Losing one's touch: Evolution of the touch‐sensitive stigma in the <i>Mimulus guttatus</i> species complex

Friedman, Jannice; Hart, Katherine S.; Bakker, Meghan C. den

doi:10.3732/ajb.1600394

Cited by 11 publications

(16 citation statements)

References 38 publications

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“…In their native sites, each monkeyflower species is surrounded by thousands of conspecifics in close proximity (∼10–1000 per m 2 ) and cross‐pollination is facilitated through a touch‐sensitive stigma, with closing triggered by pollinators (Friedman et al. 2017). The arrays we used in this study did not allow us to make an accurate estimation of reproductive interference in an ecologically realistic way.…”

Section: Discussionmentioning

confidence: 99%

“…In animal pollinated plant species, reproductive interference via competition for pollination can reduce outcrossing rates by reducing conspecific pollen transfer or increasing heterospecific pollen transfer (Bell et al 2005). In their native sites, each monkeyflower species is surrounded by thousands of conspecifics in close proximity (∼10-1000 per m 2 ) and crosspollination is facilitated through a touch-sensitive stigma, with closing triggered by pollinators (Friedman et al 2017). The arrays we used in this study did not allow us to make an accurate estimation of reproductive interference in an ecologically realistic way.…”

Section: Pollination and Reproductive Interference With Inbreeding De...mentioning

confidence: 99%

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Inbreeding depression contributes to the maintenance of habitat segregation between closely related monkeyflower species

2021

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Incompletely reproductively isolated species often segregate into different microhabitats, even when they are able to survive and reproduce in both habitats. Longer term evolutionary factors may contribute to this lack of cross‐habitat persistence. When reproductive interference reduces immigrant fitness, assortative mating, including self‐fertilization, increases immigrants’ fitness in a single generation, but longer term, inbreeding depression may reduce the chance of population persistence. Two California monkeyflower species repeatedly segregate into drier and wetter areas in their zone of sympatry. To test whether inbreeding depression may contribute to the maintenance of this segregation pattern, we transplanted outbred and successively inbred Mimulus guttatus and Mimulus nudatus into their native habitats and heterospecific habitats. We measured germination, survival, and seed set and found that recurrent selfing reduced all aspects of fitness in both species, most strongly in foreign habitats. A simulation model, parameterized from the transplant experiment, found that inbreeding reduced fitness to such an extent that sequentially inbred populations of either species would be unable to persist in heterospecific‐occupied habitats in the absence of continued gene flow. These results demonstrate that individual immigrants are unlikely to form persistent populations and thus, inbreeding depression contributes to the absence of fine‐scale coexistence in this species pair.

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Section: Discussionmentioning

confidence: 99%

Section: Pollination and Reproductive Interference With Inbreeding De...mentioning

confidence: 99%

Inbreeding depression contributes to the maintenance of habitat segregation between closely related monkeyflower species

2021

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“…1c), stigmas risk self-triggering through physical contact with the anthers or corolla tube in bud. Reopening after insufficient pollination provides touch-sensitive stigmas with a second chance to increase pollen loads (Burck 1902;Newcombe 1922Newcombe , 1924Fetscher and Kohn 1999;Jin et al 2015;Friedman et al 2017). However, selfers may have highest fitness if they remain continuously open to selfpollination until all ovules are fertilized rather closing prematurely or attempting to actively "count" pollen tubes after closure.…”

Section: Loss Of Touch-sensitive Stigma Closure -An Independent Compo...mentioning

confidence: 99%

“…Less widely known are thigmonastic movements of floral parts upon contact by animal pollinators (Braam 2005); these include moderately rapid movements of stamens and corolla (Henning et al 2018; Dai et al 2021; Li et al 2022; Tagawa et al 2022) and rapid (as little as 2 seconds) closure of stigma lobes in many members of the Lamiales (Newcombe 1922). Stigma thigmonasty is widespread, evolutionarily labile (Friedman et al 2017), and linked to reproductive fitness (Fetscher and Kohn 1999; Krishna et al 2023), making it an appealing system for understanding the evolutionary genetic of floral mechanosensing and motion. However, despite nearly 150 years of study of touch-sensitive stigma movement (Darwin 1877; Todd 1879; Miyoshi 1891; Burck 1902; Lloyd 1911; Newcombe 1922, 1924), we still know almost nothing about its genetic mechanisms.…”

Section: Introductionmentioning

confidence: 99%

Undoing the ‘nasty: dissecting touch-sensitive stigma movement (thigmonasty) and its loss in self-pollinating monkeyflowers

Fishman,

McIntosh,

Nelson

et al. 2024

Preprint

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Rapid touch-sensitive stigma closure is a novel plant reproductive trait found in hundreds of Lamiales species. The origins, mechanisms, and functions of stigma closure remain poorly understood, but its repeated loss in self-fertilizing taxa and direct tests implicate adaptive roles in animal-mediated cross-pollination. Here, we document several additional losses of stigma closure in monkeyflowers (Mimulus), then use quantitative trait locus (QTL) mapping and gene expression analyses to provide a first glimpse into the genetic and molecular basis of stigma mechanosensing and movement. Variation in stigma closure in hybrids between selfer/non-closer Mimulus nasutus and outcrosser/fast-closer M. guttatus has a moderately complex genetic basis, with four QTLs together explaining ~70% of parental divergence. Loss of stigma closure in M. nasutus appears genetically independent from other aspects of the floral selfing syndrome and from a parallel loss in M. parishii. Analyses of stylar gene expression in closer M. guttatus, M. nasutus, and a rare M. guttatus non-closer genotype identify functional candidates involved in mechanosensing, turgor regulation, and cell wall remodeling. Together, these analyses reveal a polygenic genetic architecture underlying gain and loss of a novel plant movement, illuminate selfer-outcrosser reproductive divergence, and initiate mechanistic investigations of an unusually visible manifestation of plant intelligence.

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“…Many flowering plants have evolved touch-sensitive stamens, pistils, petals, and other structures (Braam, 2005). Touch-sensitive stigmas have been found in Bignoniaceae, Mazaceae, Phrymaceae, Lentibulariaceae, Acanthaceae, and Martyniaceae (Newcombe, 1922(Newcombe, , 1924Jin et al, 2015;Friedman et al, 2017). They are structures generally composed of two or three active stigma lobelets that close after mechanical touch or pollen deposition (Henderson, 1840;Anderson, 1922) (Figure 1).…”

mentioning

confidence: 99%

Effects of heterospecific pollen on stigma behavior in Campsis radicans: Causes and consequences

Zou

Wang

Lyu

et al. 2022

American J of Botany

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Premise: Pollinator sharing of co-flowering plants may result in interspecific pollen receipt with a fitness cost. However, the underlying factors that determine the effects of heterospecific pollen (HP) are not fully understood. Moreover, the cost of stigma closure induced by HP may be more severe for plants with special touch-sensitive stigmas than for plants with non-touch-sensitive stigmas. Very few studies have assessed HP effects on stigma behavior. Methods: We conducted hand-pollination experiments with 10 HP donors to estimate HP effects on stigma behavior and stigmatic pollen germination in Campsis radicans (Bignoniaceae) at low and high pollen loads. We assessed the role of phylogenetic distance between donor and recipient, pollen size, and pollen aperture number in mediating HP effects. Additionally, we observed pollen tube growth to determine the conspecific pollen-tube-growth advantage. Results: Stigma behavior differed significantly with HP of different species. Pollen load increased, while pollen size decreased, the percentage of permanent closure and stigmatic germination of HP. Stigmatic HP germination increased with increasing aperture number. However, HP effects did not depend on phylogenetic distance. In addition, conspecific pollen had a pollen-tube-growth advantage over HP. Conclusions: Our results provide a good basis for understanding the stigma-pollen recognition process of plant taxa with touch-sensitive stigmas. We concluded that certain flowering traits drive the HP effects on the post-pollination period. To better understand the impact of pollinator sharing and interspecific pollen transfer on plant evolution, we highlight the importance of evaluating more factors that determine HP effects at the community level.

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Losing one's touch: Evolution of the touch‐sensitive stigma in the Mimulus guttatus species complex

Cited by 11 publications

References 38 publications

Inbreeding depression contributes to the maintenance of habitat segregation between closely related monkeyflower species

Inbreeding depression contributes to the maintenance of habitat segregation between closely related monkeyflower species

Undoing the ‘nasty: dissecting touch-sensitive stigma movement (thigmonasty) and its loss in self-pollinating monkeyflowers

Effects of heterospecific pollen on stigma behavior in Campsis radicans: Causes and consequences

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