Growth form evolution and hybridization in Senecio (Asteraceae) from the high equatorial Andes

Abstract

Changes in growth forms frequently accompany plant adaptive radiations, including páramo-a high-elevation treeless habitat type of the northern Andes. We tested whether diverse group of Senecio inhabiting montane forests and páramo represented such growth form changes. We also investigated the role of Andean geography and environment in structuring genetic variation of this group. We sampled 108 populations and 28 species of Senecio (focusing on species from former genera Lasiocephalus and Culcitium) and analyzed their genetic relationships and patterns of intraspecific variation using DNA fingerprinting (AFLPs) and nuclear DNA sequences (ITS). We partitioned genetic variation into environmental and geographical components. ITS-based phylogeny supported monophyly of a Lasiocephalus-Culcitium clade. A grade of herbaceous alpine Senecio species subtended the Lasiocephalus-Culcitium clade suggesting a change from the herbaceous to the woody growth form. Both ITS sequences and the AFLPs separated a group composed of the majority of páramo subshrubs from other group(s) comprising both forest and páramo species of various growth forms. These morphologically variable group(s) further split into clades encompassing both the páramo subshrubs and forest lianas, indicating independent switches among the growth forms and habitats. The finest AFLP genetic structure corresponded to morphologically delimited species except in two independent cases in which patterns of genetic variation instead reflected geography. Several morphologically variable species were genetically admixed, which suggests possible hybrid origins. Latitude and longitude accounted for 5%-8% of genetic variation in each of three AFLP groups, while the proportion of variation attributed to environment varied between 8% and 31% among them. A change from the herbaceous to the woody growth form is suggested for species of high-elevation Andean Senecio. Independent switches between habitats and growth forms likely occurred within the group. Hybridization likely played an important role in species diversification.

Keywords: Andes; Culcitium; Lasiocephalus; Neotropical montane forest; Senecio; adaptive radiation; growth forms; hybridization; páramo.

Figure 1

Growth form variation among the investigated Senecio species from the high Andes: (a) S. lingulatus, Ecuador, páramo; (b) S. longepenicillatus, Venezuela, superpáramo; (c) high‐elevation form of S. otophorus, Colombia, superpáramo; (d) S. mojandensis, Ecuador, páramo; (e) S. superandinus, Ecuador, superpáramo; (f) Senecio nivalis, Ecuador, superpáramo, (g) S. pindilicensis, Ecuador, montane forest; (h) S. patens, Ecuador, montane forest. Symbols are colored according to species assignment to the main structure clusters (see Figure 2); symbol shape indicates the growth form, that is, square–basal rosette herb, circle–narrow‐leaved subshrub, triangle–broad‐leaved liana

Figure 2

(a) Assignment of 374 individuals (entire dataset) of high‐elevation Andean Senecio into three main AFLP clusters inferred in structure; (b) Geographical locations of populations with growth form and structure cluster assignment indicated; (c) Ordination of AFLP phenotypes by use of principal coordinate analysis (PCoA) based on Jaccard distances. The symbol coloration reflects the assignment of the individuals to the main structure clusters (white–admixed individuals with assignment probability below 0.5); symbol shape indicates the growth form, that is, square–basal rosette herb, circle–narrow‐leaved subshrub, triangle–broad‐leaved liana

Figure 3

Genetic structure and geographical distribution of 149 individuals of high‐elevation Andean Senecio from cluster A. (a) Posterior probabilities for membership of each individual in the three resulting subgroups (designated by different colors) as identified in a separate structure analysis of cluster A members. (b) Geographical distribution of the analyzed populations. (c) Ordination of AFLP phenotypes (PCoA); symbol color refers to the structure subgroups (>0.5 posterior probability), symbol shape indicates species

Figure 4

Genetic structure and geographical distribution of 47 individuals of high‐elevation Andean Senecio from cluster B. (a) Posterior probabilities for membership of each individual in the five resulting subgroups (designated by different colors) as identified in a separate structure analysis of cluster B members. (b) Geographical distribution of the analyzed populations. (c) Ordination of AFLP phenotypes (PCoA); symbol color refers to the structure subgroups (>0.5 posterior probability), symbol shape indicates species

Figure 5

Genetic structure and geographical distribution of 116 individuals of high‐elevation Andean Senecio from cluster C. (a) Posterior probabilities for membership of each individual in the five resulting subgroups (designated by different colors) as identified in a separate structure analysis of cluster C members. (b) Geographical distribution of the analyzed populations. (c) Ordination of AFLP phenotypes (PCoA); symbol color refers to the structure subgroups (>0.5 posterior probability), symbol shape indicates species

Figure 6

(a) Phylogenetic reconstruction of 87 accessions of northern Andean Senecio based on sequences of ITS region of ribosomal DNA. Bayesian 50% majority rule consensus tree with posterior probabilities >0.90 and bootstrap values >50% inferred with maximum parsimony are indicated, respectively, before and after the slash above each supported branch. Supported subclades of the “forest” and “páramo” clades are marked as f1–f6 and p1–p2, respectively. Growth form of each accession is marked by a symbol, membership in the AFLP subgroups (if applicable) is denoted by corresponding letters (A1–C5), accessions with ambiguous structure assignment are marked “MIX.” The presence of highly divergent ITS sequences in the same individual of S. aff. quitensis is marked by an arrow. Senecio doryphyllus, S. decipiens, and S. alatopetiolatus, although belonging to the former Lasiocephalus, were not analyzed using the AFLPs. Reconstruction of the growth form evolution according to the equal rates (ER) model has been superimposed onto the ITS tree (see Appendix S3E for original). (b) Relationships among AFLP phenotypes of 266 nonadmixed (see Section 2) individuals of former Lasiocephalus and Senecio nivalis reconstructed in Bayesian framework. Cluster codes correspond with Figures 3, 4, 5; branches with posterior probabilities >0.95 are marked with dots