Cryptic variation in mole voles Ellobius (Arvicolinae,Rodentia) of Mongolia

The mole vole subgenus Ellobius is currently considered to include three species: Ellobius talpinus (distributed from SE Europe and Turkmenistan through Kazakhstan to SW Siberia), Ellobius alaicus (S Tianshan, Pamir-Alay) and Ellobius tancrei (East and West Central Asia, from the Amu-Darya to Mongolia and N China). A study focusing on the genetic variation in Ellobius from Mongolia was conducted using one mitochondrial and three nuclear markers. Two divergent allopatric lineages endemic to East Central Asia were revealed. The first lineage occurs from Dzungaria eastwards to central Mongolia and represents E. tancrei sensu stricto. The second lineage is found in East Gobi only and corresponds to a taxon described as Ellobius orientalis, which has been traditionally treated as a subspecies of E. tancrei. However, molecular and chromosome data indicate that orientalis is related not to E. tancrei but to E. talpinus, which is separated from the former by a distribution gap of ~2,000 km. The taxonomic status of the East Gobi mole vole is ambiguous, and its genetic distance from E. talpinus s. str. falls into the range characteristic for closely related vole species or semi-species. According to molecular estimates, the two taxa have been isolated since the late Middle Pleistocene. A similar divergence is observed between the East and West Central Asian lineages of E. tancrei. E. alaicus is placed as sister to the latter rendering E. tancrei sensu lato paraphyletic. The revealed phylogeographic pattern implies that East Central Asia was colonized by mole voles through multiple eastward dispersal events.     

Surviving in the High Arctic: dental variation in a casually introduced population of Microtus rossiaemeridionalis (Arvicolinae,Rodentia) on Svalbard

A human‐mediated invasion of a temperate rodent Microtus rossiaemeridionalis on the High Arctic Archipelago of Svalbard in the first half of the 20th century provides an opportunity to explore extent and rate of morphological divergence over decades of isolation. We studied dental size and morphology in 124 voles captured on Svalbard (Spitsbergen) in 1997–2005 and compared the data to mainland conspecific populations across northern Eurasia. Both dental and cranial sizes in the Svalbard population fall within the limits of natural variation of the species. Dental morphology suggests that the population experiences strong effects of isolation as indicated by the significant increase in the frequency of rare dental morphs, possibly caused by inbreeding. No evidence for directional shift towards increased or decreased complexity of the morphotype dental patterns is revealed. Although the population on Svalbard is phenotypically different from the mainland populations (due to increased frequency of rare morphs), those differences are not enough to support the idea of initial rapid evolution related to colonization. The limited spatial extent and environmental homogeneity of suitable habitats on the island allowed the species to initially multiply but not to diversify so that the species exhibits phenotypic conservatism but suffers the consequences of small population size.     

Heterochromatin study and geographical distribution of Microtus species (Rodentia,Arvicolinae) from Greece

In a sample of 108 underground voles from 23 Greek localities, the species Microtus felteni, M. guentheri, M. rossiaemeridionalis and M. subterraneus were identified, based on external body morphology and karyotype. Moreover, the implemented C-banding staining technique revealed the heterochromatin distribution in the chromosomes of the above species. All M. guentheri (2n=54, FN=54) and M. rossiaemeridionalis (2n=54, FN=56) specimens displayed the typical karyotypes of these species, respectively. The M. subterraneus specimens belonged to the chromosomal race with 2n=52, FN=60 of this species, apart from a single individual that demonstrated a medium-sized, subtelocentric autosome in heterozygous condition (2n=52, FN=61). Furthermore, M. felteni individuals, trapped again after many years, were karyologically studied (2n=54, FN=56) and the C-banding pattern for this species is hereby presented for the first time. Finally, the study of meiotic preparations in M. guentheri and M. rossiaemeridionalis males verified the asynaptic behaviour of their sex chromosomes. The karyotype of the four studied Microtus species does not seem to have diversified much from the putative ancestral arvicoline karyotype (2n=56, FN=56). On the other hand, the heterochromatin accumulation in the sex chromosomes, particularly prominent in M. felteni and M. rossiaemeridionalis, represents this common tendency in several Microtus species.     

Multilocus phylogeny and taxonomy of East Asian voles Alexandromys (Rodentia,Arvicolinae)

Phylogenetic relationships, taxonomy and nomenclature issues within East Asian voles Alexandromys were addressed using comprehensive species samples, including all 12 valid species of the genus, and multilocus analysis. We examined the mitochondrial cytochrome b (cytb) gene and three nuclear genes in 36 specimens. Additionally, we examined a data set of 106 specimens using only the cytb gene. Our results did not confirm the aggregation of A. kikuchii, A. montebelli and A. oeconomus into a separate clade, namely the subgenus Pallasiinus. Analysis of incomplete lineage sorting using JML software highlighted both the cases of mitochondrial introgression and incomplete lineage sorting within the genus. Thus, the sister position of A. sachalinensis and A. maximowiczii in mitochondrial trees could be explained by mitochondrial introgression, while the sister position of A. limnophilus and A. fortis in mitochondrial trees could be successfully explained by incomplete lineage sorting. Very short genetic distances, together with an absence of monophyly, of the three species, A. evoronensis, A. mujanensis and A. maximowiczii, is supported by multiple morphological data, which indicates that these three taxa should be one species—A. maximowiczii. Analysis of genetic distances and tree topology revealed that three species of short‐tailed voles—A. middendorffii, A. mongolicus and A. gromovi—are more closely related to each other than to other established species of Alexandromys. The lacustrine vole, A. limnophilus, is closely related to the group of short‐tailed voles. Analysis of the type specimens of limnophilus and flaviventris confirmed that these taxa form one species together with A. l. malygini. Our results suggest that the mountains of western Mongolia are inhabited by a new taxon of short‐tailed voles of the same rank as middendorffii, mongolicus and gromovi—A. m. alpinus ssp. n.     

Morphological variation of the five vole species of the genus Microtus (Mammalia,Rodentia, Arvicolinae) occurring in Greece

Morphometric data for the five vole species of the genus Microtus living in Greece are old, sparse, poor and insufficiently analysed. This work aims to give the first comprehensive morphometric analysis of body and skull inter‐ and intraspecific variation for M. (M.) guentheri, M. (M.) rossiaemeridionalis, M. (Terricola) subterraneus, M. (T.) felteni and M. (T.) thomasi, applying multivariate statistics to 28 linear morphometric variables. It was based on ample material (202 adult individuals) using samples from localities that adequately cover the entire distributional range of each species in Greece. The five species and the two subgenera (Microtus and Terricola) were morphometrically clearly distinguished and discriminating variables were revealed. However, morphometrics did not provide robust criteria to infer phylogenetic relations among species. Furthermore, three species, M. (M.) guentheri, M. (M.) rossiaemeridionalis and M. (T.) thomasi, exhibited considerable intraspecific size or shape variation, which was mostly random and not associated with geographical proximity. Comparisons with data in the literature, mainly concerning populations of these species from adjacent areas, indicate that the Greek M. (M.) guentheri, M. (M.) rossiaemeridionalis and M. (T.) thomasi tend to be smaller than their conspecifics, while M. (T.) subterraneus and M. (T.) felteni are about equal in size to their Balkan relatives.     

Ecological and functional correlates of molar shape variation in European populations of Arvicola (Arvicolinae, Rodentia)

Lower first molar shape in Arvicola spp. at European level has been studied by means of Geometric Morphometrics. We took into account bioclimatic variables, size, lifestyle and phylogenetic relationships. We used Partial Least Squares and Phylogenetic Independent Contrasts in order to assess which factor affects the most molar shape morphology.Once the phylogenetic history was taken into account, climate resulted the most influencing factor in explaining molar morphology, followed by size. Molar shape is not related to lifestyle. Molar shape and size, even if different among species, are not phylogenetically structured. On the opposite, lifestyle depends on the phylogeny, and size and lifestyle are significantly related even considering phylogenetic relationships. Fossorial forms are significantly smaller than semi-aquatic ones, suggesting that they are less subjected to predator pressure of semi-aquatic species and that the two lifestyles are characterized by different allometric patterns.     

Morphological convergence and coexistence in three sympatric North American species of Microtus (Rodentia: Arvicolinae)

Aim  Niche theory predicts that ecologically identical species cannot stably coexist in local communities. My aim was to investigate morphological diversity as a possible factor enabling the coexistence of a species-rich Microtus (Rodentia: Arvicolinae) fauna in a hotspot of North American mammalian diversity, the Greater Yellowstone Ecosystem (GYE).
Location  The Greater Yellowstone Ecosystem, North America.
Methods  Using in-hand morphological measurements of size and shape, I compared the morphologies of three North American vole species ( Microtus spp.), in sympatry in the GYE and in allopatry across their ranges, in order to examine: (1) whether morphologies are fixed or plastic and (2) the degree of morphological character displacement or convergence in sympatric species.
Results  Support was found for plasticity of morphology for all three vole species: M. longicaudus , M. montanus and M. pennsylvanicus. However, Microtus individuals of all species from the GYE area of sympatry were more similar to each other than to allopatric individuals of the same species.
Main conclusions  Competition among these congeners is not manifested in morphological overdispersion. The response of these congeneric species to the same local ecological conditions is convergent. The relative strength of environmental conditions appears to be stronger than the strength of competitive interactions among the study species.     

Fluctuating asymmetry in bank vole populations (Rodentia, Arvicolinae) reflects stress caused by landscape fragmentation in the Mont-Saint-Michel Bay

In intensively farmed, reclaimed areas (polders) of Mont-St-Michel Bay, France, bank voles ( Clethrionomys glareolus ) live in fragmented hedgerows, where populations are small and dispersal rates and genetic diversity are low. These small populations are likely to have been exposed to potential environmental and/or genetic stress. The sensitivity of development to stress can be measured by fluctuating asymmetry (FA). FA was calculated for three samples from a disturbed area and one sample from an adjacent, more connected and undisturbed landscape. Size FA was estimated from 16 measurements of the skull and teeth whilst shape asymmetry was estimated from the skull alone. Bank voles in fragmented hedgerows of the disturbed area had a higher degree of FA than bank voles from the more extensive and more connected hedges of the undisturbed area. These results were confirmed by the study of shape asymmetry, body mass and centroid size of the skull. There were no differences in FA between the three disturbed area samples. We conclude that FA does not reveal differences in the development of bank voles living in isolation under different local conditions in the various parts of the disturbed area. However, FA may allow differentiation between populations from greatly contrasting landscapes.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80, 37–44.     

The complete mitochondrial genome of Microtus fortis calamorum (Arvicolinae, Rodentia) and its phylogenetic analysis

Microtus fortis is a special resource of rodent in China. It is a promising experimental animal model for the study on the mechanism of Schistosome japonicum resistance. The first complete mitochondrial genome sequence for Microtus fortis calamorum, a subspecies of M. fortis (Arvicolinae, Rodentia), was reported in this study. The mitochondrial genome sequence of M. f. calamorum (Genbank: JF261175) showed a typical vertebrate pattern with 13 protein coding genes, 2 ribosomal RNAs, 22 transfer RNAs and one major noncoding region (CR region).The extended termination associated sequences (ETAS-1 and ETAS-2) and conserved sequence block 1 (CSB-1) were found in the CR region. The putative origin of replication for the light strand (O(L)) of M. f. calamorum was 35bp long and showed high conservation in stem and adjacent sequences, but the difference existed in the loop region among three species of genus Microtus. In order to investigate the phylogenetic position of M. f. calamorum, the phylogenetic trees (Maximum likelihood and Bayesian methods) were constructed based on 12 protein-coding genes (except for ND6 gene) on H strand from 16 rodent species. M. f. calamorum was classified into genus Microtus, Arvcicolinae for the highly phylogenetic relationship with Microtus kikuchii (Taiwan vole). Further phylogenetic analysis results based on the cytochrome b gene ranged from M. f. calamorum to one of the subspecies of M. fortis, which formed a sister group of Microtus middendorfii in the genus Microtus.     

Sex chromosome variability outlines the pathway to the chromosomal evolution in Microtus thomasi (Rodentia, Arvicolinae)

The underground vole Microtus thomasi , a Balkan endemic, displays remarkable variability in sex chromosome size and morphology. In the present study, we demonstrate this variability in two of its chromosomal races with 2 n  = 44 (i.e. 'thomasi' and 'atticus') with the use of C-banding on a sample of 189 individuals from 50 localities of Greece. In 'thomasi', five different, acrocentric X chromosome variants (X₀–X₄) are described, which differ significantly in size, due to heterochromatin addition. Also, three Y chromosome variants are described (Y₀–Y₂), ranging in size from very small (Y₀) to large (Y₂). The 'atticus' race displays three subtelocentric variants of the X chromosome (X_st0–X_st2), which differ in arm length ratio and heterochromatin content. In Peloponnesus, males of this race exhibit Y₀ and Y₁, whereas, in Attiki (south-east Sterea Ellada), males carry the small metacentric, Y_m. Overall, there is a trend towards sex chromosome size increase in a south to north direction. We propose that the last glaciation must have restricted M. thomasi to a refugium in southern Peloponnesus. During post-glacial colonization, limited northward expansion of its distribution area must have been accompanied by consecutive heterochromatin addition, which is proven today by comparatively larger sex chromosomes in the northern populations of 'thomasi' and 'atticus' in Greece than in their southern populations.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 685–695.     

Molecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences

Voles of the genus Microtus represent one of the most speciose mammalian genera in the Holarctic. We established a molecular phylogeny for Microtus to resolve contentious issues of systematic relationships and evolutionary history in this genus. A total of 81 specimens representing ten Microtus species endemic to Europe as well as eight Eurasian, six Asian and one Holarctic species were sequenced for the entire cytochrome b gene (1140 bp). A further 25 sequences were retrieved from GenBank, providing data on an additional 23, mainly Nearctic, Microtus species. Phylogenetic analysis of these 48 species generated four well-supported monophyletic lineages. The genus Chionomys, snow voles, formed a distinct and well-supported lineage separate from the genus Microtus. The subgenus Microtus formed the strongest supported lineage with two sublineages displaying a close relationship between the arvalis species group (common voles) and the socialis species group (social voles). Monophyly of the Palearctic pitymyid voles, subgenus Terricola, was supported, and this subgenus was also subdivided into two monophyletic species groups. Together, these groupings clarify long-standing taxonomic uncertainties in Microtus. In addition, the "Asian" and the Nearctic lineages reported previously were identified although the latter group was not supported. However, relationships among the main Microtus branches were not resolved, suggesting a rapid and potentially simultaneous radiation of a widespread ancestor early in the history of the genus. This and subsequent radiations discernible in the cytochrome b phylogeny, show the considerable potential of Microtus for analysis of historical and ecological determinants of speciation in small mammals. It is evident that speciation is an ongoing process in the genus and that the molecular data provides a vital insight into current species limits as well as cladogenic events of the past.     

DNA barcoding of Murinae (Rodentia: Muridae) and Arvicolinae (Rodentia: Cricetidae) distributed in China

Identification of rodents is very difficult mainly due to high similarities in morphology and controversial taxonomy. In this study, mitochondrial cytochrome oxidase subunit I (COI) was used as DNA barcode to identify the Murinae and Arvicolinae species distributed in China and to facilitate the systematics studies of Rodentia. In total, 242 sequences (31 species, 11 genera) from Murinae and 130 sequences (23 species, 6 genera) from Arvicolinae were investigated, of which 90 individuals were novel. Genetic distance, threshold method, tree‐based method, online BLAST and BLOG were employed to analyse the data sets. There was no obvious barcode gap. The average K2P distance within species and genera was 2.10% and 12.61% in Murinae, and 2.86% and 11.80% in Arvicolinae, respectively. The optimal threshold was 5.62% for Murinae and 3.34% for Arvicolinae. All phylogenetic trees exhibited similar topology and could distinguish 90.32% of surveyed species in Murinae and 82.60% in Arvicolinae with high support values. BLAST analyses yielded similar results with identification success rates of 92.15% and 93.85% for Murinae and Arvicolinae, respectively. BLOG successfully authenticated 100% of detected species except Leopoldamys edwardsi based on the latest taxonomic revision. Our results support the species status of recently recognized Micromys erythrotis, Eothenomys tarquinius and E. hintoni and confirm the important roles of comprehensive taxonomy and accurate morphological identification in DNA barcoding studies. We believe that, when proper analytic methods are applied or combined, DNA barcoding could serve as an accurate and effective species identification approach for Murinae and Arvicolinae based on a proper taxonomic framework.     

X-Y chromosome synapsis and recombination in 3 vole species of Asian lineage of the genus Microtus (Rodentia: Arvicolinae)

The pattern of X-Y chromosome pairing in male meiosis is an important taxonomic feature of grey voles of the genus Microtus. Asynaptic sex chromosomes have been found in the majority of species of the Palearctic phylogenetic lineage of this genus, while normal X-Y synapsis has been observed in the species of subgenus Pallasiinus belonging to the Asian phylogenetic lineage. We analyzed sex chromosome pairing and recombination in M. maximowiczii, M. mujanensis and M. fortis which also belong to the Asian phylogenetic lineage (subgenus Alexandromys). Using immunostaining for the proteins of the synaptonemal complex (SCP3) and recombination nodules (MLH1) we demonstrated that X and Y chromosomes of these species paired and recombined in a short subtelomeric region. This indicates that the sex chromosomes of these species retain an ancestral fully functional pseudoautosomal region, which has been lost or rearranged in the asynaptic species of the genus Microtus.     

Relation between climatic fluctuation and morphological variability in Microtus (Terricola) grafi (Arvicolinae, Rodentia) from Bacho Kiro (Bulgaria, Upper Pleistocene)

Morphological variability within the species Microtus (Terricola) grafi is investigated in relation to the parameters of time and climate. Microtus (Terricola) grafi has been described from the Upper Pleistocene cave of Bacho Kiro (Bulgaria), which has yielded numerous teeth from several levels reflecting climatic fluctuations. The first lower molars are analyzed by 23 biometric variables so as to quantify tooth shape and its variation with time and climate. This morphological analysis reveals a number of shape indexes reflecting whether an individual lived in warm or cold conditions. The most significant result is that individuals living in warm conditions exhibit the more primitive feature of having a less tilted pitymyan rhombus.     

Ecophenotypic variation and phylogenetic inheritance in first lower molar shape of extant Italian populations of Microtus (Terricola) savii (Rodentia)

Seventeen extant populations of Microtus (Terricola) savii have been investigated for correlations of first lower molar shape to climatic variables by means of geometric morphometrics, and controlling for phylogenetic inheritance. Comparative methods revealed that climatic variables and phylogeography provide a very similar contribution to variation in first lower molars morphology, whereas tooth size does not appear to be affected by climatic conditions. Climate‐related changes have been recognized in the anteroconid portion of the tooth. This indicates that molar tooth variation is strongly influenced by climatic conditions, although in a complex way. Calabrian populations, often ascribed to Microtus (Terricola) brachycercus, form a distinct cluster, in agreement with the most recent genetic analyses. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 632–647.     

Supraspecies relationships in the subfamily Arvicolinae (Rodentia,Cricetidae): An unexpected result of nuclear gene analysis

Phylogenetic analysis of the supraspecies relationships was carried out using partial sequences of two nuclear genes in the subfamily Arvicolinae, which is one of the youngest and species-rich groups of myomorph rodents. The analysis with the new data resolved the majority of polytomy nodes in the phylogenetic trees reported for Arvicolinae, suggesting a gradual, rather than a saltatory, mode for their evolution. Mole voles Ellobiusini, steppe voles Lagurini, and gray voles Arvicolini were fount to be a monophyletic group that corresponds to the latest third wave of radiation within the subfamily. Red-back voles Myodini (=Clethrionomini) are a sister clade to this group and correspond to the second radiation wave. The order of divergence remained unresolved for the earliest radiation wave (Ondatrini, Prometheomyini, Dicrostonychini, and Lemmini). The close relationships observed for mole, gray, and steppe voles are unexpected and contradict the conventional views that Ellobiusini are an ancient group and are separate from all other voles on evidence of the extreme simplicity of their rooted molars and the peculiar structure of their skull and postcranial skeleton. It was assumed that many of these morphological characters indicate adaptation to subterranean life and provide no phylogenetic signal.     

Genetic structure,ecological versatility,and skull shape differentiation in Arvicola water voles (Rodentia,Cricetidae)

Water voles from the genus Arvicola display an amazing ecological versatility, with aquatic and fossorial populations. The Southern water vole (Arvicola sapidus) is largely accepted as a valid species, as well as the newly described Arvicola persicus. In contrast, the taxonomic status and evolutionary relationships within Arvicola amphibiussensu lato had caused a long-standing debate. The phylogenetic relationships among Arvicola were reconstructed using the mitochondrial cytochrome b gene. Four lineages within A. amphibiuss.l. were identified with good support: Western European, Eurasiatic, Italian, and Turkish lineages. Fossorial and aquatic forms were found together in all well-sampled lineages, evidencing that ecotypes do not correspond to distinct species. However, the Western European lineage mostly includes fossorial forms whereas the Eurasiatic lineage tends to include mostly aquatic forms. A morphometric analysis of skull shape evidenced a convergence of aquatic forms of the Eurasiatic lineage toward the typically aquatic shape of A. sapidus. The fossorial form of the Western European lineage, in contrast, displayed morphological adaptation to tooth-digging behavior, with expanded zygomatic arches and proodont incisors. Fossorial Eurasiatic forms displayed intermediate morphologies. This suggests a plastic component of skull shape variation, combined with a genetic component selected by the dominant ecology in each lineage. Integrating genetic distances and other biological data suggest that the Italian lineage may correspond to an incipient species (Arvicola italicus). The three other lineages most probably correspond to phylogeographic variations of a single species (A. amphibius), encompassing the former A. amphibius, Arvicola terrestris, Arvicola scherman, and Arvicola monticola.     

Allozyme variation in bank vole,Myodes glareolus (Mammalia: Rodentia) in Northern Anatolia

A total of 94 specimens from 16 populations of Myodes glareolus, collected between 2004 and 2007, from different altitudinal distributions were analyzed, using 16 enzyme systems. We found that 10 out of 22 loci (Idh-2, α-Gpdh, Me, Pgm, Pgd, Mdh-s, Ada, Est-1, Ldh-1, and Ldh-2) were polymorphic. Group 1 included population from altitudes ranging from 27 to 605 m above sea level (ASL), and Group 2 were from altitudes ranging from 1003 to 1288 m ASL. The summaries of the genetic parameters also displayed differences between the 2 groups. The possible reasons of such fragmentation between M. glareolus populations were discussed.     

Following the rivers: historical reconstruction of California voles Microtus californicus (Rodentia: Cricetidae) in the deserts of eastern California

The California vole, Microtus californicus, restricted to habitat patches where water is available nearly year‐round, is a remnant of the mesic history of the southern Great Basin and Mojave deserts of eastern California. The history of voles in this region is a model for species‐edge population dynamics through periods of climatic change. We sampled voles from the eastern deserts of California and examined variation in the mitochondrial cytb gene, three nuclear intron regions, and across 12 nuclear microsatellite markers. Samples are allocated to two mitochondrial clades: one associated with southern California and the other with central and northern California. The limited mtDNA structure largely recovers the geographical distribution, replicated by both nuclear introns and microsatellites. The most remote population, Microtus californicus scirpensis at Tecopa near Death Valley, was the most distinct. This population shares microsatellite alleles with both mtDNA clades, and both its northern clade nuclear introns and southern clade mtDNA sequences support a hybrid origin for this endangered population. The overall patterns support two major invasions into the desert through an ancient system of riparian corridors along streams and lake margins during the latter part of the Pleistocene followed by local in situ divergence subsequent to late Pleistocene and Holocene drying events. Changes in current water resource use could easily remove California voles from parts of the desert landscape.     

No relationship between canalization and developmental stability of the skull in a natural population of Mastomys natalensis (Rodentia: Muridae)

The aim of the present work was to investigate the relationship between canalization and developmental stability under varying environmental conditions. Three different cohorts of Mastomys natalensis (Rodentia, Muridae), displaying different growth trajectories, were analysed by means of geometric morphometrics. A set of 23 landmarks was digitalized on the dorsal skull of 292 specimens from Morogoro (Tanzania). Patterns of among‐ and within‐individual (measured as fluctuating asymmetry, FA) variation were assessed and compared among and within the three groups to test for the presence of a common mechanism between canalization and developmental stability. Results showed that there was no congruence between canalization and developmental stability: (1) levels of FA and among‐individual variation varied in a discordant fashion, (2) no correspondence between the variance–covariance matrix of among‐ and within individual variation was found, and (3) environmental effects were able to alter the covariance structure of among‐individual variation leaving patterns associated with fluctuating asymmetry unaffected. These findings support the view of multiple mechanisms underlying developmental buffering of shape variation. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 207–216.