Systematics, character evolution, and biogeography of Cistus L. (Cistaceae) based on ITS, trnL-trnF, and matK sequences
Introduction
Cistus (Cistaceae) is one of the most characteristic genera of the Mediterranean flora. Shrubby species primarily occur as woodland understory and others (C. ladanifer, C. laurifolius, and C. monspeliensis) are dominant in evergreen scrub. The adaptation of the genus to Mediterranean environments is evident from ecological characteristics such as fire-dependent seed germination (Roy and Sonié, 1992, Trabaud and Renard, 1999), insect-dependent pollination (Talavera et al., 1993), flower-dependent reproduction (Herrera, 1987), and spring-dependent phenology (Herrera, 1986). A long history of human activities has favored distribution and abundance of Cistus species in the Mediterranean (Thompson, 2005). Impenetrable masses of Cistus plants are formed as early successional stages following woodland disturbances such as fire and soil overturning. Co-occurring species of Cistus are frequent, particularly in mountain ranges composed by both acidic and basic soils. Environmental specificity referring to substrate confers additional value to acidiphilous and basiphilous species as predictable indicators of woodland disturbances. In marked contrast to the detailed knowledge of ecological characteristics of Cistus, understanding of the evolution of morphological characters and phylogenetic relationships within the genus is extremely limited.
Cistaceae comprises about 180 species, typically displaying loculicidal capsules of three valves, except in Cistus that is characterized by capsules with five or more valves. Circumscription of species in the eight genera of the Cistaceae is still problematic, particularly in genera such as Helianthemum and Halimium. This has resulted in the publication of multiple combinations for the same taxon under different generic names (Arrington and Kubitzki, 2003). The taxonomy of Cistus has traditionally been based on vegetative (nerve number, shape, and hairiness of leaves) and reproductive characters (sepal number, petal color, style length, and number of fruit valves). Worldwide monographs of Cistus have recognized between 16 species (Grosser, 1903) and 28 species (Dunal, 1824) (Table 1). Following Grosser’s (1903) treatment with additional species described more recently, the genus is currently thought to comprise approximately 20 species, of which 16 occur in Europe (Warburg, 1968), 11 in Spain (Martín and Guinea, 1949), 12 in Iberia (Demoly and Montserrat, 1993), and 12 in Morocco (Soriano, 2002) (Fig. 1). The highest species diversity therefore occurs in the western Mediterranean, where 14 species are distributed in the Iberian Peninsula and northwestern Africa.
Disparate infrageneric classifications of Cistus have been proposed (Table 1). In the last taxonomic treatment three subgenera, namely Cistus, Leucocistus, and Halimioides, are described based on morphological characters (Demoly and Montserrat, 1993). The subgenus Halimioides (three species) is distributed exclusively in the western Mediterranean, whilst the subgenera Leucocistus (eight species) and Cistus (nine species) occur in the Mediterranean basin and the Canary Islands. This widespread distribution of Cistus subgenera and species clearly indicates the successful mobility of seeds and colonization in Mediterranean habitats.
Evolutionary mechanisms responsible for the morphological diversity within Cistus remain poorly understood. Plants are predominantly self-incompatible (Bosch, 1992) promoting crossing between individuals of the same and different species. Identification in the field of individuals as hybrids is relatively easy because they display characteristics that are intermediate between those of nearby, putative progenitors. Crossing between two plants of any species potentially generates offspring with intermediate traits, particularly when they are closely related congeners (Demoly, 1996). Hybrid polyploidy (allopolyploidy) has not played an important role in speciation of Cistus, as all species display a chromosome number of 2n = 18. In fact, variation of DNA content is not significant among species (Ellul et al., 2002).
A proper phylogeny of Cistus has not been proposed to date. Dansereau (1939) outlined a phyletic diagram based on morphological features. Examination of 13 isozyme loci indicates high values of genetic divergence among four Canarian species (Batista et al., 2001), although evolutionary relationships of island endemics with respect to continental species remain unknown. Phylogenetic relationships among Cistaceae genera indicate that Cistus is closely related to Halimium and Helianthemum (Arrington and Kubitzki, 2003, Savolainen et al., 2000). In addition, angiosperm phylogenies reveal that the family forms a lineage coupled with Dipterocarpaceae and Sarcolaenaceae (Soltis et al., 2000). A larger sample is needed, however, to determine sister-group relationships of Cistaceae and Cistus.
Four basic objectives are addressed in the present study: (1) to evaluate congruence between nuclear (ITS) and plastid (trnL-trnF, matK) sequences; (2) to identify major lineages and test the monophyly of infrageneric groupings recognized in existing classifications of Cistus; (3) to interpret evolution of key morphological characters; and (4) to describe biogeographic patterns in the Mediterranean basin and in the colonization of the Canary Islands.
Section snippets
DNA extraction, gene amplification, and sequencing
A total of 47 individuals representing the 20 species of Cistus, one of Fumana, two of Halimium, two of Helianthemum, and one of Tuberaria were sampled for ITS, trnL-F, and matK sequencing (Supplementary Table S1). Total genomic DNA was extracted from material collected in the field, material in the living collections of R.G. Page, O. Filippi, and the Royal Botanic Garden of Madrid, and from two herbarium specimens (MA). Field collections were dried in silica gel. DNA was extracted using Kneasy
Characteristics of trnL-F, ITS, and matK sequences
The characteristics of the three data sets are summarized in Table 2. Within Cistus, trnL-F sequence divergence ranges from 0.0% (between the 17 conspecific accessions and between C. clusii–C. munbyi, C. symphytifolius–C. chinamadensis, and C. albidus–C. creticus) to 3.15% (between C. parviflorus 1–C. monspeliensis 1) using the K-2-p model of evolution; matK sequence divergence ranges from 0.0% (between 12 conspecific accessions and between C. albidus–C. creticus, C. albidus–C. heterophyllus,
Systematic implications
Analysis of trnL-F sequences supports the monophyly of the Cistaceae genera using Fumana, Helianthemum, Tuberaria, Halimium, and Cistus (Fig. 2). All phylogenetic analyses are congruent with the monophyly of the Cistus–Halimium assemblage. A close relationship between these two genera was suggested in a phyletic diagram by Dansereau (1939). The two representatives of Halimium section Halimium (H. umbellatum) and section Commutata (H. calycinum) appear to have arisen from the same lineage
Acknowledgments
The authors thank M. Carine, R.G. Page, L. Lledó, V. Savolainen, and two anonymous reviewers for helpful discussion on the manuscript; O. Fiz, L. Lledó, and G. Nieto for advice on some analyses; E. Cano for lab assistance; M. Vorontsova for Russian-English translations; A. Fernández, O. Filippi, A. Herrero, J. Leralta, M. Luceño, J. Martínez, E. Narbona, R.G. Page, and V. Valcarcel for plant materials. This research is supported by the Spanish Dirección General de Investigación y Técnica
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