The evolvability of herkogamy: Quantifying the evolutionary potential of a composite trait

Opedal, Øystein H.; Bolstad, Geir H.; Hansen, Thomas F.; Armbruster, W. Scott; Pélabon, Christophe

doi:10.1111/evo.13258

Cited by 44 publications

(57 citation statements)

References 81 publications

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“…Interestingly, both studies detected rapid evolution of traits that exhibited greater-than-average evolvabilities. The increased rate of selfing in M. guttatus was associated with reduced herkogamy (anther-stigma separation), which appears to be a highly evolvable trait (Opedal et al, 2017;and see Results). Similarly, the evolvability of volatile concentrations in Brassica rapa, computed from the heritabilities reported by Zu et al (2016), was very high with a median of 32.3% (Table S3).…”

Section: Researchmentioning

confidence: 74%

“…(5) Herkogamy was measured on a ratio scale as defined in Opedal et al . (), i.e. as absolute anther–stigma distance.…”

Section: Methodsmentioning

confidence: 99%

“…(4) Reward traits were those representing the amount of reward produced or the rate of reward secretion. (5) Herkogamy was measured on a ratio scale as defined in Opedal et al (2017), i.e. as absolute anther-stigma distance.…”

Section: Literature Surveymentioning

confidence: 99%

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The evolvability of animal‐pollinated flowers: towards predicting adaptation to novel pollinator communities

Opedal

2018

New Phytologist

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In the event of a community turnover, population decline, or complete disappearance of pollinators, animal-pollinated plants may respond by adapting to novel pollinators or by changing their mating system. The ability of populations to adapt is determined by their ability to respond to novel selection pressures, i.e. their evolvability. In the short term, evolvability is determined by standing genetic variation in the trait under selection. To evaluate the evolutionary potential of plant reproductive systems, I compiled genetic-variance estimates for a large selection of floral traits mediating shifts in pollination and mating systems. Then, I computed evolvabilities and compared these among trait groups and against the evolvabilities of vegetative traits. Evolvabilities of most floral traits were substantial yet tended to be lower than the median for vegetative traits. Among floral traits, herkogamy (anther-stigma distance), floral-display traits and perhaps floral-volatile concentrations had greater-than-average evolvabilities, while the evolvabilities of pollinator-fit traits were below average. These results suggest that most floral traits have the potential to evolve rapidly in response to novel selection pressures, providing resilience of plant reproductive systems in the event of changing pollinator communities.

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Section: Researchmentioning

confidence: 74%

“…(5) Herkogamy was measured on a ratio scale as defined in Opedal et al . (), i.e. as absolute anther–stigma distance.…”

Section: Methodsmentioning

confidence: 99%

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The evolvability of animal‐pollinated flowers: towards predicting adaptation to novel pollinator communities

Opedal

2018

New Phytologist

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“…However, several studies found herkogamy to have a strong genetic basis (e.g., Herlihy and Eckert 2007;Luo and Widmer 2013), and a comprehensive review concluded that the trait is typically highly heritable and evolvable (Opedal et al 2017). Moreover, the profound functional implications of sexual organ position Keller et al 2012Keller et al , 2014Keller et al , 2016) justify speculating about possible adaptive explanations for the existence of high-herkogamous plants.…”

Section: Simultaneous Effects On Number Of Seeds and Mating Mode Of Smentioning

confidence: 99%

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

Vos

Keller

Zhang

et al. 2018

International Journal of Plant Sciences

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(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.

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“…In addition to exploring how selection has shaped floral changes that follow the mating system transition, we use the Qst-Fst approach to detect selection for increased selfing itself. In self-compatible morning glories, selfing rate is controlled by herkogamy (anther-stigma separation), a quantitative trait known to be evolutionarily labile in many species (Chang & Rausher, 1998;Duncan & Rausher, 2013a;Opedal, Bolstad, Hansen, Armbruster, & Pélabon, 2017). We therefore use the Qst-Fst framework to determine whether selection favored reduced herkogamy in I. lacunosa.…”

mentioning

confidence: 99%

Multiple aspects of the selfing syndrome of the morning glory Ipomoea lacunosa evolved in response to selection: A Qst‐Fst comparison

Rifkin

Liao

Castillo

et al. 2019

Ecology and Evolution

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The frequent transition from outcrossing to selfing in flowering plants is often accompanied by changes in multiple aspects of floral morphology, termed the “selfing syndrome.” While the repeated evolution of these changes suggests a role for natural selection, genetic drift may also be responsible. To determine whether selection or drift shaped different aspects of the pollination syndrome and mating system in the highly selfing morning glory Ipomoea lacunosa , we performed multivariate and univariate Qst‐Fst comparisons using a wide sample of populations of I. lacunosa and its mixed‐mating sister species Ipomoea cordatotriloba . The two species differ in early growth, floral display, inflorescence traits, corolla size, nectar, and pollen number. Our analyses support a role for natural selection driving trait divergence, specifically in corolla size and nectar traits, but not in early growth, display size, inflorescence length, or pollen traits. We also find evidence of selection for reduced herkogamy in I. lacunosa , consistent with selection driving both the transition in mating system and the correlated floral changes. Our research demonstrates that while some aspects of the selfing syndrome evolved in response to selection, others likely evolved due to drift or correlated selection, and the balance between these forces may vary across selfing species.

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The evolvability of herkogamy: Quantifying the evolutionary potential of a composite trait

Cited by 44 publications

References 81 publications

The evolvability of animal‐pollinated flowers: towards predicting adaptation to novel pollinator communities

The evolvability of animal‐pollinated flowers: towards predicting adaptation to novel pollinator communities

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

Multiple aspects of the selfing syndrome of the morning glory Ipomoea lacunosa evolved in response to selection: A Qst‐Fst comparison

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