Phylogenetic relationships, diversification and expansion of chili peppers (Capsicum, Solanaceae)

Abstract

Background and aims: Capsicum (Solanaceae), native to the tropical and temperate Americas, comprises the well-known sweet and hot chili peppers and several wild species. So far, only partial taxonomic and phylogenetic analyses have been done for the genus. Here, the phylogenetic relationships between nearly all taxa of Capsicum were explored to test the monophyly of the genus and to obtain a better knowledge of species relationships, diversification and expansion.

Methods: Thirty-four of approximately 35 Capsicum species were sampled. Maximum parsimony and Bayesian inference analyses were performed using two plastid markers (matK and psbA-trnH) and one single-copy nuclear gene (waxy). The evolutionary changes of nine key features were reconstructed following the parsimony ancestral states method. Ancestral areas were reconstructed through a Bayesian Markov chain Monte Carlo analysis.

Key results: Capsicum forms a monophyletic clade, with Lycianthes as a sister group, following both phylogenetic approaches. Eleven well-supported clades (four of them monotypic) can be recognized within Capsicum, although some interspecific relationships need further analysis. A few features are useful to characterize different clades (e.g. fruit anatomy, chromosome base number), whereas some others are highly homoplastic (e.g. seed colour). The origin of Capsicum is postulated in an area along the Andes of western to north-western South America. The expansion of the genus has followed a clockwise direction around the Amazon basin, towards central and south-eastern Brazil, then back to western South America, and finally northwards to Central America.

Conclusions: New insights are provided regarding interspecific relationships, character evolution, and geographical origin and expansion of Capsicum A clearly distinct early-diverging clade can be distinguished, centred in western-north-western South America. Subsequent rapid speciation has led to the origin of the remaining clades. The diversification of Capsicum has culminated in the origin of the main cultivated species in several regions of South to Central America.

Keywords: Capsicum; South America; chilli peppers; dysploidy; flowering features; geographical expansion; phylogeny; pungency.

Fig. 1.

Flowers and fruits of the Andean (A–G), Caatinga (H, I), Flexuosum (J–M) and Bolivian (N–Q) clades. (A, B) Capsicum dimorphum flower (A) and fruit (B). (C, D) Capsicum geminifolium flower (C) and fruit (D). (E, F) Different accessions of C. rhomboideum showing variations in corolla shape (rotate-campanulate in E vs. campanulate in F) and flower arrangement (solitary flowers in E vs. multi-flowered fascicles in F); pedicels always non-geniculate. (G) Capsicum lanceolatum flowering branch showing non-geniculate pedicels and white and violet corollas. (H) Capsicum caatingae fascicle of immature fruits (note the toothless calyx). (I) Capsicum parvifolium flower and immature fruit. (J–L) Capsicum flexuosum flower (J), fruiting branch, showing red pendant mature fruits (K) and blackish brown seeds (L). (M) Capsicum aff. flexuosum flower. (N, O) Capsicum caballeroi flower (N) and mature fruit (O) showing fully yellow corolla, non-geniculate pedicels and red pericarp. (P, Q) Capsicum minutiflorum flower (P) and mature dark red fruit (Q). Photos by G. Beltrán (A, B, D), C. Carrizo García (C, E, F, J–Q), M. Sterpetti (G, H) and G. Barboza (I).

Fig. 2.

Flowers and fruits of the Longidentatum (A), Atlantic (B–I), Purple Corolla (J–K), Pubescens (L, M), Baccatum (N, O) and Annuum (P, Q) clades. (A) Capsicum longidentatum fruit. (B) Capsicum cornutum flower with stellate corolla and geniculate pedicel. (C) Capsicum pereirae flower with spotted stellate corolla. (D) Capsicum friburgense urceolate-campanulate corolla and pedicel geniculate. (E) Capsicum mirabile stellate corolla with dark red spots. (F) Capsicum hunzikerianum flower with spotted stellate corolla. (G, H) Capsicum sp. nov. (GEB & CCG 3637) stellate corolla with golden-green spots (G) and mature greenish-golden yellow fruit, without well-developed calyx teeth (H). Note the different patterns of spots in the corolla in C and E–G. (I) Capsicum villosum var. muticum immature fruit; note the absence of well-developed teeth. (J) Capsicum cardenasii pendant flower with shortly tubular corolla and non-geniculate flowering pedicel. (K) Capsicum eximium flower with stellate corolla. (L, M) Capsicum pubescens flower (L) and longitudinal section of a mature fruit showing large blackish brown seeds (M). (N) Capsicum baccatum var. pendulum flower showing the distinctive green spots in the corolla. (O) Capsicum chacoense flower showing immaculate white corolla and geniculate flowering pedicel. (P) Capsicum annuum var. annuum flowering and fruiting branch showing typical white corolla and entire calyx without well-developed teeth. (Q) Capsicum chinense flowering branch showing pendant flowers with non-geniculate flowering pedicels and entire calyx without well-developed teeth. Photos by G. Barboza (A, B, F), M. Sterpetti (C, D) and C. Carrizo García (E, G–Q).

Fig. 3.

Schematic structure of waxy and position of the primers used in this study (the horizontal lines represent the fragments amplified/sequenced).

Fig. 4.

Phylogenetic reconstruction of Capsicum (combined data set of three markers, matK, psbA-trnH spacer and waxy) and species grouping proposed. (A) Strict consensus of two most parsimonious trees obtained from maximum-parsimony analysis. Bootstrap support values, mostly above 50 %, are given on each branch. (B) Phylogram obtained from Bayesian inference analysis. Posterior probabilities above 0·8 are given for each branch. Names of taxa and accessions correspond to those listed in the Table S1. Empty arrows point to the clades including most cultivated chillies. Nodes with low BS (<70 %) are marked with an asterisk.

Fig. 5.

Evolution of key characters in Capsicum using parsimony as reconstruction method. Character state changes are shown by black rectangles with the number of the character (see Table S2; characters 8 and 9 do not vary in Capsicum, not shown in the figure) on a maximum-parsimony consensus tree.

Fig. 6.

Fruit pericarp anatomy in Capsicum based on scanning electron microscopy in transverse section. (A) Pericarp without giant cells in C. rhomboideum. (B, C) Pericarp with giant cells in the innermost layer of the mesocarp (arrow, B) and detail of giant cells (arrow, C) in C. flexuosum. Scale bars: A, B, 500 μm; C, 200 μm.

Fig. 7.

Hypothesis of Capsicum expansion. (A) Ancestral areas reconstructed by Bayesian MCMC analysis. Pie charts are larger for the main nodes to make them more evident. Area assignment for each species is shown after taxon name. Colour codes reflect the major clades based on the phylogenetic results (grey scale for the Annuum Clade). References: A, Peru; B, Ecuador; C, Colombia; D, Venezuela; E, Central America (including Mexico); F, south-eastern Brazil (Atlantic Forest ecoregion); G, central–eastern Brazil (Caatinga ecoregion); H, north-eastern Argentina and eastern Paraguay (Alto Paraná Atlantic forests ecoregion); I, central–western Paraguay; J, north-western and central Argentina; K, northern, north-eastern and south-eastern Bolivia (mostly lowlands); L, western and south-western Bolivia (mostly highlands); M, western Brazil; and N, Galapagos Islands. (B) Schematic expansion of the species. The arrows represent clades and monotypic lineages going across and/or pointing to the areas inhabited by their species. Markings in different colours/shapes indicate selected population localities. In order not to over-complicate the presentation, the taxa of the Annuum Clade are mentioned in their appropriate place but without markings and partly without arrows.