Correlated polymorphism in cytotype and sexual system within a monophyletic species, Lycium californicum

Abstract

Background and aims: Polyploidy has important effects on reproductive systems in plants and has been implicated in the evolution of dimorphic sexual systems. In particular, higher ploidy is associated with gender dimorphism across Lycium species (Solanaceae) and across populations within the species Lycium californicum. Previous research on the association of cytotype and sexual system within L. californicum sampled a limited portion of the species range, and did not investigate evolutionary transitions between sexual systems. Lycium californicum occurs in arid regions on offshore islands and mainland regions in the south-western United States and Mexico, motivating a more comprehensive analysis of intraspecific variation in sexual system and cytotype across the full range of this species.

Methods: Sexual system (dimorphic vs. cosexual) was determined for 34 populations across the geographical range of L. californicum using field observations of pollen production, and was confirmed using morphological measurements and among-plant correlations of primary sexual traits. Ploidy was inferred using flow cytometry in 28 populations. DNA sequence data from four plastid and two nuclear regions were used to reconstruct relationships among populations and to map transitions in sexual system and ploidy.

Key results: Lycium californicum is monophyletic, ancestrally diploid and cosexual, and the association of gender dimorphism and polyploidy appears to have two evolutionary origins in this species. Compared with cosexual populations, dimorphic populations had bimodal anther size distributions, negative correlations between male and female floral traits, and larger coefficients of variation for primary sexual traits. Flow cytometry confirmed tetraploidy in dimorphic populations, whereas cosexual populations were diploid.

Conclusions: Tetraploidy and gender dimorphism are perfectly correlated in L. californicum, and the distribution of tetraploid-dimorphic populations is restricted to populations in Arizona and the Baja California peninsula. The analysis suggests that tetraploidy and dimorphism likely established in Baja California and may have evolved multiple times.

Keywords: DNA content; Lycium californicum; Solanaceae; dioecy; gender dimorphism; male sterility; plant mating system; polymorphism; polyploidy; sexual system.

Fig. 1.

Populations of Lycium californicum included in the present study (see also Table 1); open circles represent diploid, cosexual populations and closed circles tetraploid, dimorphic populations (see Results). Arrows indicate one cosexual (SMI) and one dimorphic (CDC) population with unknown ploidy. The species range (indicated by dashed lines) was taken from Chiang-Cabrera (1981) and includes southern California (including the Channel Islands), the Baja California peninsula, south-central Arizona, and mainland Mexico along the Gulf of California and in several interior states. Note that this species is found on both the mainland and offshore islands.

Fig. 2.

(A) Frequency distribution of anther length for hermaphroditic plants in cosexual populations (open bars) and males and females in dimorphic populations (shaded bars) in Lycium californicum. (B) Among-plant pairwise correlations for floral traits in cosexual (open bars) and dimorphic (shaded bars) populations. Significance is shown for three levels: ***P < 0·0001, **P < 0·005 and *P < 0·05. Numbers of populations, individuals and flowers are, respectively, 17, 227 and 1094 in cosexual populations and nine, 236 and 1146 in dimorphic populations.

Fig. 3.

Haplotype network based on four plastid regions including 142 accessions of Lycium californicum sampled from 28 populations. Haplotypes are represented by letters and the size of the circle represents the haplotype frequency in the analysis. Shading indicates the recovery of a haplotype in either cosexual (white) or dimorphic (black) populations. The haplotype with the highest outgroup probability, as determined by TCS, was haplotype A. Asterisks represent missing haplotypes.

Fig. 4.

Maximum-likelihood ancestral state reconstruction of sexual strategy (left) and cytotype (right) on the tree from a combined analysis of plastid and nuclear data. Posterior probabilities are illustrated with asterisks (*≥50 %, **≥70 %). Closed circles represent proportional likelihood support for dimorphic or 4x character states, and open circles for cosexual or 2x states. Circles with horizontal lines represent taxa for which character state data are unknown. Lycium carolinianum shows variation in sexual system and cytotype and was coded as polymorphic. Populations of L. californicum are labelled as in Table 1 and are included in the dashed box.