ISSN 20790864, Biology Bulletin Reviews, 2013, Vol. 3, No. 1, pp. 84–97. © Pleiades Publishing, Ltd., 2013. Original Russian Text © N.P. Korablev, P.N. Korablev, 2012, published in Zhurnal Obshchei Biologii, 2012, Vol. 73, No. 3, pp. 210–224.
Patterns of Morphological Variability in Reintroduced Populations with Two Beaver Subspecies Castor fiber orientoeuropaeus and Castor fiber belorussicus (Castoridae, Rodentia) as an Example N. P. Korableva and P. N. Korablevb a
b
Velikie Luki State Agricultural Academy, prosp. Lenina 2, Velikie Luki, Pskov oblast, 182112 Russia Central Forest State Nature Biosphere Reserve, Nelidovo District, Tver oblast, Zapovedny, 172513 Russia email:
[email protected] Received September 26, 2011
Abstract—The pattern of morphological variability in translocated groups of mammals has been studied based on the example of two beaver subspecies (Castor fiber orientoeuropaeus and Castor fiber belorussicus) with the documented history of population formation. The variability in the quantitative and quantitative traits in the formed populations is not characterized by a single direction. The main trend is an increase in the diversity of adaptive norms in relation to body sizes. A slightly marked increase is observed in the level of fluc tuating asymmetry, a reduction in polymorphisms in nonmetric traits, and an increase in the percentage of rare aberrations that may be associated with inbreeding taking place during the formation of prapopulations. The results of this study allow this intraspecific differentiation to be considered an effect of adaptive variability (adaptatiogenesis) or subspecies hybridization. As for stochastic processes (gene drift and founder effect), they seem to have no significant effect on the morphological variability. The differences between nonmetric and metric traits indicate the peculiarity of population groups. DOI: 10.1134/S2079086413010052
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INTRODUCTION
cussion (Savel’ev, 2000; Gabrys, Wa z na, 2003). Later, the purity of autochthons was disturbed as a result of the release of Voronezh and Belorussian beavers (or their descendants from the daughter populations) into the same basins, subsequent natural immigration, and settlements inside the region. Stable colonies of beavers were formed in the places where animals were released, in which, at the time of craniological material collection, 15–30 generations of animals had changed. From an evolutionarygenet ics standpoint, they are not true populations; rather, they should be considered prepopulations (Altukhov et al., 1997), i.e., genetic systems in which elementary adaptive events take place (Yablokov, 1987). The geographical isolation of a limited number of species is an almost ideal model of the allopatric for mation of species, which is strikingly manifested and characterized by, not the gradual isolation of geo graphical races (Zavadskii, 1968), but the one moment divergence of the maternal population into several absolutely isolated groups. The reintroduction of beavers is a unique experiment, multiple repeats of which make it possible to assess the morphological changes in artificially created populations and to reveal certain regularities of this process, which was referred to as “adaptatiogenesis” by K.M. Zavadskii (1968). The translocations of species are accompanied by events that are generally regarded in population biol
The history of the Eurasian beaver Castor fiber is a striking example of the successful restoration of a nearly extinct unit of biodiversity. Belorussian and Voronezh beavers were used as breeding material in the first stages of translocations and, since the early 1950s, Belarus has become a major source of breeding mate rial. From 1948–1958, more than 3500 beavers were exported, including those from basins of the Sozh, Berezina, and Neman Rivers, i.e., 2628, 1005, and 643 animals, respectively. Seven hundred beavers were used simultaneously to expand the natural habitats of local Belorussian populations and populations from Vitebsk, Minsk, and Brest oblasts (Safonov and Pavlov, 1973; Stavrovskii, Vatolin, 1979). Animals from Vor onezh comprised no less than 40% of the number of the introduced beavers. More than 12000 beavers were introduced altogether on the area of Russia (Savel’ev, 2003). As for the taxonomical aspect, the introduced animals were classified to two subspecies, i.e., Castor fiber orientoeuropaeus, the Eastern European beaver, and Castor fiber belorussicus, a Belorussian beaver (Lavrov, 1981). The subspecies status for Belorussian and Voronezh beaver populations was first proposed by L.S. Lavrov in 1974 and again later in 1981 based on the morphological differences and the longterm iso lated existence under different natural climatic condi tions. Nevertheless, to date, this system is under dis 84
PATTERNS OF MORPHOLOGICAL VARIABILITY IN REINTRODUCED POPULATIONS
ogy as a consequence of the action of a number of microevolutionary factors. Different types of natural selection and stochastic factors, which have no certain direction, i.e., the founder effect, bottleneck effect, genetic drift (Zavadskii, 1968; Mair, 1974; Nei et al., 1975; Altukhov, 2003), inbreeding (Müntzing, 1967), and physiological and genomic stresses (Sel’e, 1972; McClintok, 1978, in Nazarov, 2007), are among the major driving forces in the transformation of initial forms. It is quite likely that autochthon beavers were also affected by these factors taking into account their longterm insularization and the small size of local populations (Halley and Rosell, 2002). In geographic isolations, the expected microevolu tionary processes that emerged as a result of reintro duction must have provoked a genetic search (Chaik ovskii, 1976, in Nazarov, 2007) and led to substantial differentiation, which, according to A. Müntzing (1967), automatically emerges in isolation. From a phylogenetic point of view, the change of two or three dozen generations is an insignificant period; however, taking into account the randomly formed allelofond and the degree of stress, this may be sufficient for the emergence of the primary differences responsible for the direction the further morphogenesis. The aim of the present study is to assess the mor phological changes in cranial traits in autochthon C. f. orientoeuropaeus and C. f. belorussicus popula tions, as well as in daughter populations in relation to these populations (reintroduced populations). Some preliminary materials were published previously (Kor ablev N. et al., 2011).
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Metric and nonmetric variability was the object of analysis. When investigating the sizeadjust traits, only those that measure algorithms were used, which describe the variability in all morphological structures of a sample at once. An algorithm proposed by L.S. Lavrov (1960) with some modifications and sup plements was used as the basis (Korablev N. et al., 2011). Fifteen sizeadjust craniological traits were used, including nine bilaterally symmetrical traits with an accuracy of the measure in the range of 0.1–0.01 mm. In order to exclude the effect of a constant error for directed asymmetry in the bilateral measurements, the mean values from the right and left sides of traits were used. The measured results were processed using meth ods of variation statistics, including oneway ANOVA, stepwisediscriminant, canonicaldiscriminant, and cluster analyses; in the last case, the Euclidean metric was used to construct a dendrogram with nearest neighbor indexing (Puzachenko, 2004). In order to detect micro and macrogeographical variability, dis criminant analysis was performed for single samples and upon being combined into groups (autochthon and reintroduced). Skulls of males and females were analyzed together, because sexual size dimorphism was not revealed for the used measurements (Korablev N., 2005). In order to characterize interpopulation differ ences in dimensional proportions, skulls of animals aged 2.5 years and older were used. The age was deter mined by assessing the degree of closure of the basal Table 1. Geographic origin, collecting period, and number of specimens (in brackets) for each population
MATERIALS AND METHODS Osteological collections were studied that contain routine samples from populations of beavers captured in a fixed point of time. The collected material used in the study is kept in the Stock of the Central Forest, Voronezh, Berezina Biosphere Nature Reserves, and the Zoological Museum of Moscow State University (Table 1). All populations have a welldocumented history (Safonov, Pavlov, 1973). The investigated material was divided into two groups, i.e., (1) C. f. orientoeuropaeus, autochthons from the Voronezh river basin, which reintroduce animals in the Volga and Zapadnaya Dvina River Basins (Central Forest Nature Reserve, Tver’ oblast), Okskij (Oka Nature Reserve, Ryazan’ oblast), and Mordovskij Nature Reserve (Mordoviya) and (2) C. f. belorussicus, autochthons of Berezina, Sozh, and Neman River Basins and introduced in Desna (Bryansk oblast), Velikaya (Pskov oblast), and Cheka River Basins, inflows of the Tara River, Irtysh River Basin (Novosibirsk oblast), Chertola River, and an inflow of the Vasyugan River (Tomsk oblast). A total of nine samples were used from geographical popula tions, the distance between which varied from 100 to 3500 km (Fig. 1). BIOLOGY BULLETIN REVIEWS
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Number of the sample
Origin
Period of sampling
1
Voronezh Nature Reserve (85)
1975–1998
2
Okskij Nature Reserve (255)
1968–1987
3
Central Forest Nature Reserve 1982–1997 (120)
4
Mordovskij Nature Reserve (73) 1963–1972
5
Pskov oblast (72)
1976–1989
6
Belorussia* (81)
1952–1956; 1974–1975
7
Bryansk oblast (13)
8
Novosibirsk oblast (48)
9
Tomsk oblast (25)
Total
1976 1973–1979 1976
772
* The material was collected from the basins of Berezina (66 specimens), Sozh (10), Neman (5) rivers (two were col lected in the first period of sampling).
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N.P. KORABLEV, P.N. KORABLEV
60°
30°
40°
50°
60°
70°
5
80° 8
3
9
6
2
4
6 6
7 1
50°
0
500
1000
km
Castor fiber belorussicus Castor fiber orientoeuropaeus
Fig. 1. Geographical origin of the samples. Numbers of samples correspond to those in Table 1.
opening in the pulp cavity in molar teeth, for animals older than 3 years by the layer structure of cementum in the apical part of the tooth (Safonov, 1966; Klevezal’, 1988). To assess nonmetric variability, 22 craniological traits (69 variations) were used. Odontologic traits were not used due to their age variability. All bilateral symmetrical traits were considered from both sides of the skull. The used traits do not depend on the sex or age of animals (Korablev P. et al., 1997; Korablev N., 2005, 2011). The following parameters were calculated based on frequencies of nonmetric trait occurrence: parame ters showing population similarity (r) by polymorphic traits (Zhivotovskii, 1979), intrapopulation polymor phism (μ), and shares of rare phenes (h) (Zhivotovskii, 1982) and fluctuating asymmetry (Zakharov, 1987). Cross tabulation was employed in order to detect the traits that are most significant for the segregation of populations, (Zaitsev, 1984). The χ2 value with Yates’s correction (for traits with two variations) was used to assess the reliability of the coefficient of trait associa tion with the geographical origin of the sample; the χ2 Pearson index was used for cases with a larger number of degrees of freedom. The results were considered sig nificant at p ≤ 0.05. The calculations were performed using Statistica 7.1 and MS Excel program software. In order to determine the pattern of trait inheritance and to detect the association between phenotypic (dis crete) traits with a genotype, we used an approach pro posed by V.N. Orlov and N.M. Okulova (2001) based on the frequencies of equilibrium alleles according to the Hardy–Weinberg equation. The frequencies of alleles were calculated using the Binomial_pq pro
gram for frequency analysis, which was kindly pro vided by V.N. Orlov. RESULTS AND DISCUSSION Comparative Study of Autochthon Populations: Morphometric Differences All investigated samples from different river basins of Belorussia are isomorphic by metric traits. The results of univariate dispersion analysis taking into account the region of material collection showed the following: Fisher’s criterion (F) is in the range of 0.09–2.91, which is considerably lower than the sig nificance level. The results of the performed analysis formally allow us to combine all skulls into one sample of the C. f. belorussicus subspecies. The region of Belorussia covered for collections includes the basins of the Neman, Berezina, and Sozh Rivers, with an area of approximately 40000 km2. The available material allowed us to detect differences between the samples of Belorussian beavers based on phenetic traits only. The population similarity parameter (r) showed the lowest values and varied from 0.842 ± 0.043 (when compared with those from Voronezh) to 0.893 ± 0.034 (when compared to Berezina Nature Reserve) in pairwise comparisons of animal skulls collected in the basins of the Neman and Sozh Rivers with the other beavers. The intrapopulation polymorphism was low, μ = 1.961 ± 0.263, and the fraction of rare phenes h = 0.351 ± 0.067 was the highest of all studied populations. At the next stage of analysis, the significance of the divergence of autochthon morphological form of C. f. orientoeuropaeus and C. f. belorusicus beavers was assessed. For this purpose, oneway ANOVA was car BIOLOGY BULLETIN REVIEWS
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ried out taking into account the region of collection. The results of the analysis indicate the high signifi cance of differences between populations by all metric traits with an exception of the length of the diastem. The F values varied from 5.6 for the postorbital con striction to 48.1 for the length of the upper row of teeth. The majority of traits contribute significantly to interpopulation differences, the F criterion of which is no less than 27. The quantitative assessments of variability (mean sizes and limits given by squared standard deviation) are presented in Table 2. In the majority of their traits, Eastern European beavers are larger than Belorussian beavers. The differ ences in traits such as diastem length and postorbital constriction are minimal and, for the first trait, the forms of autochthon differ insignificantly. A relatively weak variability is characteristic of the length of upper and lower rows of teeth, which is likely related to lim ited variability due to the close correlations and the functional significance of these morphological struc tures of the skull. When expressed in percents, these differences were found to be in the range of 2.27 (diastem length, the difference is insignificant) to 8.59% (the rostrum length). The mean differences between the populations by significant traits com prised 5.96%. For a more complete analysis of differences taking into consideration many variables, a forward stepwise discriminant analysis with F to enter 1 and 0 to remove was applied. During the selection of traits that are sig nificant for population divergence, nine variables were picked out as having the highest discrimination level (Table 3). Based on the value of F and Wλ criterions, when using multivariate discriminant analysis, the most sig nificant traits are the lengths of the nose bones, skull, upper jaw, and the upper row of teeth. The coefficient of determination and tolerance indicate a close corre lation of traits used to construct a discriminant analy sis model. When classifying the species using the mea surements taken for the analysis, the quality of distin guishing animals from autochthon populations in discriminant analysis approaches 100% (p ≤ 0.005). By common proportions, the skull of Eastern European beavers is longer into the length, the skull of Byelorussian beavers is shorter in the rostrum length, but wider in zygomatic width, mastoid width, and ros trum. The values of common dimensional proportions coincide with the data by L.S. Lavrov (1981) and con firm morphological differences of two autochthon populations with a high level of significance. Phenogenetic Variability of Autochthon Populations. When studying the phenetic structure of populations, the frequencies of two trait variations turned out to demonstrate a high level of difference. The frequency of the FMPc phene occurrence, which encodes the configuration of the back maxillary opening, was BIOLOGY BULLETIN REVIEWS
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Table 2. Mean values and limits of craniological traits in autochthon populations Castor fiber Trait
C. f. orien C. f. belorussi Differ toeuropaeus cus ences, %*
Total skull length 138.76 ± 0.91 129.22 ± 1.17
6.88
125.4–151.0 119.6–147.3 Rostrum length
61.73 ± 0.47 56.43 ± 0.64 55.2–69.3
Nose bone length
49.5–65.6
58.33 ± 0.42 55.51 ± 0.66 49.6–64.2
8.59
4.83
47.7–63.5
Length of the 33.35 ± 0.18 31.37 ± 0.22 upper row of teeth 30.1–36.3 29.5–34.8
5.94
Upper diastem length
2.27
44.13 ± 0.41 43.13 ± 0.47 39.6–50.3
35.1–49.6
Total length of the 106.74 ± 0.69 100.37 ± 0.90 upper jaw 95.6–118.4 91.5–112.9
5.97
Rostrum width
3.91
28.93 ± 0.19 27.80 ± 0.24 22.1–32.0
Postorbital constriction
25.3–32.8
27.32 ± 0.18 26.62 ± 0.23 20.8–30.1
22.6–31.0
Zygomatic width 100.13 ± 0.71 93.33 ± 0.92 90.4–113.0 Brain capsule width Mastoid width
Length of the lower row of teeth
7.16
64.0–96.1
36.97 ± 0.19 35.21 ± 0.21 33.4–39.4
4.66
43.7–50.7
76.96 ± 0.60 71.45 ± 0.70 67.4–90.5
6.79
81.9–102.6
48.32 ± 0.25 46.07 ± 0.25 45.4–52.2
2.56
4.76
33.0–39.8
Total length of the 109.01 ± 0.80 101.88 ± 0.75 lower jaw 98.75–118.7 94.6–114.9
6.54
Lower jaw length 100.31 ± 0.75 93.12 ± 0.86
7.17
91.4–110.5 Lower jaw height
84.7–106.3
61.57 ± 0.46 56.99 ± 0.77 57.1–67.6
7.71
52.8–69.7
* The differences between subspecies are statistically significant by the measurements presented in the table.
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Table 3. List of measurements included in model of discriminant analysis and their statistical characteristics Wλ
Particular Wλ
Fisher’s criterion
Significance
Tolerance
Coefficient of determination
Rostrum width
0.207
0.916
8.490
0.004
0.021
0.979
Nose bones length
0.242
0.786
25.321
0.000
0.084
0.917
Skull length
0.230
0.825
19.759
0.000
0.027
0.974
Postorbital constriction
0.205
0.925
7.539
0.007
0.362
0.638
Length of upper row of teeth
0.222
0.854
15.894
0.000
0.077
0.923
Diastem length
0.209
0.908
9.470
0.003
0.030
0.970
Lower jaw length
0.208
0.915
8.606
0.004
0.011
0.989
Upper jaw length
0.211
0.901
10.255
0.002
0.023
0.977
Height of lower jaw
0.200
0.950
4.896
0.029
0.179
0.821
Trait
Note: Wilks’ Lambda (Wλ) = 0.19; F = 24.779; p < 0.0000.
increased in Belorussian beavers compared to Eastern European beavers (0.02); the same trend is character istic of the a variation of the CMP trait (the presence of a contact M3 with the palatine bone) by 0.17 and 0.55, respectively. With regard to the domination of many phenes, differences between autochthon populations reach a higher value. The change in a dominant phene is observed for CIF, USO, SSP, and CMM traits, which encode the form and configuration of suture of a skull and the amount of openings for nerve and blood vessel passage. In other cases, changes in domination did not occur; nevertheless, the proportions of single phene presence exert a clear fluctuation. In addition, differ ences are expressed in the changes of dominant phene frequencies (2.9% of the quantity of variations), along with the presence of marker phenes, which occur with minimal frequency. The population similarity param eter (r) in a pairwise comparison of Eastern European and Belorussian beavers was found to be 0.94 ± 0.03, which corresponds to a 6% difference by the pheno type. The μ parameters are 2.134 ± 0.123 and 2.412 ± 0.367 indicate a higher level of polymorphism in Belorussian beavers. The percentage of rare phenes h of C. f. orientoeuropaeus is 0.256 ± 0.082, which is slightly higher than for C. f. belorussicus = 0.220 ± 0.048. Comparative Study of Reintroduced Populations: Phenogenetic Variability In several dozen generations of animals living in artificially created habitations, no significant rear rangement in the phenofund structure occurred, and changes were only recorded in six dominant phenes, i.e., 8.7% of the total number of variations. Novel vari
ations in the traits of reintroduced populations do not tend to increase frequency, and their occurrence com prises 1–9%. The differences in the phenofund struc ture based on the traits that are most significant for the division of populations (χ2 = 101.23–430.15; p < 0.001) are represented graphically using lobbed charts (Fig. 2). The average phenetic structure of reintro duced animals (schemes I and II) allow one to com pare their integrated phenetic appearance with autochthon maternal populations. The results of a comparison indicate the preservation of the initial phenetic structure in the lineage of Eastern European beavers and more significant changes in the popula tions of Belorussian reintroduced animals. In the reintroduced populations, compared to autochthon populations, a decrease in the phenetic diversity occurred, e.g., in the Central Forest and Okskij Nature Reserves, the total number of variations decreased by seven and nine, respectively. In reintro duced populations, only three novel variations appeared that occur with minimal frequency. The opposite trend is observed in reintroduced Belorussian beavers in which the number of phenes increased by four times. Although averaging the frequency of phene appear ance in the formed habitations does not provide the complete reconstruction of the phenofund of maternal populations, it significantly approaches it. This is evi dence that changes in the morphological appearance of reintroducing animals occurred mainly in the scope of the formed phenofund of autochthon populations. More expressed changes in the Berezina lineage of beavers may be accounted for by both the higher het erogeneity of the initial breeding material compared to the one of Voronezh and the higher number of animals BIOLOGY BULLETIN REVIEWS
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I (b)
(c)
1.0
1.0
0.5
0.5
(e)
(a)
USOs
1.0
NMMd 0.5
CMMc
1.0
FSTm CFTc
0.5
CFOf
CIFh
OAId FFPa
FHPd FMPc
1.0
FCBu
(d)
0.5
Fig. 2. Structure of autochthon and reintroduced populations of beavers by frequency of expression of 12 phenetic variations. Traits encode morphological manifestations of variations in structure of sutures (USO, FST, CIF, FFP), openings (CFT, FHP, FCP, FMP, CFO, CMM, NMM), and presence or absence of an additional bone (OAI) on animal skulls. Encoding of traits corre sponds to the catalogue of phenes (Korablev P. et al., 1997). Designations for diagrams on the scheme I: (a) population of Voron ezh Nature Reserve, (b) population of Okskij Nature Reserve, (c) population of Central Forest Nature Reserve, (d) population of Mordovskij Nature Reserve, (e) mean frequencies of traits for reintroduced populations. Interpretation of diagrams on scheme II: (a) population of Berezina Nature Reserve, (b) population of Pskov oblast, (c) population of Bryansk oblast, (d) population of Novosibirsk oblast, (e) population of Tomsk oblast, (f) mean frequencies of traits for reintroduced populations. Numbers on axis designate percentage of occurrence of trait in shares of a unit.
preserved in the basin of the Berezina River, as well as their settlements into a wider range of ecological con ditions. The values of the r criterion between pairs of popu lations varied in the range of 0.900–0.970 and with the exception for pairs from Bryansk–Mordoviya and Bryansk–Berezina are significant (significance level W = 0.001). A hierarchical classification of popula tions was performed based on the matrix of pairwise differences of populations by the r criterion using a cluster analysis (Fig. 3). BIOLOGY BULLETIN REVIEWS
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Cluster dendrograms correspond to the origin of Belorussian and Eastern European population, except the sample from the Pskov oblast (Velikaya river basin). This sample belongs to C. f. orientoeuropaeus in its pat tern of phenetic variability. The reason for the false classification should be sought in the hybrid origin of this population. During the formation of the point of habitation, Belorussian animals were initially used, after which the beavers of the Voronezh origin were released (Ivanov et al., 2006). It is significant that, in their morphometric traits, the animals of this sample completely correspond to the Belorussian subspecies
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(b)
(c)
1.0
0.5
0.5
(f)
(a)
USOs NMMd
1.0
1.0 0.5
CMMc 0.5
CFOf
FSTm CFTc CIFh FHPd
OAId FFPa
FCBu FMPc
1.0
1.0
(e)
(d)
0.5
0.5
Fig. 2. (Contd.)
with a minimal difference from beavers of the Berezina River Basin. The pattern of inheritance was assessed for traits with three phenetic variations that correspond to the binomial term distribution formula in binomial expansion (p + q)2 = p2 + 2pq + q2. Six traits corre spond to the following conditions: USO, FIO, FMP, FPA, EFP, and FST. Of these conditions, FST and FIO encode the configuration and the number of openings for nerve and blood vessel passage on a skull; the inter pretation of other traits is given in Fig. 2. The mean frequencies for three variations of the FST and FIO traits and the theoretically predicted numbers of gen otypes turned out to be quite close. The observed fre
quency of u, d, i variations for the FIO trait comprised 0.95, 0.14, and 0.01, respectively, in shares of a unit; the expected number is 0.96, 0.14, and 0.01. The sum of squared deviations is 1.57. The frequency of p and q genes is 0.93 and 0.07. For the FST trait, the observed frequencies of m, a, l variations were found to be 0.82, 0.15, and 0.04. The expected frequency differs slightly, but it lies quite close to the frequencies observed at 0.79, 0.20, and 0.01. The sum of squared deviations is 43.44, and the frequency of genes p = 0.89 and q = 0.11. The coincidence of genotype fre quencies is observed in the simple inheritance of traits with two alleles or two groups of alleles of one gene. The observed frequencies of phenes of the rest of the BIOLOGY BULLETIN REVIEWS
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All of the dimensional traits displayed a significant correlation with the region of collection, which is indicative of marked geographical structuredness. The results of a oneway ANOVA suggest high F values that vary from 8.51 for diastem length to 43.06 for rostrum width. The trends in the variability for the common dimensional traits that are most significant for popula tion divergence are shown in Fig. 4. The metric variability has no definite direction, since in the reintroduced populations, there are no definite regularities in morphological transformations. In the Eastern European populations of beavers, the sizes only increased in the population of the Central Forest Nature Reserve. In the Mordovskij and Okskij Nature Reserves, the skull sizes decreased compared to autochthons. In the reintroduced populations of Belorussian beavers, the skull sizes increased most sig nificantly in Siberia and the Bryansk oblast. When variability was assessed based on the entire set of traits (Fig. 5), significant changes were docu mented in daughter populations of C. f. orientoeuro paeus in animals of the Mordovskij Nature Reserve, the skull of which became shorter while maintaining the same width; in other populations, the changes are less largescale and only affect various morphological structures. The skulls of the majority of reintroduced C. f. belorussicus populations became larger in com mon dimensional parameters than in animals of the maternal population. This trend is especially marked in the beavers of the Desna River Basin (Bryansk oblast). The skulls of animals that inhabit the Cheka (Novosibirsk oblast) and Chertola (Tomsk oblast) Riv ers became wider in the location of the rostrum, zygo matic arch, mastoid width, and brain capsule with an insignificant increase in length. Differences between beavers of the Berezina Nature Reserve and Pskov oblast are insignificant by a set of traits. Canonical discriminant analysis allows conclu sions to be drawn on the continuous variability of rein troduced populations C. f. orientoeuropaeus and C. f. belorussicus (Fig. 5). Eastern European beavers differ to a greater degree by the length of the skull, nose bones, rostrum, lower row of teeth, lower jaw, and the width of upper jaw. The length of the rostrum, height of the lower jaw, the width of the mastoid, the length of the upper row of teeth, and the length of the BIOLOGY BULLETIN REVIEWS
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Linkage distance
Morphometric Changes
300
200
150
100
50
9
7
8
6
5
4
3
2
1
Fig. 3. Hierarchical classification of populations of beavers based on r criterion. Numbers on abscissa correspond to numbers of samples presented in Table 1.
diastem are significant traits for the divergence of sam ples of Belorussian groups of populations. DISCUSSION AND CONCLUSION The study shows the high structuredness of autoch thon populations, which continues to remain in the reintroduced populations provided that their origin is pure. Both metric and nonmetric phenetic parameters allow one to confidently distinguish between C. f. belorussicus and C. f. orientoeuropaeus. Differ ences between animals of autochthon populations by the set of metric and nonmetric traits comprise 6%. The geographical and historical independence of these subspecies is obvious when taking into account their longterm phylogenetic history. On the whole, the Eurasian beaver Castor fiber is a multivalent species that exists in the form of several discrete adaptive norms, between which there are morphological hiatus and quite high molecular and genetical differences (Ducroz et al., 2005; Durka et al., 2005). The absence of significant differences in dimen sional proportions for the samples of Belorussian bea vers from three river basins deserves more attention. It is ambiguous that C. f. belorussicus proposed by L.S. Lavrov presumably combines three recent groups of beavers from various river basins that differ in the number of phenotypic traits (Samusenko and Fomenkov, 1983; Savel’ev, 2000). The combination of epigenetic parameters likely indicates that samples of at least two basins contained small groups of species that main tained morphological and genetical peculiarities at the expressed metapopulation structure of these species and, as a result of insularization and unavoidable inbreeding, they are characterized by a low level of ˆ
investigated traits deviated significantly from those expected in accordance with the Hardy–Weinberg theorem, which is typical of complex inheritance, e.g., when alleles are localized in different genes or at epistasis events. Therefore, we believe that the fre quency of the FST trait in radar charts most obviously demonstrates the quantitative character of genetical changes in beaver populations.
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polymorphism and high frequency of expression of rare phenes. In the Neman population, 48.1% of mel anists were recorded and, in the Sozh population, 21.6% were recorded (Samusenko and Fomenkov, 1983). The black color of beavers is a recessive trait (Lavrov, 1948), and these populations are therefore characterized by a relatively large number of recessive alleles that had an effect on the low level of interpopu lation diversity and the amount of rare phenetic aber rations. The recorded peculiarities of Belorussian ani mals serve evidence of the latest history of the species and, taking into account the current number of bea vers on the area of the republic (Kozlo et al., 2011), are most likely represent a historical artifact. Molecular and genetic studies of modern animals from various river basins should clear up more of the taxonomy of Belorussian beavers. Preliminary materials in this study have already been obtained (Savel’ev et al., 2011). The introduction of a small number of species taken from numerous populations leads to some decrease in the heterozygosity of founders’ descen dants. Nevertheless, as multiple examples of mammal translocations have shows, inbred depression among
these populations rarely occurs, which is evidence of adaptive mechanisms that help to protect against inbreeding (Sjöberg, 1996). The state of animals in artificially created populations may be judged by the level of the fluctuating asymmetry of discrete traits (Suchentrunk et al., 1998). The level of asymmetry characterizes the quality of the environment (Panka koski, 1985; Zakharov, 1987; Vasil’ev, 2005) and may have a wider array of causes, including endogenous factors of a genetic nature, primarily inbreeding (Ala dos et al., 1995), as well as be a general indicator of the physiological state of the organism (Cuervo et al., 2011). Autochthon populations are characterized by a lower level of fluctuating asymmetry of discrete traits, the mean value of which is 16.3% for the Voronezh and Berezina Nature Reserves. Nevertheless, in animals of recent populations from the Neman and Sozh River Basins, the fluctuating asymmetry is 26.5%, and pos sible reasons for this are discussed above. The mean value of fluctuating asymmetry is 22.9% for all reintro duced populations. It is characteristic that the highest value of 27.5% was recorded for the population from the Central Forest Nature Reserve. This population differs by a small number of founders (eight beavers) BIOLOGY BULLETIN REVIEWS
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Fig. 5. Canonical discriminant analysis of beavers of two autochthon morphological forms (a) is C. f. orientoeuropaeus, (b) is C. f. belorussicus) and their descendants. Coordinate system is two first axes of discriminant analysis. Ellipses represent interval of 95% confidence. Numbers correspond to numbers of samples in Table 1. BIOLOGY BULLETIN REVIEWS
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reintroduced into suboptimal conditions of the envi ronment. The morphological anomalies of the teeth system are often regarded as disturbances of onthogenesis under the effect of genetic and external factors (Wol san, 1984; Szuma, 1999), as well as inbreeding, are indicated as possible causes (Bouwmeester et al., 1989). The anomalies of the teeth system were diag nosed with a higher frequency in beavers of aborigine populations, i.e., 12.9% in Voronezh and 8.2% in the Berezina Nature Reserves. The mean frequency of anomalies was found to be 2.6% in the reintroduced populations. In all cases, deviations are expressed in anomalies of the regular teeth formula (oligodontia) and the asymmetry of tooth position in arcades. The parameters that characterize the degree (μ) and structure (h) of the interpopulation polymor phism of discrete traits may serve as integrated charac teristics of the studied samples. The level of polymor phism in Berezina beavers is slightly higher than in those Eastern European beavers, and the percentage of rare phenes is lower. On average, the degree of the interpopulation polymorphism in autochthon popula tions of beavers is higher (μ = 2.19) than in reintro duced populations (μ = 2.12); in addition to this, in many populations, the number of variations in traits does not decrease. In the local samples we studied, except Bryansk oblast, polymorphism is significantly lower than in the animals that inhabit Lithuania (Ulevicius, 1997), in which the value of μ varied in the range of 2.33–2.64 in nine spaced, isolated groups of beavers, with the highest value was recorded for bea vers of mixed origin, while the least value was recorded for the population with a low number of founders and an expressed bottle neck effect. The molecular genetic studies of beavers that inhabit Eurasia after the maximum of the last glaciation showed the presence of haplotypes, which have not been detected for cur rently living animals (Horn et al., 2009), which indi cates the substantial influence of the bottleneck effect, which determines genetic variability in currently living beavers. The high level of interpopulation polymor phism (μ = 2.41) in beavers of the Desna River Basin is determined by the history of species restoration in Bryansk oblast. The animals of the Berezina popula tion (Stavrovskii and Vatolin, 1979), Voronezh popu lation, and likely aboriginal beavers preserved in the tributaries of the Desna River (Aleinikov, 2010) partic ipated in the formation of the local population of bea vers. The beavers of this sample also differ in size from Belorussian animals. The autochthon (h = 0.24) and reintroduced (h = 0.26) populations slightly differ by the incidence of the expression of rare phenes. The increased level of rare aberrations may indicate the use of a socalled mobili zation reserve (Dubinin, 1986), i.e., a reserve of vari ability that was not needed under relatively stable liv ing conditions. In addition, in populations in contact areas, as well as in populations that have passed
through the stage of low abundance, rare phenetic variations are known to be expressed more often than in large panmixed populations. V.N. Orlov and N.M. Oku lova (2001) note that the cause of this may lie in the expression of a frequently occurring allele in the homozygote state. In our case, the increase in the inci dence of rare phenetic variations may be considered an indicator of inbreeding. During the isolated development of reintroduced animals, they preserve the main traits of the initial sub species, which follows from an analysis of the phenetic structure of populations. During the formation of daughter populations by various subspecies, their mor phometric traits deviate from the initial subspecies forms. The undefined taxonomic status of many reintroduced populations of beavers reflected by A.P. Savel’iev (2003) in a palliative title Castor fiber introductsus or G. Schwab in Castor fiber europaeus is partly explained by their hybrid origin. A similar situation is observed for the Canadian beaver Castor canadensis Kuhl. Due to huge extermination by humans or mixing as a result of migration, some forms of subspecies have become extinct (Gabrys and Wa z na, 2003). ˆ
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An increase in the morphological variability in autochthon descendants may be accompanied by the diversity of adaptive norms implemented in a wide variety of novel ecological conditions under which the animals come to live (Mednikov, 1987). The increase in size of many reintroduced populations of beavers was observed by a number of researchers (Stavrovskii, 1986; Solov’ev, 1991, Savel’ev, 2003, Monakhov, 2010). A similar pattern was established for the rein troduced population of sable (Monakhov, 1999). S.S. Schwartz (1959) recorded that the introduced species and their descendants occupy free ecological niches and, therefore, are not affected by interspecific and intraspecific competitions. The formation of novel populations using artificial introductions is a model for the restoration of popula tion abundance following its sharp decrease. In addi tion, contrary to a gradual decrease in small popula tions, the genotypes of the founder species of a novel colony at the intensive growth in the abundance of the population have no time to lose their reserves of vari ability. The great reserve of genetic variability in natu ral populations is an important factor, which favors the maintenance of heterozygosity at a level sufficient to protect against inbred depression during the formation of a novel settlement of animals. In the case with bea vers, the introductions of even small groups of animals under suboptimal conditions did not result in an inbred depression (Korablev N. et al., 2011). An anal ysis of the results of reintroductions in Europe also did not reveal inbred depression in artificially created pop ulations; nevertheless, in many autochthon popula tions, the signs of inbreeding were detected (Halley, 2011). BIOLOGY BULLETIN REVIEWS
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REFERENCES Alados, L.A., Escós, J., and Emlen, J.M., Fluctuating Asymmetry and Fractal Dimension of the Sagittal Suture as Indicators of Inbreeding Depression in Dama and Dorcas Gazelles, Can. J. Zool., 1995, vol. 73, no. 10, pp. 1967–1974. Aleinikov, A.A., Extended Abstract of Cand. Sci. (Biol.) Dis sertation, Togliatti: Inst. Ekol. Volzhsk. Basseina RAN, 2010. BIOLOGY BULLETIN REVIEWS
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The authors thank the collaborators from Voron ezh, the Berezina Nature Reserve, supervisors of col lections from the Zoological Museum of Moscow State University for their help in work with the collec tion fund. We sincerely thank A.P. Savel’ev for con structive commentaries and recommendations in the article (AllRussia Research Zhitkov Institute of Hunting Farm and Animal Breeding, Russian Acad emy of Agricultural Sciences).
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ACKNOWLEDGMENTS
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The microevolutionary processes in the studied geographical isolations may be characterized as low intensive and weakly directed. The beavers were released in places of traditional habitation in a near past, which can be estimated as optimal. K.M. Zavad skii indicated that “in some or many cases, spaced iso lation is not a contributing factor, only an accompany ing factor. Selection will be the contributing factor in relation to sets of spaceseparated climate and biotic conditions” (Zavadskii, 1968, p. 350 [in Russian]). S.S. Schwartz (1980) considered ecological factors to play a leading role in the processes of evolutionary transformations. I.I. Shmal’gauzen (1983) believed that ecological differentiation plays the most significant role in the initial divergence of forms. A.G. Vasil’ev et al. (2010) showed that similar ecological requirements of the environment lead to historical singledirection transformations of homological morphostructures in various species. A comparative analysis of microevolutionary pro cesses in reintroduced prepopulations of beavers also allow us to consider that, to a large extent, the intraspecific differentiation is due to adaptive variabil ity (adaptatiogenesis), but not random molecular genetic processes (gene drift) or significant changes in the genotypes of autochthon forms. The memory of genetic traits of the maternal population (Altukhov et al., 1997) is preserved in daughter populations, even in the absence of clear gene immigrations and, more importantly, at an initially low number of carriers of genetic information. At the same time, some differ ences in metric and nonmetric traits indicate a cer tain peculiarity of the groups, which favors the devel opment of a structured subdivided population and has a higher stability compared to the panmixed structure less population (Altukhov, 2003).
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