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First upper molar and mandible shape of wood mice (Apodemus sylvaticus) from northern Germany: ageing, habitat and insularity
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Original investigation
First upper molar and mandible shape of wood mice (Apodemus sylvaticus) from northern Germany: ageing, habitat and insularity By Sabrina Renaud UMR 5125 CNRS ‘‘Pale´oenvironnements et Pale´obiosphe`re’’, Universite´ Claude Bernard, Lyon, France Receipt of Ms. 21.6.2004 Acceptance of Ms. 28.10.2004
Abstract The patterns of shape variation of the first upper molar and mandible have been investigated within and among wood mice (Apodemus sylvaticus) populations from northern Germany. Some factors such as sex and age of the animals could be a source of within-group morphological variability interfering with among-groups patterns of differentiation. The relative importance of both sources of shape variation was investigated, in order to evaluate the robustness of patterns of fine-scale geographic differentiation. The increasing age of the animals, estimated by wear stages of the upper tooth row, caused significant variations in size and shape of the molars due to progressive abrasion of the cusps. It also involved shape changes of the mandible due to bone remodelling. However, these intrapopulational effects are of limited importance compared to geographic differentiation. Gene flow among populations should be favoured across mainland populations but lowered between mainland and islands, and to a lesser extent among close islands. Shape differences in molars are in agreement with this expected pattern of gene flow. Patterns of mandible differentiation rather match local variations in habitats. At this fine geographic scale, molar shape would vary according to the amount of genetic exchange among populations whereas mandible shape might be under local selective and/or functional constraints. r 2005 Elsevier GmbH. All rights reserved. Keywords: Murinae, evolution, island biogeography, morphometrics
Introduction Size and shape variability of small mammals like rodents has been described in regard to different factors and based on various characters. Insularity is a well-known context of morphological divergence (e.g., Berry, 1973). A growing body of evidences also points to the importance of biogeographic gradients in shaping morphological variability (Fadda and Corti 2001; Renaud and
Michaux 2003). Such shape variations have been described on skull (Fadda and Corti 2001), mandible (Duarte et al. 2000; Renaud and Millien 2001) or teeth (Renaud 1999). However, different characters are seldom analysed in a same study, although they might provide contrasting results. Additionally, some sources of populational variability, such as sex and age of the animals, might
1616-5047/$ - see front matter r 2005 Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2004.10.004 Mamm. biol. 70 (2005) 3 157–170
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Classes were established based on the four classes recognised by Adamczewska–Andrzejewska (1967). The first class included specimens with an erupted third molar (M3/) without traces of wear. Animals belonging to this class were very seldom found. Hence, WS1 was pooled with WS2 corresponding to individuals with slightly worn cusps. Stage 3 includes specimens with surfaces of all cusps joined on the third upper molar (M3/), and a close ring of six cusps on M2/ and M1/. On the M1/ the cusps of the first transverse row are connected with each other. Stage 4 corresponds to individuals with a very worn chewing surface, the enamel loops circumscribing the base of the cusps. A further class (WS5) was added according to Steiner (1967) with all molars worn flat, only the M1/ possibly showing some rest of cusps. In order to evaluate the variations in frequency of the different WS along the year, animals were grouped according to the season of trapping (Winter: December–February; Spring: March–May; Summer: June–August; Autumn: September–November).
interfere with among-group patterns of differentiation, especially when considering finescale patterns. The relative importance of the different sources of variations should be compared, in order to assess the robustness of biogeographic patterns observed from wild-caught populations. The aim of this study is to address these questions on populations of European wood mice (Apodemus sylvaticus). Several mainland and insular populations from northern Germany were selected to investigate the possible sources of fine-scale morphological variations.
Material and methods Material The study is based on specimens of wood mice (A. sylvaticus) from the collection of the Institut fu¨r Haustierkunde (Kiel, Germany). The animals were trapped between 1957 and 1974 in different localities from northern Germany (Fig. 1). Mainland localities were grouped into Holstein populations (around Kiel) and Nordfriesland populations (around Bredstedt). Three North Friesian islands were also sampled: Sylt, Fo¨hr and Amrum. The mandible was measured of 213 and the first upper molar of 170 animals (Table 1). Only mature specimens with the third molar erupted were considered. Wear stage (WS) was evaluated on the upper molar row of 169 animals. -10°
A
-5°
0°
5°
10°
15°
20°
25°
The outline describes the overall shape of morphological features. In the case of the molars, the relative position and swelling of the cusps strongly influence the outline. In the case of the mandible, the outline provides a description of the development and orientation of the processes involved in the insertion of the mastication muscles, as well as of the alveolar region bearing the cheek teeth and
8°
9°
11°
55° 0'
22
SY 25
23
24
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B Sylt
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Outline analysis of the first upper molars and the mandibles
AM
647 2 58 31
Amrum
FOE
21 20
Flensburg Leck
NF 19
Bredstedt
54° 30'
9
45°
11 12 14 10 15 13
Kiel
40°
HO
18
Preetz
Plön
16
54° 0' 17
35°
Rickling
Fig. 1. Localisation of the sampling localities of the wood mice (Apodemus sylvaticus) considered in the present study. (A) Localisation on a map of Europe of the studied area (B). Dotted areas represent the main geographic groups (cf. Table 1).
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Table 1. Trapping localities, with numbering and grouping. Number of measured mandibles (Md) per trapping locality: male (M)/female (F), season of trapping (Sp: spring; Su: summer; Fa: fall; Wi: winter). Number of measured first upper molar (UM1). Gp. AM
Amrum
FO¨E
Fo¨hr
HO
Holstein
Abbr.
#
Locality
Md
M
F
Sp
Su
Au
Wi
UM1
NORDD
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25
Nebel Norddorf Su¨ddorf Alkersum Boldixum Borgsum Oevenum Wyk Hemmelmark Kiel Kaltenhof Rathmannsdorf Fargau Scho¨nberg Scho¨nkirchen Eutin Rickling Preetz Bredstedt Leck Su¨derlu¨gum Kampen Morsum Rantum Westerland
1 13 8 4 6 22 4 15 3 7 3 7 4 6 1 1 2 58 7 1 8 4 18 7 3
1 7 4 — 5 5 2 7 2 4 2 4 2 3 1 1 — 23 4 — 2 2 4 1 —
— 6 4 4 1 16 2 8 1 3 1 3 2 3 — — 2 34 3 1 5 2 14 6 3
1 3 — 2 2 2 3 13 3 — — 2 1 — — — — 16 7 1 8 2 4 3 1
— — — — — 6 — 1 — — — — — — — — — 14 — — — — — — —
— 10 8 2 4 13 1 1 — 7 — 3 — 1 1 — 2 28 — — — 2 14 4 2
— — — — — — — — — — 3 2 3 5 — 1 — — — — — — — — —
1 9 8 2 5 13 3 8 3 6 3 7 3 4 1 1 2 54 4 1 6 4 17 4 1
SUEDD ALK BOLDX BORGS OEV WYK HEM KIEL RATH PLOEN
NF
Nordfriesland
SY
Sylt
PREETZ BRED SUEDLG KAMP MORS RANT
the incisor. In both cases, the outline analysis appears to be appropriate to describe subtle morphological changes along geographic gradients (Renaud 1999; Renaud and Michaux 2003). The outline of the first upper molar corresponds to the two-dimensional projection of the tooth viewed from the occlusal surface. The starting point of the outline was defined at the maximum of curvature on the anterior part of the tooth. The outline of the mandible corresponds to the projection of the hemi-mandible put flat on its side with the lingual side down. As the incisor can be free moving and the molars missing, only the outline of the mandibular bone is considered. The starting point was defined at the meeting point of the incisor and the bone on the upper edge of the mandible. For both the mandible and the M1/ outline, 64 points at equally spaced intervals along the outline were sampled. A radial Fourier transform (RFT) was then applied (Renaud and Michaux 2003). From the x, y-coordinates of the points, 64 radii corresponding to the distance of each point to the centre of gravity of the outline were calculated. Using the RFT, the outline is expressed as a finite
sum of trigonometric functions of decreasing wavelength, the harmonics, approximating the function of the radius varying with the cumulative distance along the outline. Each harmonic is weighted by two Fourier coefficients, An and Bn. The zeroth harmonic A0 is proportional to the size of each outline and can be used to standardise all the Fourier coefficients, in order to retain shape information only. In order to determine the rank of the last harmonic that has to be retained for a satisfactory description of the outline, two criteria can be considered: measurement error, estimated by repeated measurement, and information content (Crampton 1995). Studies on similar rodents suggested that both criteria were congruent. They indicated that considering the first nine harmonics for the M1/ (Renaud et al. 1999) and the first seven harmonics for the mandible (Renaud and Michaux 2003) offered a good compromise between measurement error, information content, and number of variables to be considered. From any set of Fourier coefficients, an outline can be reconstructed using an inverse method,
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providing a visualisation of the shape differences between sets of Fourier coefficients. RFT provides moderately accurate reconstructions because xycoordinates are re-calculated from the set of radii provided by the inverse Fourier transform (Renaud and Michaux 2003). They can nevertheless be useful to visualise the parts of the structure affected by shape changes. Accurate reconstructions of average shapes can be obtained using the elliptic Fourier transform (Kuhl and Giardina 1982; Ferson et al. 1985) as a further support for visual interpretation of shape changes.
Statistical analyses Size of the mandible or the M1/ are estimated by an univariate parameter, i.e. the zeroth harmonic amplitude A0. Differences in size according to various factors have been tested using analyses of variance (ANOVA). Size of the mandible and the M1/ were compared to the size of the animal, estimated by the body length, using a model of linear regression. The shape of each outline was described by a set of Fourier coefficients: 18 for each M1/ (2 coefficients per 9 harmonics) and 14 for each mandible (2 coefficients per 7 harmonics). These sets of Fourier coefficients had to be analysed using multivariate statistics. The existence of differences according to various factors has been tested using multivariate analyses of variance (MANOVA, test considered: Wilks’ Lambda). To display the morphological variability on a few synthetic shape axes, principal component analyses (PCA) were performed on Fourier coefficients of the mandible and the first upper molars separately. The PCA were normed, i.e. performed on the correlation coefficient matrix of the Fourier coefficients, to give the same weight to all the variables and not enhance the role of the first harmonics because of their higher numeric values. To enhance the readability of the graphs, all individuals were not plotted on the first principal axes but rather average values according to the WS and/or geographic groups. Reconstruction of the mean outline for some samples was used to visualise the shape variability. In order to compare the patterns observed on the first upper molar and the mandible, matrices of distance were constructed. The average values of Fourier coefficients per main geographic groups (HO, NF, PRE, AM, FOE, SY) or per local geographic groups (Loc. Gp. in Table 1) were calculated and distances among them estimated using Euclidean distances on the Fourier coefficients of the mandible (seven harmonics) and the first upper molar (nine harmonics). The matrices of distances of both characters were then compared using a Mantel t-test.
Results Morphological variability within a mainland population The existence of size or shape differences of the first upper molars and the mandibles due to intrapopulational factors, i.e. sex or age of the individuals, were first investigated on the largest population (Preetz, Holstein). This population also presents the advantage to minimise the importance of the interannual variability since it is almost exclusively composed of animals trapped in 1960. Sex was found to have no influence on size or shape of the M1/ nor of the mandible (Table 2). Differently, age (estimated by WS of the teeth), and to a lesser extent season, were found to have a significant impact on size and shape. The age structure of the wood mice samples varies according to the season of trapping (Fig. 2A). Whereas summer and autumn populations are composed of young animals, an important proportion of older animals is observed in spring. The seasonal effect could therefore be attributed to different compositions in WSs. The shape variability of the M1/ in Preetz (Fig. 2B) clearly shows the importance of the WS. The first principal axis (PC1, 17.3% of the total variance) corresponds to a random variability within the population whereas along PC2 (16.7%) teeth of young animals (WS1-3) are opposed to older animals (WS45). The oldest individuals (WS5) are the most Table 2. Morphological variability of the wood mouse population of Preetz (Holstein). UM1: first upper molar; Md: mandible. Size: ANOVA probability on A0. Shape: MANOVA on the Fourier coefficients of the first nine (UM1) and seven (Md) harmonics. Probability of the Wilk’s Lambda test is given. In bold significant probabilities (Po0.05). Factors
Wear Sex Season
UM1
Md
Size
Shape
Size
Shape
P
P
P
P
0.007 0.983 0.037
0.0007 0.6653 0.0025
0.181 0.360 0.309
0.0048 0.3534 0.0073
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A
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B M1/ PC2 (16.7%)
1 0
WEAR -1
1 2 3 4 5
-2 -3 -4 -2
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0
1
2
3
M1/ PC1 (17.3%) 7.0
C M1/Size (A0)
6.5
6.0
SEASON 5.5
5.0
Autumn Summer Spring 1
2
3
4
5
WEAR CLASS
Fig. 2. (A) Frequency distribution of the wear classes (based on the upper teeth) in Holstein wood mice from Preetz, as a function and the season of trapping. (B) Shape variability of the first upper molar, estimated by the first principal plane of a PCA on the Fourier coefficients of the molar outline. Different symbols correspond to the wear classes. Outlines correspond to the average shape of the wear classes. (C) Size variability of the first upper molar, estimated by A0, as a function of the wear classes and season of trapping.
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extreme along this axis. The shape change due to progressive wear of the tooth is mostly the abrasion of the posterior middle cusp (t8). Young individuals have therefore more slender molars with a sharp back part whereas older individuals display a flattened back part leading to a more rounded outline. The progressive wear of the tooth also causes a reduction of the occlusal surface and hence, a decrease in A0 (Fig. 2C; Table 2). The size of the M1/ is not correlated with the body length of the animal (R ¼ 0:170; P ¼ 0:269). The ageing of the animals had a different impact on the mandible. Size variations as a function of WS were not significant (Table 2). However, WS1-3 are more variable in size and include animals of smaller size than WS4 and 5, composed only of large specimens (Fig. 3A). This is attributable to the presence of young animals still growing in the first WSs. This relationship with continuous growth of the mandible is confirmed by a significant relationship between mandible size and body length (R ¼ 0:792; Po0:001). The influence of age on the shape of the mandible is less obvious than on the M1/ (Fig. 3B,C). The most obvious pattern is the position of the animals of WS5 at the edge of the total variability. The shape changes with increasing WS are very tenuous and involve a more curved region of insertion of the cheek teeth (alveolar region). The articular condyle is slightly higher. The coronoid process is relatively reduced. Variations among wood mice populations from mainland and North Friesian islands The composition of the populations of wood mice, regarding the season of trapping and the WSs, is very different (Fig. 4). The populations of Amrum and Holstein are dominated by young animals (WS1-2 and 3) whereas the contribution of older animals is more important in Nordfriesland, Fo¨hr and Sylt. Considering the morphological variations observed at Preetz according to the ageing of the animals, the influence of WSs on the structure of the morphological differentiation among populations has to be evaluated. Since no sexual dimorphism was detected for the M1/ or the mandible at
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Md Size (A0)
SEASON Autumn Summer Spring
35
coron.p. condyl.p.
30
alveolar r.
A
25 2
3
4
2 angul.p. 2
3
2
4
2
5
5
Wear Class 3
Md PC2 (16.5%)
2 1
C
0 -1
WS
-2 -3 -3
B -2
-1
0
1
2
3
1-2 3 4 5
Md PC1 (42.8%)
Fig. 3. Morphological variability of the mandible in the wood mice from Preetz. (A) Size, estimated by A0, as a function of the wear classes and season of trapping. (B) Shape, estimated by the first principal plane of a PCA on the Fourier coefficients of the mandible. Different symbols correspond to the wear classes. Outlines correspond to the average shape of the wear classes. (C) Reconstructed outlines for each WS, using the Elliptic Fourier Transform (EFT, 16 harmonics). The dotted shape corresponds to WS1-2, compared to following WSs. coron.p.: coronoid process; condyl.p.: condylar process; angul.p.: angular process; alveolar r.: alveolar region.
Preetz, animals of both sexes were pooled together in the subsequent analyses. Both WSs and the main geographic groups (being HO, NF, Preetz, Amrum, Fo¨hr and Sylt, see Table 1) have a significant influence on molar and mandible morphology (Table 3). The size of the M1/ is not affected by the geographic origin but by the age of the individuals (Table 3). In agreement with the observations at Preetz, older molars tend to be smaller than younger ones (Fig. 5A). Patterns of M1/ shape differentiation are influenced both by the ageing of the animals and their geographic origin (Table 3). As in Preetz, teeth belonging to WS4-5 are characterised by outlying morphologies at the
periphery of the total range of variation, on PC1 (19.3% of the total variance) for WS5teeth from Nordfriesland, Sylt and Amrum, along PC2 (13.4%) for Nordfriesland and Preetz, and along PC3 (10.7%) for Holstein, Nordfriesland, Amrum and Sylt. If this oldest WS is discarded, some geographic structure can be recognised among younger teeth (Fig. 5B,C). The four WS-samples from Fo¨hr are clustered along the three PCs and opposed along PC1 to mainland samples from Holstein (HO and Preetz). Teeth from Amrum are only segregated along PC2, whereas molars from Sylt fall consistently close to the Holstein samples. Teeth from Nordfriesland (WS3-5), although from a
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Amrum Number of observations
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WEAR CLASS
Föhr
10 12 8 6
8
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3
4
5
0
2
3
4
5
15
Sylt
SEASON Spring Summer Autumn Wint er ?
10
5
0
2
3
4
5
Fig. 4. Frequency distribution of the wear classes (based on the upper teeth) in wood mice from northern Germany, as a function of the season of trapping. Mainland: Holstein and Nordfriesland; islands: Amrum, Fo¨hr, and Sylt.
mainland origin, are segregated from Holstein M1/ along PC2. The morphological differentiation of the mandible involves both, age and geographic origin for both size and shape (Table 3). In
agreement with the results at Preetz, older animals (WS4-5) tend to have larger mandibles than younger ones (Fig. 5D). Superimposed to this intrapopulational variability due to continuous growth, some geographic
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Table 3. Morphological variability of wood mouse population from northern Germany. UM1: first upper molar; Md: mandible. Size: ANOVA probability on A0. Shape: MANOVA on the Fourier coefficients of the first nine (UM1) and seven (Md) harmonics. Probability of the Wilks’ Lambda test is given. In bold significant probabilities (Po0.05). Gp are geographic groups. Factors
Wear Gp
UM1
Md
Size
Shape
Size
Shape
P
P
P
P
0.011 0.241
0.000 0.000
0.000 0.000
0.0000 0.0000
trends may be recognised. The mandibles from Preetz are on average the smallest whereas the insular population from Fo¨hr and the mainland population from Nordfriesland display the largest mandible size. Regarding shape, mandibles from the oldest WSs (WS5) tend to diverge from the youngest morphologies (Fig. 5E,F). The WS5samples from Amrum and Holstein diverges at one side of the first principal plane defined by PC1 (35.6%) and PC2 (19.0%), whereas the WS5 from Nordfriesland diverge at the other side (Fig. 5E). The WS5 from Fo¨hr is isolated along PC3 (15.7%). Fo¨hr and Sylt mandibles from WS1-4 are clustered together and are slightly separated from the Holstein mainland samples on the first principal plane. The Amrum samples segregate along PC3. Nordfriesland mandibles diverge along PC2. Comparison of the geographic differentiation of the molar and mandible shape WS clearly interferes with the geographic patterns of differentiation. However, intermediate WSs are dominant within the trapped animals (Fig. 4) and this influence should be buffered by considering the whole population at one location. The robustness of the geographic pattern of differentiation was investigated by splitting the main geographic groups into smallest entities corresponding to more restricted geographic areas (Loc. Gp. in Table 1). Moreover, the geographic patterns of differentiation observed on different char-
acters of the same animals (first upper molar or mandible) were compared. Size of the M1/ and the mandible are only weakly correlated (R ¼ 0:518; P ¼ 0:033) and few consistent patterns emerge from the comparison (Fig. 6A). The different samples from Fo¨hr tend to be among the largest, for the molars as well as for the mandibles. A matrix comparison of the distances among geographic groups based on the M1/ or the mandible show a weak relationship between both patterns. Considering only the main geographic groups (HO, NF, PRE, AM, FOE, SY) provides a non-significant relationship between M1/ and mandible (Mantel ttest: R ¼ 0:522; t ¼ 1:551; P ¼ 0:060) although close to the significance threshold (P ¼ 0:050). Comparing the distances among the 17 local groups provides a significant result (Mantel t-test: R ¼ 0:323; t ¼ 2:425; P ¼ 0:008) but the correlation plot is fuzzy. The patterns of differentiation among local groups provide some clear indications of geographic structure for the M1/ as well as the mandible. Regarding the M1/, Fo¨hr populations are segregated from the mainland populations along both, PC1 and PC2 (Fig. 6B). This corresponds to a very subtle morphological difference, with labial (lefthand on the outline) anterior (t3) and posterior (t9) cusps slightly more pronounced compared to the central populations from Holstein exemplified by Preetz. On the other side of the first principal plane the Nordfriesland populations segregate. Their molars display a pronounced labial posterior (t9) cusp but less developed lingual (t1, t4) cusps. This divergence emerges again along PC3 that also displays a divergence of the Amrum molars (Fig. 6C). They are characterised by both, pronounced labial posterior (t9) and lingual (t1, t4) cusps. Sylt molars fall close to the mainland samples from Holstein. Mandible shape provides both, some similar features and marked discrepancies compared to the first upper molar. The Nordfriesland populations are segregated along PC1 and secondarily along PC2 (Fig. 6D). This corresponds mainly to a wider coronoid process (Fig. 6D,F). Holstein populations are clustered together and all islands populations show some divergence compared to this
ARTICLE IN PRESS First upper molar and mandible shape of wood mice northern Germany
Mandibles
6.1
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6.0
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Md Size (A0)
M1/ Size (A0)
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36 35
WS
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NI W1-2 W3 W4 W5
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A 5.5
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Geographic Groups
D OH PRE NF AM FOE SY Geographic Groups
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PRE FOE
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0.0
0.5
1.0
1.5
M1/ PC1 (19.3%)
-2 -2
F -1
0
1
2
Md PC2 (19.0%)
Fig. 5. Differentiation of the first upper molars and mandibles among wood mice from northern Germany. (A) Upper molar size as a function of the geographic groups and wear classes. (B, C) Shape differentiation on the first three principal axes of a PCA on the Fourier coefficients of the upper molar outline. (D) Mandible size as a function of the geographic groups and wear classes. (E, F) Shape differentiation on the first three principal axes of a PCA on the Fourier coefficients of the mandible. Symbols correspond to average values per geographic groups and wear classes.
basic pattern (Fig. 6D,E). Along PC1 all insular populations are shifted towards positive values showing that they share some common characteristics. Fo¨hr mandibles are
also isolated along PC2. They display a slightly wider coronoid process and a reduced angular process (Fig. 6F). Amrum mandibles tend to have a lower articular process. All
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47 BOLDX
46
OEV KAMP
MD Size
45
SUEDLG
HEM WYK
44 NORDD
MORS BORG
43 ALK
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RATH
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KIEL RANT
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D
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WYK ALK
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-0.5
RANT KIEL
RATH
NORDD
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Amr -1.0 -1.0
-0.5
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-0.5
MD PC1
0.0
0.5
1.0
MD PC1
F
HO
HO
NF
HO
AM
HO
FOE
HO
SY
Fig. 6. Geographic differentiation of the first upper molar and the mandible among wood mouse populations from northern Germany. (A) Upper molar size vs. mandible size. (B, C) Geographic differentiation of the first upper molar. (D, E) Geographic differentiation of the mandible. Principal axes are the same as on Fig. 4 (M1/) and 5 (MD) but symbols correspond to average values per geographic group. Outlines correspond to the average shape of the different geographic groups. (F) Reconstructed outline of the mandible for each geographic group, using the Elliptic Fourier Transform (EFT, 16 harmonics). The dotted shape corresponds to Holstein average mandible, compared to other groups.
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insular mandibles tend to share a more curved alveolar region and a reduced angular process (Fig. 6F).
Discussion Factors of intrapopulational morphological variations Different factors can cause morphological differences within a population. Wood mice from the locality of Preetz (Germany) show no evidence of sexual dimorphism on size or shape of the first upper molar or of the mandible. Sexual dimorphism is a common feature in groups such as carnivores (Dayan et al. 1990), and has been described for body size of rodents, including Apodemus (Adamczewska 1959). However, the present result is in agreement with previous observations on molars (Renaud 1999) or mandibles (Cardini and Tongiorgi 2003) of rodents. It allows mixing specimens of both sexes in morphometric analyses. On the other hand, the age of the animal appears to influence the shape of both, molars and mandibles. In the case of the first upper molar the progressive wear of the tooth is responsible for the shape change of the oldest WSs, also causing a decrease in the size of the molar. Once the molars are erupted, they only vary with wear and show no relationship with the body size of the animal. On the contrary, the shape change observed on the mandible exemplifies the bone growth and remodelling occurring throughout the adult life of an animal, leading to a covariation of mandible and body size. Similar effects have been described in marmots (Cardini and Tongiorgi 2003). An important growth and allometric shape changes of the mandible are observed along the 4 years of life of the animals, but this study included the phase of juvenile growth. Differently, the amount of growth documented in the present morphometric analysis was limited by selecting only specimens with erupted third molars, hence considered as adults. The shape changes observed are likely mostly related to bone remodelling which occurs due to an interaction between muscular functioning and the mandible growth
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(Lightfoot and German 1998; Bresin et al. 1999). Such a plastic shape variation can cause subtle differences between populations, since the composition of the population according to age varies with the season and possibly with the local environment. A changing age structure through the year is known for long in wood mice populations (e.g., Steiner 1967; Frynta 1993; Frynta and Vohralı´ k 1994). Mostly young animals survive the winter period, leading in late spring and summer to a mixed population of old, over-wintered animals and young adults born at the beginning of the reproductive period (Steiner 1967). Different seasons of trapping are thus likely to lead to different age structure. Furthermore, the structure of the population may vary with the quality of the environment, life expectancy being reduced in atypical environments such as marshes compared to woodlands (Canova et al. 1994). On the other hand, life expectancy has been suggested to be extended on islands (Cheylan 1986). Such hypotheses are not supported by this data set where the main factor causing a difference in age structure seems to be the season of trapping.
Gene flow and habitat shaping molars and mandibles A major interest of the model constituted by the North Friesian islands is that the timing of the insular differentiation can be dated with precision, since isolation happened during historical times. From an initial mainland zone, two large storms in 1362 and 1634 AD isolated the North Friesian islands. Isolation is therefore younger than 750 years, constituting a very short time interval for evolutionary processes in natural populations. The amount of isolation varies for the different islands considered. Since 1927 Sylt is linked to the mainland by a dyke used by railway. Water depth is nowhere important between the islands and at low tide it is possible to walk from Fo¨hr to Amrum. The most isolated island is supposed to be Amrum, at the western border of the mudflats of the Wadden Sea. Accordingly, the
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wood mice from Amrum have been found to be the most divergent from mainland ones for the patterns of molar roots (Robel 1971) and cranial morphology (Murbach 1979). Included into a large-scale geographic pattern covering Western Europe, the Amrum population was also found to be divergent regarding the shape of the mandible (Renaud and Michaux 2003). Focusing the study on the region of northern Germany and comparing both molar and mandible shape provide contrasting results. The pattern of geographic differentiation based on the first upper molar indicates a morphological relatedness of the Holstein and Nordfriesland populations. Both are located on the mainland making gene flow likely. Populations from Sylt also appear to be morphologically close to the mainland populations, in agreement with observations on the skull (Murbach 1979). Sylt is connected with the mainland by a dyke, that should favour gene flow with the mainland populations. Hence, the more pronounced divergence of Fo¨hr and Amrum can be explained by the geographic context. The shared morphological features between the populations of the three islands can also be explained by the proximity of islands. The pattern observed on the mandible is quite different. In agreement with their geographic nearness, the Holstein populations are clustered together, but the set of mainland samples from Nordfriesland appears as very divergent. Mandibles from the different islands diverge from the mainland ones, to a various extent but in a similar way. To the contrary of the molar shape, this pattern does not match the expected pattern of gene flow. However, the differentiation of the mandible may match the local environmental conditions. Mixed forest favourable to the wood mouse are frequent in Holstein, whereas Nordfriesland corresponds to low-lying areas with large extent of marshes and meadows drained by channels, with little coniferous forests. The environment on the three North Friesian islands should be comparable, with wood mice inhabiting marsh, dunes and some pine plantations, especially on Amrum (Murbach 1979).
Neither the molar nor the mandible displays a clear pattern regarding size, although this character is known to vary on islands in the wood mouse (Angerbjo¨rn 1986). However, the importance of the size increase depends on the predation pressure and the distance to the mainland (Michaux et al. 2002b). The North Friesian islands are close to the mainland and the predator fauna is not impoverished, explaining the absence of any clear ‘‘insular syndrome’’ (Foster 1964) on these islands. Timing and processes differentiation The present study shows that morphological differentiation can evolve rapidly. The differences between mainland and North Friesian islands populations occurred in less than 750 years. Even more striking, differences in mandible shape occur between animals of different ages, due to bone remodelling. Within the European wood mouse (A. sylvaticus) a latitudinal gradient in mandible shape has recently been described (Renaud and Michaux 2003). Based on genetic evidences, the wood mouse recolonised Europe after the last glaciation from an Iberic refuge zone (Michaux et al. 2002a). Hence, the formation of the latitudinal gradient has been rapid, in the order of 16,000 years. Epigenetic factors such as bone remodelling could participate to such rapid morphological differentiation, since the gradient observed on the mandible has been interpreted as due to change in diet from the north to the south of western Europe (Renaud and Michaux 2003). Such plastic variations are not expected in a feature like the molar, which does not grow after its eruption and can only be modified by wear during the life of the animal. Different patterns of variations are therefore expected depending on the character considered, since different genes are involved in different morphological modules (Atchley et al. 1992) and epigenetic late effects during the life of the animals will differ. These results show that a study based on a limited geographic range can provide useful insight into fine-scale processes involved in the morphological differentiation. The
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overwhelming importance of environmental factors over larger geographic range may obscure discrepancies among characters that are hints for different determinisms and/or selective pressure.
Acknowledgements This study would not have been possible without Prof. Dr. Dieter Kruska who pro-
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vided access to the collection of the Institut fu¨r Haustierkunde (Kiel, Germany). The technical help of Renate Lu¨cht during measurements at the institute was greatly appreciated. This manuscript benefited from the comments of Thomas Cucchi and Ingo Klaucke, who also corrected the German abstract. This study was supported by the GDR 2474 CNRS and the Rhoˆne-Alpes region (Emergence program).
Zusammenfassung Die Form von erstem oberen Molar und Unterkiefer der Waldmaus (Apodemus sylvaticus) in Norddeutschland: Alter, Habitat und Inseleffekt Die Formvariabilita¨t des Molars (M1/) und des Unterkiefers von norddeutschen Waldma¨usen (Apodemus sylvaticus) wurde untersucht. Dabei wurde sowohl die Variabilita¨t zwischen verschiedenen Populationen als auch die Variabilita¨t innerhalb einer Population studiert. So ko¨nnen Geschlecht und Alter beispielsweise die Formvariabilita¨t innerhalb einer Population verursachen. Deshalb wurde die Bedeutung dieser Faktoren mit der Variabilita¨t zwischen geographisch unterschiedlichen Populationen verglichen. Geschlechtsdimorphismus wurde nicht beobachtet. Ein zunehmendes Alter verursacht eine Variation der Gro¨Xe und der Form des Molars infolge fortschreitender Abnutzung. Der Unterkiefer a¨ndert sich auch durch spa¨tes Wachstum und Umgestaltung des Knochens. Jedoch sind diese Effekte von beschra¨nkter Bedeutung verglichen mit der Variabilita¨t von Ort zu Ort. Der GenfluX zwischen Festland-Populationen sollte begu¨nstigt sein verglichen mit dem GenfluX zwischen nordfriesischen Inseln und zwischen Inseln und Festland. Sylt nimmt dabei eine Zwischenstellung ein, weil diese Insel durch einen Damm mit dem Festland verbunden ist. Die Differenzierung des Molars stimmt mit diesem erwarteten Muster u¨berein. Die Differenzierung der Form des Unterkiefers entspricht eher den unterschiedlichen Habitaten zwischen Holstein, Nordfriesland, und den nordfriesischen Inseln. Trotz des kleinen geographischen Rahmens dieser Untersuchung lassen sich folgende Ergebnisse ableiten: Die Molaren scheinen sich mit dem GenfluX zwischen verschiedenen Populationen zu a¨ndern wa¨hrend sich der Unterkiefer durch selektive und/ oder funktionelle Besonderheiten zu a¨ndern scheint. r 2005 Elsevier GmbH. All rights reserved.
References Adamczewska, K. A. (1959): Untersuchungen u¨ber die Variabilita¨t der Gelbhalsmaus, Apodemus flavicollis flavicollis (Melchior, 1834). Acta Theriol. 3, 141–190. Adamczewska-Andrzejewska, K. A. (1967): Age reference model for Apodemus flavicollis (Melchior, 1834). Ekologia Polska, Seria A 15, 787–790. Angerbjo¨rn, A. (1986): Gigantism in island populations of wood mice (Apodemus) in Europe. Oikos 47, 47–56.
Atchley, W. R.; Cowley, D. E.; Vogl, C.; Mclellan, T. (1992): Evolutionary divergence, shape change, and genetic correlation structure in the rodent mandible. Syst. Biol. 41, 196–221. Bresin, A.; Kiliardis, S.; Strid, K. -G. (1999): Effect of masticatory function on the internal bone structure in the mandible of the growing rat. Eur. J. Oral Sci. 107, 35–44. Canova, L.; Maistrello, L.; Emiliani, D. (1994): Comparative ecology of the Wood mouse
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Apodemus sylvaticus in two differing habitats. Z. Sa¨ugetierkunde 59, 193–198. Cardini, A.; Tongiorgi, P. (2003): Yellow-bellied marmots (Marmota flaviventris) ‘in the shape space’ (Rodentia Sciuridae): sexual dimorphism, growth and allometry of the mandible. Zoomorphology 122, 11–23. Cheylan, G. (1986): Facteurs historiques, e´cologiques et ge´ne´tiques de l’e´volution de populations me´diterrane´ennes de Rattus rattus (L.). Discussion des mode`les de spe´ciation. Diss. Thesis, Universite´ des Sciences et Techniques du Languedoc, Montpellier, France. Crampton, J. S. (1995): Elliptic Fourier shape analysis of fossil bivalves: some practical considerations. Lethaia 28, 179–186. Dayan, T.; Simberloff, D.; Tchernov, E.; YomTov, Y. (1990): Feline canines: communitywide character displacement among the small cats of Israel. Am. Nat. 136, 39–60. Duarte, L. C.; Monteiro, L. R.; Von Zuben, F. J.; Dos Reis, S. F. (2000): Variation in mandible shape in Thrichomys apereoides (Mammalia: Rodentia): geometric analysis of a complex morphological structure. Syst. Biol. 49, 563–578. Fadda, C.; Corti, M. (2001): Three-dimensional geometric morphometrics of Arvicanthis: implications for systematics and taxonomy. J. Zool. Syst. Evol. Res. 39, 235–245. Ferson, S.; Rohlf, F. J.; Koehn, R. K. (1985): Measuring shape variation of two-dimensional outlines. Syst. Zool. 34, 59–68. Foster, J. B. (1964): The evolution of mammals on islands. Nature 202, 234–235. Frynta, D. (1993): Body weight structure in the Wood mouse (Apodemus sylvaticus) population in urban habitats of Prague. Acta Soc. Zool. Bohemicae 57, 91–100. Frynta, D.; Vohralı´ k, V. (1994): Reproduction in the Wood mouse (Apodemus sylvaticus) in urban habitats of Prague, III: population structure sexual maturation and breeding intensity in females. Acta Soc. Zool. Bohemicae 58, 39–51. Kuhl, F. P.; Giardina, C. R. (1982): Elliptic Fourier features of a closed contour. Comput. Graphics Image Process. 18, 259–278. Lightfoot, P. S.; German, R. Z. (1998): The effects of muscular distrophy on craniofacial growth in mice: a study of heterochrony and ontogenetic allometry. J. Morphology 235, 1–16.
Michaux, J. R.; Chevret, P.; Filipucci, M. -G.; Macholan, M. (2002a): Phylogeny of the genus Apodemus with a special emphasis on the subgenus Sylvaemus using the nuclear IRBP gene and two mitochondrial markers: cytochrome b and 12S rRNA. Mol. Phyl. Evol. 23, 123–136. Michaux, J. R.; Gou¨y de Bellocq, J.; Sara, M.; Morand, S. (2002b): Body size increase in rodent populations: a role for predators? Global Ecol. Biogeogr. 11, 427–436. Murbach, H. (1979): Zur Kenntnis von Inselpopulationen der Waldmaus Apodemus sylvaticus (Linnaeus, 1758). Z. Zool. Syst. Evol.-forsch. 17, 116–139. Renaud, S. (1999): Size and shape variability in relation to species differences and climatic gradients in the African rodent Oenomys. J. Biogeography 26, 857–865. Renaud, S.; Michaux, J. R. (2003): Adaptive latitudinal trends in the mandible shape of Apodemus wood mice. J. Biogeography 30, 1617–1628. Renaud, S.; Michaux, J.; Mein, P.; Aguilar, J. -P.; Auffray, J. -C. (1999): Patterns of size and shape differentiation during the evolutionary radiation of the European Miocene murine rodents. Lethaia 32, 61–71. Renaud, S.; Millien, V. (2001): Intra- and interspecific morphological variation in the field mouse species Apodemus argenteus and A. speciosus in the Japanese archipelago: the role of insular isolation and biogeographic gradients. Biol. J. Linnean Soc. 74, 557–569. Robel, D. (1971): Zur Variabilita¨t der Molarenwurzeln des Oberkiefers bei Inselpopulationen der Waldmaus (Apodemus sylvaticus [L.], 1758). Z. Sa¨ugetierkunde 36, 172–179. Steiner, H. M. (1967): Untersuchungen u¨ber die Variabilita¨t und Bionomie der Gattung Apodemus (Muridae, Mammalia) der Donau-Auen von Stockerau (Niedero¨sterreich). Z. Wiss. Zool. 177, 1–96.
Author’s address: Sabrina Renaud, UMR 5125 CNRS ‘‘Pale´oenvironments et Pale´obiosphere’’, Universite´ Claude Bernard, Lyon 1, 69622 Villeurbanne, France (e-mail: [email protected])
www.elsevier.de/mambio
Original investigation
First upper molar and mandible shape of wood mice (Apodemus sylvaticus) from northern Germany: ageing, habitat and insularity By Sabrina Renaud UMR 5125 CNRS ‘‘Pale´oenvironnements et Pale´obiosphe`re’’, Universite´ Claude Bernard, Lyon, France Receipt of Ms. 21.6.2004 Acceptance of Ms. 28.10.2004
Abstract The patterns of shape variation of the first upper molar and mandible have been investigated within and among wood mice (Apodemus sylvaticus) populations from northern Germany. Some factors such as sex and age of the animals could be a source of within-group morphological variability interfering with among-groups patterns of differentiation. The relative importance of both sources of shape variation was investigated, in order to evaluate the robustness of patterns of fine-scale geographic differentiation. The increasing age of the animals, estimated by wear stages of the upper tooth row, caused significant variations in size and shape of the molars due to progressive abrasion of the cusps. It also involved shape changes of the mandible due to bone remodelling. However, these intrapopulational effects are of limited importance compared to geographic differentiation. Gene flow among populations should be favoured across mainland populations but lowered between mainland and islands, and to a lesser extent among close islands. Shape differences in molars are in agreement with this expected pattern of gene flow. Patterns of mandible differentiation rather match local variations in habitats. At this fine geographic scale, molar shape would vary according to the amount of genetic exchange among populations whereas mandible shape might be under local selective and/or functional constraints. r 2005 Elsevier GmbH. All rights reserved. Keywords: Murinae, evolution, island biogeography, morphometrics
Introduction Size and shape variability of small mammals like rodents has been described in regard to different factors and based on various characters. Insularity is a well-known context of morphological divergence (e.g., Berry, 1973). A growing body of evidences also points to the importance of biogeographic gradients in shaping morphological variability (Fadda and Corti 2001; Renaud and
Michaux 2003). Such shape variations have been described on skull (Fadda and Corti 2001), mandible (Duarte et al. 2000; Renaud and Millien 2001) or teeth (Renaud 1999). However, different characters are seldom analysed in a same study, although they might provide contrasting results. Additionally, some sources of populational variability, such as sex and age of the animals, might
1616-5047/$ - see front matter r 2005 Elsevier GmbH. All rights reserved. doi:10.1016/j.mambio.2004.10.004 Mamm. biol. 70 (2005) 3 157–170
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Classes were established based on the four classes recognised by Adamczewska–Andrzejewska (1967). The first class included specimens with an erupted third molar (M3/) without traces of wear. Animals belonging to this class were very seldom found. Hence, WS1 was pooled with WS2 corresponding to individuals with slightly worn cusps. Stage 3 includes specimens with surfaces of all cusps joined on the third upper molar (M3/), and a close ring of six cusps on M2/ and M1/. On the M1/ the cusps of the first transverse row are connected with each other. Stage 4 corresponds to individuals with a very worn chewing surface, the enamel loops circumscribing the base of the cusps. A further class (WS5) was added according to Steiner (1967) with all molars worn flat, only the M1/ possibly showing some rest of cusps. In order to evaluate the variations in frequency of the different WS along the year, animals were grouped according to the season of trapping (Winter: December–February; Spring: March–May; Summer: June–August; Autumn: September–November).
interfere with among-group patterns of differentiation, especially when considering finescale patterns. The relative importance of the different sources of variations should be compared, in order to assess the robustness of biogeographic patterns observed from wild-caught populations. The aim of this study is to address these questions on populations of European wood mice (Apodemus sylvaticus). Several mainland and insular populations from northern Germany were selected to investigate the possible sources of fine-scale morphological variations.
Material and methods Material The study is based on specimens of wood mice (A. sylvaticus) from the collection of the Institut fu¨r Haustierkunde (Kiel, Germany). The animals were trapped between 1957 and 1974 in different localities from northern Germany (Fig. 1). Mainland localities were grouped into Holstein populations (around Kiel) and Nordfriesland populations (around Bredstedt). Three North Friesian islands were also sampled: Sylt, Fo¨hr and Amrum. The mandible was measured of 213 and the first upper molar of 170 animals (Table 1). Only mature specimens with the third molar erupted were considered. Wear stage (WS) was evaluated on the upper molar row of 169 animals. -10°
A
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0°
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10°
15°
20°
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The outline describes the overall shape of morphological features. In the case of the molars, the relative position and swelling of the cusps strongly influence the outline. In the case of the mandible, the outline provides a description of the development and orientation of the processes involved in the insertion of the mastication muscles, as well as of the alveolar region bearing the cheek teeth and
8°
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55° 0'
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Outline analysis of the first upper molars and the mandibles
AM
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FOE
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NF 19
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54° 30'
9
45°
11 12 14 10 15 13
Kiel
40°
HO
18
Preetz
Plön
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Rickling
Fig. 1. Localisation of the sampling localities of the wood mice (Apodemus sylvaticus) considered in the present study. (A) Localisation on a map of Europe of the studied area (B). Dotted areas represent the main geographic groups (cf. Table 1).
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Table 1. Trapping localities, with numbering and grouping. Number of measured mandibles (Md) per trapping locality: male (M)/female (F), season of trapping (Sp: spring; Su: summer; Fa: fall; Wi: winter). Number of measured first upper molar (UM1). Gp. AM
Amrum
FO¨E
Fo¨hr
HO
Holstein
Abbr.
#
Locality
Md
M
F
Sp
Su
Au
Wi
UM1
NORDD
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25
Nebel Norddorf Su¨ddorf Alkersum Boldixum Borgsum Oevenum Wyk Hemmelmark Kiel Kaltenhof Rathmannsdorf Fargau Scho¨nberg Scho¨nkirchen Eutin Rickling Preetz Bredstedt Leck Su¨derlu¨gum Kampen Morsum Rantum Westerland
1 13 8 4 6 22 4 15 3 7 3 7 4 6 1 1 2 58 7 1 8 4 18 7 3
1 7 4 — 5 5 2 7 2 4 2 4 2 3 1 1 — 23 4 — 2 2 4 1 —
— 6 4 4 1 16 2 8 1 3 1 3 2 3 — — 2 34 3 1 5 2 14 6 3
1 3 — 2 2 2 3 13 3 — — 2 1 — — — — 16 7 1 8 2 4 3 1
— — — — — 6 — 1 — — — — — — — — — 14 — — — — — — —
— 10 8 2 4 13 1 1 — 7 — 3 — 1 1 — 2 28 — — — 2 14 4 2
— — — — — — — — — — 3 2 3 5 — 1 — — — — — — — — —
1 9 8 2 5 13 3 8 3 6 3 7 3 4 1 1 2 54 4 1 6 4 17 4 1
SUEDD ALK BOLDX BORGS OEV WYK HEM KIEL RATH PLOEN
NF
Nordfriesland
SY
Sylt
PREETZ BRED SUEDLG KAMP MORS RANT
the incisor. In both cases, the outline analysis appears to be appropriate to describe subtle morphological changes along geographic gradients (Renaud 1999; Renaud and Michaux 2003). The outline of the first upper molar corresponds to the two-dimensional projection of the tooth viewed from the occlusal surface. The starting point of the outline was defined at the maximum of curvature on the anterior part of the tooth. The outline of the mandible corresponds to the projection of the hemi-mandible put flat on its side with the lingual side down. As the incisor can be free moving and the molars missing, only the outline of the mandibular bone is considered. The starting point was defined at the meeting point of the incisor and the bone on the upper edge of the mandible. For both the mandible and the M1/ outline, 64 points at equally spaced intervals along the outline were sampled. A radial Fourier transform (RFT) was then applied (Renaud and Michaux 2003). From the x, y-coordinates of the points, 64 radii corresponding to the distance of each point to the centre of gravity of the outline were calculated. Using the RFT, the outline is expressed as a finite
sum of trigonometric functions of decreasing wavelength, the harmonics, approximating the function of the radius varying with the cumulative distance along the outline. Each harmonic is weighted by two Fourier coefficients, An and Bn. The zeroth harmonic A0 is proportional to the size of each outline and can be used to standardise all the Fourier coefficients, in order to retain shape information only. In order to determine the rank of the last harmonic that has to be retained for a satisfactory description of the outline, two criteria can be considered: measurement error, estimated by repeated measurement, and information content (Crampton 1995). Studies on similar rodents suggested that both criteria were congruent. They indicated that considering the first nine harmonics for the M1/ (Renaud et al. 1999) and the first seven harmonics for the mandible (Renaud and Michaux 2003) offered a good compromise between measurement error, information content, and number of variables to be considered. From any set of Fourier coefficients, an outline can be reconstructed using an inverse method,
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providing a visualisation of the shape differences between sets of Fourier coefficients. RFT provides moderately accurate reconstructions because xycoordinates are re-calculated from the set of radii provided by the inverse Fourier transform (Renaud and Michaux 2003). They can nevertheless be useful to visualise the parts of the structure affected by shape changes. Accurate reconstructions of average shapes can be obtained using the elliptic Fourier transform (Kuhl and Giardina 1982; Ferson et al. 1985) as a further support for visual interpretation of shape changes.
Statistical analyses Size of the mandible or the M1/ are estimated by an univariate parameter, i.e. the zeroth harmonic amplitude A0. Differences in size according to various factors have been tested using analyses of variance (ANOVA). Size of the mandible and the M1/ were compared to the size of the animal, estimated by the body length, using a model of linear regression. The shape of each outline was described by a set of Fourier coefficients: 18 for each M1/ (2 coefficients per 9 harmonics) and 14 for each mandible (2 coefficients per 7 harmonics). These sets of Fourier coefficients had to be analysed using multivariate statistics. The existence of differences according to various factors has been tested using multivariate analyses of variance (MANOVA, test considered: Wilks’ Lambda). To display the morphological variability on a few synthetic shape axes, principal component analyses (PCA) were performed on Fourier coefficients of the mandible and the first upper molars separately. The PCA were normed, i.e. performed on the correlation coefficient matrix of the Fourier coefficients, to give the same weight to all the variables and not enhance the role of the first harmonics because of their higher numeric values. To enhance the readability of the graphs, all individuals were not plotted on the first principal axes but rather average values according to the WS and/or geographic groups. Reconstruction of the mean outline for some samples was used to visualise the shape variability. In order to compare the patterns observed on the first upper molar and the mandible, matrices of distance were constructed. The average values of Fourier coefficients per main geographic groups (HO, NF, PRE, AM, FOE, SY) or per local geographic groups (Loc. Gp. in Table 1) were calculated and distances among them estimated using Euclidean distances on the Fourier coefficients of the mandible (seven harmonics) and the first upper molar (nine harmonics). The matrices of distances of both characters were then compared using a Mantel t-test.
Results Morphological variability within a mainland population The existence of size or shape differences of the first upper molars and the mandibles due to intrapopulational factors, i.e. sex or age of the individuals, were first investigated on the largest population (Preetz, Holstein). This population also presents the advantage to minimise the importance of the interannual variability since it is almost exclusively composed of animals trapped in 1960. Sex was found to have no influence on size or shape of the M1/ nor of the mandible (Table 2). Differently, age (estimated by WS of the teeth), and to a lesser extent season, were found to have a significant impact on size and shape. The age structure of the wood mice samples varies according to the season of trapping (Fig. 2A). Whereas summer and autumn populations are composed of young animals, an important proportion of older animals is observed in spring. The seasonal effect could therefore be attributed to different compositions in WSs. The shape variability of the M1/ in Preetz (Fig. 2B) clearly shows the importance of the WS. The first principal axis (PC1, 17.3% of the total variance) corresponds to a random variability within the population whereas along PC2 (16.7%) teeth of young animals (WS1-3) are opposed to older animals (WS45). The oldest individuals (WS5) are the most Table 2. Morphological variability of the wood mouse population of Preetz (Holstein). UM1: first upper molar; Md: mandible. Size: ANOVA probability on A0. Shape: MANOVA on the Fourier coefficients of the first nine (UM1) and seven (Md) harmonics. Probability of the Wilk’s Lambda test is given. In bold significant probabilities (Po0.05). Factors
Wear Sex Season
UM1
Md
Size
Shape
Size
Shape
P
P
P
P
0.007 0.983 0.037
0.0007 0.6653 0.0025
0.181 0.360 0.309
0.0048 0.3534 0.0073
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A
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C M1/Size (A0)
6.5
6.0
SEASON 5.5
5.0
Autumn Summer Spring 1
2
3
4
5
WEAR CLASS
Fig. 2. (A) Frequency distribution of the wear classes (based on the upper teeth) in Holstein wood mice from Preetz, as a function and the season of trapping. (B) Shape variability of the first upper molar, estimated by the first principal plane of a PCA on the Fourier coefficients of the molar outline. Different symbols correspond to the wear classes. Outlines correspond to the average shape of the wear classes. (C) Size variability of the first upper molar, estimated by A0, as a function of the wear classes and season of trapping.
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extreme along this axis. The shape change due to progressive wear of the tooth is mostly the abrasion of the posterior middle cusp (t8). Young individuals have therefore more slender molars with a sharp back part whereas older individuals display a flattened back part leading to a more rounded outline. The progressive wear of the tooth also causes a reduction of the occlusal surface and hence, a decrease in A0 (Fig. 2C; Table 2). The size of the M1/ is not correlated with the body length of the animal (R ¼ 0:170; P ¼ 0:269). The ageing of the animals had a different impact on the mandible. Size variations as a function of WS were not significant (Table 2). However, WS1-3 are more variable in size and include animals of smaller size than WS4 and 5, composed only of large specimens (Fig. 3A). This is attributable to the presence of young animals still growing in the first WSs. This relationship with continuous growth of the mandible is confirmed by a significant relationship between mandible size and body length (R ¼ 0:792; Po0:001). The influence of age on the shape of the mandible is less obvious than on the M1/ (Fig. 3B,C). The most obvious pattern is the position of the animals of WS5 at the edge of the total variability. The shape changes with increasing WS are very tenuous and involve a more curved region of insertion of the cheek teeth (alveolar region). The articular condyle is slightly higher. The coronoid process is relatively reduced. Variations among wood mice populations from mainland and North Friesian islands The composition of the populations of wood mice, regarding the season of trapping and the WSs, is very different (Fig. 4). The populations of Amrum and Holstein are dominated by young animals (WS1-2 and 3) whereas the contribution of older animals is more important in Nordfriesland, Fo¨hr and Sylt. Considering the morphological variations observed at Preetz according to the ageing of the animals, the influence of WSs on the structure of the morphological differentiation among populations has to be evaluated. Since no sexual dimorphism was detected for the M1/ or the mandible at
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Fig. 3. Morphological variability of the mandible in the wood mice from Preetz. (A) Size, estimated by A0, as a function of the wear classes and season of trapping. (B) Shape, estimated by the first principal plane of a PCA on the Fourier coefficients of the mandible. Different symbols correspond to the wear classes. Outlines correspond to the average shape of the wear classes. (C) Reconstructed outlines for each WS, using the Elliptic Fourier Transform (EFT, 16 harmonics). The dotted shape corresponds to WS1-2, compared to following WSs. coron.p.: coronoid process; condyl.p.: condylar process; angul.p.: angular process; alveolar r.: alveolar region.
Preetz, animals of both sexes were pooled together in the subsequent analyses. Both WSs and the main geographic groups (being HO, NF, Preetz, Amrum, Fo¨hr and Sylt, see Table 1) have a significant influence on molar and mandible morphology (Table 3). The size of the M1/ is not affected by the geographic origin but by the age of the individuals (Table 3). In agreement with the observations at Preetz, older molars tend to be smaller than younger ones (Fig. 5A). Patterns of M1/ shape differentiation are influenced both by the ageing of the animals and their geographic origin (Table 3). As in Preetz, teeth belonging to WS4-5 are characterised by outlying morphologies at the
periphery of the total range of variation, on PC1 (19.3% of the total variance) for WS5teeth from Nordfriesland, Sylt and Amrum, along PC2 (13.4%) for Nordfriesland and Preetz, and along PC3 (10.7%) for Holstein, Nordfriesland, Amrum and Sylt. If this oldest WS is discarded, some geographic structure can be recognised among younger teeth (Fig. 5B,C). The four WS-samples from Fo¨hr are clustered along the three PCs and opposed along PC1 to mainland samples from Holstein (HO and Preetz). Teeth from Amrum are only segregated along PC2, whereas molars from Sylt fall consistently close to the Holstein samples. Teeth from Nordfriesland (WS3-5), although from a
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Fig. 4. Frequency distribution of the wear classes (based on the upper teeth) in wood mice from northern Germany, as a function of the season of trapping. Mainland: Holstein and Nordfriesland; islands: Amrum, Fo¨hr, and Sylt.
mainland origin, are segregated from Holstein M1/ along PC2. The morphological differentiation of the mandible involves both, age and geographic origin for both size and shape (Table 3). In
agreement with the results at Preetz, older animals (WS4-5) tend to have larger mandibles than younger ones (Fig. 5D). Superimposed to this intrapopulational variability due to continuous growth, some geographic
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Table 3. Morphological variability of wood mouse population from northern Germany. UM1: first upper molar; Md: mandible. Size: ANOVA probability on A0. Shape: MANOVA on the Fourier coefficients of the first nine (UM1) and seven (Md) harmonics. Probability of the Wilks’ Lambda test is given. In bold significant probabilities (Po0.05). Gp are geographic groups. Factors
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Shape
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P
0.011 0.241
0.000 0.000
0.000 0.000
0.0000 0.0000
trends may be recognised. The mandibles from Preetz are on average the smallest whereas the insular population from Fo¨hr and the mainland population from Nordfriesland display the largest mandible size. Regarding shape, mandibles from the oldest WSs (WS5) tend to diverge from the youngest morphologies (Fig. 5E,F). The WS5samples from Amrum and Holstein diverges at one side of the first principal plane defined by PC1 (35.6%) and PC2 (19.0%), whereas the WS5 from Nordfriesland diverge at the other side (Fig. 5E). The WS5 from Fo¨hr is isolated along PC3 (15.7%). Fo¨hr and Sylt mandibles from WS1-4 are clustered together and are slightly separated from the Holstein mainland samples on the first principal plane. The Amrum samples segregate along PC3. Nordfriesland mandibles diverge along PC2. Comparison of the geographic differentiation of the molar and mandible shape WS clearly interferes with the geographic patterns of differentiation. However, intermediate WSs are dominant within the trapped animals (Fig. 4) and this influence should be buffered by considering the whole population at one location. The robustness of the geographic pattern of differentiation was investigated by splitting the main geographic groups into smallest entities corresponding to more restricted geographic areas (Loc. Gp. in Table 1). Moreover, the geographic patterns of differentiation observed on different char-
acters of the same animals (first upper molar or mandible) were compared. Size of the M1/ and the mandible are only weakly correlated (R ¼ 0:518; P ¼ 0:033) and few consistent patterns emerge from the comparison (Fig. 6A). The different samples from Fo¨hr tend to be among the largest, for the molars as well as for the mandibles. A matrix comparison of the distances among geographic groups based on the M1/ or the mandible show a weak relationship between both patterns. Considering only the main geographic groups (HO, NF, PRE, AM, FOE, SY) provides a non-significant relationship between M1/ and mandible (Mantel ttest: R ¼ 0:522; t ¼ 1:551; P ¼ 0:060) although close to the significance threshold (P ¼ 0:050). Comparing the distances among the 17 local groups provides a significant result (Mantel t-test: R ¼ 0:323; t ¼ 2:425; P ¼ 0:008) but the correlation plot is fuzzy. The patterns of differentiation among local groups provide some clear indications of geographic structure for the M1/ as well as the mandible. Regarding the M1/, Fo¨hr populations are segregated from the mainland populations along both, PC1 and PC2 (Fig. 6B). This corresponds to a very subtle morphological difference, with labial (lefthand on the outline) anterior (t3) and posterior (t9) cusps slightly more pronounced compared to the central populations from Holstein exemplified by Preetz. On the other side of the first principal plane the Nordfriesland populations segregate. Their molars display a pronounced labial posterior (t9) cusp but less developed lingual (t1, t4) cusps. This divergence emerges again along PC3 that also displays a divergence of the Amrum molars (Fig. 6C). They are characterised by both, pronounced labial posterior (t9) and lingual (t1, t4) cusps. Sylt molars fall close to the mainland samples from Holstein. Mandible shape provides both, some similar features and marked discrepancies compared to the first upper molar. The Nordfriesland populations are segregated along PC1 and secondarily along PC2 (Fig. 6D). This corresponds mainly to a wider coronoid process (Fig. 6D,F). Holstein populations are clustered together and all islands populations show some divergence compared to this
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Fig. 5. Differentiation of the first upper molars and mandibles among wood mice from northern Germany. (A) Upper molar size as a function of the geographic groups and wear classes. (B, C) Shape differentiation on the first three principal axes of a PCA on the Fourier coefficients of the upper molar outline. (D) Mandible size as a function of the geographic groups and wear classes. (E, F) Shape differentiation on the first three principal axes of a PCA on the Fourier coefficients of the mandible. Symbols correspond to average values per geographic groups and wear classes.
basic pattern (Fig. 6D,E). Along PC1 all insular populations are shifted towards positive values showing that they share some common characteristics. Fo¨hr mandibles are
also isolated along PC2. They display a slightly wider coronoid process and a reduced angular process (Fig. 6F). Amrum mandibles tend to have a lower articular process. All
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Fig. 6. Geographic differentiation of the first upper molar and the mandible among wood mouse populations from northern Germany. (A) Upper molar size vs. mandible size. (B, C) Geographic differentiation of the first upper molar. (D, E) Geographic differentiation of the mandible. Principal axes are the same as on Fig. 4 (M1/) and 5 (MD) but symbols correspond to average values per geographic group. Outlines correspond to the average shape of the different geographic groups. (F) Reconstructed outline of the mandible for each geographic group, using the Elliptic Fourier Transform (EFT, 16 harmonics). The dotted shape corresponds to Holstein average mandible, compared to other groups.
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insular mandibles tend to share a more curved alveolar region and a reduced angular process (Fig. 6F).
Discussion Factors of intrapopulational morphological variations Different factors can cause morphological differences within a population. Wood mice from the locality of Preetz (Germany) show no evidence of sexual dimorphism on size or shape of the first upper molar or of the mandible. Sexual dimorphism is a common feature in groups such as carnivores (Dayan et al. 1990), and has been described for body size of rodents, including Apodemus (Adamczewska 1959). However, the present result is in agreement with previous observations on molars (Renaud 1999) or mandibles (Cardini and Tongiorgi 2003) of rodents. It allows mixing specimens of both sexes in morphometric analyses. On the other hand, the age of the animal appears to influence the shape of both, molars and mandibles. In the case of the first upper molar the progressive wear of the tooth is responsible for the shape change of the oldest WSs, also causing a decrease in the size of the molar. Once the molars are erupted, they only vary with wear and show no relationship with the body size of the animal. On the contrary, the shape change observed on the mandible exemplifies the bone growth and remodelling occurring throughout the adult life of an animal, leading to a covariation of mandible and body size. Similar effects have been described in marmots (Cardini and Tongiorgi 2003). An important growth and allometric shape changes of the mandible are observed along the 4 years of life of the animals, but this study included the phase of juvenile growth. Differently, the amount of growth documented in the present morphometric analysis was limited by selecting only specimens with erupted third molars, hence considered as adults. The shape changes observed are likely mostly related to bone remodelling which occurs due to an interaction between muscular functioning and the mandible growth
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(Lightfoot and German 1998; Bresin et al. 1999). Such a plastic shape variation can cause subtle differences between populations, since the composition of the population according to age varies with the season and possibly with the local environment. A changing age structure through the year is known for long in wood mice populations (e.g., Steiner 1967; Frynta 1993; Frynta and Vohralı´ k 1994). Mostly young animals survive the winter period, leading in late spring and summer to a mixed population of old, over-wintered animals and young adults born at the beginning of the reproductive period (Steiner 1967). Different seasons of trapping are thus likely to lead to different age structure. Furthermore, the structure of the population may vary with the quality of the environment, life expectancy being reduced in atypical environments such as marshes compared to woodlands (Canova et al. 1994). On the other hand, life expectancy has been suggested to be extended on islands (Cheylan 1986). Such hypotheses are not supported by this data set where the main factor causing a difference in age structure seems to be the season of trapping.
Gene flow and habitat shaping molars and mandibles A major interest of the model constituted by the North Friesian islands is that the timing of the insular differentiation can be dated with precision, since isolation happened during historical times. From an initial mainland zone, two large storms in 1362 and 1634 AD isolated the North Friesian islands. Isolation is therefore younger than 750 years, constituting a very short time interval for evolutionary processes in natural populations. The amount of isolation varies for the different islands considered. Since 1927 Sylt is linked to the mainland by a dyke used by railway. Water depth is nowhere important between the islands and at low tide it is possible to walk from Fo¨hr to Amrum. The most isolated island is supposed to be Amrum, at the western border of the mudflats of the Wadden Sea. Accordingly, the
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wood mice from Amrum have been found to be the most divergent from mainland ones for the patterns of molar roots (Robel 1971) and cranial morphology (Murbach 1979). Included into a large-scale geographic pattern covering Western Europe, the Amrum population was also found to be divergent regarding the shape of the mandible (Renaud and Michaux 2003). Focusing the study on the region of northern Germany and comparing both molar and mandible shape provide contrasting results. The pattern of geographic differentiation based on the first upper molar indicates a morphological relatedness of the Holstein and Nordfriesland populations. Both are located on the mainland making gene flow likely. Populations from Sylt also appear to be morphologically close to the mainland populations, in agreement with observations on the skull (Murbach 1979). Sylt is connected with the mainland by a dyke, that should favour gene flow with the mainland populations. Hence, the more pronounced divergence of Fo¨hr and Amrum can be explained by the geographic context. The shared morphological features between the populations of the three islands can also be explained by the proximity of islands. The pattern observed on the mandible is quite different. In agreement with their geographic nearness, the Holstein populations are clustered together, but the set of mainland samples from Nordfriesland appears as very divergent. Mandibles from the different islands diverge from the mainland ones, to a various extent but in a similar way. To the contrary of the molar shape, this pattern does not match the expected pattern of gene flow. However, the differentiation of the mandible may match the local environmental conditions. Mixed forest favourable to the wood mouse are frequent in Holstein, whereas Nordfriesland corresponds to low-lying areas with large extent of marshes and meadows drained by channels, with little coniferous forests. The environment on the three North Friesian islands should be comparable, with wood mice inhabiting marsh, dunes and some pine plantations, especially on Amrum (Murbach 1979).
Neither the molar nor the mandible displays a clear pattern regarding size, although this character is known to vary on islands in the wood mouse (Angerbjo¨rn 1986). However, the importance of the size increase depends on the predation pressure and the distance to the mainland (Michaux et al. 2002b). The North Friesian islands are close to the mainland and the predator fauna is not impoverished, explaining the absence of any clear ‘‘insular syndrome’’ (Foster 1964) on these islands. Timing and processes differentiation The present study shows that morphological differentiation can evolve rapidly. The differences between mainland and North Friesian islands populations occurred in less than 750 years. Even more striking, differences in mandible shape occur between animals of different ages, due to bone remodelling. Within the European wood mouse (A. sylvaticus) a latitudinal gradient in mandible shape has recently been described (Renaud and Michaux 2003). Based on genetic evidences, the wood mouse recolonised Europe after the last glaciation from an Iberic refuge zone (Michaux et al. 2002a). Hence, the formation of the latitudinal gradient has been rapid, in the order of 16,000 years. Epigenetic factors such as bone remodelling could participate to such rapid morphological differentiation, since the gradient observed on the mandible has been interpreted as due to change in diet from the north to the south of western Europe (Renaud and Michaux 2003). Such plastic variations are not expected in a feature like the molar, which does not grow after its eruption and can only be modified by wear during the life of the animal. Different patterns of variations are therefore expected depending on the character considered, since different genes are involved in different morphological modules (Atchley et al. 1992) and epigenetic late effects during the life of the animals will differ. These results show that a study based on a limited geographic range can provide useful insight into fine-scale processes involved in the morphological differentiation. The
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overwhelming importance of environmental factors over larger geographic range may obscure discrepancies among characters that are hints for different determinisms and/or selective pressure.
Acknowledgements This study would not have been possible without Prof. Dr. Dieter Kruska who pro-
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vided access to the collection of the Institut fu¨r Haustierkunde (Kiel, Germany). The technical help of Renate Lu¨cht during measurements at the institute was greatly appreciated. This manuscript benefited from the comments of Thomas Cucchi and Ingo Klaucke, who also corrected the German abstract. This study was supported by the GDR 2474 CNRS and the Rhoˆne-Alpes region (Emergence program).
Zusammenfassung Die Form von erstem oberen Molar und Unterkiefer der Waldmaus (Apodemus sylvaticus) in Norddeutschland: Alter, Habitat und Inseleffekt Die Formvariabilita¨t des Molars (M1/) und des Unterkiefers von norddeutschen Waldma¨usen (Apodemus sylvaticus) wurde untersucht. Dabei wurde sowohl die Variabilita¨t zwischen verschiedenen Populationen als auch die Variabilita¨t innerhalb einer Population studiert. So ko¨nnen Geschlecht und Alter beispielsweise die Formvariabilita¨t innerhalb einer Population verursachen. Deshalb wurde die Bedeutung dieser Faktoren mit der Variabilita¨t zwischen geographisch unterschiedlichen Populationen verglichen. Geschlechtsdimorphismus wurde nicht beobachtet. Ein zunehmendes Alter verursacht eine Variation der Gro¨Xe und der Form des Molars infolge fortschreitender Abnutzung. Der Unterkiefer a¨ndert sich auch durch spa¨tes Wachstum und Umgestaltung des Knochens. Jedoch sind diese Effekte von beschra¨nkter Bedeutung verglichen mit der Variabilita¨t von Ort zu Ort. Der GenfluX zwischen Festland-Populationen sollte begu¨nstigt sein verglichen mit dem GenfluX zwischen nordfriesischen Inseln und zwischen Inseln und Festland. Sylt nimmt dabei eine Zwischenstellung ein, weil diese Insel durch einen Damm mit dem Festland verbunden ist. Die Differenzierung des Molars stimmt mit diesem erwarteten Muster u¨berein. Die Differenzierung der Form des Unterkiefers entspricht eher den unterschiedlichen Habitaten zwischen Holstein, Nordfriesland, und den nordfriesischen Inseln. Trotz des kleinen geographischen Rahmens dieser Untersuchung lassen sich folgende Ergebnisse ableiten: Die Molaren scheinen sich mit dem GenfluX zwischen verschiedenen Populationen zu a¨ndern wa¨hrend sich der Unterkiefer durch selektive und/ oder funktionelle Besonderheiten zu a¨ndern scheint. r 2005 Elsevier GmbH. All rights reserved.
References Adamczewska, K. A. (1959): Untersuchungen u¨ber die Variabilita¨t der Gelbhalsmaus, Apodemus flavicollis flavicollis (Melchior, 1834). Acta Theriol. 3, 141–190. Adamczewska-Andrzejewska, K. A. (1967): Age reference model for Apodemus flavicollis (Melchior, 1834). Ekologia Polska, Seria A 15, 787–790. Angerbjo¨rn, A. (1986): Gigantism in island populations of wood mice (Apodemus) in Europe. Oikos 47, 47–56.
Atchley, W. R.; Cowley, D. E.; Vogl, C.; Mclellan, T. (1992): Evolutionary divergence, shape change, and genetic correlation structure in the rodent mandible. Syst. Biol. 41, 196–221. Bresin, A.; Kiliardis, S.; Strid, K. -G. (1999): Effect of masticatory function on the internal bone structure in the mandible of the growing rat. Eur. J. Oral Sci. 107, 35–44. Canova, L.; Maistrello, L.; Emiliani, D. (1994): Comparative ecology of the Wood mouse
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Apodemus sylvaticus in two differing habitats. Z. Sa¨ugetierkunde 59, 193–198. Cardini, A.; Tongiorgi, P. (2003): Yellow-bellied marmots (Marmota flaviventris) ‘in the shape space’ (Rodentia Sciuridae): sexual dimorphism, growth and allometry of the mandible. Zoomorphology 122, 11–23. Cheylan, G. (1986): Facteurs historiques, e´cologiques et ge´ne´tiques de l’e´volution de populations me´diterrane´ennes de Rattus rattus (L.). Discussion des mode`les de spe´ciation. Diss. Thesis, Universite´ des Sciences et Techniques du Languedoc, Montpellier, France. Crampton, J. S. (1995): Elliptic Fourier shape analysis of fossil bivalves: some practical considerations. Lethaia 28, 179–186. Dayan, T.; Simberloff, D.; Tchernov, E.; YomTov, Y. (1990): Feline canines: communitywide character displacement among the small cats of Israel. Am. Nat. 136, 39–60. Duarte, L. C.; Monteiro, L. R.; Von Zuben, F. J.; Dos Reis, S. F. (2000): Variation in mandible shape in Thrichomys apereoides (Mammalia: Rodentia): geometric analysis of a complex morphological structure. Syst. Biol. 49, 563–578. Fadda, C.; Corti, M. (2001): Three-dimensional geometric morphometrics of Arvicanthis: implications for systematics and taxonomy. J. Zool. Syst. Evol. Res. 39, 235–245. Ferson, S.; Rohlf, F. J.; Koehn, R. K. (1985): Measuring shape variation of two-dimensional outlines. Syst. Zool. 34, 59–68. Foster, J. B. (1964): The evolution of mammals on islands. Nature 202, 234–235. Frynta, D. (1993): Body weight structure in the Wood mouse (Apodemus sylvaticus) population in urban habitats of Prague. Acta Soc. Zool. Bohemicae 57, 91–100. Frynta, D.; Vohralı´ k, V. (1994): Reproduction in the Wood mouse (Apodemus sylvaticus) in urban habitats of Prague, III: population structure sexual maturation and breeding intensity in females. Acta Soc. Zool. Bohemicae 58, 39–51. Kuhl, F. P.; Giardina, C. R. (1982): Elliptic Fourier features of a closed contour. Comput. Graphics Image Process. 18, 259–278. Lightfoot, P. S.; German, R. Z. (1998): The effects of muscular distrophy on craniofacial growth in mice: a study of heterochrony and ontogenetic allometry. J. Morphology 235, 1–16.
Michaux, J. R.; Chevret, P.; Filipucci, M. -G.; Macholan, M. (2002a): Phylogeny of the genus Apodemus with a special emphasis on the subgenus Sylvaemus using the nuclear IRBP gene and two mitochondrial markers: cytochrome b and 12S rRNA. Mol. Phyl. Evol. 23, 123–136. Michaux, J. R.; Gou¨y de Bellocq, J.; Sara, M.; Morand, S. (2002b): Body size increase in rodent populations: a role for predators? Global Ecol. Biogeogr. 11, 427–436. Murbach, H. (1979): Zur Kenntnis von Inselpopulationen der Waldmaus Apodemus sylvaticus (Linnaeus, 1758). Z. Zool. Syst. Evol.-forsch. 17, 116–139. Renaud, S. (1999): Size and shape variability in relation to species differences and climatic gradients in the African rodent Oenomys. J. Biogeography 26, 857–865. Renaud, S.; Michaux, J. R. (2003): Adaptive latitudinal trends in the mandible shape of Apodemus wood mice. J. Biogeography 30, 1617–1628. Renaud, S.; Michaux, J.; Mein, P.; Aguilar, J. -P.; Auffray, J. -C. (1999): Patterns of size and shape differentiation during the evolutionary radiation of the European Miocene murine rodents. Lethaia 32, 61–71. Renaud, S.; Millien, V. (2001): Intra- and interspecific morphological variation in the field mouse species Apodemus argenteus and A. speciosus in the Japanese archipelago: the role of insular isolation and biogeographic gradients. Biol. J. Linnean Soc. 74, 557–569. Robel, D. (1971): Zur Variabilita¨t der Molarenwurzeln des Oberkiefers bei Inselpopulationen der Waldmaus (Apodemus sylvaticus [L.], 1758). Z. Sa¨ugetierkunde 36, 172–179. Steiner, H. M. (1967): Untersuchungen u¨ber die Variabilita¨t und Bionomie der Gattung Apodemus (Muridae, Mammalia) der Donau-Auen von Stockerau (Niedero¨sterreich). Z. Wiss. Zool. 177, 1–96.
Author’s address: Sabrina Renaud, UMR 5125 CNRS ‘‘Pale´oenvironments et Pale´obiosphere’’, Universite´ Claude Bernard, Lyon 1, 69622 Villeurbanne, France (e-mail: [email protected])