Quaternary International xxx (2011) 1e12
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Quaternary International
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Phylogeny and biogeography of fossil and extant Microtus (Terricola) (Mammalia,
Rodentia) of Sicily and the southern Italian peninsula based on current
dentalmorphological data
Daria Petruso a, Elisa Locatelli b, *, Giovanni Surdi a, Chiara Dalla Valle b, Federico Masini a, Benedetto Sala b
a
b
Department of Geology and Geodesy, Via Archirafi 22, 90123, Palermo, Italy
Department of Biology and Evolution, C.so Ercole I d’Este 32, 44100 Ferrara, Italy
a r t i c l e i n f o
a b s t r a c t
Article history:
Available online xxx
The fossil record of the Savi vole, Microtus (Terricola) savii, is analyzed in terms of morphological and
morphometrical variability of the first lower molar, in order to reconstruct phylogenetic relationships
between insular and mainland populations and the dispersal events. The present work gives a contribution to better understand the phylogenetic history of this taxon in Sicily and Southern Italy during the
interval Middle Pleistocene e Holocene, in an attempt to reconstruct the relationships between insular
and continental voles and to clarify some paleobiogeographical aspects. The morphometrical data have
been acquired by traditional measurements of the first lower molar and analyzed by dispersal diagrams
and Principal Components Analysis.
The fossil Sicilian samples have a greater size variation than extant ones. Two different morphological
groups have been identified and named on the basis of the similarity with European or Italian populations: a “subterraneomorph” one (characterized by a tighter symmetric anterior cap and longer
anteroconid), similar to European M. (T.) subterraneus species, and a “savimorph” one (more confluent
and asymmetric anterior cap and shorter anteroconid), occasionally with the accentuation of morphological characters of M. (T.) savii.
The results, in particular the differences between Pleistocene and Holocene Sicilian populations and
the similarities with the mainland ones, suggest that the Savi vole dispersed at least twice in Sicily. One
colonization took place likely during the cold stage MIS 6 (recorded at Isolidda 3) with dispersal events,
made possible by the sea level drop and the connection with the mainland, and a second one (documented at San Teodoro cave and other Holocene assemblages) during MIS 4 (by dispersal events) or MIS
3 (by accidental transit or limited faunal exchanges).
Ó 2011 Elsevier Ltd and INQUA. All rights reserved.
Keywords:
Microtus (Terricola) savii
Sicily
Pleistocene
Holocene
Insularism
Paleobiogeography
1. Introduction
Microtus (Terricola) savii is widespread all over Italy, with the
exception of the northeast and Sardinia, but many questions about
its origin and evolution are still unsolved. According to Tougard
et al. (2008), M. (T.) savii originated in Italy and it has close relationships with M. (T.) multiplex. Four subspecies are recognized
nowadays: Microtus (Terricola) savii savii (de Sélys Longchamps,
1838), in Northern and Central Italy; Microtus (Terricola) savii
nebrodensis (Minà Palumbo, 1868), in Sicily; Microtus (Terricola)
savii tolfetanus (Contoli, 2003) in Latium; and Microtus (Terricola)
* Corresponding author.
E-mail addresses: elisa.locatelli@unife.it, elisal40@hotmail.com (E. Locatelli).
savii niethammericus (Contoli, 2003) in Basilicata, Abruzzo and
Apulia.
The occurrence of a distinct species Microtus (Terricola) brachycercus (von Lehmann, 1961), closely related to the Savi vole, is
recognized in the Calabria peninsula, based on karyological
features (Galleni et al., 1992, 1994, 1998; Galleni, 1995; Wilson and
Reeder, 2005). The phylogenetic distance of the Northern and
Central Italian populations of M. (T.) savii from M. (T.).brachycercus
has been confirmed by molecular analyses by Jaarola et al. (2004)
and Castiglia et al. (2008). The latter authors found also a greater
affinity of the Calabria species with populations referred to M. (T.)
savii niethammericus by Contoli (2003). These results lead Contoli
and Nappi (2009) to place the subspecies “niethammericus”
within the species M. (T.) brachycercus. The morphological
distinction between the Calabrian voles (namely from Aspromonte)
1040-6182/$ e see front matter Ó 2011 Elsevier Ltd and INQUA. All rights reserved.
doi:10.1016/j.quaint.2011.03.013
Please cite this article in press as: Petruso, D., et al., Phylogeny and biogeography of fossil and extant Microtus (Terricola) (Mammalia, Rodentia)
of Sicily and the southern Italian peninsula based on current dentalmorphological data, Quaternary International (2011), doi:10.1016/
j.quaint.2011.03.013
2
D. Petruso et al. / Quaternary International xxx (2011) 1e12
and Southern Italian, particularly Sicilian, populations, was first
noted by De Luca (1998) and illustrated by Petruso (2003) based on
measurements and morphological indexes of the first lower molar
(M1). On the other hand, “small differences” between the Calabrian
vole and vole samples from Northern, Central and Southern Italy
were detected by Nappi et al. (2005) using Canonical Discriminant
Analysis on a set of linear measurement of the M1. These authors
concluded that if the Calabrian vole is proved to be a distinct
species from the Savi vole, separation must have been achieved
recently. Multivariate morphological analysis carried on first lower
molars by Piras et al. (2010), based on geometrical morphometric
methods, apparently confirms the morphological distance of Calabrian populations from some samples of M (T.) savii from Southern
Italy and two samples from Central and Northern Italy.
Nappi et al. (2006), working with the methodology of Nappi
et al. (2005) on some 50 samples distributed all over Italy and
Sicily (but not Calabria), detected a morphological differentiation
between north-central and southern populations of Italy. The
authors infer the existence of a latitudinal gradient (a morphocline)
based on the analogies between the intraspecific differences within
the Italian populations and the interspecific differences within the
Western European group - between the northern multiplex-subterraneus group (sensu Chaline, 1972) and the southern Microtus
(Terricola) duodecimcostatus (de Sélys Longchamps, 1839).
Conversely, Piras et al. (2010) deny the significance of differences
between central and southern populations and claim the influence
of a “more complex climatic effect” and the importance of phylogeographic relationships in modeling the variability among
Microtus (Terricola) populations and species. The same authors in
a previous paper (Piras et al., 2009) had already sustained some
correlations between the morphological variation of the anterior
portion of the first lower molar and the climatic fluctuations as
expressed by the d18O climatic proxy.
Even though the extant vole populations from Sicily were
referred to M. (T.) savii nebrodensis in the critical revision of Contoli
(2003), diverging opinions are expressed in the literature concerning their actual phylogenetic relationships, taxonomy and
origin. Castiglia et al. (2008) identified a noteworthy distance in
Cytochrome b haplotypes (7%) between some specimens from
Ficuzza (Palermo, western Sicily) and those of the savii e brachycercus group, suggesting a possible distinct specific status for the
former population. On the other hand, Nappi et al. (2006) on the
basis of morphological analysis, considered that the Sicilian
Microtus (Terricola) falls in the southern group of savii, having,
however, some distinctive features in the anterior part of the first
molar. Conversely, Piras et al. (2010) did not detect any significant
difference between the Sicilian populations and the Savi vole from
the Italian peninsula.
Species of the subgenus M. (Terricola) are the fossil voles
present, locally in great abundance, in many Sicilian deposits, since
the late MiddleeLate Pleistocene. However, until the 1990s, information on its occurrence was limited to a specimen from La Costiera (PA; Burgio and Kotsakis, 1987). Previously, limited attention
was given by paleontologists to non-endemic small mammals of
Sicily and very little (if any) sediment from the 170 Quaternary
deposits known on the island had been sieved for collecting
microfauna (Petruso et al., 2008). Even fewer works, specifically
addressed to the detailed analysis of the Savi vole morphology,
have been produced to clarify the relationships between the Sicilian
populations and the peninsular ones. The first finding, reported by
Burgio and Kotsakis (1987) from the site of La Costiera, consisted of
a unique remain (a mandible fragment) referred to as “Pitimys¼Microtus (Terricola) cf. savii” and doubtfully ascribed to the
Late Glacial Castello Faunal Complex (FC). Subsequently,
Tagliacozzo (1993) documented the diffusion of Microtus (Terricola)
in the early Holocene deposit of Uzzo cave (San Vito lo Capo, TP)
and confirmed its occurrence in pre-Holocene (Late Glacial) levels.
Bonfiglio et al. (1997) described samples from two new fossil sites
and referred them to M. (T.) ex gr. savii: the Late Pleistocene sample
from Contrada Pianetti (RG), later referred by Bonfiglio et al. (2002)
to the Grotta di San Teodoro e Pianetti FC (MIS4-2), and a sample
from the Late Pleistocene layer of site K22 (San Vito lo Capo, TP).
The authors stressed the differences between the two fossil populations and suggested they could have derived from two distinct
dispersal events from the continent, considering the one that gave
rise to the Contrada Pianetti vole as older. The first comparative
study of the extant Savi vole from Sicily, an extant population from
Aspromonte and the Late Pleistocene sample from site K22, was
carried on shortly after (De Luca, 1998). In the comparison, all the
analyzed populations were attributed to the savii group, with the
exception of the sample from Calabria, which showed morphological features closer to the multiplex-subterraneus group. A deeper
and more extended comparative analysis of the fossil material of
this species from more numerous Late PleistoceneeEarly Holocene
Sicilian sites (San Teodoro Cave, Acquedolci, ME; Uzzo Cave, Castello shelter, PA; K22) was carried on by Petruso (2003), who
attributed all the Sicilian samples to the savii group and detected
a more complex and assorted coexistence of different characters in
the Maltese sample from the Last Glacial deposit of Ghar Dalam
(Malta; Storch, 1974). The comparison noted the wide size variation
among the populations, ascribable to different micro-environmental features. Locatelli (2007) analyzed the late Middle Pleistocene-Late Pleistocene vole remains from Isolidda 3 cave (San Vito lo
Capo, TP), and the results show a marked difference between these
old Sicilian populations and the aforementioned younger ones. A
detailed study of the San Teodoro vole remains is reported in
Bonfiglio et al. (2008), pointing out the morphological differences
between samples coming from different sectors and different layers
of the cave.
Despite the efforts of the last 10 years, the details of the dispersal
history of this vole in Sicily and the question if it reached the island
only one time, and then evolved in Sicily, with sporadic contacts with
the mainland populations, or if it reached the island more than once,
is still particularly challenging. Morphological divergence in respect
to the peninsular populations due to endemic processes is expected
as a result of geographical isolation, while greater similarities with
the peninsular samples of different ages would be indicative of
possible connections with the mainland. The aim of this study is to
detect, by the morphometrical analysis of the first lower molar of
Microtus (Terricola) ex gr. savii of extant and fossil Sicilian populations and their comparison with peninsular and Western European samples, the possible similarities between different
populations that could suggest a strict phylogenetic relation. Thus
the dispersal events of this vole during late MiddleeLate Pleistocene
could be outlined, hypothesizing the presence of temporary land
bridges with the mainland, also forming a contribution to the
reconstruction of the Sicilian paleobiogeography.
2. Materials and methods
The systematic study was carried on by means of morphometric
analysis on voles’ first lower molars from 22 localities, including 13
fossil deposits and 9 extant populations. The location of the sites is
shown in Fig. 1. The total number of samples examined was 34, as in
some fossil sites with a clear stratigraphic succession (Isolidda 3 cave,
Cavallo cave, Grotta Grande di Scario cave, Uzzo cave and San Teodoro
cave), specimens from different levels have been analyzed separately.
The samples used in the analysis have been chosen for both
chronological and geographical reasons. With regard to Sicilian
samples, all the known fossil sites with Microtus (Terricola) have
Please cite this article in press as: Petruso, D., et al., Phylogeny and biogeography of fossil and extant Microtus (Terricola) (Mammalia, Rodentia)
of Sicily and the southern Italian peninsula based on current dentalmorphological data, Quaternary International (2011), doi:10.1016/
j.quaint.2011.03.013
D. Petruso et al. / Quaternary International xxx (2011) 1e12
3
Fig. 1. Location map.
been considered (with the exception of La Costiera unique remain,
which has been lost), while the extant populations come from
localities with different geographical features (some are located
near coastal areas, and others close to mountain chains). For the
Italian peninsula samples, sites coeval with the Sicilian ones and
located in different regions of Italy have been considered, in order
to separate geographical data from chronological ones. Eventually,
two extant populations belonging to Microtus (Terricola) subterraneus (France) and Microtus (Terricola) lusitanicus (Spain) have
also been considered as a sort of “out-group” for comparisons. The
list of the localities, fossil and extant ones, together with the age of
their deposits (single or distinguished into different levels), the
distinctive code used in the diagrams, the number of specimens of
each sample and the references for the chronology of fossil sites, are
reported in Table 1.
Measurements have been taken according to the plan proposed
by Van der Meulen (1973) and modified by Masini (in Bonfiglio
et al., 1997; Masini et al., 2005) with the integration of some
measures according with the Brunet-Lecomte and Chaline (1992)
scheme (Fig. 2) with a Leica MZ8 orthoplan microscope. At Ferrara university it was provided with a Parker 4508DM positioning
stage (straight-line accuracy 2 mm).
The analysis has been carried out by bivariate diagrams using
the measurements and morphological indexes computed from the
single measures such as: AL (A/L*100), A2A (A2/A*100), BW (B/
W*100), CW (C/W*100), DW (D/W*100), DE (D/E*100), L45 (L4/
L5*100). To trace the evolutionary pattern and to find out possible
relations between different populations, the mean values of each
measurement or morphological indexes are plotted on the abscissa,
while on the vertical axis discrete intervals of time (time slices),
related to important paleoclimatic events are reported. Principal
Component Analysis (PCA) with correlation metric has been carried
out on the means of measurements and indexes of the considered
samples using PAST software (Hammer et al., 2001).
3. Results
The analysis demonstrated that extant Sicilian populations are
fairly separate from continental ones. Fossil populations show
a more diversified pattern.
3.1. Size variation
Fig. 3 illustrates the variation in size related both to time and to
geography inferred by the length of M1. Most of the fossil Sicilian
populations are on the average larger than the continental ones.
The greatest size was reached during MIS 3 (San Teodoro trench
03e04 and square A B C, TEO0304ABC), the Late Glacial (Castello
Shelter e RC) and especially in the ancient Holocene (Uzzo Mesolithic II and Neolithic levels, UZ mII e UZn). However, very small
sized or “normal” sized samples (namely Contrada Pianetti, Oriente
Cave and San Teodoro square D) occur among the fossil Sicilian
voles of these time slices. In older samples, the size difference
between insular populations (Isolidda 3) and continental ones
(Cavallo cave, Grotta Grande di Scario) seems to be less relevant,
even though Sicilian samples are already slightly larger.
3.2. Morphological variation
Beside the size variation, the analysis demonstrated important
morphological variation in tooth shape. The relative proportions of
the anteroconid (ACC, the anterior portion of the first lower molar,
Fig. 2) respect to the total length of M1 have been investigated by
measures A, A2, L and the related indexes, AL and A2A. It is possible
to notice a difference between insular and continental populations
(Figs. 4 and 5); the latter have longer anteroconid complex (A) and
anterior cap (A2) relative to the Sicilian Savi voles. The extant Savi
sample from Melendugno, in the Salento peninsula, represents an
exception, as it is closer to Sicilian populations than to peninsular
ones.
As the ACC represents the most variable part of the first lower
molar, this part of the tooth is particularly important for the
taxonomy of the group and its morphology has been investigated
more in the details. In order to analyze the degree of constriction of
the triangles, three parameters (D, E, W) and their indexes have
been used (Figs. 6 and 7). The variable D measures the degree of
constriction of the anterior cap; E describes the width of the
triangles T6 and T7 that in the maximum development shapes
a rhombus (Fig. 2); W conveys the width of the next pair of triangles (T5eT4), the so-called pitymyan rhombus (Fig. 2), peculiar for
the morphology of Microtus (Terricola). Peninsular populations are
Please cite this article in press as: Petruso, D., et al., Phylogeny and biogeography of fossil and extant Microtus (Terricola) (Mammalia, Rodentia)
of Sicily and the southern Italian peninsula based on current dentalmorphological data, Quaternary International (2011), doi:10.1016/
j.quaint.2011.03.013
4
D. Petruso et al. / Quaternary International xxx (2011) 1e12
Table 1
Localities. List of the localities, fossil and extant ones, together with the age of their deposits (single or distinguished into different levels), the distinctive code used in the
diagrams, the amount of each sample and the literature used as reference for the chronology of fossil sites.
Country
Area
Locality
Code
Taxon
Age
N
France
Spain
Italy
Italy
Italy
Italy
Italy
Italy
Italy
Italy
Apulia
Tuscany
Tuscany
Calabria
Sicily
Sicily
Sicily
Sicily
Sarcey-Rhone (FR)
Lamilla-Burgos (E)
Melendugno (LE)
San Miniato (PI)
Cascina (PI)
Aspromonte (RC)
Borgo Lupo (TP)
Piana di Gela (CL)
Mazzarino (CL)
Uzzo Cave (TP)
sub
lus
Mel
Smin
Cas
Asp
BLu
Gel
Maz
UZmI
M. (T.) subterraneus
M. (T.) lusitanicus
M. (T.) savii
M. (T.) savii
M. (T.) savii
M. (T.) s. brachycercus
M. (T.) s. nebrodensis
M. (T.) s. nebrodensis
M. (T.) s. nebrodensis
M. (T.) ex gr. savii
5
27
32
38
45
30
22
26
12
39
Tagliacozzo (1993)
Italy
Sicily
Uzzo Cave (TP)
UZmII
M. (T.) ex gr. savii
32
Tagliacozzo (1993)
Italy
Sicily
Uzzo Cave (TP)
UZn
M. (T.) ex gr. savii
15
Tagliacozzo (1993)
Italy
Italy
Sicily
Sicily
Cala Mancina (TP)
Castello shelter (PA)
MAN
RC
M. (T.) ex gr. savii
M. (T.) ex gr. savii
60
6
Martini et al. (in press-b)
Petruso (2003)
Italy
Sicily
OR
M. (T.) ex gr. savii
41
Martini et al. (in press-a)
Italy
Italy
Campania
Apulia
Oriente Cave -Favignana
island (TP)
Serratura Cave (SA)
Cavallo Cave (LE) layer B
SER
CavB
M. (T.) ex gr. savii
M. (T.) ex gr. savii
Extant
Extant
Extant
Extant
Extant
Extant
Extant
Extant
Extant
Early Holocene
Mesolithic 1
Early Holocene
Mesolithic 2
Early Holocene
Neolithic
Early Holocene
Late Glacial - Holocene
(MIS2e1)
Late Glacial
(MIS2)
Late Glacial (MIS2)
Late Glacial (MIS2)
96
29
Italy
Sicily
K22 (TP)
K22
M. (T.) ex gr. savii
Würm (MIS3e2?)
35
Italy
Sicily
TEO98
M. (T.) ex gr. savii
Würm (MIS3)
22
Italy
Sicily
TEOABC
M. (T.) ex gr. savii
Würm (MIS3)
12
Bonfiglio et al. (2008)
Italy
Sicily
TEOD
M. (T.) ex gr. savii
Würm (MIS3)
16
Bonfiglio et al. (2008)
Italy
Apulia
S.Teodoro Cave (ME)
trench 1998
S.Teodoro Cave (ME) trench
2003e04 ABC sectors
S.Teodoro Cave (ME) trench
2003e04 D sector
Cavallo Cave (LE) layer F
Martini (1993), Bertolini et al. (1996)
Palma di Cesnola and Borzatti
von Löwestern (1964)
Petruso (1996), De Luca (1998),
Di Maggio et al. (1999)
Bonfiglio et al. (2008)
CavF
M. (T.) ex gr. savii
Würm (MIS3)
45
Italy
Malta
Italy
Sicily
Contrada Pianetti (RG)
Ghar Dalam Cave (Malta)
Grotta Grande di Scario
(SA) trench A
CP
GD
GGSA
M. (T.) ex gr. savii
M. (T.) melitensis
M. (T.) ex gr. savii
Würm (MIS3)
Würm?
Post-Tyrrhenian
(MIS5d-a)
31
28
18
Italy
Campania
Grotta Grande di Scario
(SA) trench F
GGSF
M. (T.) ex gr. savii
Post-Tyrrhenian
(MIS5d-a)
24
Italy
Apulia
Cavallo Cave (LE) layer M
CavM
M. (T.) ex gr. savii
45
Italy
Apulia
San Sidero 3 (LE)
SS3
M. (T.) sp.
24
De Giuli (1983)
Italy
Italy
Apulia
Campania
Cavallo Cave (LE) layer N
Grotta Grande di Scario (SA)
trench C lower
CavN
GGSCi
M. (T.) ex gr. savii
M. (T.) ex gr. savii
Post-Tyrrhenian
(MIS5d-a)
Post-Tyrrhenian
(MIS5 s.l.)
Eemian (MIS5e)
Pre-Tyrrhenian (MIS6)
Palma di Cesnola and Borzatti
von Löwestern (1964)
Bonfiglio et al. (1997)
Storch (1974)
Abbazzi and Masini (1998), Boscato
and Ronchitelli (2004), Ronchitelli
et al. (1998, 2008)
Abbazzi and Masini (1998), Boscato
and Ronchitelli (2004), Ronchitelli
et al. (1998, 2008)
Sarti et al. (2002)
33
48
Italy
Campania
Grotta Grande di Scario (SA)
trench C upper
GGSCs
M. (T.) ex gr. savii
Pre-Tyrrhenian (MIS6)
25
Italy
Italy
Italy
Sicily
Sicily
Sicily
Torre Isolidda 3 (TP) US 15, lower
Torre Isolidda 3 (TP) US 13, middle
Torre Isolidda 3 (TP) US 12, upper
TI3i
TI3m
TI3s
M. (T.) sp.
M. (T.) sp.
M. (T.) sp.
Pre-Tyrrhenian?
Pre-Tyrrhenian?
Pre-Tyrrhenian?
42
45
45
Sarti et al. (2002)
Abbazzi and Masini (1998), Boscato
and Ronchitelli (2004), Ronchitelli
et al. (1998, 2008)
Abbazzi and Masini (1998), Boscato
and Ronchitelli (2004), Ronchitelli
et al. (1998, 2008)
Martini et al. (in press-c)
Martini et al. (in press-c)
Martini et al. (in press-c)
Campania
well separated from insular ones, with the exception of the oldest
samples, as Sicilian (Isolidda 3) and peninsular (Scario) samples are
closer to each other. From MIS 3 to Holocene, all Sicilian populations are very homogeneous in the EW diagram (Fig. 6), showing
slight variation as do the living ones, but having smaller values
(T6eT7 rhombus respect to the pitymyan rhombus relatively
smaller than in the continental populations). On the other hand, the
anterior complex of Sicilian populations since MIS 3 underwent an
opening (DE index), with the higher value found in the living
populations, thus increasing the distance from the northern
samples that maintain rather small values. Considering all samples
together, although EW does not show a great variation (standard
deviation of the mean values of EW of each sample is 2.64), DE is
Reference for the chronology
of fossil sites
highly variable (8.85) and extant northern populations are clearly
separated from the Sicilian ones. The Apulian living population
from Melendugno plots with Sicilian samples, while the Aspromonte Microtus (Terricola) brachycercus is always within the
multiplex-subterraneus group and the two Central Italy Savi
populations.
A different pattern is shown by pre-Tyrrhenian samples. The
Isolidda 3 populations are close to the contemporary continental
samples from Grotta Grande di Scario, both in the EW and in DE
diagrams. Fossil Apulian populations from levels M and N of
Cavallo cave are well isolated from all the other ones in showing
plesiomorphic features (namely, high values of DE and small
values of EW).
Please cite this article in press as: Petruso, D., et al., Phylogeny and biogeography of fossil and extant Microtus (Terricola) (Mammalia, Rodentia)
of Sicily and the southern Italian peninsula based on current dentalmorphological data, Quaternary International (2011), doi:10.1016/
j.quaint.2011.03.013
D. Petruso et al. / Quaternary International xxx (2011) 1e12
5
Fig. 2. Nomenclature and measures. (a) Nomenclature of dental parts of the first lower molar in occlusal view. (b) Plan of measurements, according to Van der Meulen (1973) and
modified by Masini (in Bonfiglio et al., 1997). (c) Plan of measurements, according to Brunet-Lecomte and Chaline (1992) scheme in Masini et al. (2005).
3.3. PCA
The PCA (Fig. 8) considers the first two components that account
for 75% of total variance (47.14% and 28.17% respectively, Table 2).
Interpretation of the morphological meaning of components 1
and 2 is not particularly straightforward because most variables are
correlated to both axes (see factor loadings in Table 3). Variables
expressing the size of teeth are loaded positively on the first
component, and negatively on the second. Variation in size therefore ranges along the diagonal with larger teeth scattering mostly
in the II square of the diagram. The variables and indexes that
account for the elongation of the ACC (including AC2) are negatively correlated on both axes, so that samples with more elongated
ACC tend to scatter in the III square. The same is true for E and EW,
while D, DE and DW are positively correlated to both components
Fig. 3. Length. Dispersion diagram illustrating the variation in size of the first lower
molar in time. The abscissa represents the mean value of L, the ordinate discrete
intervals of time. Sicilian samples are grouped inside the boxes.
so that teeth with an open AC2 tend to scatter in the first square.
Measure B and index BW also are both positively correlated to
components 1 and 2, but they are more weighted on the first one.
Therefore, teeth that tend to be smaller, with elongated ACC and
AC2, narrow AC2, wide T6eT7 rhombus and narrow constriction
between the pitymyan rhombus and AC2, are distributed on the
lower left side of the diagram, where M. (T.) subterraneus and M. (T.)
lusitanicus samples are placed.
Thus, the PCA confirms the previous results. Populations of the
same area and the same age tend to plot together in the PC1e2
diagram, with the exception of the Apulian samples. With regard to
extant populations, samples from Calabria and Central Italy are
Fig. 4. AL. Dispersion diagram illustrating the variation in time of the anteroconid
length compared to total length. The abscissa represents the mean value of the index
AL, the ordinate discrete intervals of time (the legend of time slices is reported in
Table 2). Sicilian samples are grouped inside the boxes.
Please cite this article in press as: Petruso, D., et al., Phylogeny and biogeography of fossil and extant Microtus (Terricola) (Mammalia, Rodentia)
of Sicily and the southern Italian peninsula based on current dentalmorphological data, Quaternary International (2011), doi:10.1016/
j.quaint.2011.03.013
6
D. Petruso et al. / Quaternary International xxx (2011) 1e12
Fig. 5. A2A. Dispersion diagram illustrating the variation in time of the relative
proportion of the anteroconid. The abscissa represents the mean value of the index
A2A, the ordinate discrete intervals of time. Sicilian samples are grouped inside the
boxes.
clearly separated from those from Sicilian localities and from
Apulia. The first are close to the multiplex-subterraneus voles, while
the others tend to disperse on the opposite side. Fossil samples
from Isolidda 3 are rather homogeneous and disperse close to
Calabrian, Central Italian and subterraneus voles. Fossil samples
from Grotta Grande di Scario are more scattered, and plot rather
close to Isolidda 3 and the peninsular samples. The Sicilian populations of younger age (MIS2e3) are rather isolated (high degree
of endemism), plotting alone on the positive part of Axis 1 (47.14%
Fig. 7. DE. Dispersion diagram illustrating the variation in time of the closing of the
anterior cap. The abscissa represents the mean value of the index DE, the ordinate
discrete intervals of time. Sicilian samples are grouped inside the boxes.
variance) and the negative part of Axis 2. The sample of Microtus
(Terricola) from Malta stands isolated in the same square and is
characterized by extremely negative values of Component 2. The
fossil sample for the Hyblean Plateau (Contrada Pianetti) is also
separate from the other Sicilian samples, falling very close to the
continental fossil populations. Apulian samples from Cavallo cave
are the most scattered, notwithstanding that they come from
a single geographic location. In particular, there is a great difference
between the ancient populations (CavM and CavN), which show
very marked “savimorph” characters, and the more recent ones
(CavF and CavB), which seem to be closer to the peninsular samples.
San Sidero 3 plots in an intermediate position among extant Apulian Terricola, fossil Savi vole from Grotta Grande di Scario and the
less “endemic” Würmian Sicilian samples.
4. Discussion
The morphometric study of Southern Italian fossil Microtus
(Terricola) carried on by comparative analysis produced a series of
results and raised some questions.
4.1. Size variation
Fig. 6. EW. Dispersion diagram illustrating the variation in the width of the anterior
cap related to the width of the pytimian complex. The abscissa represents the mean
value of the index EW, the ordinate discrete intervals of time. Sicilian samples are
grouped inside the boxes.
The comparison of the length of the first lower molar gives an
immediate idea of the body size variation occurring in Sicilian
samples and in the southern peninsula ones. Mammals in a “normal”
continental regime may reduce or increase their size, always to
a slight extent, mainly in relation to variation in climatic and environmental conditions (Bergmann rule), while on islands, body size
usually varies in one direction only and its variation is ruled mainly
by several ecological factors typical of the island environment (e.g.
area of the island, availability of resources, reduced predatory
pressure etc.; Lomolino, 2005). By and large, according to the socalled “island rule” (Foster, 1964; Van Valen, 1973; Sondaar, 1977),
geographic isolation on islands is expected to produce “giant” small
mammals and “dwarf” large mammals, i.e. small mammals should
acquire a larger size respect to their mainland counterparts, while
the reverse is expected in large mammals. The increase in size of
Please cite this article in press as: Petruso, D., et al., Phylogeny and biogeography of fossil and extant Microtus (Terricola) (Mammalia, Rodentia)
of Sicily and the southern Italian peninsula based on current dentalmorphological data, Quaternary International (2011), doi:10.1016/
j.quaint.2011.03.013
7
D. Petruso et al. / Quaternary International xxx (2011) 1e12
Fig. 8. PCA. Principal Component Analysis on the symmetric correlation matrix, Joliffe cut-off 0.7. Samples from different periods and different areas are grouped inside the boxes.
The explanation for the abbreviations is reported in Table 1.
small mammals may be explained by competitive interactions, that
is by the benefit that a larger size gives in the individual exploitation
of food supply in consideration of the small area of the island; the
bigger they are, the better they prevail in the competition within the
populations of the same species and/or with individuals of the other
species. Sicily is a sort of limiting case for this rule, as it is a large
island (the largest in the Mediterranean Sea) and it is separated from
the mainland only by a sea corridor, the Strait of Messina. This
particular geographical and geological configuration made the
isolation unstable, at least from the Late Middle Pleistocene
onwards, thus reducing the above-mentioned effects on the faunal
association and the body size variation.
Considering the mean value of the length (L) of each sample,
Sicilian Savi voles are on average some 5% (computed on the mean L
of each sample) larger than the peninsular populations of Terricola,
but a distinction among samples of different age has to be made.
The extant Sicilian populations are rather variable in size, but they
are quite small, about the same size as the extant mainland ones.
This homogeneity between insular and mainland populations could
be due to frequent human and faunal exchanges between the island
and the mainland, and to the influence of humans on the insular
mammal ecology (with the introduction of foreign taxa, terrestrial
predators, habitat fragmentation for agriculture purposes and
domestication) that has reduced, perhaps annulled, the insular
condition and consequently the endemic evolutionary pressure
(Sarà, 1998; Petruso et al., in press). A rather different situation can
be observed in populations of the Early Holocene, when the Sicilian
Microtus (Terricola) reaches its maximum size, and in samples from
Table 2
PCA eingenvalues and variance. The eigenvalues and the percentage of variance of
the first 10 components of the PCA analysis are reported.
PC
Eigenvalue
% Variance
1
2
3
4
5
6
7
8
9
10
8.9559
5.35137
1.33966
1.10228
0.838771
0.565951
0.302736
0.235157
0.104046
0.0813695
47.136
28.165
7.0508
5.8015
4.4146
2.9787
1.5933
1.2377
0.54761
0.42826
Late Glacial and MIS3, where the difference with the coeval
peninsular samples is 7.88% (computed among the means of L of
each sample). Such a large size is in accordance with the general
trend of size increase predicted for insular small mammals by the
“island rule”. Even if this is not a true gigantism episode, the
increment in size is conspicuous and is likely to be the result of
isolation, perhaps due to the reduced interspecific competitive
pressure, as the small mammal community is poor and other
species of arvicolids are absent on the island. It should be noted,
however, that the MIS3 time slice includes also two smaller-sized
populations, from San Teodoro D (dated older than 33 ka) and, even
more so, from Contrada Pianetti, which are in the range of extant
populations of the Savi vole from Sicily and from the peninsula. A
climate effect on the size variation can be excluded for several
reasons. Firstly, extant samples from Tuscany are of the same size as
those from Sicily, even though climatic conditions are different.
Secondly, samples from MIS3 (younger levels of San Teodoro cave)
and samples from the early Holocene at Uzzo Cave (UZ mII, UZ nI),
have more or less the same size, even though climatic conditions
are expected to be much different. Furthermore, a direct correlation
between climate and body size has been excluded also by Piras et al.
(2010), based on the study of extant populations. On the other
Table 3
PCA factor loadings.
Component 1
L
A
A2
W
C
B
E
D
WT
L4
L5
AL
A2A
BW
CW
DW
EW
DE
L4L5
0.2905
2.40E-01
0.1044
0.2588
0.2757
2.48E 01
0.1614
0.2651
0.274
0.3117
0.3143
0.1395
0.167
0.2182
0.1651
0.2013
0.1336
0.2003
0.234
Component 2
0.172
0.2765
0.3831
0.2183
0.04708
0.1046
0.3271
0.2116
0.1295
0.09115
0.04492
0.3323
0.2864
0.1642
0.08125
0.3131
0.2487
0.3244
0.1283
Please cite this article in press as: Petruso, D., et al., Phylogeny and biogeography of fossil and extant Microtus (Terricola) (Mammalia, Rodentia)
of Sicily and the southern Italian peninsula based on current dentalmorphological data, Quaternary International (2011), doi:10.1016/
j.quaint.2011.03.013
8
D. Petruso et al. / Quaternary International xxx (2011) 1e12
hand, even in peninsular populations a very high variation in size
occurs between samples from different geographical locations (e.g.
Serratura Cave, Campania on the Tyrrhenian side, and Cavallo Cave
layer B, Southern Salento, at the Ionian Sea), confirming that
different ecological conditions may influence body size.
When considering the older samples (time slices 6, 7 and 8, that is
MIS 5 aed, MIS 5 e and MIS 6) the Sicilian samples from Isolidda 3
(TI3), here referred to MIS6 (?), are smaller than those of MIS 3 e
Early Holocene, and have roughly the same size of extant Sicilian and
peninsular Savi voles. When compared to samples of the same age,
they are close to or even smaller than the peninsular ones (Grotta
Grande di Scario). At Isolidda 3 the vole occurs after the disappearance of the endemic dormouse Leithia sp., but together with very
endemic small mammals such as Maltamys and Crocidura, forming
a poorly diversified assemblage that is suggestive of isolated
conditions. In such a context, the small “normal” size of the vole
might suggest the absence of endemism. Isolidda populations were
rather close in time to the dispersal event of this species on the
island, and therefore they had not yet achieved endemic features.
4.2. Morphological variation
The morphology of the anteroconid allows recognition of two
distinct groups among the extant samples. According to Petruso
(2003), they can be named as “savimorph” (from the Savi vole)
and “subterraneomorph” (from the common pine vole). Even if
almost all the Microtus (Terricola) considered here, except Microtus
(Terricola) lusitanicus, and Microtus (Terricola) subterraneus, are
referred to as M. (T.) ex gr. savii (i.e. they have a simplex M3, Chaline
and Graf, 1988), the anterior portion of the first lower molar shows
a remarkable degree of variation that indicates the morphological
distinction. In “subterraneomorph” populations, the anterior cap is
more constricted (lower B and D, as can be seen in the DE diagram of
Fig. 7) and the anteroconid is more elongated and articulated (higher
A, A2 and E in Figs. 4e6). Conversely, in the “savimorph” populations
the anterior cap is less constricted, and the anteroconid is shorter
and looks more squat and asymmetric. This means that samples
belonging to the first group plot closer to the M. (T.) subterraneus and
M. (T.) lusitanicus populations, while the other ones plot on the
opposite side. The populations from Tuscany (San Miniato e Smin e
and Cascina e Casc e, Figs. 4e6), and the one from Aspromonte
(Calabria), are part of the subterraneomorph group, while all the
Sicilian populations and the one from Meldendugno (Mel e Apulia,
Figs. 4e6), belong to the savimorph group. These observations,
although based on a small number of samples (n ¼ 7), support the
conclusions of Nappi et al. (2006) and Castiglia et al. (2008), who
found a differentiation among Northern-Central and Southern Italy
populations, more than the suggestion of Piras et al. (2010), who
denied such differences. On the other hand, as already reported by
Petruso (2003), the sample from Aspromonte is fairly distinct from
the savimorph M1s. It is close to the Central Italy samples as well as to
M.(T.) lusitanica and M.(T.) subterraneus and must be referred to the
species M.(T.) brachycercus. The occurrence of morphological
distinction of M.(T.) brachycercus respect to the other southern
Microtus (Terricola) populations apparently does not support the
conclusions of Nappi et al. (2005), while it has been recently
confirmed by Piras et al. (2010).
Considering the Early Holocene, Late Glacial and MIS3 time slices, the savimorph group is still visible, particularly in plots which
report the ACC elongations (AL and A2A, Figs. 4 and 5). The savimorphs are also identifiable considering the width of T6-T7 complex
(index EW, Fig. 6), with the exception of CavB, which displays, for
this feature only, subterraneomorph values. On the other hand,
considering the width of the anterior cap (index DE, Fig. 7), even
though the two morpho-groups are still distinguishable, in the
savimorph populations there is a trend towards enlargement of the
anterior cap in younger samples.
The Sicilian fossil populations from Oriente cave, Uzzo cave, Cala
Mancina, K22, Castello Shelter, San Teodoro cave as well as the extant
Sicilian samples can be clearly assigned to the savimorph group,
notwithstanding the aforementioned differences in size. The Salento
(Apulia) sample of Cavallo F (MIS 2) and the Campanian sample of
Serratura (Late Glacial) belong to this group as well, while sample
CavB (Late Glacial) is distinguished by a very wide T6eT7, a feature
that could denote a drift due to isolation or, perhaps, the phenotypic
effects of migrations from central to north Italian peninsula.
When considering also the older time slices, interpretation of
the results is less straightforward. The samples from Grotta Grande
di Scario are rather homogenous and show intermediate characters
between the two morpho-groups, fairly closer to the subterraneomorph group. The tooth looks quite elongated, but not as
much as the extant Central Italy ones. The younger sample from the
Serratura cave (SER) is close to Grotta Grande di Scario (Fig. 8), but it
has the smallest size (Fig. 3).
The three samples from the oldest Sicilian deposit of Isolidda 3
are clearly distinct from the younger Sicilian samples. They are
close to the extant subterraneomorph populations from Central
Italy and to Grotta Grande di Scario samples (pre- and post-Tyrrhenian in age). They definitely cannot be included in the savimorph group and apparently they are not even very suitable
forerunners for the later Sicilian Savi vole. The similarity with the
continental Scario voles coupled with the aforementioned
“normal” size may be further confirmation that the Isolidda 3 vole
is not much modified by endemic evolution. The vole from Contrada Pianetti (MIS3) is somewhat distinct from the other Sicilian
MIS3-Holocene populations, being smaller and morphologically
closer to the Grotta Grande di Scario southern peninsular samples,
thus suggesting a low degree of endemization.
The vole samples from Cavallo cave represent a remarkable case,
as some of them show peculiar characters that cannot be found in
any other sample. Firstly, there is a great difference among samples
of different age. While younger samples (CavF e MIS3 and CavB e
MIS2) are more similar to those coeval from the peninsula (see in AL,
A2A and DE diagrams of Figs. 4, 5 and 7 respectively), the oldest ones
(CavN e MIS5e and CavM e MIS5d-a) are noticeably different from
any other population in having a rather shorter ACCeAC2 and the
widest neck of AC2 (D, DE). Curcio et al. (2005) already noticed
a peculiarity in the Apulian populations, interpreted as linked to the
role of glacial refuge assumed by this area during cold climatic
oscillations. However, the most distinct morphology is shown by the
sample from the “warm” Eemian layer N from Cavallo cave deposit.
Cavallo cave is located at the extreme south of the Salento peninsula,
and therefore it is peripheral with respect to the species geographical range. The observed morphological divergence could be interpreted as the result of geographic isolation during the Eemian
interglacial, while the minor divergence observed in the younger
sample CavM is possibly the result of contacts with population from
the peninsula that migrated southwards in response to the cooler
climatic fluctuations of MIS 5. The Late Glacial vole from Cavallo cave
(CavB) is distinct from the other savimorphs for having a wide T6eT7
rhombus, a feature which can denote contacts with more northern
populations. On the other hand, the sample from the MIS5aed
Apulia site San Sidero 3 (SS3) has typical savimorph characters and is
indistinguishable from smaller-sized Sicilian samples and is also
very close to the extant populations of Savi vole from Apulia (Mel).
Microtus (Terricola) melitensis from the Maltese site of Ghar
Dalam (GD) is different from Microtus (Terricola) savii in having
some strong subterraneomorph features (like the high EW and the
low DE values, Figs. 6 and 7) coupled to a shorter ACC (AL and A2A
in Figs. 4 and 5) and a wide constriction between the T6 and T7 and
Please cite this article in press as: Petruso, D., et al., Phylogeny and biogeography of fossil and extant Microtus (Terricola) (Mammalia, Rodentia)
of Sicily and the southern Italian peninsula based on current dentalmorphological data, Quaternary International (2011), doi:10.1016/
j.quaint.2011.03.013
D. Petruso et al. / Quaternary International xxx (2011) 1e12
9
Fig. 9. Dispersals. This figure shows the distribution in time of the sites considered in the analysis and the location of the dispersal events. The MIS curve changes scale at 0.12 Ma.
Boxes and arrows indicate the time and direction of dispersals.
the pitymyan rhombuses (high B and BW). It has a fairly large size,
comparable with the bigger M1 from the Sicilian sites, indicative of
its endemic status, and is characterized by poorly differentiated
enamel walls of the dental triangles, a feature that is primitive
within genus Microtus (Martin, 1987; Petruso, 2003). Its M3 is of the
simplex type, as in the savii group (Petruso, 2003). In summary, the
Ghar Dhalam sample shares a mixture of characters, some primitive
and other more evolved. The most parsimonious hypothesis is that
the Maltese species derives from some primitive Sicilian populations belonging to the savii group e the Isolidda vole could be
a suitable ancestor e that underwent a genetic drift resulting from
long isolation in a small island such as Malta, and having the very
conspicuous size recognized in the analysis (Fig. 3). Unfortunately,
the age of this dispersal phase is unknown as no numerical dating
exists, but a relative chronological attribution to the Würmian,
provided by Storch (1974) is available for this taxon, thus placing
the Maltese taxon coeval with the Sicilian Savi vole, and opening
several phylogenetic and paleogeographic problems.
4.3. The role of climate
To attempt to find out which are the factors acting on the
variation of the tooth size and morphology, the role that climatic
and environmental fluctuations could have played in generating
such variation must be considered. As usual in the continental
record of mammals, the sample does not allow fine correlation of
the frequent and short climatic variations of the MiddleeLate
Pleistocene with the modifications in dental structure, as the
paleontological documentation is fragmentary in time (for example
there are no populations from MIS4) and space (samples are not
present for every area for every period) and the dating of the
deposits is not always very precise. Nevertheless, it is possible to
concentrate only on the major climatic events for checking
evidences that support or contradict the existence of a significant
climatic influence on the characters analyzed.
If the morphological variation of the anteroconid of Microtus
(Terricola) was correlated to environmental factors (change in
temperature and humidity for instance), there should be a high
variation of measurements and indexes in conformity with the
major climatic fluctuations of the last glacial cycle. However,
considering the AL, A2A and EW indexes (see Figs. 4e6) for the
Sicilian samples during MIS3, Late Glacial and the ancient Holocene
(a time span characterized by a dramatic climatic change), there is
no significant variation. Furthermore, even if the DE index displays
a strong difference between MIS3 and ancient Holocene (Fig. 7),
this difference is even stronger in living Sicilian populations, and
the variation is linear (a continuous increase) and so difficult to
associate with climatic variations (ancient Holocene had dramatically different climatic conditions than LGM, Late Glacial and
nowadays, with a strong increase in the mean temperature and
humidity). This supports the hypothesis of a morphological stasis in
extinct populations of Microtus (Terricola), thus being in agreement
with Maul et al. (1998) and Piras et al. (2009).
According to Masini et al. (2008), climate affects insular biodiversity mainly as a promoter of dispersals from the mainland, and
seems to have a minor impact on the evolution of the resident
endemic species, that, in strongly isolated systems, can last for
a long time with minor, or no morphological modifications. In the
samples analyzed and in the characters considered, the effects of
climate cannot be detected. This does not mean at all that
morphology is not susceptible to environmental changes, but its
influence cannot be read in the dataset, perhaps because other
factors more strongly affect the variables analyzed. In these
samples, the variation seems to be more correlated to phylogenetic
factors, that is to the history of each population and their ancestors,
at least on a finer scale.
It is possible to detect traces of the climate molding in similarities among populations which are well separated in time and
space. For example, the similarities between some extant and fossil
Apulian samples (Mel, SS3, CavM) with the Sicilian ones is rather
hard to explain by a very strict phyletic link. It could be better
explained as a homoplasy due to parallel evolution, likely as
a response to quite similar environmental conditions between
Sicily and the Salento peninsula.
Furthermore, it is possible to detect a northesouth trend, with
northern samples characterized by elongated teeth with
Please cite this article in press as: Petruso, D., et al., Phylogeny and biogeography of fossil and extant Microtus (Terricola) (Mammalia, Rodentia)
of Sicily and the southern Italian peninsula based on current dentalmorphological data, Quaternary International (2011), doi:10.1016/
j.quaint.2011.03.013
10
D. Petruso et al. / Quaternary International xxx (2011) 1e12
constricted anteroconid, and southern samples (with the exception
of the Calabrian population, that has been also assigned to
a different species), whose antericonid is shorter, compressed and
made up of highly confluent triangles. These characteristics are the
same pointed out by Nappi et al. (2006) and seem to be related to
the geography of the area. Thus, if at a local scale it is not possible to
correlate the variation of these features to environmental factors,
traces of this relation are recognizable at a regional scale.
4.4. Dispersals to Sicily
According to the data gathered and discussed above, M. (Terricola) voles underwent at least two different dispersal events from
Italian peninsula to Sicily (Fig. 9) during Middle and Late Pleistocene. This hypothesis is supported by the marked difference
occurring among the older Sicilian samples from Isolidda 3 and the
younger Würmian (MIS3) populations, which resemble recent and
fossil populations of Savi vole from the southern Italian peninsula.
Although the occurrence of a gap in the documentation between
Isolidda 3 and the younger samples requires caution, the hypothesis of a direct phyletic link between Isolidda 3 and the younger
voles would imply the development of an amount of homoplasies,
due to parallel evolution on the island and on the mainland, which
is rather improbable. Furthermore, some smaller-sized Würmian
populations such as those from Contrada Pianetti or San Teodoro
square D are suitable to be considered as new arrivals and ancestors
of the endemic Savi vole populations of the island. Eventually, the
dispersals of several taxa to the island during the Würmian render
the hypothesis of the evolution in isolated conditions since the lastbut-one glacial (MIS6) even more unlikely.
The following interpretation is presented. The ancestor of the
vole from Isolidda 3 first reached the island during an ancient low
stand phase of the sea level, probably during MIS6 (no numerical
dating at present). The absence in Isolidda 3 samples of southern
savimorph feature, their close similarity with the peninsular
populations from the site of Grotta Grande di Scario (GGSC
attributed to MIS6, Table 1) as well as their small size, support the
hypothesis of such an old dispersal for this vole, and that the age of
Isolidda should be rather close to that of the dispersal event. On
the other hand, the second dispersal from the peninsula involved
Microtus (Terricola) savii populations already characterized by
well-developed “southern” savimorph features. The dispersal
might have occurred during the low stand phase related to the
glacial peak of MIS4. Possibly during the following MIS3, characterized by alternating cool and relatively warmer fluctuations,
might have been a period of partial isolation for the Sicilian populations, allowing the voles to develop a large size. It is difficult to
assess if the climate deterioration of MIS2 and the following Late
Glacial, determining the probable connection with the mainland
that introduced the Epi-Paleolithic man onto the island, did affect
the evolution of the Sicilian voles by the introduction of continental populations or groups of individuals from the mainland.
Actually, if it was so, such contacts did not left traces on the vole’s
size, which are still large in the Late Glacial sites and particularly so
in the early Holocene.
5. Conclusions
The morphometric analysis of the first lower molars of Microtus
(Terricola) from Sicily, Malta, peninsular Italy, France and Spain
proved to be helpful in the attempt to reconstruct the phylogenetic
relationships between Sicilian Savi vole and the peninsular ones as
well as to detect the dispersal events from the mainland to the
island. The following points can be drawn.
1. The analysis allows identification, within the Savi vole latu
sensu, of two main morphotypes or morpho-groups: “subterraneomorh” e for the affinity with the common pine vole
morphology e and “savimorph” e from the southern Savi vole
populations.
2. Concerning the extant populations, there is a clear separation
between Sicilian Microtus (Terricola) savii and the central
peninsular populations (which show subterraneomoroph
features). These results are in agreement with Nappi et al.
(2006) and Castiglia et al. (2008), but dissent from Piras
et al. (2010). The Apulia population is close to Sicilian ones,
in agreement with the occurrence of a “southern” group of
Savi voles as affirmed by Nappi et al. (2006). The small size of
the extant Savi vole of the island is likely due to the anthropogenic impact that reduces or cancels the effects of
geographic isolation. As a by-product, although based on few
samples, the morphological distinction of the Calabrian vole
referred to M. (T.) brachycercus, already noticed by Petruso
(2003), is supported by the analysis, in agreement with Piras
et al. (2010).
3. Since the MIS3 till the early Holocene, the morphology of the
fossil Sicilian Savi vole is close to the Southern Italy populations. Several Sicilian populations, however, show markedly
larger size than continental ones, while a few others are of the
same size as the continental voles. Larger size is interpreted as
an effect of geographic isolation. This would suggest that voles
of the savii group during the Würmian glaciation dispersed
from the mainland, and then became isolated, developing
endemic features during the late part of the glaciation (Fig. 9).
The possibility that some exchanges with the mainland
repeatedly occurred during the cooler phases cannot be ruled
out. This reconstruction is apparently in contrast with Castiglia
et al. (2008), who suggested a species status for the Sicilian vole
based on the divergence indicated by molecular data. Isolation
and drift may have played an important role in determine such
a high divergence.
4. Pre-Tyrrhenian Sicilian populations from the site Isolidda 3,
referable to the last-but-one glaciation (MIS6), are distinctly
different from post-MIS4 populations, and are closer to coeval
population from the Tyrrhenian side of the peninsula, thus
suggesting that they originate from an older dispersal event
that took place during the sea - level low stand of MIS6 (Fig. 9).
5. The M. (T.) melitensis sample from Ghar Dalam (Malta) is
a mosaic of subterraneomorph and savimorph features, and
occupies an isolated position. The result of the comparisons, as
well as the primitive enamel pattern of the M1, apparently rules
out its derivation from a Late Pleistocene Savi vole dispersed
from Sicily, and support the hypothesis of an older dispersal.
6. Climatic changes do not seem to have a direct effect on size and
morphology of the insular voles, while dispersals from the
mainland, likely stimulated by climatic driven environmental
changes and facilitated by the eustatic effects of climatic
changes, are responsible for species substitution in the island.
In summary, the work provides a large amount of original
information regarding the Sicilian voles, and a new piece of information to the reconstruction of the evolutionary history of Microtus
(Terricola) in the Southern Italian regions. Further studies,
regarding both extant and fossil populations could help in unraveling the problems that are still open.
Acknowledgements
The present work results from the following individual contributions: Daria Petruso, most of the Sicilian samples and Ghar
Please cite this article in press as: Petruso, D., et al., Phylogeny and biogeography of fossil and extant Microtus (Terricola) (Mammalia, Rodentia)
of Sicily and the southern Italian peninsula based on current dentalmorphological data, Quaternary International (2011), doi:10.1016/
j.quaint.2011.03.013
D. Petruso et al. / Quaternary International xxx (2011) 1e12
Dalam; Elisa Locatelli, Isolidda 3, Cala Mancina cave, Oriente cave;
Giovanni Surdi, Grotta Grande di Scario cave, Serratura cave, extant
samples from Cascina and S. Miniato; Chiara Dalla Valle, Cavallo
cave; Federico Masini and Benedetto Sala coordinated the work.
The paper has been elaborated conjunctly by the research teams of
Palermo and Ferrara Universities. The work is supported by Italian
MIUR (PRIN 2008, 2008RTCZJH), by the Ferrara University (FAR
funding 2007) and by the Palermo University (Athenaeum Grants e
FAR-year 2008). Elisa Locatelli was supported by the PhD program
“Scienze and Tecnologie per l’Archeologia e i Beni culturali” at
Ferrara University; Giovanni Surdi is supported by PhD fellowship
program “I micromammiferi tardo quaternari della Sicilia e del Sud
della penisola italiana”, Palermo University.
The authors thank Prof. Laura Bonfiglio of the University of
Messina, for the material of Grotta San Teodoro; Prof. Annamaria
Ronchitelli and Prof. Paolo Boscato of the Department of Environmental Sciences “G. Sarfatti”, Siena University, for the material from
Grotta Grande di Scario; Prof. Fabio Martini of the Department of
Antiquity Sciences, Florence University, for the material from Isolidda 3, Cala Mancina cave, Oriente cave and Cavallo cave; Prof.
Maurizio Sarà for the extant Sicilian samples of Borgo Lupo, Mazzarino, Gela, and for the sample from Aspromonte.
Supplementary data
Supplementary data associated with this article can be found, in
the online version, at doi:10.1016/j.quaint.2011.03.013.
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