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Hypotheses on rostral shield evolution in fossorial lizards derived from the phylogenetic position of a new species of Paracontias (Squamata, Scincidae)

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In squamate reptiles the rostral shield constitutes one of the most advanced cases of reduction in the number of scales in the rostral region, an evolutionary trend clearly associated with a burrowing lifestyle. This structure is characterized by the fusion of the rostral scale with all adjacent scales into a large, smooth and conical plate covering the snout, totally encompassing the nostrils, with a horizontal groove running posteriorly from either nostril. In lizards this structure evolved several times independently, in various lineages of limbless skinks and in the family Dibamidae. We performed a multilocus phylogenetic analysis of combined mitochondrial and nuclear DNA sequences from the fossorial genus Paracontias, including P. vermisaurus, a new species described herein under an integrative taxonomic approach. The resulting phylogeny supports monophyly of Paracontias, with the following internal topology: [P. kankana (P. vermisaurus sp. n. (((P. minimus + P. brocchii) (P. manify + P. hildebrandti)) (P. rothschildi + P. fasika)))]. The molecular data, coupled with a comparative morphological study, allows us to investigate the evolution of the snout scales into a single large rostral shield in Paracontias. We discuss the evolutionary processes through which the rostral shield may have originated (e.g. fusion of scales, number and order of steps involved), and conclude that intuitive and apparently obvious hypotheses for scale homologies based on position and size only (as usually formulated in squamate taxonomy) may be highly misleading, even in closely related species. We develop the hypothesis that the rostral shield may provide several functional advantages for fossorial species in facilitating burrowing and protecting the head from strong physical stress, e.g. smoother surface reducing friction between the tegument and the substrate, reduction in the number of flexible sutures resulting in strengthened tegument, and the rostral tip likely playing a role as a shock-absorbing buffer. KeywordsBurrowing lifestyle–Scincidae– Paracontias vermisaurus sp. n.–Madagascar–Scalation–Molecular phylogeny
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ORIGINAL ARTICLE
Hypotheses on rostral shield evolution in fossorial lizards
derived from the phylogenetic position of a new species
of Paracontias (Squamata, Scincidae)
Aurélien Miralles &Jörn Köhler &David R. Vieites &
Frank Glaw &Miguel Vences
Received: 6 August 2010 /Accepted: 21 February 2011 /Published online: 5 March 2011
#Gesellschaft für Biologische Systematik 2011
Abstract In squamate reptiles the rostral shield consti-
tutes one of the most advanced cases of reduction in the
number of scales in the rostral region, an evolutionary
trend clearly associated with a burrowing lifestyle. This
structure is characterized by the fusion of the rostral
scale with all adjacent scales into a large, smooth and
conical plate covering the snout, totally encompassing
the nostrils, with a horizontal groove running posteriorly
from either nostril. In lizards this structure evolved
several times independently, in various lineages of
limbless skinks and in the family Dibamidae. We
performed a multilocus phylogenetic analysis of com-
bined mitochondrial and nuclear DNA sequences from
the fossorial genus Paracontias, including P. vermisaurus,
a new species described herein under an integrative
taxonomic approach. The resulting phylogeny supports
monophyly of Paracontias, with the following internal
topology: [P. kankana (P. vermisaurus sp. n. (((P. minimus +
P. brocchii)(P. manify +P. hildebrandti)) (P. r o t h sc h i l d i +P.
fasika)))]. The molecular data, coupled with a comparative
morphological study, allows us to investigate the evolution
of the snout scales into a single large rostral shield in
Paracontias. We discuss the evolutionary processes through
which the rostral shield may have originated (e.g. fusion of
scales, number and order of steps involved), and conclude
that intuitive and apparently obvious hypotheses for scale
homologies based on position and size only (as usually
formulated in squamate taxonomy) may be highly
misleading, even in closely related species. We develop the
hypothesis that the rostral shield may provide several
functional advantages for fossorial species in facilitating
burrowing and protecting the head from strong physical
stress, e.g. smoother surface reducing friction between the
tegument and the substrate, reduction in the number of
flexible sutures resulting in strengthened tegument, and the
rostral tip likely playing a role as a shock-absorbing buffer.
Keywords Burrowing lifestyle .Scincidae .Paracontias
vermisaurus sp. n. .Madagascar .Scalation .Molecular
phylogeny
Introduction
Numerous recent studies have highlighted the multiple
convergent adaptations to highly specialized burrowing
lifestyles that have occurred in the evolutionary history of
squamate reptiles (e.g. Brandley et al. 2008; Crottini et al.
2009; Greer 2002; Kohlsdorf and Wagner 2006; Mott and
Vieites 2009; Shapiro 2002; Skinner et al. 2008; Whiting et
A. Miralles (*):M. Vences
Division of Evolutionary Biology, Zoological Institute,
Technical University of Braunschweig,
Spielmannstr. 8,
38106 Braunschweig, Germany
e-mail: miralles.skink@gmail.com
J. Köhler
Hessisches Landesmuseum Darmstadt,
Friedensplatz 1,
64283 Darmstadt, Germany
D. R. Vieites
Museo Nacional de Ciencias Naturales,
Consejo Superior de Investigaciones Científicas (CSIC),
C/José Gutierrez Abascal 2,
Madrid 28006, Spain
F. Glaw
Zoologische Staatssammlung München,
Münchhausenstr. 21,
81247 München, Germany
Org Divers Evol (2011) 11:135150
DOI 10.1007/s13127-011-0042-6
al. 2003; Wiens et al. 2006; Wiens and Slingluff 2001).
Most of these works have focused on the most striking
adaptive response to the requirements of a subterranean life
style, i.e. the reduction or loss of limbs. However, limb loss
has often been accompanied by a combination of several
other spectacular morpho-anatomical transformations, such
as regression of the eyes, closure of the ear opening,
increase in the number of vertebrae together with a
lengthening of the body shape, miniaturization, or loss of
pigmentation (Gans 1974,1975; Lee 1998; Pianka and Vitt
2003; Sakata and Hikida 2003).
Legless fossorial tetrapods (squamates and amphibians)
essentially dig the soil using their snout, which incurs
strong constraints on the tip of the animals head. Most of
these forms have a highly derived skull that has evolved in
response to their specialized head-first burrowing lifestyle.
For instance, Uropeltoidea and scolecophidian snakes,
amphisbaenians, dibamids and caecilians all have compact
skulls with a solidly enclosed braincase and reduced
arcades (Gans 1974,1975; Measey and Herrel 2006;
Rieppel 1984; Rieppel et al. 2009; Rieppel and Maisano
2007). Virtually unexplored until now, the cephalic scala-
tion is also expected to be relevant as a morpho-anatomical
adaptation of burrowing squamates. Indeed, many lineages
of fossorial Squamata have convergently followed the
general trend of reduction in the number of scales on the
anteriormost part of the head. This has led to a wide
diversity of cephalic scalation patterns, all characterized by
the presence of bigger scales, giving a smooth aspect to the
cephalic tegument (e.g. scolecophidians and several colu-
brid snakes, amphisbaenians, dibamids, the gymnophthal-
mid genus Bachia; Ávila-Pires 1995; Broadley and Wallach
2009; Gans 1974; Marx and Rabb 1970; Miralles 2001;
Savitzky 1983; present study).
On the other hand, given its very high diversity of
patterns, cephalic scalation has always constituted one of
the most important sources of morphological characters for
squamate systematics. This is particularly true for groups
showing large and geometrical plates, for which many
homology hypotheses have been proposed on the basis of
their relative shapes and positions, leading to the design of
an accurate terminology constantly improved over the last
decades. Nevertheless, despite the universally acknowledged
value of these characters in taxonomy, astonishingly few
studies have paid attention to their evolution, to the role they
can play in terms of morpho-functional adaptations to extreme
environments, lifestyles and behaviour, or to the reliability of
the homologies hypothesised in phylogenetic contexts for
each of the scales covering the head. As these integumentary
structures constitute the interface between the organism and
its environment, they can be expected to be subject to
important biomechanical constraints. This applies in particu-
lar to limbless fossorial squamates, because these usually dig
in the soil using the tip of the snout. Interestingly, a
remarkable structure usually referred to as the rostral
shield has evolved convergently in various lineages of
the Scincidae and Dibamidae, always in groups highly
specializedtoburrowinghabits. This structure represents
the most advanced case of reduction in the number of
scales in the rostral region of Squamata, with all the
anteriormost scales of the snout being fused into a single,
smooth and roughly conical plate covering the anterior-
most part of the head (Fig. 1).
During our recent work on scincid lizards of Madagascar,
we obtained new taxonomic and molecular phylogenetic data
that might help to shed light on the evolution of the rostral
shield from more plesiomorphic kinds of rostral scalation.
Malagasy lizards in the subfamily Scincinae form by far the
most specioseand morphologically diverse radiation of skinks
on the island (Crottini et al. 2009; Schmitz et al. 2005;
Whiting et al. 2004), with 57 described species currently
recognized (Glaw and Vences 2007;Köhleretal.2009,
2010). Among these are several highly specialized fossorial
forms, such as the species in the genera Voeltzkowia,
Sirenoscincus,Pseudoacontias,andParacontias. The latter
is a poorly known genus of skinks characterized by the total
absence of limbs and ear openings, fusion of the anterior-
most scales of the snout, and partially by an extreme
miniaturization (in some species, the width of the body and
head does not exceed 23 mm).
Here we analyse the evolution of the rostral shield in
Paracontias, on the basis of a newly discovered species and
of its phylogenetic position within the genus. We selected
Paracontias as a model group for this study, as it contains
species showing different levels of specialization of the
head scalation: either with a complete rostral shieldsensu
stricto (large, smooth and conical plate covering the snout,
resulting from fusion of the rostral scale with all adjacent
scales, totally encompassing the nostrils, and with a
horizontal groove running posteriorly from either nostril)
or with an incomplete rostral pseudo-shield(less modified
structure, not completely encompassing the nostrils, with-
out horizontal grooves) that we hypothesize to represent an
intermediate evolutionary condition.
Material and methods
Taxonomic framework
A recent phylogenetic analysis based on six mitochondrial
and five nuclear genes strongly supports the monophyly of
the genus Paracontias, here including P. minimus (which
formerly constituted the monotypic genus Cryptoposcincus;
Crottini et al. 2009). Two formerly undescribed species of
Paracontias included in the phylogeny published by
136 A. Miralles et al.
Crottini et al. (2009) under the names Paracontias sp. aff.
tsararano and Paracontias sp. have recently been described
as P. kankana and P. fasika, respectively (Köhler et al.
2009,2010).
The definitions and taxonomic concepts of Amphiglossus
stylus,Paracontias fasika, P. hafa, P. hildebrandti, P.
kankana, P. manify, P. minimus and P. tsararano as used
in the present paper are based on morphological examina-
tions of the respective type specimens. The definition of P.
milloti is based on the original description only, those of P.
rothschildi and P. holomelas on the original descriptions
complemented with the redescriptions by Angel (1942), and
the definition of P. brocchii on the original description plus
data published by Brygoo (1980) and Andreone and Greer
(2002).
Morphological study
The specimens examined (all preserved in 70% ethanol) are
deposited in the Museum National dHistoire Naturelle,
Paris (MNHN), Museo Regionale di Scienze Naturali,
Torino (MRSN), Senckenberg Forschungsinstitut und
Naturmuseum, Frankfurt am Main (SMF), Museum für
Naturkunde, Berlin (ZMB), Zoologisches Forschungsmuseum
Alexander Koenig, Bonn (ZFMK), and Zoologische Staats-
sammlung München (ZSM). The abbreviations ZCMV and
DRV refer to M. Vences and D. R. Vieites field numbers,
respectively. Measurements of specimens were recorded to the
nearest 0.1 mm using a digital caliper. Meristic, mensural and
qualitative characters examined here are routinely used in the
taxonomy of Scincidae, such as scale counts, presence or
absence of homologous scale fusions, or the variability in
color patterns. Scale nomenclature, scale counts, and
measurements used in the morphological analyses are
essentially based on Andreone and Greer (2002). The
frontal scale is considered as hourglass shaped when
constricted by the first supraocular, as bell-shaped when
this is not the case (see Greer and Shea 2000). Nuchal
scales are defined as enlarged scales of the nape,
transversely occupying the place of two or more rows of
dorsal cycloid scales (Miralles 2006). Pretemporal scales
are presently defined as scales anterior to temporals and
parietals, separating the last supraocular from the primary
temporal scale; Andreone and Greer (2002:p.155,fig.13)
held that Paracontias hafa shows a single pretemporal
scale, but did not identify the adjacent lower scale.
D
F
A
B
C
Scincidae Dibamidae
E
G
12
3
4
5
Fig. 1 Shape and extension of rostral shield in five convergent
lineages of Squamata. AAcontias meleagris.BTyphlosaurus cregoi.
CAcontias rieppeli.DNessia layardi.ETyphlacontias rohani.
FParacontias hafa.GDibamus ingeri.ac redrawn after Fitzsimons
(1943), d after Smith (1935), f after Andreone and Greer (2002), g
after Das and Lim (2003)
Hypotheses on rostral shield evolution in Paracontias 137
According to our definition of a pretemporal, P. h a f a and
the new species described below are the only two species
in the genus that possess two pretemporals, whereas
almost all the remaining species have a single pretemporal
scale. Paracontias minimus seems to lack pretemporal
scales, but the highly modified head scalation of this
species renders the formulation of homology hypotheses
for several head scales extremely tentative.
Traditionally, herpetologists use the term fusionfor
the transition from a state with two or more small scales
to a state with a single larger scale occupying more or
less the same place (shape and expansion) as the
previous scales, and thus supposed to be homologous
with them. In the present paper we follow this definition
for obvious practical reasons. It is nevertheless essential
to stress the fact that it does not insinuate any
morphogenetic process, but only refers to a transition
from one state to another in evolutionary history,
regardless of the mechanism involved.
Drawings were made using Adobe Illustrator CS2 and
a WACOM CTE-640 graphic tablet, after photographs
taken through a ZEISS SteREO Discovery. V12 stereo
microscope.
Molecular sampling
Five new DNA sequences (HQ891854 to HQ891858) were
generated from the specimen ZSM 597/2008 (field number
ZCMV 11211), the holotype of the new species, and
deposited in GenBank. They have been added to the dataset
published by Crottini et al. (2009) (with the exception of
Amphiglossus crenni and Pseudoacontias menamainty, for
which only mitochondrial sequences were available), both
to test whether the new species is a member of the genus
Paracontias, as suggested by morphological examination,
and to infer its phylogenetic affinities within the genus. One
cordylid (Cordylus sp.) was used as out-group; further taxa
used as hierarchical out-groupswereTiliqua and Eumeces
sensu lato. Among the non-Malagasy skinks, previous more
inclusive studies (Schmitz et al. 2005; Whiting et al. 2004)
suggested that species of Eumeces s. l. are relatively close to
the Malagasy radiation. It should be noted that for the three
out-group taxa we had to use concatenated chimera
sequences of different species compiled from GenBank
(see Table 1and Crottini et al. 2009), a procedure not
completely free of risks (it assumes, for instance, that the
various taxa composing each chimera form a monophyletic
group; see Malia et al. 2003).
Molecular procedures
Total genomic DNA was extracted using proteinase K
(10 mg/ml) digestion, followed by a standard salt-
extraction protocol (Bruford et al. 1992). From the
mitochondrial DNA (mtDNA) we amplified fragments of
the 16S rRNA to ND1 genes. Additionally, fragments of
three nuclear DNA genes (nuDNA) were amplified: brain-
derived neurotrophic factor (BDNF), recombination acti-
vating gene 2 (Rag2), and phosducin (PDC). Standard
polymerase chain reactions were performed in a final
volume of 12.5 μl containing 0.3 μleachof10pmol
primer, 0.25 μl of total dNTP 10 mM (Promega), 0.1 μlof
5 U/ml GoTaq, and 2.5 μl of GoTaq Reaction Buffer
(Promega). For primers and PCR conditions used, see
Crottini et al. (2009). The successfully amplified products
were purified using the ExoSAP-IT purification kit
according to the manufacturers instruction. Purified PCR
templates were sequenced using dye-labeled dideoxy
terminator cycle sequencing on an ABI 3130 automated
DNA sequence. Chromatographs were checked and
sequences were edited using CodonCode Aligner (v. 2.0.6,
Codon Code Corporation).
Phylogenetic analyses
We conducted maximum parsimony (MP) and partitioned
Bayesian inference searches based on the full concate-
nateddataset.WeusedPAUP*4.0b10(Swofford2002)
to perform MP analyses with 100 random addition
sequence replicates, equal character weighting, tree bisec-
tion and reconnection (TBR) branch swapping, and gaps
coded as missing data. Nodal support was obtained
using bootstrap analyses (Felsenstein 1985), with 10,000
replicates, 10 random addition sequences replicates, and
TBR branch swapping. Partitioned Bayesian analyses
were performed with MrBayes 3.1.2 (Ronquist and
Huelsenbeck 2003), using the same 21 partitions (12S
rRNA,16SrRNA,tRNAs,andthe respective separated
1st, 2nd and 3rd positions of ND1, BDNF, C-mos, alpha-
Enolase, PDC and Rag2) and the same parameters as
obtained by Crottini et al. (2009). We performed one run
of 20 million generations (started on random trees) and
four incrementally heated Markov chains (using default
heating values) each, sampling the Markov chains at
intervals of 1,000 generations. Stabilization of likelihood
values occurred after nine million generations. The first
ten million generations were conservatively discarded, and
10,000 trees were retained post burn-in and summed to
generate the majority rule consensus tree. Both this tree
and the sequence alignment data have been deposited at
TreeBase, under the study accession number S11140 (tree
accession number Tr26690; matrix accession number
M7561). Genetic distances between all species in Paracontias
were estimated with MEGA 4.1 (Tamura et al. 2007)by
calculating uncorrected p-distances based on the ND1 and
phosducin genes.
138 A. Miralles et al.
Table 1 List of taxa and material included in the present study, with respective collecting localities, voucher field numbers, institutional catalogue numbers (where available), and GenBank
accession numbers per gene region sequenced; asterisk indicates that respective holotype has been sequenced; newly determined sequences shown in boldface
Taxon Locality Voucher field
number
Institutional
catalogue no.
Accession numbers
12S 16S ND1 BDNF C-mos Rag2 a-Enolase PDC
Amphiglossus
anosyensis Ambatolahy ZCMV 591 ZMA 20342 FJ667609 FJ667621 FJ744569 FJ667634 FJ667663 FJ667721 FJ744551 FJ667692
astrolabi Ranomafana FG/MV 2002312 ZSM 201/2003 AY315474 AY315523 FJ744570 FJ667635 FJ667664 FJ667722 AY391213 FJ667693
frontoparietalis Ambohitsara ZCMV 153 ZMA 20341 FJ667610 FJ667622 FJ744571 FJ667636 FJ66766 FJ667723 FJ744560 FJ667694
macrocercus Ankaratra FG/MV 20022142 ZSM 1016/2003 AY315484 AY315533 FJ744572 FJ667637 FJ667666 FJ667724 AY391216 FJ667695
mandokava Montagne dAmbre FGZC 1240 ZSM 2167/2007 FJ667611 FJ667623 FJ744573 FJ667638 FJ667667 FJ667725 AY391217 FJ667696
melanurus Maroantsetra MVTIS 2002-A6 AY315502 AY315551 FJ744574 FJ667639 FJ667668 FJ667726 AY391218 FJ667697
punctatus Ambatolahy ZCMV 519 ZMA 20230 AY315489 FJ667624 FJ744575 FJ667640 FJ667669 FJ667727 AY391221 FJ667698
reticulatus Berara MVTIS 2000-E44 AY315490 AY315539 FJ744576 FJ667641 FJ667670 FJ667728 AY391224 FJ667699
tanysoma Berara MVTIS 2000-D58 AY315498 AY315547 FJ744577 FJ667642 FJ667671 FJ667729 FJ744561 FJ667700
sp. robustusAndasibe ZCMV 373 ZMA 20228 FJ667612 FJ667625 FJ744562 FJ667643 FJ667672 FJ667730 FJ744546 FJ667701
sp. phaeurusAndasibe ZCMV 3062 UADBA uncat FJ667613 FJ667626 FJ744563 FJ667644 FJ667673 FJ667731 FJ744547 FJ667702
sp. variegatusMontagne des Francais FGZC 482 ZSM 246/2004 FJ667614 FJ667627| FJ744564 FJ667645 FJ667674 FJ667732 FJ744548 FJ667703
Androngo
trivittatus Tolagnaro FGZC 2306 ZSM 389/2005 FJ667615 AY151444| FJ744565 FJ667646 FJ667675 FJ667733 FJ744549 FJ667704
Madascincus
igneocaudatus Ibity MVTIS 2001-D14 AY315476| FJ667629 FJ744567 FJ667648 |FJ667677 FJ667735 AY391214 FJ667706
intermedius Ampijoroa MVTIS 2001-B55 AY315479 AY315528 FJ744568 FJ667649 FJ667678 FJ667736 AY391215 FJ667707
mouroundavae Antsahamanara MVTIS 2001-F17 AY315487 AY315536 FJ744578 FJ667650 FJ667679 FJ667737 AY391219 FJ667708
polleni Berara MVTIS 2000-E18 AY315497 AY315546 FJ744579 FJ667651 FJ667680 FJ667738 AY391222 FJ667709
sp. baeusAndasibe ZCMV 2283 UADBA uncat. FJ667617 AY315542 FJ744580 FJ667652| FJ667681 FJ667739 FJ744552 FJ667710
Paracontias
brocchii Montagne dAmbre FGZC 476 ZSM 244/2004 AY315507 AY391155 FJ744583 FJ667655 FJ667684 FJ667742 AY391225 FJ667713
fasika* Baie de Sakalava FGZC 1347 ZSM 2256/2007 FJ667619 FJ667632 FJ744589 FJ667661 FJ667690 FJ667748 FJ744558 FJ667719
hildebrandti Montagne des Francais FGZC 1946 ZSM 1578/2008 FJ667620 FJ667633 FJ744590 FJ667662 FJ667691| FJ667749 FJ744559 FJ667720
kankana* Mahasoa forest DRV 5711 ZSM 1810/2008 AY315509 FJ667631 FJ744582 FJ667654 FJ667683 FJ667741 AY391227 FJ667712
manify* Antsahamanara MVTIS 2001-F58 MRSN R1887 AY315510 AY315559 FJ744584 FJ667656 FJ667685 FJ667743 FJ744554 FJ667714
minimus Baie de Sakalava FGZC 1027 ZSM 2251/2007 FJ667616 FJ667628 FJ744566 FJ667647 FJ667676 FJ667734 FJ744550 FJ667705
rothschildi Baie de Sakalava FGZC 1020 ZSM 2246/2007 FJ667618 FJ667630 FJ744581 FJ667653 FJ667682 FJ667740 FJ744553 FJ667711
vermisaurus* Makira ZCMV 11211 ZSM 0597/2008 HQ891855 HQ891854 HQ891856 HQ891858 HQ891857
Pygomeles
braconnieri Ifaty FG/MV 20022048 AY315514 AF215235 FJ744585 FJ667657 FJ667686 FJ667744 FJ744555 FJ667715
Voeltzkowia
Hypotheses on rostral shield evolution in Paracontias 139
Results
Molecular phylogenies
The results of the phylogenetic analyses are summarized in
Fig. 2. Despite the fact that the deepest nodes of the MP
tree are not resolved, the MP and Bayesian results are
relatively congruent. The only exception concerns the
position of P. hildebrandti, which resulted as the sister
species of P. manify in the Bayesian analysis (PP = 0.98),
whereas it was the sister taxon to the poorly supported
clade [(P. manify (P. brocchii +P. minimus)] in the MP
analysis (bootstrap support 58%). In both approaches,
monophyly was supported for the Malagasy scincines (PP
1.0/bootstrap 96%), for clade A(1.0/68%) and clade B
(1.0/84%) as previously defined by Whiting et al. (2004),
and for Paracontias (1.0/62%), as was the case in the study
by Crottini et al. (2009). The Bayesian analysis suggested
P. kankana, the only included species from eastern
Madagascar, as the most basal species in the genus (1.0),
followed by P. vermisaurus sp. n. (1.0). Nevertheless, the
most basal relationships within Paracontias were not
resolved in the MP analysis, which produced a polytomy
with four main clades: (1) the P. kankana clade, (2) the P.
vermisaurus clade, (3) the (P. rothschildi +P. fasika)
clade, and the [P. hildebrandti {P. manify (P. brocchii +P.
minimus)}] clade.
The uncorrected p-distances calculated among species
in the genus Paracontias, both for the most divergent and
for the most conservative gene (ND1 and phosducin,
respectively), are provided in Table 2.Thedistances
calculated for the new species in relation to the other
species of Paracontias range from 14.8% to 18.3% for the
ND1 gene fragment, and from 1.4% to 2.4% for the
phosducin gene fragment; these values are on the same
order as those observed between other accepted species in
the genus.
Taxonomic section
The new species described below in the genus Paracontias
Mocquard, 1894 has been recognized using an integra-
tive taxonomic approach. The concept of integrative
taxonomy (sensu Dayrat 2005) is based on the general
lineage species concept (de Queiroz 1998,2007), rejects
the superiority of any particular set of characters
(morphological, behavioral or molecular), and advocates
the combined and integrated use of such methods (Padial
et al. 2010). In the present case, both morphological data
(qualitative and quantitative scalation characteristics,
coloration) and molecular data (phylogenetic position,
genetic distances) congruently support the distinctiveness
of the new species.
Table 1 (continued)
Taxon Locality Voucher field
number
Institutional
catalogue no.
Accession numbers
12S 16S ND1 BDNF C-mos Rag2 a-Enolase PDC
fierinensis Arboretum Tulear FG/MV 2000569 UADBA uncat. AY315516 AY315563 FJ744586 FJ667658 FJ667687 FJ667745 FJ744556 |FJ667716
lineata Anakao FGZC 2683 ZSM 384/2005 AY315518 AF215238 FJ744587 FJ667659 FJ667688 FJ667746 AY391228 FJ667717
sp. pallidaAnakao FG/MV 20021536 UADBA uncat. AY315589 AY315565 FJ744588 FJ667660| FJ667689 FJ667747 FJ744557 FJ667718
Outgroup
Cordylus sp. ––AF236036 DQ249038 AY315566 AY987981 AY987981 DQ119627 ––
Eumecess. l. spp. ––EU278021 EU278085 AY315600 EF646320 EF646320 DQ119628 AY2180
Tiliqua sp. ––AB057376 AY217965 –––EF534983 AY218053 EF534856
Collection Abbreviations: DRV = D.R. Vieites field numbers; FG/MV, FGZC, ZCMV F. Glaw and/or M. Vences field numbers; MRSN Museo Regionale di Scienze Naturali, Torino; MVTIS tissue
collection of M. Vences; UADBA Université dAntananarivo, Département de Biologie Animale (not yet catalogued); ZMA Zoölogisch Museum Amsterdam; ZSM Zoologische Staatssammlung
München
140 A. Miralles et al.
Paracontias vermisaurus sp. n.
(Figures 3and 4a)
Etymology The specific epithet is derived from the Latin
vermis (worm) to the Greek sauros (lizard); it is to be treated
as a noun in apposition for the purposes of nomenclature.
Type material Holotype (ZSM 597/2008; field number
ZCMV 11211), apparently an adult specimen; north-
eastern Madagascar, Makira Reserve, site locally named
Angozongahy, 15°2613.3S, 49°0707.0E, 1,009 m a.s.l.,
collected 2022 June 2009 by C. Patton, J. Patton, E.
Rajeriarison, T. Rajoafiarison, R. D. Randrianiaina, F.
Ratsoavina,, M. Vences and D. R. Vieites. Paratype (ZSM
598/2008; field number DRV 5935), adult; data as for
holotype, except site locally named Ampofoko, 15°2522.3
S, 49°0715.1E, 1,034 m a.s.l., 28 June 2009.
Diagnosis Small brownish apodous scincine species in
Paracontias Mocquard, as revealed by sequence analyses
of mitochondrial and nuclear genes as well as by the
absence of legs, supranasals and postnasals, the main
morphological synapomorphies that in combination differen-
Fig. 2 Phylogenetic tree of
Malagasy Scincinae recon-
structed using Bayesian
inference (20 Mio. generations;
trees sampled every 1000
generations; burn-in 10,000),
based on 3,936 bp DNA
sequences of 12S and 16S
rRNA, ND1, BDNF, Rag2,
Cmos, Enol and phosducin.
Legless fossorial lineages high-
lighted in grey. Cordylus,
Tiliqua and Eumecessensu lato
used as out-group (not shown).
Numbers at nodes are Bayesian
posterior probabilities followed
by bootstrap support
values >50% from Maximum
Parsimony analysis (10,000
replicates)
12345678
1P. minimus 11.6 13.2 8.7 11.9 14.8 13.0 14.8
2P. rothschildti 1.1 14.3 13.0 14.1 14.8 13.9 15.4
3P. kankana 2.2 2.7 15.2 14.5 17.0 15.0 18.3
4P. brocchii 0.3 0.8 2.4 11.6 15.4 12.1 15.4
5P. manify 0.8 0.8 2.4 1.1 15.4 11.6 15.7
6P. fasika 1.1 1.1 2.7 1.4 0.8 15.4 16.6
7P. hildebrandti 1.1 1.1 2.7 1.4 0.8 1.1 17.9
8P. vermisaurus sp. n. 1.9 1.9 1.4 2.2 2.2 2.4 2.4
Tab l e 2 Summary of genetic
divergences (uncorrected
p-distances, shown as percen-
tages) in the genus Paracontias;
below table diagonal: most con-
servative gene (phosducin),
mean interspecific distance =
1.6± 0.7, range = 0.3 to 2.7;
above diagonal: most divergent
gene (ND1), mean interspecific
distance = 14.3± 0.02, range =
8.7 to 18.3
Hypotheses on rostral shield evolution in Paracontias 141
tiate the genus from other Malagasy scincines, including from
limbless species assigned to Amphiglossus.
Paracontias vermisaurus sp. n. differs from congeneric
species by the following combination of character states:
presence of loreals separated from each other by the rostral
to the frontonasal (versus very large loreals extending and
meeting each other at dorsal midline in P. kankana, loreals
absent in P. milloti); two supralabials between the rostral
and the subocular supralabial (three in Amphiglossus stylus;
one in P. hildebrandti), hourglass-shaped frontal (bell-
shaped in P. brocchii, P. kankana, P. manify, P. minimus,
P. rothschildi, P. tsararano); 20 scale rows around midbody
(16 in P. rothschildi and P. fasika;18inP. milloti and P.
minimus;21inP. kankana and P. tsararano;22inP.
manify;26inP. brocchii;31inP. holomelas); nostril in
contact with first supralabial (nostril deeply within rostral
and posteriorly connected by distinct narrow join with first
supralabial in P. hafa,P. hildebrandti,P. holomelas, P.
minimus,P. manify and P. tsararano); three supraoculars
largely in contact with the frontal (two in P. brocchii, P.
milloti, P. kankana, P. tsararano, P. rothschildi; one in P.
minimus), eye opening not covered by scales (eye sunken
below ocular scale in P. minimus); a uniform dark
coloration (bicolored pattern with lighter wide medio-
dorsal stripe in P. fasika and P. rothschildi). Additionally,
P. vermisaurus differs from the morphologically similar P.
hafa in having a relatively larger eye with a prominent
supraocular region (versus a flat, laterally depressed supra-
ocular region), and by brownish live coloration with a faint
violet tint (versus pale with pinkish tint).
Description of holotype In good state of preservation,
except for the tail that has been autotomised 8 mm
posterior to the cloaca. Unsexed, apparently adult speci-
men. Snout-to-vent length 53.8 mm, width at midbody
3.5 mm, head width at level of parietal eye 3.6 mm.
In general appearance, a brown skink of relatively small
size, slender, with both pairs of limbs completely absent.
Snout blunty rounded in both dorsal and lateral aspect, with
a rostral tip blunty rounded in dorsal aspect. Rostral wider
than long, contacting first supralabial, loreal and fronto-
nasal. Supranasals absent, apparently fused with rostral.
Frontonasal roughly trapezoidal, wider than long, contacting
loreals, first supraciliaries and first suproculars. Prefrontals
absent. Frontal approximately as wide as long, wider
posteriorly, in contact with frontonasal, first three supra-
Fig. 3 Head of Paracontias
vermisaurus sp. n. (holotype,
ZSM 597/2008). aDorsal view.
bVentral view. cLateral view
142 A. Miralles et al.
oculars, parietals and interparietal. Supraoculars four, the
second and third pairs longer in size, the posteriormost pair
significantly smaller. Frontoparietals absent. Interparietal
triangular, longer than wide, well separated from supra-
oculars; parietal eyespot present, with parietal eye
evident. Parietals contact each other posterior to inter-
parietal. Parietal in contact with two pairs of cycloid
dorsal scales; enlarged nuchals absent. Nasal only
slightly larger than nostril, contacting rostral and first
supralabials. Postnasals absent, apparently fused with
rostral. Loreal single, about as high as long. Preocular
wider dorsally than ventrally, single. Presubocular
lozenge-shaped, single. Five supraciliaries on either side,
in continuous row; first, second and last pairs signifi-
cantly larger and longer than intermediate ones; last pair
projecting onto supraocular shelf. Upper palpebrals
small, except for last which projects dorsomedially.
Pretemporals two, the upper contacting the parietal, the
lower the primary temporal scales, both contacting upper
secondary temporal. Postsuboculars single, contacting
penultimate supralabial, primary temporal and lower
pretemporal. Lower eyelid moveable, scaly; five rectan-
gular lower palpebrals in contact with eye, the last being
the largest. Contact between upper palpebrals and supra-
ciliaries apparently direct but flexible, i.e. palpebral cleft
narrow. Primary temporal single. Secondary temporals
two; the upper long, broadly contacting the upper and
barely the lower pretemporals anteriorly. Two tertiary
temporals bordering lower secondary temporal. Supralabials
five, the third being the enlarged subocular contacting scales of
lower eyelid. Postsupralabial single. External ear opening
absent, with no indication of its former position. Mental wider
than long, posterior margin straight. Postmental pentagonal
diamond-shaped, wider than long, contacting first pair of
infralabials. Infralabials four. Three pairs of large chin scales;
members of first pair in contact behind postmental, members of
second pair separated by a single median scale row, members
of third pair separated by three scale rows. No scales extending
between infralabials and large chin scales; two asymmetrical
postgenials posterolaterally in contact with third pair of chin
scales. Gulars similar to ventrals in size and outline. All scales
except head shields cycloid, smooth and imbricate. Longitu-
dinal scale rows on flanks disrupted at level of two weak lateral
depressions with reduced scales, indicating former position of
forelimbs. Longitudinal scale rows at midbody 20; para-
vertebrals 109, similar in size to adjacent scales; ventrals 103.
Inner preanals larger and longer than outer ones.
For live coloration, see Fig. 4a. In preservative, ground
coloration dark brown; head immaculate dark brown,
rostral, first supralabial and mental scales with milky
slightly paler color, supraoculars darker than other supra-
cephalic scales; parietal eyespot visible as beige spot; lower
eyelid whitish, with upper part bordering the eye dark
brown; dorsal body scales brown with dark brown color at
their posterior and pale beige at their lateral edges;
numerous minute irregular beige flecks and spots present
within scales; tail base (posterior tail amputated) slightly
darker than rest of body; from throat to cloaca, flanks
slightly paler than dorsal scales due to spreading of pale
coloration within each ventral scale row.
Variation The only other known specimen, the paratype, is
slightly larger than the holotype: snout-to-vent length
60.5 mm, width at midbody 4.5 mm, head width at level
of parietal eye 4.3 mm. Cephalic scalation identical to
holotype; longitudinal scale rows at midbody 20; para-
vertebrals 105, ventrals 98. Coloration in preservative
identical to holotype.
Distribution and natural history Only known from two
sites in the primary rainforest of Makira reserve located
close to each other, both close (<50 m) to streams and
around 1,000 m a.s.l. (Fig. 5). The rainforest is somewhat
degraded at both sites; at Ampofoko (the paratype locality)
multiple traces of cattle were found. The holotype was
captured in a pitfall line (10 l buckets in the ground at 10 m
distances, connected by a plastic barrier of a total length of
50 m); the paratype was found by field assistants while
actively searching under rotten logs and leaf litter.
Fig. 4 Live habitus of holotypes of Paracontias vermisaurus sp. n. a
and P. ha f a b. Photographs by M. Vences and F. Andreone,
respectively
Hypotheses on rostral shield evolution in Paracontias 143
Discussion
Taxonomic validity of Paracontias vermisaurus sp. n
Of the total of currently 12 recognized species of Paracontias,
six have been described only during the last 8 years
(Andreone and Greer 2002;Köhleretal.2009,2010). For
almost all of them, no reliable data on variation, reproduction
and habits are available, except for some general information
on the habitat and few prey items found in stomachs (Köhler
et al. 2010). Several reasons may explain this insufficient
knowledge. First, the type specimens of several of the
historically oldest nomina in the genus seem to be lost, or in
such a poor state of preservation that they are now virtually
unidentifiable. Additionally, species of Paracontias are very
rare in collections. Most of them are known by very few
specimens, sometimes only by the holotype. This
considerably complicates the study of this genus as it
prevents us to obtain an estimateeven a rough oneof
the intraspecific variability or of the distribution for each
species of Paracontias.
Morphologically, P. vermisaurus sp. n. differs from
almost all remaining species of Paracontias by three or
more distinct characters in scalation (see diagnosis above).
However, the distinction between P. vermisaurus and P.
hafa is less obvious. Scalation is superficially similar,
differing only by a single character of the rostral region: P.
hafa has the nasal (pierced by nostrils) deeply within the
rostral scale, and posteriorly connected with the first
supralabial by a distinct narrow join, whereas P. vermisaurus
has the nasal in contact with both the rostral and the first
supralabial (= rostral shield and pseudoshield, respectively,
see below for more details). The molecular data, both the
topology (see Fig. 2) and the very high genetic divergence
(Table 2), strongly support the distinctness of P. vermisaurus
from several other species of the genus but, unfortunately, no
molecular sample of P. hafa (which is only known from the
holotype) has been available to us. Due to the limited total
number of available specimens, it is thus impossible to
directly assess the intraspecific variability of that rostral
character within these two species. Nevertheless, larger
series of specimens of two other species of Paracontias
were available to us and can be used to assess intraspecific
variation in this character. In P. r o t h s c h i ld i ,100%ofthe
examined specimens (n=30, from 2 different localities) have
the nasal in contact with the first supralabial, whereas in P.
minimus all specimens (n=21, 3 localities) have the nostril
within the rostral, thus supporting the hypothesis of
intraspecific stability of the respective character state. Based
on these data, we hypothesize that the character is highly
reliable for taxonomy, thus supporting the distinction between
P. vermisaurus sp. n. and P. hafa.
Other, more subtle and less clear-cut characters also
support this hypothesis, such as the relatively larger eyes
in P. v e r m i s a u r u s , with a more prominent supraocular
region (versus a flat, laterally depressed supraocular
region in P. h a f a ), and the differences in live coloration.
Evolution of the rostral shield in Paracontias
Loss or fusion of scales of the anteriormost part of the head
are commonly encountered in different lineages of fossorial
snakes (Marx and Rabb 1970; Miralles 2001; Savitzky
1983). For instance, several colubrid snakes (sensu lato)
with such habits show different patterns of scalation
characterised by a reduction in the number of scales on
the snout, e.g. bilateral fusion between internasals and
prefrontals in the genus Calamaria, fusion of both
prefrontals to a single median scale in Aparallactus niger,
fusion of both internasals to a single median anterior plate
and fusion of both prefrontals to a single median scale most
posteriorly in Prosymna meleagris, or fusion of both
internasals and prefrontals to a single large scale in the
genus Poecilopholis (Chippaux 2001; Koch et al. 2009;
Miralles 2001). The same trend is also present in several
lineages of fossorial lizards. The rostral shield that
characterizes several of them constitutes a remarkable case
of reduction in the number of scales in the rostral region
Fig. 5 Rainforest at Makira
Reserve (>1,000 m a.s.l.). a
General view. bAt the
collecting locality of the
paratype, a site locally
named Ampofoko
144 A. Miralles et al.
among Squamata. This state has evolved at least four times
independently in skinks (at least two times independently in
Africa, in the Typhlacontias clade, and in the clade containing
Acontias,Acontophiops and Typhlosaurus, a third time in the
Malagasy genus Paracontias, and likely a fourth time in the
Sri Lankan endemic genus Nessia), and a very similar
structure has evolved in the family Dibamidae (Fig. 1). The
members of all these taxa have fossorial habits and share
many of the adaptative characters usually associated with
subterranean life: elongated body, absence or regression of
the limbs, the ear opening, and the eye (Table 3; Andreone
and Greer 2002; Broadley 2006; Daniels et al. 2006; Das and
Lim 2003;Fitzsimons1943;Smith1935; Somaweera and
Somaweera 2009; Whiting et al. 2003,2004).
The genus Paracontias constitutes an informative model
to study the evolution of the rostral shield, because a
complete shield is present in only some species of the genus
while others have a less modified structure. In most of the
four-legged scincine skinks of Madagascar closely related
to Paracontias (namely Madascincus, Amphiglossus), the
plesiomorphic state of scalation of the rostral region
(Fig. 6a) is constituted by a rostral scale (R), a pair of
supranasals (SN), a pair of postnasals (PN), and three pairs
of supralabials (1, 2, 3) between the rostral and the
subocular supralabial (SubO). In all species of Paracontias,
the supranasal and postnasal scales are absent, likely fused
with the rostral scale into a single large plate (Fig. 6b and c),
and the number of supralabials is reduced (only two scales
between the rostral and the subocular supralabial, versus
most frequently three in the genus Madascincus and
Amphiglossus). Nevertheless, some species of Paracontias
may have nostrils within the rostral scale (a pattern we refer
to as the rostral shield sensu stricto, cf. Fig. 6c), whereas
others may have a less modified structure, with nostrils being
in contact with the rostral but not completely embedded
within it (the rostral pseudo-shield, cf. Fig. 6b).
Comparative examination of the rostral scalation within
the genus Paracontias (using Madascincus as out-group)
suggests two hypotheses on the evolutionary origin of the
rostral shield in this particular genus. In both hypotheses,
the same intermediate state (step 0) is necessary (namely
the fusion of the rostral with the supranasals and the
postnasals), but the subsequent steps significantly differ
between those hypotheses.
The one stephypothesis Only based on size and position
homologies, as it is usually done in squamate taxonomy, this
hypothesis considers the rostral shield to result from fusion of
the first supralabial with the rostral scale. Indeed, (1) the
posterior extension of the rostral shield fits very well, both in
terms of size and position, with the first supralabial in
Madascincus, and (2) the presence of the horizontal groove
extending posteriorly to the nostril recalls the suture
delimiting the postnasal from the first supralabial in
Madascincus.Inthatcase(Fig.6C1), the suture delimitating
the rostral shield from the new first supralabial (= second
supralabial in Madascincus) would not be homologous
between the Paracontias having a rostral shield and those
having a rostral pseudo-shield (Fig. 6b, C1).
The two stephypothesis This alternative is based on the
phylogenetic hypothesis of the genus Paracontias derived
from our molecular tree (Fig. 1). According to the topology
obtained, it is not possible to determine whether the rostral
shield evolved at least two times independently within the
genus, or whether it appeared only once and then regressed
in P. brocchii, both these hypotheses being equally
parsimonious (box in Fig. 6). However, in both cases the
rostral shield is always derived from the rostral pseudo-
shield state, which likely constitutes the plesiomorphic state
within Paracontias. This implies that the rostral pseudo-
shield constitutes an intermediate step always present
during the process leading to the forming of the rostral
shield (step 1), followed by the backward extension of the
rostral pseudo-shield, together with a regression of the first
supralabial (step 2). According to this hypothesis, supra-
Table 3 The rostral shield as defined in the present paper has been
found in six genera of Scincidae and in the genus Dibamus
(Dibamidae), representing at least five instances of convergent
evolution of this feature within Squamata (clades 15); members of
all these genera are known for their fossorial habits and share many of
the morphological characters usually associated with this lifestyle
Family Clade Genus Limbs Eyes External ear opening
Scincidae 1 Acontias absent small, with eyelid hidden
Typhlosaurus absent hidden hidden
2Typhlacontias absent exposed, without eyelid hidden
3Paracontias absent exposed or hidden hidden
4Nessia absent or vestigial exposed hidden or minute
Dibamidae 5 Dibamus male: single pair of flaplike hind
limbs female: absent
hidden hidden
Hypotheses on rostral shield evolution in Paracontias 145
labials are homologous between both morphological groups
of Paracontias (species with a rostral shield and those with
a rostral pseudo-shield), whereas the horizontal groove
extending posteriorly from the nostril is not homologous to
the suture delimiting the postnasal scale from the first
supralabial in Madascincus.
The two step hypothesis appears to be more likely, as it
takes into account the phylogenetic relationships within
Paracontias, the essential framework in any evolutionary
inference. This result is particularly interesting because (1)
it cautions that intuitive and seemingly obvious scale
homologies only based on position and size (as usually
formulated in squamate taxonomy) may be highly misleading,
even in closely related species (see also Köhler et al. 2010),
and (2) it indicates that the rostral pseudo-shield might be a
preliminary adaptation prerequisite to rostral shield forma-
Fig. 6 Evolutionary origin of the rostral shield in Paracontias.Two
hypotheses may explain genesis of the rostral shield; both involve the
same first evolutionary step: fusion of the rostral with the supranasals
and the postnasals. In the one step hypothesis, the rostral shield results
from fusion of the first supralabial with the rostral scale. In the two
step hypothesis, a rostral pseudo-shield constitutes an intermediate
state resulting from fusion of the first two supralabials (step 1),
followed by backward extension of the rostral pseudo-shield, together
with regression of the first supralabial (step 2). aPlesiomorphic state
in Madascincus (M. polleni), characterized by presence of a pair of
supranasal and postnasal scales. bRostral pseudo-shield in Paracontias
(P. vermisaurus). cRostral shield in P. hafa
146 A. Miralles et al.
tion. The latter is either (1) because it constitutes a more
advantageous structure (preferable to the rostral shield)
for species of moderately fossorial habits (including the
ancestral species of Paracontias), and the fully developed
rostral shield is only of selective advantage for fully
fossorial species, or (2) because developmental constraints
prevent the fusion of the rostral with the first supralabial,
thus forcing an evolutionary pathway in which a rostral
shield originates via this alternative and somewhat less
parsimonious way.
Functional implications of the rostral shield
The rostral shield occurs in different lineages of exclusively
fossorial Squamata, strongly suggesting that this feature
represents an adaptive response to this highly specialized
lifestyle. The occurrence of such a large plate (rather than
several smaller scales) may provide several advantages for
fossorial species, both facilitating the burrowing activity
and protecting the head from the strong physical con-
straints. First, it results in a smoother snout, thus reducing
friction between the substrate and the skin; second, it
should strengthen the tegument on the snout by reducing
the number of sutures that act as flexible joints between two
adjacent scales. Additionally, we have observed that in
most of these groups (eg. Nessia,Acontias,Paracontias),
the rostral shield frequently shows a very particular milky
coloration significantly lighter than the adjacent scales, and
gives the impression of being slightly turgid and thicker
(see Fig. 4). It is also important to note that in all the skinks
for which high resolution X-ray computer tomography
images were available to us at the Digital Morphology
Library (http://digimorph.org/), osteoderms always appear
to be absent (Chalcides,Eumeces,Scincus,Sphenomorphus,
Tiliqua)or weak and lacunar (Eugongylus)from the
rostral to the anteriormost supralabials, whereas they are
present and well ossified in almost all the other cephalic
scales (see Fig. 7). Interestingly, these unossified scales are
those usually involved in the formation of the rostral shield,
which suggests that osteoderms should likely be absent from
the rostral shield. Unfortunately, none of these genera
studied by tomography represent legless fossorial forms
nor do they have rostral shields, which prevents us from
verifying this hypothesis. Nevertheless, we suppose this may
indicate that in fossorial species the nature of the tissue
constituting the rostral tegument is distinct from those of
other cephalic scales, and that probably most of the snout
surface, which is almost exclusively covered by the rostral
shield, is not ossified (whereas osteoderms are only absent
from the rostral tip in non-fossorial forms). These observa-
tions lead us to consider that the rostral shield may likely
play the role of a shock-absorbing buffer in the fossorial
species. Only a histological study could answer these
questions, by determining whether the skin or the underlying
connective tissue displays any unusual structural and
functional properties.
Lastly, the horizontal postnasal groove constitutes
another characteristic of the rostral shield, as it is always
present. Given that it always runs to posterior from the
nostril, we suggest that it may act as a gutter draining
impurities out of the nostril during burrowing activity.
Conclusions
The present study allows us to formulate various hypotheses
on the evolution and function of head scalation in fossorial
squamates, although a thorough test of these was not possible
within the limited scope of this work. Future approaches, e.g.
involving histology, functional anatomy or developmental
biology, will help to better understand the internal structure,
properties and formation of the rostral shield. Additionally,
comparative studies involving larger taxonomic sampling,
encompassing a more comprehensive number of fossorial
skink lineages, and also including genera without rostral
shield (e.g. Lerista in Australia, Neoseps in North America,
or Voeltzkowia in Madagascar), will be informative to
determine whether certain factors (e.g. substrate, prey,
locomotion) exist that may explain the convergent presence
(or plesiomorphic absence) of the rostral shield in these
different taxa. As an example, our observations led us
hypothesize that the rostral shield may be more frequently
associated with the fossorial species having a rounded snout
and living in the leaf litter of humid forests, whereas it may
be more frequently absent in the species having a spade-
shaped snout usually living in sandy areas. Moreover, the
absence of osteoderms from the rostral scale in probably
mostif not allskinks leads us to wonder whether the
rostral tip can also show some functional particularity in the
non-fossorial forms. Does the rostral scale in these species
Skull
osteoderms
Fig. 7 Tomographic image of Eumeces schneideri highlighting
presence of osteoderms in all scales covering the head (outlined in
white), with the notable exception of those present in the anteriormost
part of the snout. Source: DigiMorph.org
Hypotheses on rostral shield evolution in Paracontias 147
play a similar role as a shock-absorbing buffer (for instance
during prey capture or when they suddenly take refuge under
the substrate to escape predators)? Or does this structure
have a different, unknown function, thus constituting a case
of exaptation exploited in different ways by the fossorial
lineages?
Fossorial legless lizards such as Paracontias are among
those lineages of vertebrates that have experienced adapta-
tions to a burrowing lifestyle to the most extreme level.
Despite all the remarkable features that make them
excellent models for studying macroevolutionary trans-
formations in body plan, most of these species remain
poorly known and dramatically understudied. Nearly all the
species of Paracontias are considered as very rare, as they
are frequently known from few or even only a single
specimen. Almost nothing is known about the biological,
ecological, physiological or behavioral traits of these
enigmatic organisms, whereas we can reasonably expect
those traits to be as modified as the morphological features.
It seems that these species have been largely ignored by the
scientific community because of their very secretive
fossorial way of life, their very small size, and possibly
their microendemic and patchy distribution. As a conse-
quence, these species are rare in collections, but most
probably most of them are not rare in nature, as
suggested by the discovery of larger numbers of
individuals of P. m i n i m u s and P. rothschildi which were
easy to find after some information about their habitats
and habits had been gathered from local people (Köhler et
al. 2010). The high rate of recent species descriptions and
the scarcity of knowledge on the genus point to intensified
collecting of Paracontias asafruitfulsourceofnew
discoveries, and encourage the development of fossorial
species-oriented prospecting protocols, including more
specific trapping methods.
Acknowledgements We are grateful to Franco Andreone (MRSN),
Annemarie Ohler and Ivan Ineich (MNHN) for giving us access to
collection specimens, and to Jessica Maisano (UTA) and the Digital
Morphology Library (http://digimorph.org/) for making available the
tomographic picture of Eumeces.WewishalsotothankTheo
Rajofiarison, Jim and Carol Patton, Emile Rajeriarison, Fanomezana
Mihaja Ratsoavina and Roger-Daniel Randrianiaina who helped
collect specimens, Florent and François Randrianasolo from the
WCS for their help to companionship in the field, and our drivers
Claude and Samy for safely carrying us to the bases of the Makira
slopes. This work was carried out in the framework of a collaboration
accord between the Département de Biologie Animale, Université
dAntananarivo, and the Technical University of Braunschweig. We
are grateful to the Malagasy authorities for research and export
permits, and to the Wildlife Conservation Society for supporting our
research activities at Makira. Funding was provided by the Volkswa-
gen Foundation to MV, a Ministry of Science and Innovation grant
(CGL200910198) to DRV, and a postdoctoral Research Fellowship
from the Alexander von Humboldt Foundation to AM.
Appendices
Appendix 1 list of specimens examined
Amphiglossus stylus MRSN R1732 (holotype), Masoala
Peninsula, Campsite 5 (Menamalona), Antalaha Fivondronana,
Antsiranana Faritany, 15°22.87S, 49°59.27E, 780 ma.s.l.,
northeastern Madagascar.
Paracontias brocchii ZSM 244/2004, Montagne dAmbre,
12°31S, 49°10E, ca. 1,000 ma.s.l., Antsiranana Province,
northern Madagascar.
Paracontias fasika ZSM 2256/2007 (holotype), Baie de
Sakalava, 12°1624S, 49°2333E, 11 ma.s.l., Forêt
dOrangea, Antsiranana Province, northern Madagascar.
Paracontias hafa MRSN R1825 (holotype), Anjanaharibe-Sud
Massif, Analabe Valley, Campsite W1, Befandriana
Fivondronana, Mahajanga Faritany, 14°46S, 49°27E,
1,0001,100 ma.s.l., northeastern Madagascar.
Paracontias hildebrandti ZMB 9695 (holotype), nordwes-
tliches Madagaskar; ZSM 1578/2008, Montagne des
Français, 12°20S, 49°22E, 120 ma.s.l., northern
Madagascar.
Paracontias kankana ZSM 1810/2008 (holotype), Mahasoa
forest (pitfall camp), near Ambatodisakoana village,
17.29769° S, 48.70199° E, 1032 ma.s.l., eastern Madagascar.
Paracontias manify MRSN R1887 (holotype), Antsahama-
nara, Manarikoba Forest, RNI de Tsaratanana, Marovato
Fivondronana, Antsiranana Faritany, 14°02.55S, 48°46.79
E, about 1,000 ma.s.l., northern Madagascar.
Paracontias minimus MNHN 1905.270 (lectotype),
MNHN 1905.270A (paralectotype), Madagascar; ZFMK
8805188052, ZSM 22492253/2007, ZSM 2268/2007,
ZSM 15851586/2008, Baie de Sakalava, Forêt dOrangea,
12°1624S, 49°2333E, 11 ma.s.l.; ZSM 1584/2008,
south-east of Ivovona, Forêt dOrangea, 12°1958S, 49°
2420E; ZSM 1583/2008, Ampombofofo, Babaomby
region, 12°0553S, 49°1949E, Antsiranana Province,
all from northern Madagascar.
Paracontias rothschildi ZFMK 8804888050, ZSM 2074/
2007, ZSM 2235/2007, ZSM 22462247/2007, ZSM
22602269/2007, ZSM 15801582/2008, Baie de Saka-
lava, Forêt dOrangea, 12°1624S, 49°2333E, 11 ma.s.
l.; ZSM 1579/2008, south-east of Ivovona, Forêt dOran-
gea, 12°1958S, 49°2420E, Antsiranana Province,
northern Madagascar.
148 A. Miralles et al.
Paracontias tsararano MRSN R1787 (holotype), Tsarar-
ano Forest, Campsite 1, 14°54.4S, 49°41.2E, 710 m a.s.l.,
Antsarahanny Tsararano, northeastern Madagascar.
Appendix 2 corrigenda to original description
of Paracontias fasika
Re-examination of the holotype of Paracontias fasika has
revealed some mistakes in the original description (Köhler
et al. 2010) that need to be corrected.
Contrary to what is written in its diagnosis, the holotype
of Paracontias fasika has no supranasals. In the dorsal view
of the head (Köhler et al. 2010: 154, Fig. 5a), the two scales
in contact with the nostrils, the rostral and the frontonasals
are actually loreals.
On the lateral view of the head (Fig. 5b), the shape and
the size of the loreal scales have been incorrectly
represented. These scales would have been drawn in frank
contact with the rostral, as it has been correctly done in the
Fig. 6a.
In the same figure, the fourth reduced supraocular is
lacking, only the last enlarged supraciliaries being repre-
sented. The dorsal view (Fig. 5a) gives a correct represen-
tation of these scales.
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... These, together with Greer (1991) and Das et al., (2008) have helped to highlight a high degree of cryptic diversity within the various genera. Recently, Miralles et al. (2011Miralles et al. ( , 2016 showed that reduction of number of scales on the anteriomost part of the head might have contributed to high species diversity in fossorial skinks. They also recognized convergent evolution of Nessia of Sri Lanka with three other Scincidae genera and another single genus of family Dibamidae. ...
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(Abstract in english) Halfway through a process of modernization undertaken some twenty years ago, the challenges facing contemporary α-taxonomy are multiple, and are as much quantitative (accelerating the inventory of living organisms) as qualitative (having reliable species hypotheses). They consist, among others, of: appropriation of concepts and techniques developed in evolutionary biology; standardization / formalization of decision-making processes (when to describe a species hypothesis?); integration of new types of data (genome, transcriptome, Ctscan); and development of adapted digital tools (interoperable and specimen-centered databases, tools dedicated to species delimitation, assessment of confidence in species hypotheses, etc.). The extent of these changes and those to come also highlights the need to revise and strengthen the epistemological basis on which this multi-secular branch of biology rests. Beyond my works on squamates systematics (mainly phylogenies and integrative revisions of tropical skinks), this dissertation will focus on my generalist contributions, i.e. those addressed to all practitioners regardless of their field of specialization. After a presentation of the different notions related to the α-taxonomy and a historical overview intended to better measure the extent of the paradigm shift this discipline is going through, a detailed synthesis of my contributions to methodological or technical questions will be presented. They are addressing, among others, issues related to taxonomic data (characterization, management, sharing and integration) and to the objective comparison of partitions resulting from different species delimitation analyses.
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