Insights into Neogene Mediterranean biogeography based on phylogenetic relationships of mountain and lowland lineages of Narcissus (Amaryllidaceae)

Abstract

Aim Our aims were: (1) to reconstruct the phylogenetic relationships of daffodils (Narcissus), focusing on the lowland subgenus Hermione and the mountain section Apodanthi; (2) to estimate the temporal setting of diversification; (3) to reconstruct the migration patterns of the lineages; and (4) to examine the microevolutionary differentiation of the wide‐ranging Narcissus tazetta group across the Mediterranean. Location The Mediterranean Basin. Methods Plastid (trnT–L, trnL–F and ndhF) sequences were obtained from 63 populations representing 23 species of Narcissus and combined with published data from 16 species. Phylogenetic relationships and dating were inferred by Bayesian analysis based on geological events and divergence estimates of closely related taxa. A dispersal–extinction–cladogenesis analysis was performed using maximum likelihood methods to infer ancestral geographical distributions, and phylogeographical reconstruction was performed using coalescence analysis. Results Subgenus Hermione is not recognized as a monophyletic group because two of the nine species were found to have a close relationship with the subgenus Narcissus. The results on section Apodanthi confirmed previous findings of its monophyly and phylogenetic relationships within this mountain group. Molecular dating and ancestral range reconstructions suggest that the ancestor of Narcissus originated in the Iberian Peninsula during the Late Oligocene–Early Miocene. Eastward expansion of the lineage range proceeded from the western Mediterranean and involved colonization of mountain ranges in northern Africa. The phylogeography of the N. tazetta group revealed a widespread distribution of certain haplotypes, suggesting wide dispersal and a high level of colonization in the Mediterranean Basin. Main conclusions Our study points to the role of three key historical events in Narcissus diversification: tectonic shifts of the Alboran domain in the western Mediterranean, the Messinian salinity crisis, and the onset of the Mediterranean climate followed by periods of repeated glaciation. Diversification of section Apodanthi probably resulted from allopatric speciation, while subgenus Hermione may have shown more sympatric speciation and high dispersal, despite the lack of apparent adaptations to long‐distance dispersal. This is best exemplified by the presence of both ancestral and recent haplotypes of N. tazetta across the Mediterranean.

Population Genetics Methods Applied to a Species Delimitation Problem: Endemic Trumpet Daffodils (NarcissusSectionPseudonarcissi) from the Southern Iberian Peninsula

“…5A). Our data therefore corroborate the findings of Jiménez et al (2009), inferred from ribosomal DNA (ITS) and ISSR sequencing, suggesting that N. bujei was highly divergent from the remaining species of Narcissus inhabiting the Baetic Ranges as well as other phylogenies that relate the green and blue groups to very different clades of the Pseudonarcissi section (Graham and Barrett 2004;Rønsted et al 2008;Santos-Gally et al 2012), which may indicate that they originated in two different colonization events. Our results are also in accordance with the marked differentiation in genome sizes between N. bujei and other closely related species reported by Zonneveld (2008) and support as well the morphological distinctiveness criteria proposed by this author for N. bujei, which include solitary and 513 bright yellow flowers, spirally twisted tepals and leaves, and a black spot on the anthers (Zonneveld 2010).…”

“…The acknowledged basis for this decision was a difficulty to delimit recognizable taxonomic entities within this geographic region because of insufficient morphological differences (Aedo, forthcoming). This treatment ignores and is incongruous with the major phylogenetic reconstruction of the genus Narcissus based on DNA sequence data performed by Graham and Barrett (2004), in which N. longispathus and N. nevadensis are unambiguously separated from N. pseudonarcissus and are also well separated from each other (with a bootstrap value of 76%; see also Rønsted et al 2008;Santos-Gally et al 2012). Aedo (forthcoming) also negates the distinctness of N. bujei and N. longispathus on the basis of internal transcribed spacer (ITS) and inter-simple sequence repeat (ISSR) sequences reported by Jiménez et al (2009).…”

“…Mediterranean mountains have been the site of a significantly high number of speciation events (Martín-Bravo et al 2010), which have resulted in a high number of endemic species and an exceptionally rich flora (Gó mezCampo 1985;Sainz-Ollero and Moreno-Saiz 2002). The genus Narcissus is also a remarkable example of Mediterranean lineage with a complex evolutionary history (Graham and Barrett 2004;Santos-Gally et al 2012). The taxonomy of Narcissus is unsettled and problematic (Webb 1980;Blanchard 1990;Mathew 2002;Zonneveld 2008;Aedo, forthcoming); in particular, the trumpet daffodils (section Pseudonarcissi) are one of the most controversial groups of the genus and are a clear example of the confounding views on both the discrimination of taxa and the assignment of rank (see below).…”

Phenotypic integration in style dimorphic daffodils (Narcissus, Amaryllidaceae) with different pollinators

“…The phenotypic integration observed in the two species could reflect possible effects of common ancestry [38,40,41]. However, N. papyraceus and N. tazetta are not sister species [49,82], and other species with different stylar condition (fixed monomorphism in N. serotinus or dimorphism in N. broussonetii) are in the same clade. Assuming that legitimate pollinators in dimorphic species and populations are long-tongued insects, as the floral syndrome suggests [49], and that L-monomorphism with pollination by shorttongued insects is a derived condition [49,59,83], similar levels of integration in dimorphic populations (15.6% for N. papyraceus and 18.5% for N. tazetta), which differ greatly from the 10-fold variation in other species of the clade rstb.royalsocietypublishing.org Phil.…”

Towards a Molecular Understanding of the Biosynthesis of Amaryllidaceae Alkaloids in Support of Their Expanding Medical Use

“…Species from the genus Leucojum are known as snowflakes, Leucojum aestivum is an industrial source for galanthamine production in Eastern Europe, but collection from the wild has endangered natural populations [11,29]. The genus Narcissus is native to Europe and North-Africa, with its centre of biodiversity found on the Iberian Peninsula [30]. Due to the existence of natural hybrids, extensive cultivation and breeding, and escape and naturalisation, the number of recognised species of Narcissus varies from 26 to circa 80.…”