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Morphometrical relationships between South-east Asian deer (Cervidae, tribe Cervini): evolutionary and biogeographic implications

Profile image of Colin GrovesColin Groves

2004, Journal of Zoology

https://doi.org/10.1017/S0952836904005011
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18 pages

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Abstract

Two hundred and fourteen skulls of Asian deer species (Cervini) were measured and the resulting craniometric data analysed using multivariate statistics. Our results suggest that elements of skull shape as determined by morphometrics can be used as phylogenetic characters and depict phylogenetic relationships among Cervini deer species that is not far removed from the picture given by molecular studies and other characters. Morphometricsbased phylogeny was used in combination with other phylogenies and palaeoenvironmental reconstructions to investigate factors that may have influenced evolutionary changes. Our data indicate the need for a revision of the genus and subgenus level taxonomy of the Cervini.

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What explains the distinct grouping of Elaphurus among Cervini species?add

The study finds that Elaphurus is craniometrically distinct from other Cervini due to significant length and width measurements, marking a high correlation with the first principal component of skull morphology.

How do morphometric analyses inform phylogenetic relationships within Cervini?add

Research demonstrates that cranial measurements can act as reliable phylogenetic indicators, as evidenced by a 82.4% accuracy in discriminant analysis classifying species groupings.

When did the first antlered deer evolve and disperse across regions?add

Antlered deer originated in the Middle to Late Tertiary, with key divergences during the Pleistocene, notably as early as 12.5-9.5 Ma for the three-pronged deer groups.

What factors influenced the divergence of deer species across Southeast Asia?add

Environmental shifts from humid forests to open grasslands during the Pliocene and Pleistocene, combined with ancient hybridization events, likely fueled diversification within Cervini.

How did hybridization impact the evolutionary trajectory of Elaphurus?add

Evidence indicates Elaphurus may have a hybrid origin involving a Cervus ancestor, with controlled breeding experiments yielding over 300 viable hybrids with Cervus elaphus in captivity.

Figures (19)
Table 1. Species of Cervinae in East, South, and South-east Asia (Lekagul & McNeely, 1977; Corbet & Hill, 1992; Wemmer, 1998), and numbers of specimens and their sex used in this research  and other data in the literature with the specific aim to: (1) investigate the monophyly of the genera Cervus and Axis and their subgenera Rusa, Rucervus, Cervus, Axis and Hyelaphus; (2) assess the relationships between taxa on the South-east Asian islands and those on the mainland; (3) develop a historic biogeographical model explaining the dispersal and divergence of Cervini in island South- east Asia.
Table 1. Species of Cervinae in East, South, and South-east Asia (Lekagul & McNeely, 1977; Corbet & Hill, 1992; Wemmer, 1998), and numbers of specimens and their sex used in this research and other data in the literature with the specific aim to: (1) investigate the monophyly of the genera Cervus and Axis and their subgenera Rusa, Rucervus, Cervus, Axis and Hyelaphus; (2) assess the relationships between taxa on the South-east Asian islands and those on the mainland; (3) develop a historic biogeographical model explaining the dispersal and divergence of Cervini in island South- east Asia.
Fig. 1. Map of the areas mentioned in the text.
Fig. 1. Map of the areas mentioned in the text.
Table 2. Correlation matrix of a principal component analysis for mature Cervinae specimens (see Fig. 2)
Table 2. Correlation matrix of a principal component analysis for mature Cervinae specimens (see Fig. 2)
Fig. 2. Principal component analysis of all mature Cervini skulls.
Fig. 2. Principal component analysis of all mature Cervini skulls.
Table 3. Correlation matrix of a principal component analysis fc mature specimens of Cervus and Axis (see Fig. 3)
Table 3. Correlation matrix of a principal component analysis fc mature specimens of Cervus and Axis (see Fig. 3)
Fig. 3. Principal component analysis for mature specimens of Cervus and Axis. For group numbers 1-4, see text.
Fig. 3. Principal component analysis for mature specimens of Cervus and Axis. For group numbers 1-4, see text.
Table 4. Structure matrix of the principal component analysis of all mature specimens of Cervus and Axis (see Fig. 4)  Table 5. Structure matrix of a discriminant analysis of all mature specimens of Cervus and Elaphurus (see Fig. 5)
Table 4. Structure matrix of the principal component analysis of all mature specimens of Cervus and Axis (see Fig. 4) Table 5. Structure matrix of a discriminant analysis of all mature specimens of Cervus and Elaphurus (see Fig. 5)
Fig. 4. Discriminant analysis for mature Cervinae specimens (excluding C. elaphus).
Fig. 4. Discriminant analysis for mature Cervinae specimens (excluding C. elaphus).
Table 6. Correlation matrix of a principal component analysis for mature specimens of the Hyelaphus and Axis subgenera and one fossil specimen of A. lydekkeri (see Fig. 7)
Table 6. Correlation matrix of a principal component analysis for mature specimens of the Hyelaphus and Axis subgenera and one fossil specimen of A. lydekkeri (see Fig. 7)
Fig. 5. Discriminant analysis for mature specimens of the genera Cervus and Elaphurus.
Fig. 5. Discriminant analysis for mature specimens of the genera Cervus and Elaphurus.
Fig. 6. Ratio between GTL and N1 for each of the Cervini species in this research. Number of specimens per species, x-axis; dark. horizontal lines in boxes, median value; boxes, interquartile ranges; thin lines on either sides of boxes, outliers; extreme individual variables, numbered circles.
Fig. 6. Ratio between GTL and N1 for each of the Cervini species in this research. Number of specimens per species, x-axis; dark. horizontal lines in boxes, median value; boxes, interquartile ranges; thin lines on either sides of boxes, outliers; extreme individual variables, numbered circles.
Fig. 7. Principal component analysis of the Axis and Hyelaphu subgenera in relation to one fossil specimen of A. lydekkeri.
Fig. 7. Principal component analysis of the Axis and Hyelaphu subgenera in relation to one fossil specimen of A. lydekkeri.
Fig. 8. Bivariate plot of the BR vs CBR in five species of Axis (including one fossil species).
Fig. 8. Bivariate plot of the BR vs CBR in five species of Axis (including one fossil species).
Fig. 9. Neighbour-joining species tree for Cervini based on craniometric similarities.
Fig. 9. Neighbour-joining species tree for Cervini based on craniometric similarities.
*1, Groves & Grubb (1987); 2, Flerov (1952); 3, Benirschke (1983); 4, Wemmer (1983); 5, Bubenik (1966; 1975 in Wemmer (1983); 6, Geist (1998); 7, Randi, Mucci, Claro-Hergueta et al. (2001); 8, Emerson & Tate (1993); 9, Cronin ef al. (1996); 10, X.-H. Liu et al. (2003).  Table 7. Resemblances of Elaphurus to other species of Cervini reported in the literature and possibly suggesting phylogenetic affinity
*1, Groves & Grubb (1987); 2, Flerov (1952); 3, Benirschke (1983); 4, Wemmer (1983); 5, Bubenik (1966; 1975 in Wemmer (1983); 6, Geist (1998); 7, Randi, Mucci, Claro-Hergueta et al. (2001); 8, Emerson & Tate (1993); 9, Cronin ef al. (1996); 10, X.-H. Liu et al. (2003). Table 7. Resemblances of Elaphurus to other species of Cervini reported in the literature and possibly suggesting phylogenetic affinity
Fig. 10. Discriminant analysis for mature specimens of eldi, duvauceli, schomburgki, timorensis, and unicolor.
Fig. 10. Discriminant analysis for mature specimens of eldi, duvauceli, schomburgki, timorensis, and unicolor.
Fig. 11. Phylogenetic tree of the Cervinae based on our craniometrics and data by Randi, Mucci, Claro-Hergueta et al. (2001), and rescaled after data by Miyamoto, Kraus & Ryder (1990). For explanations of nodes 1-12 see Table 8.
Fig. 11. Phylogenetic tree of the Cervinae based on our craniometrics and data by Randi, Mucci, Claro-Hergueta et al. (2001), and rescaled after data by Miyamoto, Kraus & Ryder (1990). For explanations of nodes 1-12 see Table 8.
Appendix. Continued
Appendix. Continued

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A Craniometric Analysis of the Subfamily Cervinae (Cervidae, Mammalia)

Fossil Studies, 2024

This study employs Principal Component Analysis to examine cranial measurements from both extant and fossil specimens spanning 38 species and comprising over 300 individuals within the subfamily Cervinae. Our findings elucidate craniometric distinctions among cervids characterized by varying body sizes and certain evolutionary adaptations. While our results generally corroborate previous assertions regarding the limited craniometric variability among plesiometacarpal deer, they also unveil specific cranial adaptations within certain genera and species. The Principal Component Analysis of craniometric data revealed that giant and large-sized deer display significantly broader ecomorphological diversity in cranial shape compared to small-sized deer. Secondly, small-sized deer exhibit greater uniformity in their cranial shape, appearing densely clustered on the factorial map. Thus, we conclude that body size imposes ecological constraints, limiting the available niches due to eco-physiological factors. This study demonstrates that endemic insular deer do not evolve consistent craniometric features attributable to insular isolation, while the cranial proportions of medium-to-small-sized deer delineate a ubiquitous morphological archetype characteristic of numerous cervid taxa spanning diverse phylogenetic lineages and sharing comparable body sizes. This group of “Dama-like” deer, characterized by similar body size, metabolic rates, ecological needs, and cranial morphometry, is referred to here as the fundamental eco-physiological type, typical of warm regions within the Palearctic and Oriental biogeographic realms.

Exploration of the taxonomy of some Pleistocene Cervini (Mammalia, Artiodactyla, Cervidae) from Java and Sumatra (Indonesia): a geometric-and linear morphometric approach

Third molars of extant-and fossil Southeast Asian deer were metrically compared using a linear-and geometric morphometric approach and discussed in relation to known taxonomic information from the literature. Our analysis suggests the presence of medium sized deer of the genus Axis and large sized taxa of the genus Cervus s. l. in Java. Axis lydekkeri and Axis javanicus are considered valid taxa, with A. lydekkeri probably related to the subgenus Hyelaphus. The large deer, such as Cervus kendengensis, Cervus stehlini and Cervus problematicus are most likely of the subgenus Rusa, the former two closely related to extant Cervus timorensis. The Sumatran fossils are members of the subgenus Rusa, but not necessarily conspecific with extant Cervus (Rusa) unicolor.

Evolution and phylogeny of old world deer

The phylogenetic pattern and timing of the radiation of Old World deer was determined based on the complete mitochondrial cytochrome b gene from 33 Cervinae taxa. Using rooted and unrooted phylogenies derived from distinct theoretical approaches, strong support was achieved for monophyly of the Old World deer with muntjacs as sister group as well as for the divergence of at least three distinct genera: Rucervus, Dama, and Cervus. The latter clade comprises what have previously been regarded as the genera or subgenera Panolia, Rusa, Cervus, Sika, and probably Przewalskium. Our data also consistently confirmed paraphyly of nominate C. elaphus and did not support the monophyly of Axis. We used these molecular phylogenies to assess the homoplastic evolution of morphological, geographical, ecological, and selected behavioural character state differences within the Cervinae. Reliable fossil calibrations, large molecular data sets, and improved dating methods are shaping a molecular time scale for the evolutionary radiation of Old World deer that occurred at the Miocene/Pliocene transition and is largely compatible with existing palaeontological evidence. Using node ages estimated from sequence data, we estimated an average per-lineage diversification rate of 0.51 ± 0.1 species per million years (my) over roughly the last 6 mya.

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2020

Deer from Late Miocene to Pleistocene of Western Palearctic: matching fossil record and molecular phylogeny data

Zitteliana B, 2014

The report proposes a revision of poorly known fossil cervid forms and a new look on Late Neogene cervid phylogeny with implication of known already data from mitochondrial and nuclear genetic analysis. Pliocervus matheroni from Late Miocene of Europe is poorly known with unclear systematic position. Some characters (parallel orientation of long pedicles situated very close each from another; antler shape, dental morphology, developed upper canines) place P. matheroni close to Late Miocene Pavlodaria orlovi from the Hipparion fauna of Kazakhstan. Pliocervus and Pavlodaria, must be phylogenetically very close or even synonymous. Both Pliocervus and Pavlodaria share the same orientation and position on the skull of pedicles as modern Capreolus. The analysis of cranial morphology and dentition of Procapreolus moldavicus revealed a set of primitive capreoline cranial characters, combined with orientation of pedicles as in modern Odocoileus and primitive Muntiacus-like characters (large upper canines, long pedicles, deep and large preorbital fossae). P. moldavicus stands closer to a forerunner of the stock that radiated to New World deer than to modern Capreolus. Apparently, several lineages of Capreolinae evolved in Northern Eurasia before Mio-Pliocene boundary: the archaic Procapreolus lineage that does not have direct descendants in the modern fauna; the little known P. loczii that seems to be closer to the hypothesized forerunner of New World Capreolinae; and the Pliocervus-Pavlodaria lineage that may be close to modern Capreolus and Hydropotes. The dichotomy of Cervinae and Capreolinae, perhaps, is a consequence of the first expansion of Miocene ancestors of Capreolinae into the ecologically less favorable parts of Central and Boreal Asia. This may explain the generally more advanced degree of evolutionary specialization in Capreolinae, the development of additional enamel folds in the molars (the Palaeomeryx fold and the protoconal fold), which are better developed in the Capreolinae, and a more advanced specialization of premolars in the Capreolinae if compared to the Cervinae. The biogeographic expansion of Cervinae is recorded in Europe during Early Pliocene. Apparently, this expansion coincides with the first successful radiation of the Old World deer that gave such fossil forms as Arvernoceros ardei, Praeelaphus perrieri, Metacervocerus pardinensis and possibly modern Axis axis and Rucervus duvaucelii. A. ardei and R. duvaucelii share the same plane of antler construction, so Arvernoceros and Rucervus may be closely related genera, or even synonymous. The second important radiation of Cervinae took place by the end of Villafranchian, when appeared modern rich in forms Cervus, Pzewalskium, and extinct giant Praemegaceros, which together with Eucladoceros, apparently, also belongs to Rusa-Cervus stock. Dama, Megaloceros, and Megaceroides represent another stock of Cervinae that evolved in Western Eurasia and Mediterranean area.

New data on the Pleistocene deer Candiavervus sp. II (Cervinae, Mammalia)

CFS Courier Forschungsinstitut Senckenberg

A skeleton of the endemic Pleistocene Cretan deer Candiacervus sp. II (Liko, Crete, Greece) was mounted using bones of different individuals. This composite skeleton contributes to the study of the taxonomy of insular ungulates as it reveals some additional features which had not been detected in the isolated elements. Candiacervus sp. II differs from all known recent and extinct mainland deer, mainly in its proportions. Although its considerably shortened distal limbs had been already noted in the past, Candiacervus sp. II now appears at the same time to have had more or less the same vertebral column length as its large-sized continental counterparts, and a moderately upwards curved lumbar section, two features more remindful of the insular dwarf bovid Myotragus than of the small-sized mainland Axis axis. Combined with an increased massiveness of all the bones and with pronounced muscle scars, this change in body proportions indicates that Candiacervus sp. II evolved towards the n...

Historical development and geographical distribution of giant deer (Cervidae, Megacerini)

Paleontological Journal, 2011

The origin, trends in adaptatiogenesis and ecogenesis of megacerines reviewed. The major phylo genetic lineages are described, the main evolutionary events are dated and compared with changes in envi ronments. It is shown that the major evolutionary changes in megacerines developed against a background of considerable changes in environments, which corresponded to global climatic and great regional landscapeclimatic events.

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    Forest Fruit Production Is Higher on Sumatra Than on Borneo

    PLoS ONE, 2011

    Background: Various studies have shown that the population densities of a number of forest vertebrates, such as orangutans, are higher on Sumatra than Borneo, and that several species exhibit smaller body sizes on Borneo than Sumatra and mainland Southeast Asia. It has been suggested that differences in forest fruit productivity between the islands can explain these patterns. Here we present a large-scale comparison of forest fruit production between the islands to test this hypothesis.

    {"__content__"=>"Human-mediated introduction of introgressed deer across Wallace's line: Historical biogeography of and .", "i"=>[{"__content__"=>"Rusa unicolor"}, {"__content__"=>"R. timorensis"}]}

    Ecology and evolution, 2018

    In this study we compared the phylogeographic patterns of two Rusa species, and , in order to understand what drove and maintained differentiation between these two geographically and genetically close species and investigated the route of introduction of individuals to the islands outside of the Sunda Shelf. We analyzed full mitogenomes from 56 archival samples from the distribution areas of the two species and 18 microsatellite loci in a subset of 16 individuals to generate the phylogeographic patterns of both species. Bayesian inference with fossil calibration was used to estimate the age of each species and major divergence events. Our results indicated that the split between the two species took place during the Pleistocene, ~1.8 Mya, possibly driven by adaptations of to the drier climate found on Java compared to the other islands of Sundaland. Although both markers identified two well-differentiated clades, there was a largely discrepant pattern between mitochondrial and nucl...

    The Middle Pleistocene vertebrate fauna from Khok Sung (Nakhon Ratchasima, Thailand): biochronological and paleobiogeographical implications

    ZooKeys, 2016

    The fluviatile terrace deposits of Khok Sung, Nakhon Ratchasima province, have yielded more than one thousand fossils, making this the richest Pleistocene vertebrate fauna of Thailand. The excellent preservation of the specimens allows precise characterization of the faunal composition. The mammalian fauna consists of fifteen species in thirteen genera, including a primate, a canid, a hyaenid, proboscideans, rhinoceroses, a suid, cervids, and bovids. Most species correspond to living taxa but globally (Stegodon cf. orientalis) and locally (Crocuta crocuta ultima, Rhinoceros unicornis, Sus barbatus, and Axis axis) extinct taxa were also present. The identification of Axis axis in Khok Sung, a chital currently restricted to the Indian Subcontinent, represents the first record of the species in Southeast Asia. Three reptilian taxa: Crocodylus cf. siamensis, Python sp., and Varanus sp., are also identified. Faunal correlations with other Southeast Asian sites suggest a late Middle to early Late Pleistocene age for the Khok Sung assemblage. However, the Khok Sung mammalian fauna is most similar to that of Thum Wiman Nakin, dated to older than 169 ka. The Khok Sung large mammal assemblage mostly comprises mainland Southeast Asian taxa that migrated to Java during the latest Middle Pleistocene, supporting the hypothesis that Thailand was a biogeographic pathway for the Sino-Malayan migration event from South China to Java.

    Demographic and genetic structure of a severely fragmented population of the endangered hog deer (Axis porcinus) in the Indo- Burma biodiversity hotspot

    The population of the globally endangered hog deer (Axis porcinus) has declined severely across its geographic range. Intensive monitoring of its demographic and genetic status is necessary. Northeast India is a stronghold of the species; however, in recent years the population has been getting fragmented, and it is vulnerable to extinction. We examined the demographic and genetic structure of a small hog deer population in the floating meadows of Keibul Lamjao National Park (KLNP), located on the western fringe of the Indo-Burma biodiversity hotspot for conservation planning. We used a double-observer distance sampling method to derive the hog deer abundance and population structure. We also derived the genetic diversity of the population through microsatellite screening and bottleneck detection. Our study revealed that the abundance of the deer in the park was 1.82–4.32 individuals/km2. The adult male to female ratio and fawn to doe ratio were 36.2 ± 1.9 males/100 females and 16.5...

    Genetic analysis of endangered hog deer (Axis porcinus) reveals two distinct lineages from the Indian subcontinent

    Scientific reports, 2018

    The hog deer (Axis porcinus) is threatened by habitat alteration, fragmentation, and poaching, which have led to a drastic decline of its wild population. Two subspecies of A. porcinus have been described from its distribution range. A. p. porcinus is reported to occur from Pakistan along the Himalayan foothills through Nepal, India and Myanmar, and A. p. annamiticus is found in Thailand, Indo-China, Laos, Cambodia, and Vietnam. However, the current distribution range of A. p. annamiticus is still unclear. We used the partial control region (CR) of mitochondrial DNA (mtDNA) and seven microsatellite loci to investigate the intra-species structure, differentiation, and demographic history of hog deer populations from three landscapes, the Terai Arc, Northeast, and Indo-Burma (Keibul Lamjao National Park (KLNP), Manipur, India) landscapes. We also carried out divergence time estimation using the complete mitogenome. The level of variation was ~4%, and the time of divergence of the KLNP...

    Demographic and genetic structure of a severely fragmented population of the endangered hog deer (Axis porcinus) in the Indo-Burma biodiversity hotspot

    PLOS ONE

    The population of the globally endangered hog deer (Axis porcinus) has declined severely across its geographic range. Intensive monitoring of its demographic and genetic status is necessary. We examined the demographic and genetic structure of a small hog deer population in Keibul Lamjao National Park (KLNP), located on the western fringe of the Indo-Burma biodiversity hotspot for conservation planning. The distribution pattern of hog deer in the Park was derived based on the presence/absence of faecal pellets in 1 km × 1 km grids. We used double-observer distance sampling method to derive the hog deer abundance and population structure and compared with previous data to derive the population trend. We determined the genetic diversity of the population through microsatellite screening and bottleneck detection. The overall pellet density was 0.34 ± 0.02 pellets km-2 restricted to only 22.34 ± 0.20 km 2 area of the park. The estimated density of the deer in the park was 1.82-4.32 individuals km-2. The population showed a declining trend from 2006-08 (p < 0.05, R 2 = 0.916) with 8% annum-1 and an increasing trend from 2003-2018 (p < 0.05, R 2 = 0.9304) with 10% annum-1. The adult male-to-female ratio and fawn-to-doe ratio were 36.2 ± 1.9 males per 100 females and 16.5 ± 0.4 fawns per 100 females, respectively. The molecular examination suggested that the mean number of alleles at 23 loci was 2.70 ± 0.18, the observed heterozygosity (Ho) ranged from 0.26 to 0.63 (mean 0.42 ± 0.02), the expected heterozygosity (He) ranged from 0.23 to 0.73 (χ = 0.51 ± 0.03), and the polymorphic information content (PIC) ranged from 0.2 to 0.67 (χ = 0.43 ± 0.03) indicating a moderate level of genetic diversity. Although no bottleneck in the population was observed, the loss of genetic diversity may affect the evolutionary potential of the species at the site by limiting the selection flexibility. Conservation planning coupled with scientific management regime will help in the long term persistence of the population in the region.

    The island rule explains consistent patterns of body size evolution in terrestrial vertebrates

    Nature Ecology & Evolution, 2021

    Island faunas can be characterized by gigantism in small animals and dwarfism in large animals, but the extent to which this so-called 'island rule' provides a general explanation for evolutionary trajectories on islands remains contentious. Here we use a phylogenetic metaanalysis to assess patterns and drivers of body size evolution across a global sample of paired island-mainland populations of terrestrial vertebrates. We show that 'island rule' effects are widespread in mammals, birds and reptiles, but less evident in amphibians, which mostly tend towards gigantism. We also found that the magnitude of insular dwarfism and gigantism is mediated by climate as well as island size and isolation, with more pronounced effects in smaller, more remote islands for mammals and reptiles. We conclude that the island rule is pervasive across vertebrates, but that the implications for body size evolution are nuanced and depend on an array of context-dependent ecological pressures and environmental conditions. .

    Unexpectedly high levels of lineage diversity in Sundaland puddle frogs (Dicroglossidae: Occidozyga Kuhl and van Hasselt, 1822)

    Molecular Phylogenetics and Evolution, 2021

    Phylogeny and evolution of the genus Cervus (Cervidae, Mammalia) as revealed by complete mitochondrial genomes

    Scientific Reports

    Mitochondrial DNA (mtDNA) lineages are recognized as important components of intra- and interspecific biodiversity, and allow to reveal colonization routes and phylogeographic structure of many taxa. Among these is the genus Cervus that is widely distributed across the Holarctic. We obtained sequences of complete mitochondrial genomes from 13 Cervus taxa and included them in global phylogenetic analyses of 71 Cervinae mitogenomes. The well-resolved phylogenetic trees confirmed Cervus to be monophyletic. Molecular dating based on several fossil calibration points revealed that ca. 2.6 Mya two main mitochondrial lineages of Cervus separated in Central Asia, the Western (including C. hanglu and C. elaphus) and the Eastern (comprising C. albirostris, C. canadensis and C. nippon). We also observed convergent changes in the composition of some mitochondrial genes in C. hanglu of the Western lineage and representatives of the Eastern lineage. Several subspecies of C. nippon and C. hanglu h...

    {"__content__"=>"The modular organization of roe deer () body during ontogeny: the effects of sex and habitat.", "i"=>{"__content__"=>"Capreolus capreolus"}}

    Frontiers in zoology, 2018

    As a small artiodactyl, the roe deer ( L.) is characterized by biological plasticity and great adaptability demonstrated by their survival under a wide variety of environmental conditions. In order to depict patterns of phenotypic variation of roe deer body this study aims to quantify variation during ontogenetic development and determine how sex-specific reproductive investment and non-uniform habitat differences relate to phenotypic variation and do these differential investments mold the patterns of phenotypic variation through modular organisation. Patterns of phenotypic correlation among body traits change during the ontogeny of roe deer, with differential influence of sex and habitat type. Modularity was found to be a feature of closed habitats with trunk+forelimbs+hindlimbs as the best supported integration/modularity hypothesis for both sexes. The indices of integration and evolvability vary with habitat type, age and sex where increased integration is followed by decreased ...

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