Testudines

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Testudines
Tartarugas, cágados e jabutis: os
tetrápodas de casco
São Amniotas
• Mamíferos, aves e “Répteis”
• Junto com Aves e os Répteis: Saurópsida
– São grupo-irmão dos archosaura (Aves+Crocodilianos)
• Sinapomorfias dos Amniota
– Ovo Amniótico
– pele impermeável
– Ventilação por pressão negativa
• Origem evolutiva das tartarugas
– Por muito tempo um mistério!
– Envoltas por uma casca óssea
• Membros por dentro das costelas!
Eunotosauros -260milhões de anos
atrás, descrito em 2013
Lyson et al., 2013
Origem Fossorial das tartarugas!
Lyson et al., 2016
Testudines
• Em contraste com lepidosauros e anfíbios…
– Baixa diversidade de histórias de vida
– Ovíparos, sem cuidado parental***
• Está assim no livro, mas alguns exibem!
• Especializações morfológicas
– Hábitos terrestres, aquáticos
– Grandes migrações!
• Mecanismos de navegação semelhantes
• Vida longa
– baixa capacidade de crescimento populacional rápido
– Muitos ameaçados
• Principalmente grandes jabutis e tartarugas marinhas
– DST dificulta programas de manejo
Formas de corpo dos quelônios
Divisão em função da fenestra 
temporal
• Anápsida – Testudines
– condição derivada
– Eunotosauros diápsido!
• Sinapsida – Mamíferos
• Diápsida – Aves e demais Répteis
à Condição Anapsida
à Condição Sinapsida
à Condição Diapsida
Testudines
• Tartarugas, Cágados e Jabutis
• Casco ósseo:
– carapaça (porção superior) 
– plastrão (porção inferior)
• Morfologia do casco e membros
– Refletem especializações para seus hábitas
• Nadadeiras e cascos achatados: aquáticas
• Membros colunares, cascos altos: terrestres
• Carapaça e plastrão
– Recobertos por escudos dérmicos duros
• Queratina
• Não coincidem em N nem posição com ossos abaixo
Casco e coluna vertebral de 
uma tartaruga. (A) Escudos 
dérmicos da carapaça e 
plastrão. A carapaça tem uma 
fileira central (vertebral) de 5 
escudos com 4 escudos laterais 
(pleurais) em cada lado e 10–12 
escudos marginais. O plastrão 
tem 6 escudos emparelhados. 
(B) Ossos dérmicos da carapaça 
e plastrão. (C) Coluna vertebral, 
vista de dentro da carapaça. 
Observe que, anteriormente, as 
costelas se articulam com dois 
centros vertebrais. (Depois de 
Zangerl 1969.)
Algumas tem cascos móveis
Jabutis
• Casco alto e patas robustas tipo elefante
Cágado
• Casco achatado dorso-ventralmente
• membranas interdigitais
Tartarugas
• Casco achatado dorso-ventralmente
• patas em forma de remos
Características Gerais
• Não possuem Dentes
– Bico córneo
• Existem arborícolas, mas não existem
voadoras ou planadoras
• maioria é onívora
• ovíparos de fertilização interna
– sexo definido, às vezes, pela temperatura
– cuidado parental escasso
– várias ameaçadas de extinção
Relações Filogenéticas de Testudines
Lu et al., 2013. Plos One. Nov 21; 8(11):e79348. 
Cryptodira, Pleurodira
https://www.australianfreshwaterturtles.com.au/threads/need-help-
identifying-your-turtle-warning-lots-of-images.4637/
Pleurodira: 93 espécies
Cryptodira: 255 espécies
or
ig
in
of
‘m
aj
or
lin
ea
ge
s’
an
d
cl
ad
es
th
at
ha
ve
be
en
re
co
gn
iz
ed
as
fa
m
ili
es
,e
sp
ec
ia
lly
in
N
or
th
A
m
er
ic
a)
.
W
e
as
si
gn
ea
ch
lin
ea
ge
to
a
co
nt
in
en
t
ba
se
d
on
th
e
th
ei
r
ar
ea
of
or
ig
in
as
sh
ow
n
by
th
e
fo
ss
il
re
co
rd
(s
te
m
ta
xa
).
Fo
r
th
e
ti
m
in
g
of
ev
en
ts
w
e
us
e
th
e
si
m
pl
e
ap
pe
ar
an
ce
of
lin
ea
ge
s
in
th
e
fo
ss
il
re
co
rd
us
ed
to
co
ns
tr
uc
t
di
ve
r-
ge
nc
e-
da
ti
ng
pr
io
rs
by
Jo
yc
e
et
al
.(
20
13
).
Fo
r
th
e
di
ve
rg
en
ce
s
di
s-
cu
ss
ed
be
lo
w
,t
he
fo
ss
il
re
co
rd
of
tu
rt
le
s
is
co
m
pl
et
e
en
ou
gh
th
at
th
er
e
is
no
di
sc
re
pa
nc
y
be
tw
ee
n
pr
io
r
an
d
po
st
er
io
r
es
ti
m
at
es
(J
oy
ce
et
al
.,
20
13
)
an
d
so
m
ol
ec
ul
ar
di
ve
rg
en
ce
da
ti
ng
of
th
e
U
CE
ph
yl
og
en
y
w
ou
ld
be
su
pe
rfl
uo
us
.
Th
e
ea
rl
ie
st
fo
ss
ils
of
st
em
te
st
ud
in
oi
ds
,s
te
m
tr
io
ny
ch
ia
ns
,a
nd
st
em
cr
yp
to
di
re
s
ar
e
fr
om
Eu
ra
si
a
(D
an
ilo
v
an
d
Pa
rh
am
,
20
06
,
20
08
;
Jo
yc
e
et
al
.,
20
13
;
Pé
re
z-
G
ar
cí
a
et
al
.,
20
14
).
M
ap
pi
ng
th
es
e
da
ta
on
to
th
e
U
CE
ph
yl
og
en
y
de
m
on
st
ra
te
s
th
at
cr
yp
to
di
re
s
ha
ve
a
Ju
ra
ss
ic
(>
14
5
M
a)
Eu
ra
si
an
or
ig
in
(F
ig
.3
c)
.T
he
em
er
ge
nc
e
of
cr
yp
-
to
di
re
s
in
Eu
ra
si
a
is
co
m
pl
em
en
te
d
by
th
e
co
nc
ur
re
nt
or
ig
in
of
pa
n-
pl
eu
ro
di
re
s
in
th
e
So
ut
he
rn
H
em
is
ph
er
e
(G
on
dw
an
a;
Jo
yc
e
et
al
.,
20
13
).
G
iv
en
th
e
di
st
ri
bu
ti
on
of
th
e
cl
ad
es
an
d
th
e
ti
m
in
g
of
th
ei
r
or
ig
in
,
th
e
ge
og
ra
ph
y
of
th
e
cr
yp
to
di
re
-p
le
ur
od
ir
e
sp
lit
ca
n
be
pl
au
si
bl
y
lin
ke
d
to
th
e
br
ea
ku
p
of
th
e
su
pe
rc
on
ti
ne
nt
Pa
n-
ga
ea
(S
co
te
se
,2
00
1;
Ro
ge
rs
an
d
Sa
nt
os
h,
20
03
;S
m
it
h
et
al
.,
20
04
).
In
th
is
w
ay
tu
rt
le
s
de
m
on
st
ra
te
a
pa
tt
er
n
co
m
m
on
to
ot
he
r
te
rr
es
-
tr
ia
lv
er
te
br
at
es
(e
.g
.,
pl
ac
en
ta
lv
s.
m
ar
su
pi
al
m
am
m
al
s)
.
D
es
pi
te
th
ei
r
Ju
ra
ss
ic
(>
14
5
M
a)
or
ig
in
,
cr
yp
to
di
re
s
di
d
no
t
do
m
in
at
e
th
e
no
rt
he
rn
co
nt
in
en
ts
fo
r
al
m
os
t
10
0
m
ill
io
n
ye
ar
s
(u
nt
il
th
e
Ce
no
zo
ic
).
In
st
ea
d,
st
em
tu
rt
le
s
(e
sp
ec
ia
lly
th
e
ex
ti
nc
t
cl
ad
e
Pa
ra
cr
yp
to
di
ra
)w
er
e
di
ve
rs
e
an
d
ab
un
da
nt
in
N
or
th
A
m
er
ic
a
th
ro
ug
ho
ut
th
e
Cr
et
ac
eo
us
(1
45
–6
6
M
a)
an
d
in
to
th
e
Ce
no
zo
ic
(<
66
M
a;
Ly
so
n
an
d
Jo
yc
e,
20
09
;L
ys
on
et
al
.,
20
11
).
In
th
e
La
te
Cr
e-
ta
ce
ou
s
(1
00
–6
6
M
a)
,c
ry
pt
od
ir
es
(t
ri
on
yc
hi
an
s
an
d
du
ro
cr
yp
to
d-
ir
es
)
be
ga
n
to
ap
pe
ar
in
N
or
th
A
m
er
ic
a,
in
va
di
ng
th
ro
ug
h
hi
gh
la
ti
tu
de
di
sp
er
sa
l
ro
ut
es
(H
ir
ay
am
a
et
al
.,
20
00
;
Pa
rh
am
an
d
Durocryptodira
Po
do
cn
em
is
 
Li
ss
em
ys
 
M
es
oc
le
m
m
ys
Pe
lo
m
ed
us
a 
N
ils
so
ni
a 
R
hi
no
cl
em
m
ys
 
C
ro
co
dy
lu
s
Ag
rio
ne
m
ys
 
St
er
no
th
er
us
 
C
yc
le
m
ys
 
Py
th
on
 
Sp
he
no
do
n
C
he
ly
dr
a 
/ C
he
ly
dr
id
ae
Te
rra
pe
ne
 
Er
ym
no
ch
el
ys
 
C
hr
ys
em
ys
 
Ki
no
st
er
no
n 
An
ol
is
 
G
op
he
ru
s 
St
au
ro
ty
pu
s 
G
eo
em
yd
a Ap
al
on
e 
Pe
lo
di
sc
us
 
D
ei
ro
ch
el
ys
 G
al
lu
s
De
rm
at
em
ys
 m
aw
ii
St
ig
m
oc
he
ly
s 
Pe
lu
si
os
 
G
ra
pt
em
ys
 
De
rm
oc
he
ly
s 
co
ria
ce
a
Pl
at
em
ys
 
Ki
no
st
er
ni
da
e
Tr
io
ny
ch
id
ae
Trionychia
Ca
re
tto
ch
el
ys
 in
sc
ul
pt
a
Po
do
cn
em
id
id
ae
Pe
lo
m
ed
us
id
ae
Ch
el
id
ae
Emydidae
Pl
at
ys
te
rn
on
 m
eg
ac
ep
ha
lu
m
G
eo
em
yd
id
ae
Te
st
ud
in
id
ae
Americhelydia
Emysternia
Testuguria
Pleurodira
Ki
no
st
er
no
id
ea
Ch
el
on
io
id
ea
Pe
lo
m
ed
us
oi
de
s
Chelydroidea
Testudinoidea
Cryptodira
Testudines
Archelosauria
Ar
ch
os
au
ria
Lepidosauria
Sq
ua
m
at
a
Sauria 0.
02
Le
pi
do
ch
el
ys
 
C
he
lo
ni
a
Ch
el
on
iid
ae
Em
ys
Tr
ac
he
m
ys
H
om
o
Amniota
Fi
g.
2.
Ph
yl
og
en
et
ic
hy
po
th
es
is
ba
se
d
on
RA
xM
L
an
al
ys
is
of
U
CE
da
ta
sh
ow
in
g
ph
yl
og
en
et
ic
al
ly
de
fin
ed
cr
ow
n
cl
ad
es
of
tu
rt
le
s
(T
es
tu
di
ne
s)
.A
ll
cl
ad
es
w
er
e
su
pp
or
te
d
by
lik
el
ih
oo
d
bo
ot
st
ra
p
pe
rc
en
ta
ge
s
of
10
0
ex
ce
pt
fo
r
th
e
po
si
ti
on
of
Ch
el
yd
ra
in
th
e
ST
A
R
sp
ec
ie
s
tr
ee
,
w
hi
ch
ha
s
a
bo
ot
st
ra
p
su
pp
or
t
of
68
.
Th
e
sc
al
e
ba
r
is
in
un
it
s
of
su
bs
ti
tu
ti
on
s
pe
r
si
te
.
25
4
N
.G
.C
ra
w
fo
rd
et
al
./
M
ol
ec
ular
Ph
yl
og
en
et
ic
s
an
d
Ev
ol
ut
io
n
83
(2
01
5)
25
0–
25
7
Crawford NG, Parham JF, Sellas AB, Faircloth BC, Glenn TC, Papenfuss TJ, Henderson JB, Hansen MH, Simison WB (2015).
A phylogenomic analysis of turtles. Molecular Phylogenetics and Evolution 83:250-257.
Filogenia das 7 espécies de tartarugas
marinhas
Superimposition of protein template and models was performed
using the ‘‘Magic Fit’’ function in the Swiss PDB viewer, and trans-
membrane domains were identified according to Efremov and
Sazanov (2011).
3. Results
3.1. Phylogenetic analyses
Contig assembly for the 24 mitogenomes produced in this study
yielded complete mitogenome lengths between 16281 and
16719 bp (Table 1). The complete mitogenome alignment of the
32 sequences (24 from this study plus eight GenBank sequences)
revealed a total of five shared haplotypes within the species C.
caretta, E. imbricata, C. mydas, and D. coriacea (see Table 1 for
mitogenomic haplotype naming in this study). This revealed a pro-
portion of 0.83 (25/30) unique sea turtle haplotypes (number of
unique haplotypes/total number of samples), and nucleotide diver-
sities (mean proportion of variable sites in pairwise comparison/
alignment length) of 0.0078 (variance = 0.0033) for C. caretta,
0.014 (variance = 0.005) for L. olivacea, 0.0002 (variance = 0.0002),
for L. Kempii, 0.011 (variance = 0.004) for E. imbricata, 0.006 (vari-
ance = 0.0017) for C. mydas, and 0.00036 (variance = 0.00016) for
D. coriacea.
Model testing for the complete mitogenome showed a prefer-
ence for GTR+G as the best substitution model. The proportion of
variable sites was different among regions, the D-Loop having the
highest variability, and the Stem-loop having the lowest (see
Fig. S1 for gene positions). Base frequencies were not homoge-
neous among regions; the G content was particularly variable
(Table S1).
Maximum likelihood and all Bayesian phylogenetic analyses
revealed the same topology with comparable support values
(bootstrap and posterior probabilities) (Fig. 1). This topology sup-
ported major relationships found in previous studies based on
combined nuclear and mitochondrial data (Naro-Maciel et al.,
2008), but it was inconsistent with phylogenetic reconstructions
using mitochondrial D-Loop and ND4L (Dutton et al., 1996), Cytb
(Bowen et al., 1993), and morphology (Zangerl, 1980). All nodes
in Fig. 1 within and between species had bootstrap and poster-
ior-probability supports of 100% and 1.00, respectively, except
within D. coriacea (within node VI), where the intra-specific haplo-
type relationships had a low support of 47% and 0.44 (Fig. 1).
One finding of particular importance was high support for N.
depressus as the sister taxon to C. mydas. Previous studies based
on mitochondrial 12S and 16S, and nuclear markers BDNF, Cmos,
R35, Rag1, and Rag 1 (Naro-Maciel et al., 2008) have supported this
relationship, whereas D-Loop, ND4, and tRNA data have placed this
species as the sister taxon to the clade containing Eretmochelys,
Lepidochelys and Caretta (Dutton et al., 1999).
There was a common phylogeographic pattern for three of five
globally distributed species (E. imbricata, C. mydas and D. coriacea).
Phylogenetic groupings show two clades consisting of haplotypes
from the geographic range extremes: The Atlantic and Indian,
and Pacific ocean regions (see color coding in Figs. 1 and 2), as sug-
gested by previous studies (Bowen et al., 1998, 1994; Bowen and
Karl, 2007; Dutton et al., 1999; Encalada et al., 1996). In contrast,
C. caretta did not display phylogenetic concordance with current
geographic distributions, given the high support in node XII
(Fig. 1 and Table 2) for the Pacific haplotype (C caretta HI Pe) being
nested within two Atlantic samples (C caretta FL1 and C caretta
FL2), with a median TMRCA of 2.37 Million Years Before Present
(Ma) (1.24–3.89 Highest Posterior Density (HPD)), as shown in
Table 2. Within L. olivacea, the major split was approximately
2.7 Ma (2.40–3.36 HPD) between Indian Ocean samples and all
others, with samples from the Pacific clustering with high support
Fig. 1. Chronogram for complete mitogenomic analysis with haplotype key for Fig. 2. Branch support is shown for Posterior probability/Bootstrap support (maximum
likelihood) only for branches where these values were below 0.99 and 95, respectively. Roman numbering corresponds to nodes listed in Table 2. Tip label colors represent
haplotype geographic distribution as shown in Fig. 2.
S. Duchene et al. /Molecular Phylogenetics and Evolution xxx (2012) xxx–xxx 5
Please cite this article in press as: Duchene, S., et al. Marine turtle mitogenome phylogenetics and evolution. Mol. Phylogenet. Evol. (2012), http://
dx.doi.org/10.1016/j.ympev.2012.06.010
Filogenia das tartarugas de casco mole 
(Tryonichia)
Santonian–early Campanian of Asia and have served as
evidence of the dispersal from Asia to America. The
Beringia landbridge is the most probable migration
route for this dispersal. A previous study has indicated
that the Bering Strait formed about 100 MA and
opened periodically during warm periods until the
Danian (61.6–66.0 MA) (Zakharov et al., 2011), and
was used by different groups of organisms to invade
North America during these particular periods, includ-
ing turtles (Sanmartin et al., 2001; Danilov et al., 2011,
2014; Le et al., 2014). Moreover, Patton (Patton & Tail-
leur, 1977) suggested that east–west compression of
North American and Eurasian continents shortens the
crustal distance between the North American and Eura-
sian continents during late Mesozoic or early Cenozoic
times, facilitating indirect contact between these conti-
nents and providing a route for the ancestor of Apalone
to North America (Fig. 4b); this is roughly in agree-
ment with our estimation for the data when an ances-
tor of Apalone invaded North America. In addition,
thermal maximum made Beringia habitable for softshell
turtles (Zachos et al., 2001).
Ancestral area reconstruction shows that the ancestor
of Chitra indica might have invaded India twice, with
the ancestor arriving at around 63 MA (node 49), fol-
lowed by a second event at around 45 MA (node 48).
The position of the Indian plate as it moved northwards
has been under intense scrutiny and debate for decades,
and the time of the India–Asia collision has been esti-
mated to range from 65 to 38 MA (Beck et al., 1995).
Previous study has suggested that prior to the final colli-
sion of India with Eurasia, a Palaeogene biogeographic
link existed between South-East Asia (SE) and India. Ali
& Aitchison (2008) proposed that India’s northward pas-
sage towards Asia involved the north-east corner of the
subcontinent coming into contact with Sumatra and
Burma from ~ 57 MA ago (late Palaeocene), which was
followed by a hard collision (~ 35 MA) with Asia. A
recent study has found European affinities co-existed
with relict taxa from Gondwana before the India–Asia
collision in Ypresian (47.8–56 MA) and suggested that
India had not yet collided with Asia at 54.5 MA (Smith
et al., 2016). Our results support that the position of
India was in the north and might have come in contact
100200300
JUR LOWER CRE UPPER CRE
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
3540
 Osteolaemus tetraspis
Mecistops cataphractus
Carettochelys insculpta
Lissemys punctata
Lissemys scutata
Trionyx triunguis
Chitra indica
Pelochelys cantorii
Pelochelys cantorii
Apalone ferox
Apalone spinifera
Rafetus swinhoei
Pelodiscus sinensis
Palea steindachneri
Dogania subplana
Nilssonia formosa
Amyda cartilaginea
Pelomedusa subrufa
Podocnemis unifilis
Sternotherus carinatus
Macrochelys temminckii
Chelydra serpentina
Chrysemys picta
Cyclemys oldhami
Cyclemys atripons
33
34
Cyclemys dentata
Mauremys mutica
Mauremys reevesii
Mauremys sinensis
Trachemys scripta
Manouria impressa
Indotestudo elongata
Psammobates pardalis
Caretta caretta
Eretmochelys imbricata
Platysternonmegacephalum
Kinosternon leucostomum
8
9
10
11
2
133
14
15
16
4444 26
25
3333333
RE PAL MIO
5
3
C
C
353535335
32 C
Fig. 3 Divergence times using the program BEAST 1.8. The blue lines indicate the 95% confidence interval values of each node. The
numbers of each node refer to Table 4. The black curve in the inset represents the temporal variation in the global mean surface
temperature from 70 MA to today (Zachos et al., 2001). The light red columns represent the accelerated diversification events and global
warming episodes.
ª 20 1 7 EUROPEAN SOC I E TY FOR EVOLUT IONARY B IOLOGY . J . E VOL . B I OL . 3 0 ( 2 0 17 ) 1 0 1 1 – 1 02 3
JOURNAL OF EVOLUT IONARY B IOLOGY ª 2017 EUROPEAN SOC I E TY FOR EVOLUT IONARY B IO LOGY
1020 H. L I ET AL.
http://research.amnh.org/users/esg/
Características
• Reprodução
– Diretamente influenciada pela temperatura
• Determinação sexual
• Maturação sexual tardia
• Reprodução muitas vezes próxima à água
• Ameaçadas
Quelônios Brasileiros
• 31 espécies continentais
• 5 marinhas
– Caretta caretta
– Chelonias mydas
– Dermochelys coriacea
– Eretmochelys imbricata
– Lepidochelys olivacea
Família Cheloniidae
4 espécies
Caretta caretta
Tartaruga cabeçuda
Chelonias mydas
Tartaruga verde
Eretmochelys imbricata
Tartaruga de Pente
mais comum do RN
Lepidochelys olivacea
Tartaruga oliva
Família Dermochelidae
1 espécie
Dermochelys coriacea
Tartaruga de Couro
Família Emydidae
2 espécies
Trachemys adiutrix
• Capininga ou cágado do maranhão
• Em perigo de extinção
Família Geoemydidae
1 espécie
Rhinoclemmys punctularia
Família Kinosternidae
1 espécie
Kinosternon scorpioides
Família Testudinidae
2 espécies
Chelonoidis carbonaria
Família Podocnemididae
Tartarugas da Amazônia
5 espécies
Podocnemis expansa
Podocnemis expansa
Família Chelidae
20 espécies
7 gêneros
Chelus fimbriata
Amazônica – Mata mata
Macrochelys temminckii
Aligator snapping turtle
Apalone ferox
tartaruga de casco mole da Flórida
Heosemys spinosa
tartaruga espinhosa da Ásia