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Historical biogeography aims to understand the drivers of speciation including the roles played by plate tectonics and climatic change Lomolino et al. Middle and Central Asia have one of the oldest desert areas. Desertification started at least Various paleogeographic factors played major roles in the shifting of Central Eurasian climate Ramstein et al. Aridization led to the disappearance of forests and formation of desert ecosystems Cerling et al.
In the late Cenozoic, dramatic climatic changes influenced the origins, diversification and distribution of Central Eurasian reptiles Macey et al. However, the dearth of phylogenetic and historical biogeographic studies for Central Eurasia does not allow the testing of hypotheses on the biological consequences of Cenozoic climatic events.
The reptile fauna of the Central Asian deserts is particularly diverse, yet we still have limited understanding of the drivers of evolution of the constituent species Melville et al. The agamid genus Phrynocephalus Kaup,or toad-headed lizards, is one of the most speciose genera in its family. The species are ecologically important components of the Central Eurasian desert fauna and are highly adapted to sand dunes and stony montane deserts from sea level up to 6, m a.
They exhibit high levels of variation in ecological and morphological diversity, and the species range from being habitat generalists to specialists Clemann et al. Considerable taxonomic, morphological, allozyme, karyological, osteological, and ethological research has been conducted on the charismatic Phrynocephalus of Central Asia for a brief review on history of phylogenetic studies of the genus Phrynocephalus see Supplemental Information 1.
The most complete genealogic hypothesis obtained up to date Solovyeva et al. Herein, we explore a number of unresolved questions by using both mitochondrial and nuclear DNA markers based for 36 species of Phrynocephalus that cover the entire range of the genus. Specifically, we pursue three main objectives: It helps to resolve longstanding phylogenetic and biogeographic issues of Central Eurasian biogeography and provides insights into the biogeographic consequences of Cenozoic aridization.
Our analyses used the mitochondrial DNA dataset of Solovyeva et al. We also amplified exons of four nuclear DNA genes as follows: The total length of these data was 4, bp Table S3.
Thirty-seven agamid species were selected as outgroup taxa for phylogenetic inference and time-tree calibration. Leiolepis Cuvier, and Australian taxa Amphibolurinae: The most distant outgroup taxa also included representatives of Chamaeleonidae, Phrynosauridae, Dactyloidae, Iguanidae, Corytophanidae, Tropiduridae, Polychrotidae, Leiocephalidae, Lacertidae, Opluridae, Crotaphytidae, including representative taxa of the following agamid genera: Details on taxonomy, GenBank accession numbers and associated references were summarized in Tables S1 and S2.
Subsequently, the alignment was checked and manually revised if necessary using Seqman 5. Genetic distances were calculated using MEGA 6.
Phylogenetic tree reconstructions were performed with the following data sets: To test whether the inclusion of distant outgroups can introduce any bias into results of tree inference, the nuclear and mitochondrial concatenations were put through an additional set of reconstructions omitting all non-agamid and non-agamine taxa, respectively.
The optimum partitioning schemes for nuclear and mitochondrial alignments were identified with PartitionFinder Lanfear et al. The ML trees were generated in Treefinder v. March Jobb, For each subset, the best fitting substitution model was selected using the Bayesian Information Criterion in Treefinder.
Bayesian inference was performed in MrBayes v3. We checked the convergence of the runs and that the effective sample sizes were all above by exploring the likelihood plots using TRACER v1. Prior to the analysis, the molecular clock assumption was tested separately for each exon by hierarchical likelihood ratio tests using PAML v4. Following the results of these tests, we used a strict clock model for BDNF and uncorrelated lognormal relaxed clock models for the other three loci.
No calibration information was utilized; the clock rate for BDNF was set to one. We used the same models and partitioning scheme as in the ML analysis. A Yule prior for the species-tree shape and the piecewise constant population size model were assumed. Default priors were used for all other parameters.
Partition homogeneity test Farris et al. We tested if the mitochondrial genealogy of Solovyeva et al. ML trees with unconstrained and alternative constrained topologies were generated for the mitochondrial and nuclear datasets by using Treefinder v. Treefinder was also used to calculate site-wise log-likelihoods and to perform the approximately unbiased tree-selection test AU; Shimodaira, Significant discordance would have precluded a total evidence approach that evaluated together the mtDNA and nuDNA datasets because we wanted to differentiate between the initial cladogenic event s and the timing of interspecific hybridization sif present.
The mtDNA dataset of Solovyeva et al. Site and clock models were set as in the species-tree reconstruction. Analyses were run for million of generations and the Yule model was set as the tree prior. Because no reliable paleontological data have been reported for Phrynocephaluswe used ten fossils from non-agamid outgroup taxa and outgroup Agamidae as calibration points see Table S5 ; Fig.
We used the ML of Lagrange Ree et al. Transitions between discrete states ranges along tree branches were modeled as a function of time, thus enabling ML estimation of the ancestral states at cladogenic events. We defined seven regions for the analyses: The maximum number of regions included in one area was limited to two.
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We set two periods of time: This date echoed the considerable uplifting of the Pamir, Tianshan, and Karakoram mountains. The matrices of the modern distribution areas were given in Table S6.
To account for topological uncertainty, the analysis was repeated based on a tree sample from the posterior distribution produced by BEAST. Substrate niche was coded using six character states: Transitions between states were formalized using step-matrix Table S7. To examine the evolution of body size in Agaminae, we used weighted squared-change parsimony Maddison, as implemented in Mesquite v3.
We tested maximum SVL of taxa reported in literature or based on examination of voucher specimens. Information on the length of the fragments and variability were given in Table S3. Topological patterns were in general congruent across analyses and the results of Solovyeva et al. The ML tree is shown in Fig. Phrynocephalus was unambiguously monophyletic in all analyses Fig. Several nodes in the mitochondrial tree appeared insufficiently resolved.
Nevertheless all species of Phrynocephalus were consistently assigned to one of the ten strongly supported matrilines for their distribution see Fig.
Near and Middle East Phrynocephalus: Phrynocephalus arabicus Anderson, and Phrynocephalus maculatus Anderson, Fig.
Subgenus Megalochilus Eichwald,including the 443-1, sand-dwelling Phrynocephalus mystaceus Pallas, from Middle Asia Fig. Subgenus Oreosaura joining viviparous Tibetan species Fig. Middle Asian sun-watchers encompassing Phrynocephalus helioscopus and allied taxa Fig. Tibetan oviparous Phrynocephalus axillaris Blanford, Fig. Phrynocephalus versicolor species complex, inhabiting northern plains of Central Asia Fig.
The versicolor -group had two sublineages: Phrynocephalus hispidus Bedriaga, from Mongolian Dzungaria and Phrynocephalus sp. Phrynocephalus guttatus species complex, widespread in plains of Kazakhstan and northern Caspian region Fig. Within the guttatus- group, P. Exclusion of non-agamid taxa did not change the topology significantly Fig. Phylogenetic trees resulted from separate analyses of individual genes were shown in Figs.
Monophyly of Phrynocephalus received high support as did several species-groups: Monophyly of the clade containing the P. The nuDNA topology depicted three main clades Fig. Most notably, the placements of Megalochilus fin Oreosaura differed in important ways. Dim notable conflicts also occurred. The nuclear phylogeny did not depict a shared heritage for P. The phylogenetic position of P. Similarly, the phylogeny placed P. We performed additional AU tree-selection test to 4534-1 for significant differences between matrilineal genealogy and the nuclear phylogeny, including whether one or both datasets rejected alternative placements of particular clades.
The test evaluated the conflicting positions of P.
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The matrilineal genealogy was forced to the nuclear dataset and vice versa. The alternative nuclear hypotheses for the clades A—E and D—H were not rejected by mitochondrial data.
The matrilineal position of P.
The AU test for P. Finally, dkn tested topologies of trees based on each nuclear marker against final topology. The BDNF dataset rejected the topology. In contrast, original RAG-1 topology was rejected. S10 and S11respectively. Timing of the internal nodes was summarized in detail in Table S All analyses proposed that the ancestor of Phrynocephalus originated between the end of Oligocene and beginning of the Miocene mtDNA: