scholarly journals Comparative analysis of pollen release biomechanics inThalictrum: implications for evolutionary transitions between animal and wind pollination

2019 ◽  
Vol 224 (3) ◽  
pp. 1121-1132 ◽  
Author(s):  
David Timerman ◽  
Spencer C. H. Barrett

2014 ◽  
Vol 11 (101) ◽  
pp. 20140866 ◽  
Author(s):  
David Timerman ◽  
David F. Greene ◽  
Javier Urzay ◽  
Josef D. Ackerman

In wind pollination, the release of pollen from anthers into airflows determines the quantity and timing of pollen available for pollination. Despite the ecological and evolutionary importance of pollen release, wind–stamen interactions are poorly understood, as are the specific forces that deliver pollen grains into airflows. We present empirical evidence that atmospheric turbulence acts directly on stamens in the cosmopolitan, wind-pollinated weed, Plantago lanceolata , causing resonant vibrations that release episodic bursts of pollen grains. In laboratory experiments, we show that stamens have mechanical properties corresponding to theoretically predicted ranges for turbulence-driven resonant vibrations. The mechanical excitation of stamens at their characteristic resonance frequency caused them to resonate, shedding pollen vigorously. The characteristic natural frequency of the stamens increased over time with each shedding episode due to the reduction in anther mass, which increased the mechanical energy required to trigger subsequent episodes. Field observations of a natural population under turbulent wind conditions were consistent with these laboratory results and demonstrated that pollen is released from resonating stamens excited by small eddies whose turnover periods are similar to the characteristic resonance frequency measured in the laboratory. Turbulence-driven vibration of stamens at resonance may be a primary mechanism for pollen shedding in wind-pollinated angiosperms. The capacity to release pollen in wind can be viewed as a primary factor distinguishing animal- from wind-pollinated plants, and selection on traits such as the damping ratio and flexural rigidity may be of consequence in evolutionary transitions between pollination systems.



2010 ◽  
Vol 365 (1537) ◽  
pp. 99-109 ◽  
Author(s):  
Spencer C. H. Barrett

Flowering plants display spectacular floral diversity and a bewildering array of reproductive adaptations that promote mating, particularly outbreeding. A striking feature of this diversity is that related species often differ in pollination and mating systems, and intraspecific variation in sexual traits is not unusual, especially among herbaceous plants. This variation provides opportunities for evolutionary biologists to link micro-evolutionary processes to the macro-evolutionary patterns that are evident within lineages. Here, I provide some personal reflections on recent progress in our understanding of the ecology and evolution of plant reproductive diversity. I begin with a brief historical sketch of the major developments in this field and then focus on three of the most significant evolutionary transitions in the reproductive biology of flowering plants: the pathway from outcrossing to predominant self-fertilization, the origin of separate sexes (females and males) from hermaphroditism and the shift from animal pollination to wind pollination. For each evolutionary transition, I consider what we have discovered and some of the problems that still remain unsolved. I conclude by discussing how new approaches might influence future research in plant reproductive biology.





Author(s):  
Elliot M. Gardner ◽  
Mira Garner ◽  
Robyn Cowan ◽  
Steven Dodsworth ◽  
Niroshini Epitawalage ◽  
...  

AbstractWe present a densely-sampled phylogenomic study of the mulberry tribe (Moreae, Moraceae), an economically important clade with a global distribution, revealing multiple losses of inflexed stamens, a character traditionally used to circumscribe Moreae. Inflexed stamens facilitate ballistic pollen release and are associated with wind pollination, and the results presented here suggest that losses of this character state may have evolved repeatedly in Moraceae. Neither Moreae nor several of its major genera (Morus, Streblus, Trophis) were found to be monophyletic. A revised system for a monophyletic Moreae is presented, including the reinstatement of the genera Ampalis, Maillardia, Taxotrophis, and Paratrophis, and the recognition of the new genus Afromorus, based on Morus subgenus Afromorus. Pseudostreblus is reinstated and transferred to the Parartocarpeae, and Sloetiopsis is reinstated and transferred to the Dorstenieae. The tribe Olmediae is reinstated, replacing the Castilleae, owing to the reinstatement of the type genus Olmedia, and its exclusion from Moreae. Streblus s.s. is excluded from Moreae and transferred to the Olmediae, which is characterized primarily by involucrate inflorescences without regard to stamen position. Eight new combinations are made.



2018 ◽  
Vol 285 (1893) ◽  
pp. 20182251 ◽  
Author(s):  
David Timerman ◽  
Spencer C. H. Barrett

Wind pollination has evolved from insect pollination in numerous angiosperm lineages and is associated with a characteristic syndrome of morphological traits. The traits initiating transitions to wind pollination and the ecological drivers involved are poorly understood. Here, we examine this problem in Thalictrum pubescens , an ambophilous (insect and wind pollination) species that probably represents a transitional state in the evolution of wind pollination. We investigated wind-induced pollen release by forced harmonic motion by measuring stamen natural frequency ( f n ), a key vibration parameter, and its variability among nine populations. We assessed the repeatability of f n over consecutive growing seasons, the effect of this parameter on pollen release in a wind tunnel, and male reproductive success in the field using experimental manipulation of the presence or absence of pollinators. We found significant differences among populations and high repeatability within genotypes in f n . The wind tunnel assay revealed a strong negative correlation between f n and pollen release. Siring success was greatest for plants with lower f n when pollinators were absent, but this advantage diminished when pollinators were present. Our biomechanical analysis of the wind–flower interface has identified f n as a key trait for understanding early stages in the transition from insect to wind pollination.



2013 ◽  
Vol 280 (1765) ◽  
pp. 20130913 ◽  
Author(s):  
Spencer C. H. Barrett

Flowering plants are characterized by striking variation in reproductive systems, and the evolutionary lability of their sexual traits is often considered a major driver of lineage diversification. But, evolutionary transitions in reproductive form and function are never entirely unconstrained and many changes exhibit strong directionality. Here, I consider why this occurs by examining transitions in pollination, mating and sexual systems, some of which have been considered irreversible. Among pollination systems, shifts from bee to hummingbird pollination are rarely reversible, whereas transitions from animal to wind pollination are occasionally reversed. Specialized pollination systems can become destabilized through a loss of pollinator service resulting in a return to generalized pollination, or more commonly a reliance on self-pollination. Homomorphic and heteromorphic self-incompatibility systems have multiple origins but breakdown to self-compatibility occurs much more frequently with little evidence for subsequent gains, at least over short time-spans. Similarly, numerous examples of the shift from outcrossing to predominant self-fertilization are known, but cases of reversal are very limited supporting the view that autogamy usually represents an evolutionary dead-end. The evolution of dioecy from hermaphroditism has also been considered irreversible, although recent evidence indicates that the occurrence of sex inconstancy and hybridization can lead to the origin of derived sexual systems from dioecy. The directionality of many transitions clearly refutes the notion of unconstrained reproductive flexibility, but novel adaptive solutions generally do not retrace earlier patterns of trait evolution.



2010 ◽  
Vol 365 (1539) ◽  
pp. 351-368 ◽  
Author(s):  
Spencer C. H. Barrett

Charles Darwin studied floral biology for over 40 years and wrote three major books on plant reproduction. These works have provided the conceptual foundation for understanding floral adaptations that promote cross-fertilization and the mechanisms responsible for evolutionary transitions in reproductive systems. Many of Darwin's insights, gained from careful observations and experiments on diverse angiosperm species, remain remarkably durable today and have stimulated much current research on floral function and the evolution of mating systems. Here I review Darwin's seminal contributions to reproductive biology and provide an overview of the current status of research on several of the main topics to which he devoted considerable effort, including the consequences to fitness of cross- versus self-fertilization, the evolution and function of stylar polymorphisms, the adaptive significance of heteranthery, the origins of dioecy and related gender polymorphisms, and the transition from animal pollination to wind pollination. Post-Darwinian perspectives on floral function now recognize the importance of pollen dispersal and male outcrossed siring success in shaping floral adaptation. This has helped to link work on pollination biology and mating systems, two subfields of reproductive biology that remained largely isolated during much of the twentieth century despite Darwin's efforts towards integration.



Sign in / Sign up

Export Citation Format

Share Document