Phylogenetic data reveal a surprising origin of Euphorbia orphanidis (Euphorbiaceae) and environmental modeling suggests that microtopology limits its distribution to small patches in Mt. Parnassus (Greece)

Abstract

The Mediterranean Basin is one of the most biodiverse areas in the world, harboring 25,000 plant species, of which 60% are endemic. Some of them have narrow distributions, such as Euphorbia orphanidis, which is only known from alpine screes on Mt. Parnassos in Greece. Its exact distribution in this mountain was, however, poorly known, and its phylogenetic origin was also unclear. We performed extensive field work in Mt. Parnassos and could register E. orphanidis only in five patches of limestone screes in the eastern part of this mountain range, emphasizing its very narrow distribution, which is likely limited by topography influencing water availability as indicated by environmental modeling. We also registered 31 accompanying species and thus characterized its habitat. Using nuclear ribosomal internal transcribed spacer and plastid ndhF-trnL and trnT-trnF sequences, we show that it belongs to E. sect. Patellares, despite not having connate raylet leaves typical for this section, and not to E. sect. Pithyusa as previously suggested. The relationships among the species of E. sect. Patellares are poorly resolved, suggesting their simultaneous divergence that dated to the late Pliocene, which coincided with the establishment of the Mediterranean climate. The relative genome size of E. orphanidis is in the range of that for the other members of E. sect. Patellares, suggesting that it is diploid. Finally, we performed multivariate morphological analyses to generate a comprehensive description of E. orphanidis. Based on its narrow distribution and the anticipated negative impact of global warming, we consider this species endangered. Our study demonstrates how microrelief can limit the distribution of plants in topographically heterogeneous mountain environments and likely plays an important, yet neglected, role in shaping the distribution patterns of plants in the Mediterranean Basin.

Keywords: Mediterranean basin; endangered species; endemism; environmental modelling; morphometry; phylogeny; taxonomy.

Figure 1

Distribution of populations of Euphorbia sect. Patellares used in phylogenetic and partly relative genome size analyses. The population numbers correspond to Supplementary Table S1 and are not indicated for Euphorbia orphanidis.

Figure 2

Distribution of Euphorbia orphanidis on Mt. Parnassus (green), with indicated areas as to where the species was searched for but not found (red stars). The map was adopted from Google Earth .

Figure 3

Phylogenetic relationships inferred from internal transcribed spacer sequences among the members of Euphorbia sect. Patellares. (A) Bayesian consensus phylogram; the numbers above the branches are posterior probability values >0.5, while those below the branches are maximum parsimony bootstrap values >50%. The clades of all species including multiple accessions, except that of Euphorbia orphanidis, are collapsed, and the complete tree is shown in Supplementary Figure S1 . (B) NeighborNet.

Figure 4

Bayesian consensus chronogram (Maximum Clade Credibility tree) inferred from internal transcribed spacer sequences. The numbers above the branches are posterior probability values >0.90, the bold numbers associated with the nodes indicate the median crown group ages in millions of years of the clades diversifying at those nodes, and the bars correspond to 95% highest posterior density of the age estimates. The population numbers of Euphorbia sect. Patellares correspond to the data in Supplementary Table S1 and Figure 1 , while those of the outgroup sections correspond to the data in Supplementary Table S2 .

Figure 5

Bayesian consensus phylograms of plastid ndhF–trnL (A) and trnTF (B) sequences showing the phylogenetic relationships among the members of Euphorbia sect. Patellares and outgroup species. The numbers above the branches are posterior probability values >0.5, while those below the branches are maximum parsimony bootstrap values >50%. The population numbers of E. sect. Patellares correspond to the data in Supplementary Table S1 and Figure 1 , while those of the outgroup sections correspond to the data in Supplementary Table S2 .

Figure 6

Relative genome size (RGS) variation in Euphorbia orphanidis and other species of Euphorbia sect. Patellares. The boxplots are based on the RGS population mean values presented in Supplementary Table S1 . A scatterplot representing the mean values and standard deviation of all investigated populations is shown in Supplementary Figure S2 .

Figure 7

Euphorbia orphanidis in its natural habitat on Mt. Parnassos with parts of the inflorescences showing cyathial glands and fruits.

Figure 8

Density distribution of the mean topographic predictors of randomly distributed points (repeated 10,000 times). The red lines depict the 95% confidence interval of these random samples, while the black vertical lines depict the mean predictor values of the populations of Euphorbia orphanidis.

Figure 9

Seeds of five Euphorbia species growing on Mt. Parnassus (above, ventral view; below, dorsal view).

Figure 10

Iconography of Euphorbia orphanidis: (A) whole plant, (B) plant in its habitat, (C) capsule, (D) seed, and (E) inflorescence with fruit and nectarial glands. Drawings by (F) Faltner.