Mixed Mating in Homostylous Species: Genetic and Experimental Evidence from an Alpine Plant with Variable Herkogamy,Primula halleri

Abstract

(2018). Mixed mating in homostylous species: genetic and experimental evidence from an alpine plant with variable herkogamy, Primula halleri. Editor: Christina CarusoPremise of research. Self-compatibility is a requirement for reproductive assurance via selfing and may therefore be beneficial in environments with infrequent or unpredictable pollinator service. However, selfcompatible plants may spatially separate anthers from stigmatic surface within flowers (herkogamy), potentially preventing autonomous self-pollination while promoting outcrossing. We investigated the effects of herkogamy on patterns of mating in a self-compatible, homostylous alpine herb, Primula halleri, which evolved from obligately outcrossing, heterostylous ancestors. Primula halleri displays diminishing herkogamy during anthesis, affecting its capacity for self-pollination. Specifically, we tested whether higher herkogamy at the end of anthesis (terminal herkogamy) promotes higher outcrossing rates at the cost of lower seed set, while lower terminal herkogamy ensures seed set via self-pollination at the cost of inbreeding.Methodology. We estimated family-and population-level genetic outcrossing rates in four populations using microsatellites and derived an estimate for inbreeding depression. We tested effects of different levels of terminal herkogamy on means and variances of outcrossing rates. We also assessed whether seed set was resource or pollen limited. We interpreted results in light of previously published data on seed set with and without pollinator-exclusion treatment. Pivotal results. Population-level outcrossing rates ranged between 0.5 and 0.8. Outcrossing rates of plants with higher terminal herkogamy had similar means but lower variances than those of plants with lower terminal herkogamy. This result demonstrates that separation between sexual organs larger than 1 mm in mature flowers favors outbreeding, while below this threshold, delayed selfing ensures reproduction.Conclusions. Contrary to long-held notions about the association of homostyly and selfing, we provide new genetic evidence that the homostylous P. halleri adopts a mixed mating system due to variable herkogamy. Moreover, our results support a trade-off between seed number and seed quality effected through variation in herkogamy, illustrating that herkogamy affects multiple aspects of reproductive fitness simultaneously.

Evolution of Autonomous Selfing in Marginal Habitats: Spatiotemporal Variation in the Floral Traits of the Distylous Primula wannanensis

“…Further analysis revealed that the average seed set rate via selfing was relatively high (> 0.55 for all herkogamy classes; Figure 8 ) and showed no significant difference among herkogamy classes with separation less than 1.0 mm; however, the seed set rate sharply decreased to less than 0.10 with an increase in separation ( Figure 8 ). This sharp decline in the seed set rate could be explained based on the assumption that the HE value of 1.0 mm possibly represents an approximate threshold, consistent with previous studies on the homostylous species P. halleri ( de Vos et al, 2014 , 2018 ) and distylous species Primula chungensis ( Jiang et al, 2018 ), suggesting that this threshold likely has wider applicability, although experimental confirmation is needed.…”

“…Autonomous selfing is a common strategy employed by plants to accommodate an unpredictable pollinator environment because selfed seeds can provide reproductive assurance ( Lloyd, 1992 ; Barrett, 2002 ). The spatial and/or temporal separation of female and male organs within flowers of self-compatible plants is generally assumed to have a direct impact on the degree of selfing and the capacity to autonomous self-pollination ( Barrett, 2002 ; Nishihiro et al, 2000 ; Brys and Jacquemyn, 2011 ; de Vos et al, 2014 , 2018 ). In distylous species, a commonly exhibited heteromorphic incompatibility system prevents self- and intramorph mating, and a significant component of phenotypic disassortative mating is maintained under the interaction of pollinator and reciprocal herkogamy in distylous species exhibiting self- and/or intramorph compatibility (e.g., Luculia pinceana ; Zhou et al, 2015 ).…”

Herkogamy, a Principal Functional Trait of Plant Reproductive Biology

“…de Vos et al 2018 Turnera ulmifolia Turneraceae Population + Positive relationship between herkogamy and outcrossing rate among 13 populations.…”

Mating system ofDatura inoxia: association between selfing rates and herkogamy within populations

“…When associations among selfing rate (s), inbreeding coefficient (F) and herkogamy are maintained over time, within-population covariance among these variables may be established at the lineage level. Significant associations between high outcrossing rate and approach herkogamy have been reported before (Takebayashi, Wolf & Delph, 2006;De Vos et al, 2018; but see Chen et al, 2009;Brys & Jacquemyn, 2012;Opedal, Armbruster & Pélabon, 2015;Toräng et al, 2017). However, few studies have evaluated the association between herkogamy and outcrossing rate within-populations (Epperson & Clegg, 1987;Motten & Antonovics, 1992;Carr & Fenster, 1994;Karron et al, 1997;Brunet & Eckert, 1998;Takebayashi & Delph, 2000;Elle & Hare, 2002;Medrano, Herrera & Barret, 2005;Herlihy & Eckert, 2007) and even fewer have considered relationships among herkogamy, inbreeding coefficient and mating system.…”