Associations between sex‐organ deployment and morph bias in related heterostylous taxa with different stylar polymorphisms

Abstract

Heterostyly is a genetic polymorphism in which populations are composed of two (distyly) or three (tristyly) fl oral morphs that differ in the reciprocal placement of stigmas and anthers within fl owers ( Darwin, 1877 ;Barrett, 1992 ). Th e genetic control of the polymorphism in distylous plants usually involves a single Mendelian diallelic locus in which the long-styled morph is of genotype ss and the short-styled morph is of genotype Ss , although in several species the dominance relations at the S -locus are reversed ( Lewis and Jones, 1992 ). Th e fl oral morphs are maintained in populations by negative frequency-dependent selection resulting from intermorph (disassortative) mating. With this genetic system and disassortative mating, a 1:1 morph ratio (isoplethy; Finney, 1953 ) is expected in equilibrium populations.Th e classic textbook depiction of heterostyly as a balanced polymorphism (e.g., Roughgarden, 1979 ;Silvertown and Charlesworth, 2009 ;Charlesworth and Charlesworth, 2010 ) is largely based on knowledge of distyly in Primula and emphasizes how the reciprocal positioning of sex organs (reciprocal herkogamy) associated with a self and intramorph incompatibility system (heteromorphic incompatibility) promotes outcrossing in populations. PREMISE OF THE STUDY:Populations of heterostylous species are characterized by two or three fl oral morphs with reciprocal positioning of stigmas and anthers. Theoretical models predict equal morph frequencies (isoplethy) when disassortative mating is prevalent in populations, but biased morph ratios may occur when variation in the expression of heterostyly causes deviations from intermorph mating. METHODS:We explore the role of sex-organ deployment in governing morph ratios in two closely related genera of Boraginaceae, exhibiting striking variation in fl oral traits associated with the heterostylous syndrome. We sampled 66 populations of six species of Glandora and 39 populations of three species of Lithodora across their distributional range in the Mediterranean. In each population we estimated morph ratios and measured several fl oral traits. We used phylogenetically corrected and noncorrected regressions to test the hypothesis that diff erences in sex-organ reciprocity and herkogamy are associated with deviations from isoplethy.KEY RESULTS: Biased morph ratios occurred in 24% of populations, particularly in Lithodora . Populations biased for the long-styled morph (L-morph) were more frequent than the short-styled morph (S-morph). Distylous species were less likely to exhibit biased ratios than species with stigma-height dimorphism. In Lithodora fruticosa , a species lacking reciprocity, decreased herkogamy in the S-morph was associated with increasing L-morph bias, perhaps resulting from self-interference. CONCLUSION:Striking variation in the expression of heterostyly in Glandora and Lithodora is associated with biased morph ratios, which probably result from pollinator-mediated mating asymmetries within populations.

Gender specialisation and stigma height dimorphism in Mediterranean Lithodora fruticosa (Boraginaceae)

“…These observations partly confirm conclusions reached in previous work on the species (Ferrero et al . ,c, ), which also point to stigma height dimorphism as ancestral to reciprocal herkogamy (distyly) found elsewhere in the genus (Ferrero et al . ).…”

“…In contrast, the biased morph ratios found by Ferrero et al . () suggest that, in the populations they observed with an excess of long‐styled plants, within‐morph mating occurred among long‐styled more frequently than among short‐styled individuals.…”

“…Interestingly, Ferrero et al . () surveyed 22 populations of L. fruticosa in eastern Spain, of which only eight were isoplethic and 13 showed an excess of the long‐styled morph. Isoplethy in the population studied here is consistent with the maintenance of polymorphism with strongly (or even exclusively) disassortative mating.…”

“…Note that I measured the length of the floral tube as a reference point for the other measurements, whereas Ferrero et al . () measured the full corolla length rather than diameter and floral tube length.…”

“…In this article, I present evidence for a divergence in gender between morphs of large population of the Mediterranean species Lithodora fruticosa (Boraginaceae), a small woody shrub that displays a stylar height dimorphism (Ferrero et al . , ,b,c, ). In contrast to M. pubescens just cited (Li et al .…”