The colonization history of Juniperus brevifolia (Cupressaceae) in the Azores Islands

Abstract

Background: A central aim of island biogeography is to understand the colonization history of insular species using current distributions, fossil records and genetic diversity. Here, we analyze five plastid DNA regions of the endangered Juniperus brevifolia, which is endemic to the Azores archipelago.

Methodology/principal findings: The phylogeny of the section Juniperus and the phylogeographic analyses of J. brevifolia based on the coalescence theory of allele (plastid) diversity suggest that: (1) a single introduction event likely occurred from Europe; (2) genetic diversification and inter-island dispersal postdated the emergence of the oldest island (Santa Maria, 8.12 Ma); (3) the genetic differentiation found in populations on the islands with higher age and smaller distance to the continent is significantly higher than that on the younger, more remote ones; (4) the high number of haplotypes observed (16), and the widespread distribution of the most frequent and ancestral ones across the archipelago, are indicating early diversification, demographic expansion, and recurrent dispersal. In contrast, restriction of six of the seven derived haplotypes to single islands is construed as reflecting significant isolation time prior to colonization.

Conclusions/significance: Our phylogeographic reconstruction points to the sequence of island emergence as the key factor to explain the distribution of plastid DNA variation. The reproductive traits of this juniper species (anemophily, ornithochory, multi-seeded cones), together with its broad ecological range, appear to be largely responsible for recurrent inter-island colonization of ancestral haplotypes. In contrast, certain delay in colonization of new haplotypes may reflect intraspecific habitat competition on islands where this juniper was already present.

Figure 1. The Azores archipelago.

Island groups and maximum geological ages according to França et al. .

Figure 2. Phylogenetic relationships within Juniperus section inferred from trnL and trnL-trnF, and divergence time-scale derived from BEAST.

Numbers before taxon names refer to the coding no. given in Tables 1/S1. Numbers above branches are BEAST posterior probabilities; numbers below branches are Maximum Likelihood bootstrap support values (before slashes); and Maximum Parsimony bootstrap support values (after slashes). Asterisks indicate absence of support. Gray bars represent divergence times (95% highest posterior density intervals) for each node, while numbers in white circles represent calibration points obtained from Mao et al. : (1) split between sects. Juniperus-Caryocedrus (49.1–29.9 Mya), (2) crown of sect. Juniperus (29.9–11.1 Mya) and (3) crown of BSG in sect. Juniperus (17.5–4.7 Mya). BEAST posterior probability values for calibration nodes were inferred from Mao et al. .

Figure 3. cpDNA (petN-psbM/trnS-trnG/trnT-trnL) haplotype network and its spatial distribution in the Azores archipelago.

Each haplotype is represented by both a number and a color. Haplotype sizes are proportional to the number of individuals displaying them. Distinct clades (A and B) are shown within boxes.

Figure 4. Relaxed molecular-clock chronogram and phylogeographic reconstruction of Juniperus brevifolia.

Maximum clade credibility tree summarized from the geospatial Bayesian analysis of cpDNA (petN-psbM, trnS-trnG and trnT-trnL sequences) of 71 individuals of J. brevifolia. Pie charts represent posterior probability distributions of ancestral range at well-supported nodes of interest. Colored rectangles represent the sample's island of origin. The haplotype relatedness is also shown in the well-supported clades. Colonization routes supported by a BF>3 are shown on the map. The color of each route represents its relative support, with more intense colors indicating stronger support. Arrows specify directionality in the colonization route, inferred from well-supported nodes of interest in the geospatial Bayesian analysis. The map is based on satellite images available in Google Earth (http://earth.google.com).