Introgression in peripheral populations and colonization shape the genetic structure of the coastal shrub Armeria pungens

Abstract

The coastal shrub Armeria pungens has a disjunct Atlantic-Mediterranean distribution. The historic range expansion underlying this distribution was investigated using the nuclear internal transcribed spacer region, three plastid regions (namely trnL-F, trnS-fM and matK) and morphometric data. A highly diverse ancestral lineage was identified in southwest Portugal. More recently, two areas have been colonized: (1) Corsica and Sardinia, where disjunct Mediterranean populations have been established as a result of the long-distance dispersal of Portuguese genotypes, and (2) the southern part of the Atlantic range, Gulf of Cadiz, where a distinct lineage showing no genetic differentiation among populations occurs. Genetic consequences of colonization seem to have been more severe in the Gulf of Cadiz than in Corsica-Sardinia. Although significant genetic divergence is associated with low plastid diversity in the Gulf of Cadiz, in Corsica-Sardinia, the loss of plastid haplotypes was not accompanied by divergence from disjunct Portuguese source populations. In addition, in its northernmost and southernmost populations, A. pungens exhibited evidence for ancient or ongoing introgression from sympatric congeners. Introgression might have created novel genotypes able to expand beyond the latitudinal margins of the species or, alternatively, these genotypes may be the result of surfing of alleles from other species in demographic equilibrium into peripheral populations of A. pungens. Our results highlight the evolutionary significance of genetic drift following the colonization of new areas and the key role of introgression in range expansion.

Figure 1

(a) Distribution and sampling of A. pungens. Locations sampled for the morphological and molecular studies (three cpDNA regions trnL-F, trnS-fM matK and nrDNA ITS) are numbered as populations from 1 to 23, and the total distribution of the species is represented in the background (in gray). (b) Distribution and sampling of the congeners sympatric to A. pungens. A total of 19 populations of coastal and subcoastal Armeria species were sampled for sequencing of three cpDNA regions (trnL-F, trnS-fM and matK) and partly for the nrDNA ITS. The approximate distribution of the nine species studied is represented according to Bernis (1955); Arrigoni (1970) and Nieto Feliner (1990). Population names and sample information are provided in Supplementary information S1 and S2B.

Figure 2

Main genetic groups in A. pungens. (a) Geographic distribution of the 16 plastid haplotypes (trnL-F, trnS-fM, matK) found in 112 individuals from 23 populations of A. pungens (numbered as in Supplementary information S1). (b) Statistical parsimony network showing the genealogical relationships among the 16 plastid haplotypes. (c) Geographic distribution of ITS profiles across 59 individuals from 23 populations of A. pungens: R1a denotes typical Western Mediterranean ribotype (Fuertes Aguilar and Nieto Feliner, 2003), without polymorphic sites in direct sequencing; R1b, R1c, R1d, R1e indicate polymorphic site in different positions that are interpreted as intragenomic cooccurrence of more that one ITS sequence (Table 1).

Figure 3

Geographic distribution of the leaf pubescence in A. pungens. The percentages of ciliate (black), glabrous (white), dense pubescent (gray) and puberulous (patterned) leaves are indicated for each population. A. pungens individuals are labeled with population numbers as described in Supplementary information S1 and Figure 2a.

Figure 4

Chloroplast phylogenetic tree (trnL-F, trnS-fM, matK) of A. pungens and sympatric congeners. Overall, 50% majority rule consensus of 87 MP trees depicting the phylogenetic relationships between the plastid haplotypes of 23 populations of A. pungens and 36 individuals from 19 populations of 10 coastal and subcoastal congeners. Bootstrap supports above 50% are indicated above the branches both without (in bold) and with an additional binary character representing the presence/absence of indels. Posterior probabilities of the Bayesian analysis are indicated below branches. The names of chloroplast haplotypes and main genetic groups in A. pungens are indicated according to Figures 2a and b. A. pungens individuals are labeled with population numbers as described in Supplementary information S1 and Figure 1a. The name and population of origin of the other species follow Supplementary information S2 and Figure 1b.