atractosteus ­spatula, Lepisosteidae), the white sturgeon
(Acipenser transmontanus, Acipenseridae) and the beluga (Huso huso,
Acipenseridae). Large marine actinopterygians are comparatively
scarce and include the oarfish (Regalecus glesne, Regalecidae) and
the marlins (genus Makaira, Istiophoridae), and reasons for this ap-
parent size contrast between environments remain to be explored.
However, body size evolution has been frequently linked with time
and traditionally referred to as the Cope’s rule [­referred to as the
Depéret’s rule by Bokma et al. (2016)]. Cope’s rule suggests an
­increase in body size throughout lineages evolution, or more pre-
cisely, the tendency of clades to evolve from small sizes (Kurtén,
1953; Stanley, 1973). The Cope’s rule is one of the rare macro-
evolutionary processes that has been observed in a wide array of
continental and marine clades (e.g. Alroy, 1998; Avaria-­Llautureo
et al., 2012; Baker, Meade, Pagel, & Venditti, 2015; Benson, Frigot,
Goswami, Andres, & Butler, 2014; Brown & Maurer, 1986; Clauset &
Erwin, 2008; Gingerich, 1980; Heim, Knope, Schaal, Wang, & Payne,
2015; Laurin, 2004; MacFadden, 1986; McKinney, 1986) and can
better be tested by including information from the analysis of the
GUINOT and CAVIN
fossil record (Bokma et al., 2016). Although partly included in some
large-­scale analyses on Cope’s rule, fish clades have not been con-
sidered specifically using a phylogenetic framework and data from
the fossil record. Based on molecular phylogenies, Knouft and Page
(2003) addressed the body size evolution in North American fresh-
water groups and challenged Cope’s rule. These results might have
been affected, though, by the absence of data from the fossil record.
Recent advances in the understanding of the actinopterygian
evolutionary history and diversification dynamics based on genus-­
level supertrees and fossil record covering 100 million years (Late
Jurassic to Palaeocene) of evolution of the clade provide valuable
data to address the patterns of body size evolution and habitat col-
onization of today’s most diverse vertebrate group. Based on ances-
tral state reconstruction and comparative phylogenetic methods,
we explore habitat shifts between marine, freshwater and mixed-­
environment taxa and test for constraints on the fish body size
evolution.
2 | M ATE R I A L S A N D M E TH O DS
2.1 | Phylogenetic framework
We used one of the actinopterygian genus-­level super-­tree recently
published (Guinot & Cavin, 2016), which includes all actinopterygian
genera known in the Oxfordian–Thanetian interval as well as repre-
sentatives of pre-­Oxfordian clades. Because clades with their fossil
record appearing in post-­Thanetian times (or clades without known
fossil record) may branch within pre-­Thanetian clades, each of the
post-­Thanetian families is represented in our tree by a terminal
taxon. This super-­tree includes 777 terminal taxa and was referred
to as Betancur-­Patterson in Guinot and Cavin (2016). Phylogenetic
relationships are mainly based on Betancur-­R et al., (2013) for ex-
tant clades and on Patterson, (1977) for stem teleosts. Complete
information on this tree topology can be found in Guinot and Cavin
(2016) and Data S1.
The phylogeny was time-­calibrated on the basis of stratigraphic
ranges provided in Guinot and Cavin (2016) for each terminal branch,
using the function timePaleoPhy of the R-­package “paleotree” (Bapst,
F I G U R E   1   Box plot (a) and histogram (b) of log-­transformed body lengths for actinopterygian taxa included in the super-­tree, by habitat
type. 1: marine, 2: freshwater, 3: mixed environments [Colour figure can be viewed at wileyonlinelibrary.com]
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2012). Because subsequent analyses required trees to be fully di-
chotomous, polytomies were resolved in stratigraphic order with an
arbitrary minimum branch length of 0.1 Ma between resolved nodes
to avoid zero-­length branches.
2.2 | Ancestral habitat reconstruction
The environmental distribution of each genus was taken from
Guinot and Cavin (2016) using one of the following three charac-
ter states: (i) marine (all taxa within the genus are exclusively known
from marine environments), (ii) freshwater (all taxa within the genus
are exclusively known from freshwater environments) and (iii) mixed
­environment. The latter character state either includes diadromous
taxa or taxa from brackish environments as well as genera with
widespread environmental distribution that gather some marine,
freshwater and/or brackish taxa.
Ancestral state reconstruction was performed based on max-
imum likelihood using the function ace of the R-­package “ape”
(Paradis, Claude, & Strimmer, 2004). Analyses were ran using three
different models: (i) all transition rates are different (ARD), (ii) tran-
sition rates are symmetrical (SYM), where the transition rate from
environment 1 to 2 equals that from environment 2 to 1, and (iii)
all transition rates are equal (ER). Model fits were then computed
using the Akaike information criterion (AIC). For each node in a tree,
a character state was considered unambiguous when its scaled like-
lihood was >0.33.
Significance of habitat 3 that includes different kinds of environ-
ments may be difficult to assess. Hence, although analyses were run
on our three-­environment data, we also considered reconstructed
ancestral habitats resolving environment 3 as marine or freshwater
according to posterior probabilities of ancestor. For each terminal or
internal node initially coded as mixed environment, we assigned a hab-
itat code (either marine or freshwater) corresponding to the habitat of
parent node. An alternative to this would have been to assign a marine
or freshwater habitat a priori to each terminal branch prior to ASR
analyses. Yet, this method would be arbitrary and most assignments to
freshwater or marine habitat would be arguable, especially for diadro-
mous taxa or taxa gathering species of different habitats.
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4       GUINOT and CAVIN
2.3 | Ancestral body length reconstruction
Total body length values were collected for each terminal taxon
represented in the phylogenetic tree, along with their corre-
sponding habitat distribution (Figure 1). Body lengths for fossil
genera were extracted from the literature, notably from Albert,
Johnson, and Knouft (2009), using the maximum value among all
species of a given genus. Body length values for taxa represent-
ing post-­T hanetian families where mostly extracted from Albert
et al. (2009) and fishbase (Froese & Pauly, 2016). When only
standard length was available, we estimated the total length by
adding a percentage of the total length corresponding to the cau-
dal fin based on the gross morphology of representatives of the
clade. Ancestral body length reconstruction was performed using
maximum-­likelihood ancestral state reconstruction provided by
the fastAnc function of the R-­p ackage “phytools” (Revell, 2012).
Because raw (untransformed) size data are highly right-­skewed,
size values were log10 -­t ransformed to allow an increase or de-
crease of a certain amount with equal probability (see O’Meara,
Ané, Sanderson, & Wainwright, 2006).
2.4 | Modelling body length evolution
In order to test for potential effects of environment of habitat on
fish body size evolution, we used the function OUwie from the R-­
package “OUwie” (Beaulieu & O’Meara, 2016) to fit likelihood mod-
els for a continuous character (here body length) evolving under
a discrete selective regime (habitat). Fit of actinopterygian body
length evolution was compared between Brownian motion models
(BM) and different Ornstein–Uhlenbeck models (OU). Among the
tested models, two of them represent independent evolution of
body size and habitat: the single-­r ate Brownian model (BM1) and
the OU model with a single optimum (θ) for all taxa (OU1). Other
tested models represent an influence of the selective regime over
body size evolution, these include: Brownian motion with different
rate parameters for each state on the tree (BMS), OU model with
different state means and a single strength of selection (α) and rate
2 ancestor’s state, with 55 shifts from marine to freshwaters and
of stochastic motion around the optima (σ ) for all selective regimes
(OUM), and OU models that assume different state means and mul-
tiple σ2 (OUMV), or different state means and multiple α (OUMA),
or different state means with multiple α and σ2 per selective regime
(OUMVA).
All analyses were performed using R version 3.2.2 (R
Development Core Team, 2010).
3 |   R E S U LT S
3.1 | Habitat shifts
Maximum-­likelihood analyses indicate that among the three tested
models for habitat reconstruction, the ARD model allowing for dif-
ferent transition rates in any environment shift direction has the
best fit based on both AIC and log-­likelihood scores (Table 1). ARD
TA B L E   1   Fit of alternative models of ancestral state
reconstruction for environmental distribution of actinopterygians
Models AIC ∆AIC AIC weights -­lnL
ER 1121.635 18.48071 9.658497e-­05 −559.8176
ARD 1103.155 0.00000 9.952811e-­01 −545.5773
SYM 1113.899 10.74428 4.622271e-­03 −553.9494
ER, Equal rates; ARD, All rates different; SYM, symmetrical.
models tend to be more supported by log-­likelihood because of their
higher complexity in comparison with other models. However, AIC
score computation penalizes models proportionally to the num-
ber of included parameters (the transition rates, in our case) and
hence compensates for this potential complexity effect. Therefore,
habitat reconstructions based on the ARD model were used in our
analyses (Figure 2). Under this model, all nodes were given a pos-
terior probability above 0.5, except node 989 (lik = 0.41) and are
all considered unambiguous (lik > 0.33). Nevertheless, regardless
of the models’ fits, all three models support a similar trend in the
polarity of habitat shifts among ray-­f inned fish taxa (Table 2; Table
S1). All models agree on a strong dominance of habitat shifts (120
according to the ARD model) originating from the marine realm
towards other habitats (freshwater or mix). Conversely, coloniza-
tion events of marine and mixed environments by primarily fresh-
water clades appear scarcer in the actinopterygian evolutionary
history (18 and 11, respectively). These colonizations originating
from the freshwater environment typically involve a single termi-
nal taxon in the tree, either towards the marine realm (Coccolepis,
Scheenstia, Tomognathus, Solnhofenamia, Pachyamia, Protelops,
Pseudoegertonia, Prognathoglossum, Thorectichthys, Rhombichthys,
Triplomystus, Tycheroichthys, Chanoides, Sorbinicharax) or to-
wards the mixed environments (Huso, Acipenser, Araripelepidotes,
Calamopleurus, Brychaetus, the post-­T hanetian percichthyids,
Kwangoclupea, Arius). The majority of habitat shifts occurred to-
wards the mixed environment, mainly from primarily marine
clades. A similar trend is recovered when nodes coded as mixed en-
vironments were passed to marine or freshwater according to their
21 shifts in reverse direction (Table S2). Maximum-­likelihood esti-
mates of transition rates under the ARD model indicate low rates
for the marine-­freshwater, freshwater-­marine and freshwater-­
mixed transfers whereas highest rates are found for mixed marine,
mixed freshwater and marine ­mixed (see Table S3).
Our results indicate a marine ancestry for the entire actinopte-
rygian clade. Basal-­most clades such as Cladistia, Chondrostei,
Lepisosteiformes, Amiiformes, whose living representatives are
known from freshwater or mixed environments all arose from a marine
ancestry. In addition, all major freshwater clades within teleosts (e.g.
Osteoglossomorpha, Ostariophysi) and freshwater clades included in
otherwise mostly marine clades (Elopomorpha, Paracanthomorpha,
Euacanthomorphacea) originated from a marine ancestor.
Time-­scaling of the actinopterygian super-­tree allowed the iden-
tification of periods of habitat shifts for the three-­habitat data set
GUINOT and CAVIN |
      5

F I G U R E   2   Time-­calibrated actinopterygian genus-­level super-­tree with mapped reconstructed habitat distributions (left) and body
lengths (right) [Colour figure can be viewed at wileyonlinelibrary.com]
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6       GUINOT and CAVIN

TA B L E   2   Number of environmental shifts identified across phylogeny with the ARD model (see Table S1 for results provided by other
models)

Shifts 1 to 2 1 to 3 2 to 1 2 to 3 3 to 1 3 to 2 to 1 to 2 to 3 from 1 from 2 from 3

Terminal 27 62 14 8 15 9 29 36 70 89 22 24
Internal 18 13 4 3 7 3 11 21 16 31 7 10
Total 45 75 18 11 22 12 40 57 86 120 29 34

1: marine, 2: freshwater, 3: mixed environment.

(Figure 3), where shift ages as used here correspond to the stem age
of a clade. Results indicate that habitat colonizations realized by pri-
marily marine taxa regularly occurred in the actinopterygian evolu-
tionary history but habitat shifts from a marine ancestry reached
peaks in the Kimmeridgian and Cenomanian. Conversely, coloniza-
tions of the marine realm by non-­marine ray-­finned clades are scarce
in the Late Jurassic-­Palaeocene interval and are largely achieved
by primarily mixed-­environment clades (Kimmeridgian, Berriasian,
Albian; Figure 3b). An exception to this is the Hauterivian where
marine colonizations are achieved by primarily freshwater taxa
(Figure 3b,c), most of which (four out of five) belong to Cenomanian
clupeomorph genera (Thorectichthys, Rhombichthys, Triplomystus,
Tycheroichthys) (see below). Our two-­habitat data set indicates the
same trend with a high number of freshwater colonizations by ma-
rine taxa (Figure S1).
3.2 | Shifts in body length and environment
In order to qualitatively assess shifts in body size through the ac-
tinopterygian tree, we extracted size data for each node in the
tree based on our ML ancestral state reconstruction (Figure 2).
Size shifts were acquired by taking the difference between sizes
at a node/terminal branch and at its corresponding parent node.
Major positive and negative shifts in size were identified by se-
lecting values lying above and below the upper and lower whisk-
ers, respectively, of the box-­a nd-­w hisker plot performed on all
size shifts over the tree. Shift ages were identified by selecting
the stem age of a node and the environment corresponding to
the size shift is the state of the node under concern. This allowed
the identification of the proportion of positive and negative shifts
in size according to environments (Figure 4). This indicates that

F I G U R E   3   Temporal (geological stages) distribution of habitat shifts (blue: marine; green: freshwater; red: mixed environment) in the
actinopterygian tree. Shift ages of a taxon correspond to the age of its parent node [Colour figure can be viewed at wileyonlinelibrary.com]
GUINOT and CAVIN |
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F I G U R E   5   Proportion of major and minor positive and negative

F I G U R E   4   Proportion of size shifts within stable environment
and during environmental transitions
most size shifts (88%) did not occur during environment coloni-
zations, but within a given environment. However, the ratio of
the number of major size shifts/total size shifts is higher during
environmental colonizations than within environments, for both
size shifts according to environment and environmental colonization
events (1: marine; 2: freshwater; 3: miwed environments) [Colour
figure can be viewed at wileyonlinelibrary.com]
positive and negative major size shifts (Figure 4). An exception
to this is the negative size shifts during habitat colonizations for
clades originating from freshwater environments (Figure 5), which
include only one major negative shift (Sorbinicharax, from fresh-
water to marine). Nevertheless, although major positive shifts ac-
count for a limited proportion of total shifts in marine fish clades

F I G U R E   6   Temporal distribution of size shifts. Major size shifts are represented in color (blue: marine; green: freshwater; red: mixed
environments) with corresponding environmental context according to habitat distribution of parent and descendent nodes [Colour figure
can be viewed at wileyonlinelibrary.com]
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8       GUINOT and CAVIN

environments are linked with positive shifts in size (over 90.9%

F I G U R E   7   Variations of mean (Log) body lengths (including
internal nodes values) through time per environments. Blue: marine,
green: freshwater, red: mixed environments [Colour figure can be
viewed at wileyonlinelibrary.com]
(94 out of 974), a large fraction (13) of the top 20 most dramatic
size increases occurred in the marine realm (Data S2). Figure 5
shows that a large proportion of habitat shifts towards mixed
from freshwater and 70.6% from marine), including a number of
major shifts (45.5% from freshwater and 36% from marine) (see
below). A similar trend, although less marked, is found for positive
shifts towards the marine realm, particularly when taxa originate
from freshwater environments. More generally, there is a trend to
size increase during habitat shifts for taxa originating from fresh-
waters. Conversely, size shifts related to colonization of freshwa-
ter habitats are dominated by negative trends. Once turned to
binary (Figures S2 and S3), our data show that habitat coloniza-
tions of marine environment are mainly linked with size increases,
whereas environmental shifts towards freshwaters mainly involve
size decreases.
Our time-­c alibrated tree allowed the identification of the tim-
ing of major size shifts in their environmental settings (Figure 6; see
also Data S2) during the time interval of interest here (Oxfordian–
Thanetian). The upper Jurassic (Oxfordian–Kimmeridgian) is rep-
resented by a high proportion of major positive size shifts either
within or originating from the marine environment (mainly towards

TA B L E   3   Parameters of the regression equations and mean body size for each main actinopterygian clade

MBS, Mean body size (Log) of the clade; ANS, ancestral node size (log) of the clade; MSA, mean size (log) for actinopterygians (=2.3636).
*Indicate statistically significant results.
Colors refer to environment (green: freshwater; blue: marine; red: mixed environments).
[Colour table can be viewed at wileyonlinelibrary.com]
GUINOT and CAVIN       9 |
the mixed environments). All size shifts in the Oxfordian occurred from the marine realm). As for the Campanian, the greater part of
within stable environments. The Hauterivian and Barremian stages major positive size shifts occurring during environmental transfers
include a majority of major positive size shifts either within or occur during colonization of mixed environments. These trends are
originating from the freshwater environment, but many major size also observed when habitat data are restricted to marine and fresh-
decreases also occurred within this environment. The Cenomanian waters (cf. Figure S4 and Data S3).
shows a high proportion of major positive shifts in size related to the We computed the variations of mean body size through time
marine environment, either within or originating from this environ- (Figure 7) according to environment (marine, freshwater and mix) of
ment. The greater part of major positive size shifts occurring during both internal nodes and terminal taxa for all geological stages con-
environmental colonizations originate from the marine realm. This sidered here. There is a clear trend in the dominance of large fishes
stage is also marked by a high number of major negative size shifts in the marine realm during the Oxfordian–Aptian interval (with the
occurring within the marine realm, although the two most dramatic exception of the Tithonian) whereas freshwater fishes show the low-
negative size shifts occurred within freshwater clades (Pantodon est mean size. This trend is inverted after the Aptian where mixed-­
and Serenoichthys, see below). All these Cenomanian negative environment clades show an increase of their mean size, which
shifts occurred in stable environments. The Turonian–Santonian exceeds the mean marine fish size. A marked mean size decrease
interval includes very few major size shifts during environmental characterizes the Hauterivian-­Barremian interval for freshwater
colonizations with only two positive shifts (from marine to mixed taxa. This is apparently contrasting with the number of major size
environment). Most of major size shifts occurring in the Campanian increases in this interval and is related to the high number of coeval
are within the freshwater or marine realms. Yet, the bulk of major major and minor size decreases in this environment. Mean size in-
Campanian size shifts occurring during environmental transfers is creases markedly during the Aptian–Cenomanian interval for fresh-
positive and occurs during colonization of mixed environments (e.g. water groups and stays relatively stable until the Selandian peak.
the Megalopidae, which show the biggest size increase, originate Dramatic mean size decreases occurred in the Kimmeridgian and
from a marine clade). Similar trends are found for the Maastrichtian, Cenomanian for marine taxa, which both correspond to marked di-
although this stage includes a lower number of shifts. Most major versifications (Guinot & Cavin, 2016). A strong mean size increase oc-
negative size shifts occur in marine clade during the Palaeocene and curred following the Cenomanian and a second one is present in the
very few during environmental colonizations (mainly originating Danian. Mean size of mixed-­environment taxa gradually increases
during the mid-­Cretaceous and stays high until the Cainozoic. Similar
TA B L E   4   Fits of macroevolutionary models for actinopterygian trends are observed for binary data (Figures S5).
body size evolution (refer to text for model descriptions) Results of body size reconstruction were subset into 28 datasets
representing major actinopterygian clades. Body size values of inter-
Models AIC ∆AIC AIC weights
nal nodes, terminal taxa and parent node of the clade were extracted
BM1 972.5297 196.39347 2.255890e‐43
for each of the selected groups, and linear regressions between time
OU1 932.0075 155.87132 1.420990e-­3 4 and body size values were calculated. Table 3 shows parameters of
BMS 952.1017 175.96551 6.154487e-­39 the regression equations and mean body size for each main acti-
OUM 934.8657 158.72947 3.403701e-­35 nopterygian clade. Among the 28 selected clades, 85.7% (24 clades
OUMA 790.2056 14.06942 8.799964e-­0 4 including 12 with p < .05) show a trend for size increase through time
OUMV 925.6864 149.55015 3.351321e-­33 and 14.3% (4 clades including 2 with p < .05) show a size decrease
OUMVA 776.1362 0.00000 9.991200e-­01 though time (Table 3).

TA B L E   5   Summary of parameter values for models of actinopterygian body size evolution

BM1 (SE) BMS (SE) OU1 (SE) OUM (SE) OUMA (SE) OUMV (SE) OUMVA (SE)

Θ[1] 2.3689 (0.4211) – 2.3812 (0.1246) 2.3806 (0.1254) 2.5304 (0.0468) 2.3801 (0.1368) 2.5165 (0.0508)
Θ[2] – – – 2.5642 (0.4369) 2.5841 (0.0975) 2.6402 (0.3769) 2.5425 (0.0971)
Θ[3] – – – 4.1860 (1.7939) 2.8490 (0.3422) 4.5315 (1.9059) 2.6008 (0.0874)
α[1] – – 0.0040 (0.1450) 0.0040 (0.1461) 0.0221 (0.1102) 0.0039 (0.1551) 0.0210 (0.1302)
α[2] – – – – 0.0216 (0.1165) – 0.0213 (0.1230)
α[3] – – – – 0.0225 (0.1091) – 0.0289 (0.0849)
σ2[1] 0.0083 (0.0507) 0.0090 (0.0674) 0.0124 (0.0830) 0.0124 (0.0832) 0.0119 (0.0806) 0.0138 (0.0962) 0.0122 (0.0819)
σ2[2] – 0.0049 (0.1448) – – – 0.0074 (0.1643) 0.0082 (0.5680)
σ2[3] – 0.0108 (0.1762) – – – 0.0139 (0.1880) 0.0001 (0.9311)

Θ: phenotypic optimum; α: strength of selection; σ2: rate of stochastic motion; 1: marine; 2: freshwater; 3: mixed environment; SE: standard error.
 |
10       GUINOT and CAVIN

F I G U R E   8   Schematic representation
of body size and environmental shifts of
actinopterygian lineages between the
Late Jurassic and the Palaeocene. Only
examples taken from the categories
“Freshwater invaders” and “Predominantly
marine dwellers” are figured. Large
silhouettes illustrate major positive
body size shifts associated with deep
nodes (shift associated with terminal
taxa are excluded), and small silhouettes
illustrate major negative body size shifts
associated with deep nodes. See text for
details [Colour figure can be viewed at
wileyonlinelibrary.com]

4 | D I S CU S S I O N
3.3 | Effect of environment on body
length evolution
4.1 | Evolutionary histories of specific clades
Brownian motion models received less support than any of the
In this section, we highlight the main trends observed in habitat col-
OU models. The OUMVA model allowing each habitat to take
onization and in body size evolution observed among the main ac-
a separate optimum, strengths of selection (α) to vary among
tinopterygian clades during the Late Jurassic-­Palaeocene interval.
habitats and rate of stochastic motion (σ 2) to vary away from
Although each fish clade has its own evolutionary history, which
the optimum received best AICc support (Table 4). All alterna-
depends of intrinsic biological factors as well as external abiotic
tive models received low support (AICw < 8.79 × 10 −4) with
factors, we were able to recognize three main trends that involve
ΔAIC > 14 for the second best-­s upported candidate models
different, non-­phylogenetically-­related clades: (i) the freshwater in-
(OUMA). The OUMVA model and other OU model all indicate
vaders, (ii) the predominantly marine dwellers and (iii) the environ-
larger optimal size in mixed-­e nvironment taxa than in other
mentally labile fishes. Figure 8 synthetizes these observations for
habitats (Table 5), and thetas for freshwater taxa are slightly
categories 1 and 2. Category 3 shows too complex patterns to be
higher than for marine taxa. These results agree with our results
illustrated in this way. In this figure, environmental shifts are repre-
on size shifts showing a large majority of size increases within
sented in a simplistic way (not all habitat shifts are represented) and
mixed-­e nvironment clades. Maximum-­likelihood estimates sug-
only major body size shifts (large silhouettes for positive shifts and
gest differences among the various parameters, but standard
small silhouettes for negative shifts) occurring in deep nodes (i.e.
errors indicate these differences might not be significant. A
not those affecting terminal genera in our phylogeny) are depicted.
parametric bootstrap using 10 replicates was performed to esti-
mate the confidence interval for each parameter in the OUMVA
models (Table S4), but this provided overlapping scores between
4.1.1 | Freshwater invaders
environments.
Once turned to binary (marine and freshwater), the OUMA Cladistia plus some “palaeonisciforms”
model that allows body size to evolve towards different peaks with This clade was artificially found in the computed phylogeny based
different strengths of pull towards the peak (but with equal rates) on the stratigraphic distribution of the occurrences. In our data set,
was best supported (Table 4). However, the OUMVA model also re- the non-­monophyletic “palaeonisciforms” gather various genera of
ceives strong support and all OU models better fit the data than the doubtful affinities, mostly Asian forms from the Late Jurassic and
BM model. In all OU models, thetas for freshwater taxa are higher Early Cretaceous (Uighuroniscidae and other genera). They gather
than for marine taxa, but differences are not significant (overlapping late representatives of older lineages locked in freshwater environ-
score with standard errors). ments, which acted as a refugium (Cavin, 2017). Some nodes within
GUINOT and CAVIN
this non-­monophyletic group are associated with major size in-
creases, none with major size decreases.
The cladistia is a distinctive clade, which appeared in our analysis
in the fossil record in the basal late Cretaceous of Africa (Dutheil,
1999). One major size increase is detected for Polypterus, and one
major size decrease is observed for Serenoichthys, which is the only
Cretaceous genus known by articulated material. The average body
size of the clade is slightly lower than the average mean body size
of ray-­finned fishes, and there is a significant body size increase in
time, but the slope of the regression is shallow. Because most of the
Cretaceous cladistians are imperfectly known and the phylogenetic
relationships are unresolved, we regard these results as tentative.
Giles, Xu, Near, and Friedman (2017) showed that a set of Triassic
scanilepid genera actually belong to the polypterid lineage. Most of
these fishes are found in freshwater deposits of Central Asia (Xu,
Gao, & Finarelli, 2014). In Giles et al.’s phylogeny, the sister clade
of polypterids plus other Actinopterygii is Saurichthys, an ubiquitous
Triassic genera, whose most species lived in marine environment
(Maxwell, Romano, Wu, & Furrer, 2015). If true, this pattern indi-
cates that cladistians moved towards freshwater environment prob-
ably at the end of the Palaeozoic.
Acipenseriformes
Based on our phylogeny, the three families of acipenseriforms
(peipiaosteids, polyodontids and acipenserids) experienced three
distinct shifts towards freshwater environments. This pattern is
caused by the marine distribution of Chondrosteus, which is situ-
ated in a basal position within the clade. Interestingly, the anadr-
omous habitus of the extant Huso and Acipenser (Bemis, Findeis,
& Grande, 1997) is interpreted here as a return to a partly marine
mode of life from strictly freshwater ancestors. This scenario cor-
responds to the evolutionary sequence proposed by Gross (1987)
for the origin of anadromy in the temperate zone. Acipenserifoms
have the second largest average body size among the set of com-
pared clades, and their show a positive correlation of size with
time, although barely not significant (p = .052). Within the clade,
six nodes are associated with major size decreases and five are
associated with major size increases, including the highest value
of positive size shift for all compared clades at the supporting
node of all acipenseriforms (not visible on Figure 6 because it
happened 251 mya). All increases concern terminal genera. The
significant size increase detected at the origin of the group is fol-
lowed by several decreases of body size affecting deep nodes as
well as terminal genera. Interestingly, most body size decreases
occurred in the Jurassic and in the Late Cretaceous, while most
size increases occurred in the terminal Cretaceous and the
Paleogene (plus the initial one). Although mostly found in fresh-
water environments since the Cretaceous and hence included in
the “freshwater invaders” group (#1), the history of acipenseri-
forms shares evolutionary features with environmentally labile
fishes (see below), such as multiple invasions towards freshwater
and anadromy.
|
      11
Ginglymodi
Two shifts from marine towards freshwater are observed in this
clade. One of the shifts concerns a likely artificial group of three gen-
era (Sinolepidotus, Neolepidotes and Lepidotyle), whose relationships
with other ginglymodians are unresolved in the original phylogeny
and which are grouped together here because of stratigraphy. The
other shift corresponds to a node resolved in most recent phylog-
enies. It corresponds to the lepisosteiforms (sensu López-­Arbarello,
2012) minus the basal-­most Lepidotes and Scheenstia, which were
both marines. During the Cretaceous, most lepisosteiforms were
from freshwater with only a few brackish forms (obaichthyids,
Araripelepidotes). The crownward lepisosteids (sensu Grande, 2010)
were exclusively from freshwater since the Late Cretaceous up to the
present, with just some incursions in brackish or marine waters for
Atractosteus today. The major size increases occurred mostly in ma-
rine environments, although two major positive shifts also occurred
in freshwater for two genera (Paralepidosteus and Atractosteus). One
is associated with a shift from freshwater to marine environment
(Scheenstia). It corresponds to one of the rare body size increase
associated with a shift from freshwaters to marine environments.
It worth noting, however, that although always resolved as a basal
lepisosteiform, the exact phylogenetic position of Scheenstia is still
debated (see for instance Deesri, Lauprasert, Suteethorn, Wongo,
& Cavin, 2014; Gibson, 2013; López-­Arbarello, 2012; Sun & Ni,
2017). Consequently, the shift associated with Scheenstia is not il-
lustrated in Figure 8. The only positive major size shifts associated
with deep nodes (i.e. excluding nodes supporting terminal genera)
concern the lepisosteiforms (Lepidotes and crownwards) and a clade
of macrosemiids (Macrosemius and Macrosemiocotzus). Both oc-
curred in marine environment (the former is not visible in Figure 6
because it happened 226 mya). Among the five negative major body
size shifts, three concern deep nodes: two clades of macrosemiids in
marine environment and the probable artificial clade Sinolepidotus,
Neolepidotes and Lepidotyle discussed above. The average body size
of the ginglymodians is slightly higher than of the actinopterygians
in average, and there is a good positive correlation of body size with
time, although the slope is shallow.
Halecomorphi
In this clade, a single shift from marine to freshwater environments
occurred at the node corresponding to the Amioidea (sensu Grande &
Bemis, 1998). Within this clade gathering 14 genera, the only returns
to marine conditions are Solnhofenamia, Pachyamia and Tomognathus
[the latter is here resolved as the sister group of sinamiids but this
relationship remains uncertain (Cavin et al., 2007; Forey & Patterson,
2006)]. Calamopleurus was possibly living in brackish environments
as indicates its occurrence in the Moroccan Kem Kem beds. As for
the ginglymodians, the Late Cretaceous and Cainozoic records of
halecomorphs are exclusively from freshwater environments. The
major negative size shifts affected exclusively terminal genera. The
only major positive size shift associated with a deep node (i.e. ex-
cluding the three most important ones that affected Calamopleurus,
 |
12       GUINOT and CAVIN
Macrepistius and Melvius) concerns the node Amiiformes sensu
Grande and Bemis (1998), that is Caturoidea and Amioidea. This body
size increase occurred in marine environment. The node associated
with the main shift from marine to freshwaters is not associated with
any major size shifts. Body size evolution of halecomorphs resembles
the body size trends observed in ginglymodians, that is an average
body size slightly higher than the average actinopterygian body size,
and a significant positive correlation of body size with time charac-
terized by a shallow slope (slow increase with time).
Basal teleosts
In our fully dichotomous time-­scaled phylogeny, a mostly freshwa-
ter clade is branched as the sister group of pachycormiforms plus
more derived teleosts. This artificial clade (i.e. an original poly-
tomy resolved on the basis of the stratigraphic distribution of taxa)
contains two identified but poorly defined freshwater families,
the Siyuichthyidae and the Archaeomaenidae, which are gathered
with two genera of basal marine teleosts with uncertain affini-
ties, Oligopleurus and Pholidophorichthys. Recently, Sferco, López-­
Arbarello, and Báez (2015) identified another clade of freshwater
basal teleosts composed of three genera restricted to Gondwana
(Waldmanichthys, Cavenderichthys and Luisiella). Although no mor-
phological evidences support a clade gathering these stem teleosts,
which are characterized by a low morphological disparity (Clarke
et al., 2016), it is noteworthy that basal teleosts have thrived in
freshwaters very early in their evolutionary history.
Osteoglossomorpha and Otophysi
These living freshwater clades are phylogenetically not related to each
other, but they share environmentally and morphological traits during
their evolutionary history. Only the first part of the evolutionary histo-
ries of these clades, in particular of the otophysans, is addressed here
because of the selected time interval chosen. Based on our phylogeny,
a single shift occurred from marine to freshwater realms at the base of
both clades, probably in the Jurassic for the osteoglossomophs and in
the Early Cretaceous for the otophysans. No true basal osteoglosso-
morphs have been recognized in marine deposits, but their marine ori-
gin is inferred from the ancestral habitat reconstruction. Several stem
ostariophysan genera, contrariwise, are known from marine or brack-
ish environments, in particular Clupavus, Lusitanichthys and Chanoides.
In the first part of their evolutionary history, Osteoglossomorpha and
Otophysi share general morphological trends, such as a relatively
small average body size (Table 3) and relatively few major body size
shifts. The shift towards freshwater is associated with a major positive
body size shift for otophysans, but not for osteoglossomorphs. In the
osteoglossomorph lineage, three major positive size shifts are identi-
fied during the Early Cretaceous. In the otophysan lineage, one major
positive size shift occurred at the origin of the gymnotiforms and one
major negative size shift among siluriforms (Incaichthys + Hoffstetteric
hthys), both occurring at the end of the Cretaceous. The body size in
both clades is highly positively correlated with time.
Both clades also experienced returns to marine and mixed
environment at the beginning of the Cainozoic. Among the
osteoglossomorphs the returns concern the marine Phareodus,
Ridewoodichthys, Opsithrissops and Magnigena and among otophysans
the returns concern the mixed ariids. In our phylogeny, the freshwater
extant Scleropages is resolved as the sister genus of the marine extinct
Magnigena, a pattern which implies a secondary return from marine to
freshwater for Scleropages, which is furthermore associated to a major
body size increase. Because of the weak support of this phylogenetic
hypothesis (resolved on the basis of the stratigraphic ranges of gen-
era), we regard this relationship and its environmental implication as
tentative (the shift is not figured in Figure 8). Other, more dubious
Cretaceous returns to the marine realm have been suggested for both
clades, that is Prognathoglossum in the Cenomanian among osteoglos-
somorphs and Sorbinicharax in the terminal Cretaceous among oto-
physans. Both marine invasions are associated with major body size
shifts. These environmental and body size shifts, however, should be
regarded with caution. The highest measured size decrease (−1.01) is
associated with the sister genus of Prognathoglossum, that is Pantodon
and the second size decrease is associated with Sorbinicharax it-
self. The phylogenetic position of Sorbinicharax used here rests on
the original study of this fish by Taverne (2003), who assigned it
to the Characiformes. However, a recent revision of this species
(Mayrinck, Brito, Meunier, Alvarado-Ortega, & Otero, 2017) indicates
that Sorbinicharax is not an otophysan but should be regarded as a
Teleostei incertae sedis on the basis on the available material. The size
decreases associated with Pantodon rests on Taverne and Capasso
(2012)’s identification of Prognathoglossum as a pantodontid (a result
used in our phylogeny) because this odd-­looking fish shares cranial
characters with Pantodon. But Prognathoglossum also exhibits fea-
tures very different from pantodontids, especially in the post-­cranial
skeleton. Consequently, we consider the systematic affiliation of this
genus as uncertain for the moment and we regard the very important
size decrease for Pantodon, as well as the shift from freshwaters to
marine environment identified for Prognathoglossum, as highly tenta-
tive. If Prognathoglossum will prove to be a pantodontid, however, it
is worth noting that its strong morphological disparity compared to
its sister genus Pantodon is in contradiction with the morphological
stasis observed in the extant Pantodon (Lavoué et al., 2011). These
two possible Cretaceous marine incursions (Prognathoglossum and
Sorbinicharax) are not figured in Figure 8.
4.1.2 | Predominantly marine dwellers
Pachycormiformes, Tselfatiiformes and Aulopiformes
The three clades, phylogenetically distant, are exclusively marine
except the mixed or freshwater Concavotectum (a tselfatiiform not
included in Figure 8) and of the mixed aulopiform family synodon-
tids. Pachycormiforms and tselfatiiforms are extinct and charac-
terized by an average large body size, and the three clades show
body size increase with time (but the correlation is significant
only for the tselfatiiforms). Pachycormiforms have proportionally
more major size shifts, with a larger proportion of positive shifts
than the tselfatiiforms and the aulopiforms. The pachycormiforms
comprise the largest ray-­f inned fishes ever (Friedman et al., 2010).
GUINOT and CAVIN
The highest size shift increase in the clade concerns a group of
giant genera (Bonnerichthys, Rhinconichthys, Leedsichthys and
Astenocormus). This shift is among the highest (the 4th) for all com-
pared ray-­f inned fishes. In tselfatiiforms, one major size increase
occurred at the origin of the group. Pachycormiforms and tselfatii-
forms were affected by major size decreases, but these concerned
only terminal genera. Among aulopiformes, two major body size
shifts, a positive one and a negative one affected clades at the base
of the Late Cretaceous.
Aspidorhynchiformes, Ichthyodectiformes and
Protobramoidei-­Pachyrhizodontoidei
The three clades, whose phylogenetic relationships among teleoste-
ans, are still debated but which are not related to each other, went
extinct at the end-­Cretaceous mass extinction. Aspidorhynchiforms
and ichthyodectiforms are well-­characterized clades, while
protobramoids-­pachyrhizodontoids is an unnamed clade of stem
clupeocephalans found by Cavin (2001), whose monophyly remains
to be confirmed. Aspidorhynchiforms and ichthyodectiforms have
among the highest average body size of all compared clades (only
overpassed by pachycormiforms) and both display a significant
positive correlation between size and time (Table 3). The slope of
the regressions is steep compared to other basal teleosts or non-­
teleosteans (only some acanthomorphs have steeper slopes), in-
dicating a rapid increase of body size during the Cretaceous. The
mean body size for the protobramoids-­pachyrhizodontoids is close
to the average actinopterygian body size, and the correlation be-
tween body size and time is positive but not significantly. In as-
pidorhynchiforms and ichthyodectiforms, major positive body size
shifts occurred at the base of the clade for the former and near the
base of the clade for the latter (i.e. the node gathering Thrissops and
more derived clade). Some of the largest calculated body size shifts
affecting terminal taxa concern three Late Cretaceous giant genera
included in these groups, Pachyrhizodus within the pachyrhizodon-
toids, and Ichthyodectes and Xiphactinus within the ichthyodecti-
forms. Major size decreases are absent in aspidorhynchiforms, but
they affected a group of two genera among ichthyodectiforms
(Heckelichthys plus Garganoichthys) and a clade of three Libanese
genera among protobramoidei (Abisaadichthys, Eusebichthys and
Protobrama).
The three clades experienced several shifts towards mixed or
freshwater environments, but few are associated with major body
size shifts. A positive body size shift affected the ichthyodecti-
form Aidachar during its shift towards freshwater, and a positive
body size shift affected the pachyrhizodontoid Notelops during
its shift towards mixed environments. The mainly marine ich-
thyodectiform fishes colonized freshwater environments during
the Early Cretaceous in Eastern Asia (Chuhsiungichthyidae), and
mixed and freshwater environments during the “mid”-­C retaceous
(Cladocyclus, Chiromystus, Aidachar) in Western Gondwana.
Among the poorly diversified aspidorhynchiforms, Vinctifer was
possibly euryhaline and Belonostomus freshwater during the Late
Cretaceous. Within the protobramoids-­p achyrhizodontoids group,
|
      13
Notelops, Rhacolepis and Araripichthys were dwellers of mixed
environments.
Pycnodontiformes
The clade comprises mostly marine genera but also a handful of gen-
era from mixed and freshwater environments. The average body size
is smaller than the average ray-­finned fish body size, but there is no
significant correlation between body size and time. Two major posi-
tive body size shifts are detected in marine environment for deep
nodes (grouping Abdobalistum and Palaeobalistum on the one hand,
and Phacodus, Micropycnodus and Hadrodus on the other hand). No
major body size decreases are observed for deep nodes, but inter-
estingly, both shifts towards freshwaters are associated with major
body size decreases (Stenamara and Ocleodus).
Lampridiformes, Polymixiiformes, Beryciformes and
Holocentridae
The four exclusively marine clades are placed at the base of
the Acanthomorphata for the former and at the base of the
Euacanthomorphacea for the three latter (the polymixiiforms are
the sister group of the later clade). Lampridiforms are character-
ized by a large average body size and the other three are character-
ized by some of the smallest body size among all compared clades.
Beryciforms are characterized by a good correlations between size
and time with a steep regression slope (rapid size increase), while
the correlation is not significant in the three other clades. The four
clades are characterized by major positive size shifts affecting two
deep nodes in lampridiforms (including one of the highest observed
shift associated with the node “other lampridiforms”), one deep node
in beryciforms, and the nodes “other holocentrids” and “other poly-
mixiids.” One major size decrease affected a clade of holocentrids,
and other major negative shifts concern only terminal genera.
4.1.3 | Environmentally labile fishes
Elopomorpha
Elopomorphs experienced several shifts towards mixed and
freshwater environments. During the Cretaceous, these shifts in-
volved elopiforms (Ichthyemidion), megalopiforms (Arratiaelops and
Paratarpon) and the enigmatic phyllodontids. Among phyllodontids,
two genera from mixed environments (Casierius and Paralbula) oc-
curred earlier in time than two genera from freshwater environ-
ments (Phyllodus and Egertonia). This sequence may indicate a
possible progressive adaptation to continental environments for the
phyllodontids. The fossil record confirms the marine origin of the
catadromous extant eels (Inoue et al., 2010; Tsukamoto, Aoyama, &
Miller, 2002). The marine beginning of eels also confirms the gen-
eral pattern proposed by Gross (1987) for explaining origin of cata-
dromy. Elopomorphs have an average body size slightly higher than
the average body size of ray-­finned fishes, but there is no significant
correlation between body size and time. Two major body size in-
creases affected deep nodes among the clade in marine environ-
ment: one occurred at the origin of the megalopids and one among
 |
14       GUINOT and CAVIN
the albulids. Moreover, three major body size increases, among
the highest ones for all compared taxa, are associated with shifts
towards mixed environments. They involve terminal taxa, which
gather several genera: the “other megalopids,” the “other elopids”
and the “other anguilloids.”
Clupeomorpha
The clupeomorph fossil record indicates many environmental shifts,
which are not detailed here. The constituent clades, the ellimmich-
thyiforms and the clupeiforms, show opposite evolution size trends.
The former experienced a decreasing body size shift with time and
the latter an increasing body size shift with time, although both show
no significant correlations. Both clades have an average body size
smaller than the average actinopterygian body size. Murray and
Wilson (2013) proposed a phylogeny of the ellimmichthyiforms,
which is used here. They also discussed the evolutionary history of
the lineage and pointed out the complexity of the palaeogeographi-
cal scenario, which is characterized by several shifts from marine
towards freshwater environments together with long marine disper-
sals. Our results also indicate that four Cenomanian marine ellim-
michthyiform genera stemmed from four distinct immigration events
from freshwater to salty environments during the Hauterivian. This
complex pattern should be regarded with caution as it rests on a
phylogenetic framework, which is still poorly supported and very
dependent of future discoveries.
Lavoué, Miya, Musikasinthorn, Chen, and Nishida (2013) and
Lavoué, Konstantinidis, and Chen (2014) explored the geographi-
cal origin of the clupeoids and their environmental shifts based on
a molecular-­b ased phylogenetic analysis, together with a discus-
sion of the fossil record. They found the tropical marine precursor
of the present Indo-­West Pacific region as the centre of origin of
the clade in the Early Cretaceous. This region corresponds to the
eastern Tethys Sea. They detected not less than 11 independent
transitions from marine to freshwater environments happening
mostly during the Cainozoic. A series of transfers of clupeoids
lineages from the sea to freshwaters, and vice et versa, has also
been pointed out by Bloom and Lovejoy (2014). Our study cannot
assess these complex Cainozoic scenarios, but our study shows
that stem clupeoids already shifted between environments in the
Mesozoic as reveal the marine Pseudoellimma and the euryhaline
Santanaclupea. Associated with these environmental vagaries, the
node supporting Pseudoellimma and the derived clupeoids is as-
sociated with a major positive body size shift. Contrariwise, the
node, supporting Satanaclupea and more derived forms, is associ-
ated with a major negative body size shift. Other major body size
decreases concern a clade of basal clupeomorphs (Clupavichthys,
Spratticeps and Eoknightia) and a clade of extinct clupeoids.
Eventually, a major body size increase affected the “other clupe-
ids” plus Sardinella and Knightia. The Sundasalangidae is associated
with one of the major negative body size shift, which is associ-
ated with a shift from marine to freshwater environments in the
Albian. However, this result rests on the phylogenetic position
of this family considered as the sister group of the clupeids plus
pristigasterids (Lavoué, Miya, Saitoh, Ishiguro, & Nishida, 2007),
while a more recent study found this fish deeply nested within the
clupeids (Lavoué et al., 2014).
Gonorynchiformes
Several environmental shifts occurred within this clade, especially
among the Chanoidei. These fishes are smaller in average body
size than the average actinopterygian body size, and they display
a not-­significant positive correlation between body size and time.
The single major positive body size shift affecting a deep node in-
volves a clade of chanids from mixed environments, which contains
the extant Chanos plus Dastilbe, Parachanos and Tharrias. The four
major body size decreases observed in this clade involve terminal
genera only. They concern the extant genus Gonorhynchus in ma-
rine environment and three terminal genera of Rubiesichthyinae
(sensu Amaral & Brito, 2012). Two of them are associated with en-
vironmental shifts from mixed environments to freshwaters. Among
gonorynchids, it is worth to mention that the single shift towards
freshwater, Notogoneus, is associated with the second major size in-
crease of the group. Miniaturization occurred today in some species
of kneriids among gonorynchiforms, but the absence of fossils of this
family in the time interval under study prevent us to recognize evi-
dence of this event.
For the next three clades, only the very beginning of their evolu-
tionary histories is captured here because our study ends at the end
of the Palaeocene, that is before their full diversification. Studies
based on molecular phylogenies indicated that several clades not
considered in our analyses experienced multiple shifts from marine
towards freshwater environment after the Palaeocene, such as the
ariids (Betancur-­R ., Ortí, Stein, Marceniuk, & Alexander Pyron, 2012)
and the tetraodontids (Santini et al., 2013). In the latter study, fresh-
water lineages exhibit accelerated rates of body size evolution.
Protacanthopterygii and Stomiati
Based on our phylogeny and on the fossil record, Protacanthopterygii
invaded freshwater twice with the esocids and with Stompooria,
and mixed environments with the salmonids. The salmonids shift is
associated with a major body size increase. Other major body size
shifts are associated with terminal genera and with groups prob-
ably not monophyletic, but gathered on the basis of stratigraphy.
Protacanthopterygii have an average body size smaller than the
average actinopterygian body size. The body size increases with
time, but the regression shows no significant correlation. Stomiati
show the same general trends with several shifts from marine
to freshwater and mixed environments. Major positive body size
shifts affect three clades, the Plecoglossidae, the Sternoptychidae
and “other Osmeridae” (considered as a terminal taxa in our phy-
logeny), and a single negative major body size shift that affected
Paravinciguerria. The average body size of Stomiati is smaller than
the actinopterygian average body size and although the size in-
creased with time, the correlation between both parameters is not
significant.
GUINOT and CAVIN
Paracanthomorphacea
Two clades are recognized in this group, the Percopsaria and the
Zeiogadaria. The single shift towards freshwater is observed in
Percopsaria with the percopsiforms plus Amblyopsidae clade,
which is associated with a major body size increase. This pattern is
reminiscent to the pattern observed in the otophysans, for which
the shift towards freshwater is also associated with a major body
size increase. Among freshwater percopsiforms, a major nega-
tive body size shift affected the amblyopsids. Knouft and Page
(2003) observed a decrease in body size for this family by study-
ing size distribution among a phylogeny of extant species, but
their r­ esult can hardly be compared with ours since they associ-
ated in their analysis the Aphredoderidae to the amblyopsids. The
extinct sphenocephalids are restricted to marine environments.
The Zeiogadaria are mostly marine with only shifts towards mixed
environments for the Bregmacerotidae and the Gadidae. The
­e nvironmental shift of bregmacerotids is associated with a major
negative body size shift. Several major body size shifts affected
other deep nodes or terminal families of Paracanthomorphacea in
marine environment, such as a negative shift for the Ranicipitidae
and positive shifts for the Oreosomatidae, the Zeniontidae and
the “other Parazenidae.” Paracanthomorphacea as a whole have
an average body size lower than the average actinopterygian av-
eraged body size, and their body size shows a significant positive
correlation with time.
Percomorphacea
We do not discuss in detail this clade because its fossil record is
scarce during the time interval when compared to the other clades.
Most of the terminal taxa in our phylogeny are represented by
post-­T hanetian taxa, whose environmental and body size features
were not collected on fossils but from data on extant families. The
four clades distinguished in our data sets (Pelagiaria, Carangaria,
Ovalentaria and Eupercaria) are characterized by many shifts
­b etween environments. The ancestral node of each clade is marine
then shifts occurred mostly towards mixed environments. In our
dataset, the only shifts towards freshwaters concern two transfers
from mixed environment among Ovalentaria (Polycentridae and
Poeciliidae) and two transfers from marine environment among
Eupercaria (Percichthys and Properca). Carangaria and Pelagiaria
are characterized by average large body size and Ovalentaria and
Eupercaria by small average body size. Body size of Carangaria
and Eupercaria is significantly positively correlated with time.
Frédérich, Marrama, Carnevale, and Santini (2016) showed that
for some Carangaria, that is, the extant carangoids, marine shifts
to non-­reef environments are associated with increased rates of
morphological diversification expressed as body size and shape.
Body size of Ovalentaria and Pelagiaria is significantly negatively
correlated with time. Interestingly, these are the only examples
of significant body size decreases with time among the compared
clades. For Pelagiaria, however, the negative correlation is possi-
bly an artefact caused by the incompleteness of the sampling (see
below).
|
      15
4.2 | General trends in environment occupancy
Carrete Vega and Wiens (2012) observed, based on a maximum-­
likelihood reconstruction of ancestral environments of a calibrated
molecular phylogeny including 22 major extant actinopterygian
clades that all extant marine actinopterygian clades were derived
from freshwater ancestors. They provided a second analysis includ-
ing some fossil taxa, which confirmed their hypothesis that the most
recent common ancestor of marine clades was a freshwater dweller.
However, the set of extinct taxa included in their second analysis
is very small and some of the assumed palaeoenvironments of fos-
sil taxa as exclusively freshwater (e.g. Cheirolepis) are incorrect. It
has been demonstrated that including fossil data in ancestral state
reconstructions approaches adds evidence of directional trends
and hence provides more reliable reconstructions (Finarelli & Flynn,
2006; Finarelli & Goswami, 2013; Slater, Harmon, & Alfaro, 2012).
Betancur-­R et al. (2015) showed that including more fossil taxa in
the fish phylogeny provides strong evidence of marine ancestry for
lineages now restricted to freshwaters. The Betancur-­R et al. (2015)
set of extinct taxa (240 species) encompasses the whole time-­range
of ray-­finned fishes (i.e. Devonian to Recent), while our set of ex-
tinct taxa is larger (642 extinct genera) for a shorter time interval
(Oxfordian–Thanetian). Although our sampling is comparatively low
at the base of the actinopterygian tree, we obtain a pattern simi-
lar to the one by Betancur-­R et al. (2015), that is a marine ancestry
for all freshwater clades. Betancur-­R et al. (2015) already provided
convincing explanations for the apparent erasure of a marine origin
for freshwater clades: a high extinction rate in marine environment,
a refugium function of freshwater environments for several basal
clades, and an insufficient sampling of extinct taxa in Carrete Vega
& Wiens’s study. A higher rate of extinction for marine clades than
for freshwater clades was also observed on the basis of an analysis
of computed phylogenetic diversities including extinct taxa (Guinot
& Cavin, 2016).
Betancur-­R et al. (2015) also identified that transitions from ma-
rine to freshwater are more frequent than transitions from freshwa-
ter to marine. Although we found approximately three times more
transitions of the first type than of the second type in our analyses,
transition rates appear similar for both colonization directions and
are relatively low compared to transition rates involving mixed en-
vironments (Table S3). Reasons for these low rates but high number
of marine to freshwater colonization events might be found in the
higher number of marine taxa in the tree associated to their scattered
position at the base of most clades (marine ancestry for freshwater
clades). Moreover, shifts from marine towards freshwater environ-
ments are more often followed by biological diversifications than
shifts towards the marine realm. During the Late Mesozoic and the
beginning of the Paleogene, diversifications following freshwater in-
vasions concerned high-­diversity clades such as the Ginglymodi, the
Osteoglossomorpha and the Otophysi (although the main diversifi-
cation of the latter occurred after the Palaeocene). Other examples
of freshwater diversifications that occurred after the time interval
studied here, but which obviously followed freshwater invasion, are
 |
16       GUINOT and CAVIN
the Poeciliidae, the Percichthyidae, the Cyprinodontiformes, the
Atherinopsidae (Bloom et al., 2013) and the Cichlidae. At a short
temporal scale, the success of freshwater invaders is observed
during the deglaciation events of the past several millennia and
during the more recent impact of human introduction (Lee & Bell,
1999). At this scale, freshwater invaders are often diadromous spe-
cies locked in freshwater habitats, such as the Salmonidae (Turgeon,
Estoup, & Bernatchez, 1999). Gross (1987) suggested that diadro-
mous species may correspond to evolutionary history stages, which
are intermediate between the marine and freshwater modes of life.
At the geological time scale used in our study, however, most transi-
tions from marine to freshwater habitats appear to have been direct
without the presence of stages in mixed environments. Rapid transi-
tions from marine to freshwater environments, without transitional
diadromous phase, were observed in the clupeiform lineage, which
shows multiple examples of environmental shifts (Bloom & Lovejoy,
2014). Reasons for the overabundance of freshwater invasions by
marine clades on the reverse situation remain to be understood, but
physiological stresses induced by migration from hypotonic to hy-
pertonic environments might require more physiological adaptations
than the opposite (Betancur-­R et al., 2015). Occurrences of taxa from
mixed environments appear to be randomly distributed in our phy-
logenetic tree. As mentioned above, most of the transfers towards
mixed environments originated from the marine realm and several
of them are associated with major positive body size shifts. At a su-
prageneric level, the concerned clades belong mostly to the teleosts,
such as “other megalopids,” “other Elopidae,” “other Anguilloidei,”
“other albuliforms,” Morinidae, Tetraodontoidei, Sparidae plus
Sillaginidae, Scatophagidae, “other Perciformes,” Serranidae plus
stem genera, “other Percoidei,” “Lutjanidae,” “other Scombriformes,”
“other Scombridae” and Salmonidae. These clades correspond to
fishes with various modes of life, some being diadromous and some
dwelling brackish water for feeding or for reproduction. They in-
dicate that colonization of brackish water and development of
a diadromous mode of life for marine fishes are a successful life
strategy. Contrariwise, few suprageneric clades invaded marine en-
vironments from mixed environments and only a handful are asso-
ciated with major positive body size shifts. Among them, some are
dubious because they rest on a phylogeny resolved in part on the
basis of stratigraphy (the pycnodonts Phacodus, Micropycnodus and
Hadrodus), but some other might be real (the Sphyraenidae, a clade
of basal clupeomorphs, a clade of basal gonorynchids). The propor-
tionally large number of transfers from marine to freshwaters and
transfers from marine to mixed environments (including diadromous
forms) compared to transfers in the other direction explain in part
the proportionally high taxic diversity of freshwater fishes compared
to the marine fishes diversity in connection with the aquatic volume
available.
4.3 | Body size evolution and Cope’s rule
We tested for some effects of habitat over body size evolution
across the actinopterygian tree. The effect of habitat and its indirect
impacts on the intrinsic physiological adaptation of organisms is
sometimes evoked to explain size variations among clades. Size dif-
ferences between marine and non-­marine species were found in dia-
toms (Litchman et al., 2009; Nakov et al., 2014) and phytoplankton
in general (Roselli & Basset, 2015) where contrasting nitrogen and
phosphorus supply result in larger marine taxa. Yet, the effect of
habitat on size remains uncertain within vertebrates. As observed in
terminal taxa of the super-­tree (Figure 1), we found a trend towards a
larger size optimum in mixed-­environment taxa using both compara-
tive phylogenetic methods and direct reading of the data. Similarly,
our binary data (freshwater and marine) indicate larger sizes in fresh-
water taxa, but these environmental differences are not statistically
supported. Our evolutionary modelling analyses imply that although
habitat has an effect on general trends in actinopterygian body size
evolution, this is not a strong predictor of the evolution of body size
across the actinopterygian tree, although some clades might show
marked trends. Detecting trends in body size shifts within the mixed
environment is difficult because taxa related to this environment
are sparsely distributed over the phylogeny. However, some pre-
dominantly freshwater clades such as the osteoglossomorphs show
a dominance of positive body size shifts throughout the freshwa-
ter phase of their evolutionary history. Similarly, otophysans shows
a major positive body size shift directly associated with the envi-
ronmental transfer towards freshwaters, then a major positive size
shift occurred at the origin of the gymnotiforms and a negative one
occurred among the siluriforms during the studied time interval.
Outside actinopterygians, a comparable pattern was found among
lungfishes where all major positive body size shifts occurred during
the second, freshwater phase of their evolutionary history. During
the first Palaeozoic phase of the evolutionary history of lungfishes,
mostly marine, negative body size shifts occurred principally (Kemp,
Cavin, & Guinot, 2017).
Our data allowed the assessment of the actinopterygian body size
evolution pattern through time, independently of habitat. Although clear
trend of continuous body size increase through time is not observable
for all actinopterygians taken together in the studied time interval, con-
sidering main clades separately resulted in a majority of size increases
through time. This result confirms that testing the Cope’s rule provides
contrasting results depending on the taxonomic level used (Hone &
Benton, 2007). Among the 28 identified clades, 24 show an increase in
body size with a significant correlation for 12 of them (Table 3). These are
most of the freshwater invaders (Cladistia, Ginglymodi, Halecomorphi,
Osteoglossomorpha, Otophysi) and most of the strictly marine dwellers
(Tselfatiiformes, Eupercaria, Ichthyodectiformes, Aspidorhynchiformes,
Beryciformes, Carangaria). Clades for which the correlation is not
significant, either positive or negative, are mostly environmentally
labile fishes (Elopomorpha, Protacantopterygii, Gonorynchiformes,
­
Ellimmichthyiformes, Clupeiformes). Increase in body size through time
appears to be a general trend in actinopterygian clades, especially when
those are restricted for long periods of time in the same environments,
either marine or freshwater. Transfers between environments may lead
to new evolutionary strategies, which disturb the regular body size
increase that affect lineages in a single environment. The clades with
GUINOT and CAVIN
the shallower regression slope (i.e. with the lower rate of size increase)
are three non-­teleostean taxa (Halecomorphi, Cladistia, Ginglymodi),
while the three clades with the steepest slopes are acanthomorphs
(Paracanthomorphacea, Beryciformes, Carangaria). This indicates that
body size increases occurred in a more pronounced way during the first
phase of diversification of new clades, when average body sizes are still
small.
Heim et al. (2015) observed that the Cope’s rule affected all
marine animals taken together since the Cambrian. This increase,
which also affected subgroups of marine animals such as marine
vertebrates, was caused by a differential diversification of large-­
bodied classes and not by a neutral drift. When Heim et al. (2015)
allowed their model to change at the era-­bounding mass extinc-
tions, the best-­fit model in the Palaeozoic and in the Cainozoic is a
trend towards larger sizes, but the best-­fit model for the Mesozoic
is a stasis. This model corresponds roughly to the trend obtained
here for all marine actinopterygians between the Late Jurassic and
the Palaeocene, although most clades taken individually show clear
body size increases. It should be noticed, however, that data for
fishes compiled by Heim et al. (2015) were extracted from a single
bibliographic source, Frickhinger (1995), which cannot be regarded
as a reliable data source for assessing body sizes of fishes from the
Cambrian to the present.
Mass extinctions affect “fish” body size, but in different ways
depending on the event considered. The Devonian witnessed a reg-
ular increase of the average “fish” body size, which was stopped by
the end-­Devonian (Hangenberg) event (Sallan & Galimberti, 2015).
Interestingly, this mass extinction did not mark a sudden drop in
body size followed by a new increase, but rather a regular decrease
of body size that lasted during the whole Mississippian. This de-
crease was driven by active selection caused by biotic factors rather
than it is the result of Lilliput effect following abiotic events (Sallan
& Galimberti, 2015). At the Permian-­Triassic boundary, the bony fish
fossil record shows a significant body size decrease of freshwater
forms, but not of the marine ones (Romano et al., 2016). Although
the marine bony fish body size indicates no significant variation at
the Permian-­Triassic boundary, the turnover of the marine fauna,
especially of the apex predator, was important and indicates that
the mass extinction events affected not only freshwater fish assem-
blages, but also the marine ones (Romano et al., 2016). The pattern
obtained here for the actinopterygians at the Cretaceous/Paleogene
boundary differs from both end-­Devonian and end-­Triassic patterns:
a drop in body size of fishes from mixed environments; an increase
of the average body size of marine fishes; and a slight decrease of
the body size of the freshwater fishes. These three trends provoke
a constriction of the size range of actinopterygians just after the
boundary in the Danian. The body size increase of marine actinopte-
rygians across the Cretaceous/Paleogene boundary is surprising
since it has been demonstrated that most of the victims of the end-­
Cretaceous mass extinction were mostly large pelagic marine ray-­
finned fishes (Cavin, 2002; Friedman, 2009; Guinot & Cavin, 2016).
Indeed, the largest terminal Maastrichtian genera are among victims
of the mass extinction (Bonnerichthys, Xiphactinus, Protosphyraena,
|
      17
Pachyrhizodus, Saurocephalus) and overpass in size the largest Danian
marine actinopterygians (“other lampridiforms,” Phosphonatator,
Sarda, etc.). What makes the Danian average body size larger than
the Maastrichtian one is a series of deep nodes within the Pelagiaria,
which will produce later several post-­Danian clades of large fishes,
mostly among scombriforms (Miya et al., 2013). Although the fos-
sil record of articulated large marine actinopterygians is still poor
in the Danian, the ichthyolith (dermal denticles and teeth) record
recovered from marine cores indicates a deep change in the fish
community structure at the Cretaceous/Paleogene boundary and
an increase of actinopterygian teeth size in the Danian (Sibert &
Norris, 2015). Thus, as for the Permian–Triassic boundary (Romano
et al., 2016), the change in average body size of marine ray-­finned
fishes is not high, but the turnover is strong and new large forms
quickly arose. Romano et al. reported a drop in body size among ma-
rine bony fishes between the Early Triassic and the Anisian, which
is interpreted as corresponding to a radiation of new small forms.
This event is equivalent to the radiation of small forms of acantho-
morphs that we detected in the Cenomanian and to the radiation of
some clades (pycnodontiforms, halecomorphs and elopomorphs) in
the Oxfordian. These radiations induce a drop in the mean body size
for marine taxa. A similar trend in mean size decrease is observed
for freshwater fishes in the Hauterivian-­Barremian interval, which
also corresponds to a diversification event among continental ray-­
finned fishes. These associations between diversification events
and drops in mean body size suggest that most osteichthyan clades
originate from small-­sized ancestors. Comparing the reconstructed
body size of the last common ancestor of the 28 analysed clades
with the mean body size of the whole dataset confirms this trend. All
but three clades (Pelagiaria, Aulopiformes and Pachycormiformes)
take their origins from an ancestor of which reconstructed body size
is smaller than the mean value of the whole dataset.
Although Cope’s rule has been tested for a large range of tax-
onomic groups, a few of these studies incorporate phylogenetic
frameworks (Alroy, 1998; Avaria-­Llautureo et al., 2012; Baker et al.,
2015; Benson et al., 2014; Bokma et al., 2016; Clauset & Erwin,
2008; Laurin, 2004) where large-­sized clades tend to originate from
small-­sized ancestors. This tendency for new clades to originate at
small sizes was pointed out by Stanley (1973). He showed that the
body size evolution from a small ancestor within a closed morpho-­
space would necessarily lead to a passive trend towards larger body
size (the “Stanley effect” according to Albert & Johnson, 2012).
Hence, the frequency of Cope’s rule in the evolution of fishes and,
to a greater extent of vertebrates, might be more related to the rela-
tive small size of the clades’ ancestors compared to the clade’s opti-
mum than to the intrinsic clade evolution. Among the exceptions of
this, Pelagiaria is one of the two clades that originate from an above
average-­sized ancestor and it is also one of the few actinopterygian
clades that do not follow Cope’s rule because they show a decreas-
ing trend through time. This observation is surprising because it is
in this clade that some fish lineages experienced the largest body
size increase in the Late Miocene, possibly triggered by a transition
from pelagic–neritic to pelagic-­oceanic habitats (Santini, Carnevale,
 |
18       GUINOT and CAVIN
& Sorenson, 2014). The reason of this unexpected result is that the
time span used here grasps only the very beginning of the evolution
of this group. The observed size decreases concern members of the
extinct syngnathiform family Rhamphosidae, which obscures a major
size increase present in “other scombriforms”. Thus, this apparent
size decrease trend detected in the Pelagiaria is probably caused by
a sampling artefact. Hence, small size might be considered as what
Gould (1994) called the “left wall” in evolution, a metaphor originally
used for illustrating the evolution of anatomical complexity trough
time. The mean fish body size used here can be considered close to
the left wall of size, as it is the commonest size encountered in fish
clades. Radiating clades would have to evolve towards larger sizes
(to the right of the wall) to move away from the occupied morpho-­
spaces (Cope’s rule), while those that move back to the left (towards
smaller sizes) would be less frequent as they would be absorbed by
the already occupied morpho-­spaces. However, larger taxa tend to
have higher extinction probabilities (Cardillo et al., 2005; Clauset &
Erwin, 2008; Gaston & Blackburn, 1995; McKinney, 1997; Pimm,
Jones, & Diamond, 1988; Purvis, Gittleman, Cowlishaw, & Mace,
2000) related to their small population size, density, growth rates,
which tend to free morpho-­spaces to the right of the wall (but see
Puttick et al., 2017). Although time appears to be a dominant driver
of body size evolution, other intrinsic factors such as morphological
and/or physiological adaptations played important roles that might
become predominant in some of the rare clades that do not follow
Cope’s rule. Knouft and Page (2003) found opposite results for
North American freshwater fishes as some of these groups exhibit
decreasing size and originate from phylogenetically large taxa. Yet,
this study does not consider fossil taxa that, as shown above, add
strength to phylogenetic approaches in providing past trait states
and additional evidence of polarity trends.
5 |  CO N C LU S I O N S
During the approximately 100 million years of the Late Jurassic–
Palaeocene time interval, most of the observed ray-­f inned fish di-
versification occurred in marine environment and the basal-­most
nodes of all fish clades are located in marine environments. This
observation is possibly biased in part because the freshwater fos-
sil fish record is poorer than the marine record, but also because
most of the otophysans diversification, which counts today for
two-­t hirds of the freshwater ray-­f inned diversity and ca 27% of the
total ray-­f inned diversity, occurred mostly during the Cainozoic.
Most of the detected environment shifts are from marine to fresh-
water environments and more importantly from marine to mixed
environments. Transfers from mixed environments towards fresh-
water environments, which could have been expected as common
events if invasion of continental waters is a step by step progres-
sive phenomenon, are surprisingly rare. The rare shifts from conti-
nental to marine environment involve mostly low-­diversity clades
(mainly terminal taxa in our phylogeny). In each clade, the gen-
eral trend is an increase in body size through time, which is more
marked in the marine environment. There are proportionally more
major body size shifts associated with environmental transitions
than within a given environment, and this is especially marked for
major positive body size shifts towards mixed environments.
Freshwater and marine actinopterygian clades show a positive
and significant correlation of body size with time, but this correlation
in generally not significant for environmentally labile fishes (elopo-
morphs, ellimmichthyifoms, clupeiforms, gonorynchiforms). All lin-
eages restricted for long periods of time in the same environments,
either marine or freshwater, increase in size through time, confirming
Cope’s rule observed in other groups. However, the average body
size of the whole actinopterygian clade does not increase during the
studied interval because of occurrence of new clades diversifying
from small-­sized ancestors and possibly because extinctions tend to
hit large-­sized taxa.
The general turnover of the ray-­f inned fish fauna the Late
Jurassic–Palaeocene time interval can be globally described as
follows: (i) a succession of marine clades, each showing a general
increase in the body size of their representatives (pachycormi-
forms, aspidorhychiforms, ichthyodectiforms, pachyrhizodontoids,
tselfatiiforms, aulopiforms, polymixiiforms, beryciforms, holocen-
trids). Shifts towards brackish and freshwater are rare. One clade,
the pycnodontiformes are mostly marine but experienced a few
shifts towards freshwater realm associated with negative body size
shifts; (ii) clades that shifted a few times (possibly once for some of
them) towards freshwaters where they diversified in the Mesozoic
and/or in the Cainozoic (acipenseriforms, ginglymodians, haleco-
morphs, osteoglossomorphs, otophysans). They experienced rare
returns to brackish and marine environments. Most of them show
an increase of body size with time; (iii) clades that shifted several
times from marine towards mixed and freshwater environments,
with environmental shifts generally associated with major positive
body size shifts (elopomorphs, protacanthopterygii).
AC K N OW L E D G E M E N T S
We thank Jeremy Beaulieu (University of Arkansas) who provided
support with R codes. This paper is a contribution to the project
“Fish response to long-­term global changes” supported by the
Swiss National Science Foundation (200021-­140827). We thank
Francesco Santini and an anonymous reviewer for their constructive
comments.
ORCID
Guillaume Guinot  http://orcid.org/0000-0003-3363-6972
Lionel Cavin  http://orcid.org/0000-0001-9666-5864
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How to cite this article: Guinot G, Cavin L. Body size
evolution and habitat colonization across 100 million years
(Late Jurassic–Palaeocene) of the actinopterygian
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