Abstract The study of adaptation helps explain biodiversity and predict future evolution. Yet the process of adaptation can be difficult to observe due to limited phenotypic variation in contemporary populations. Furthermore, the scarcity of male fitness estimates has made it difficult to both understand adaptation and evaluate sexual conflict hypotheses. We addressed both issues in our study of two anther position traits in wild radish (Raphanus raphanistrum): anther exsertion (long filament − corolla tube lengths) and anther separation (long − short filament lengths). These traits affect pollination efficiency and are particularly interesting due to the unusually high correlations among their component traits. We measured selection through male and female fitness on wild radish plants from populations artificially selected to recreate ancestral variation in each anther trait. We found little evidence for conflicts between male and female function. We found strong evidence for stabilizing selection on anther exsertion and disruptive selection on anther separation, indicating positive and negative correlational selection on the component traits. Intermediate levels of exsertion are likely an adaptation to best contact small bees. The function of anther separation is less clear, but future studies might investigate pollen placement on pollinators and compare species possessing multiple stamen types.
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Rapid evolution of a family‐diagnostic trait: artificial selection and correlated responses in wild radish, Raphanus raphanistrum
Summary The mechanisms underlying trait conservation over long evolutionary time scales are poorly known. These mechanisms fall into the two broad and nonmutually exclusive categories of constraint and selection. A variety of factors have been hypothesized to constrain trait evolution. Alternatively, selection can maintain similar trait values across many species if the causes of selection are also relatively conserved, while many sources of constraint may be overcome over longer periods of evolutionary divergence. An example of deep trait conservation is tetradynamy in the large family Brassicaceae, where the four medial stamens are longer than the two lateral stamens. Previous work has found selection to maintain this difference in lengths, which we call anther separation, in wild radish, Raphanus raphanistrum . Here, we test the constraint hypothesis using five generations of artificial selection to reduce anther separation in wild radish. We found a rapid linear response to this selection, with no evidence for depletion of genetic variation and correlated responses to this selection in only four of 15 other traits, suggesting a lack of strong constraint. Taken together, available evidence suggests that tetradynamy is likely to be conserved due to selection, but the function of this trait remains unclear.
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- PAR ID:
- 10451170
- Date Published:
- Journal Name:
- New Phytologist
- Volume:
- 239
- Issue:
- 6
- ISSN:
- 0028-646X
- Page Range / eLocation ID:
- 2382 to 2388
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Traits conserved across evolutionary time often provide compelling examples of key adaptations for a given taxonomic group. Tetradynamy is the presence of four long stamens plus two short stamens within a flower and is conserved across most of the roughly 4000 species in the mustard family, Brassicaceae. While this differentiation in stamens is hypothesized to play a role in pollination efficiency, very little is known about the potential function of the two stamen types. The present study sheds new light on this mystery using wild radish (Raphanus raphanistrum), a widespread and well-studied tetradynamous plant. We used data collected from slow-motion videos of pollinators visiting wild radish flowers to test three adaptive hypotheses (not mutually exclusive): (H1) short and long stamens are specialized for either feeding or pollinating; (H2) short and long stamens are specialized for different pollinator taxa; and (H3) the presence of short and long stamens increases pollinator movement and thus effectiveness. We find evidence consistent with hypothesis H3, but no evidence for hypotheses H1 or H2. Thus, tetradynamy may be an adaptation for generalized pollination, enabling effective visits by the variety of pollinators visiting most species of Brassicaceae.more » « less
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Abstract Background and AimsFew studies of angiosperms have focused on androecial evolution in conjunction with evolutionary shifts in corolla morphology and pollinator relationships. The Western Hemisphere clade of Justiciinae (Acanthaceae) presents the rare opportunity to examine remarkable diversity in staminal morphology. We took a phylogenetically informed approach to examine staminal diversity in this hypervariable group and asked whether differences in anther thecae separation is associated with phylogenetically informed patterns of variation in corolla morphology. We further discuss evidence for associations between anther diversity and pollinators in this lineage. MethodsFor the Dianthera/Sarotheca/Plagiacanthus (DSP) clade of Western Hemisphere Justiciinae, we characterized floral diversity based on a series of corolla measurements and using a model-based clustering approach. We then tested for correlations between anther thecae separation and corolla traits, and for shifts in trait evolution, including evidence for convergence. Key ResultsThere is evolutionary vagility in corolla and anther traits across the DSP clade with little signal of phylogenetic constraint. Floral morphology clusters into four distinct groups that are, in turn, strongly associated with anther thecae separation, a novel result in Acanthaceae and, to our knowledge, across flowering plants. These cluster groups are marked by floral traits that strongly point to associations with pollinating animals. Specifically, species that are known or likely to be hummingbird pollinated have stamens with parallel thecae, whereas those that are likely bee or fly pollinated have stamens with offset, divergent thecae. ConclusionsOur results suggest that anther thecae separation is likely under selection in concert with other corolla characters. Significant morphological shifts detected by our analyses corresponded to putative shifts from insect to hummingbird pollination. Results from this study support the hypothesis that floral structures function in an integrated manner and are likely subject to selection as a suite. Further, these changes can be hypothesized to represent adaptive evolution.more » « less
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Shaw, Ruth; Connallon, Tim (Ed.)Abstract Traits that have lost function sometimes persist through evolutionary time. Persistence may occur if there is not enough standing genetic variation for the trait to allow a response to selection, if selection against the trait is weak relative to drift, or if the trait has a residual function. To determine the evolutionary processes shaping whether nonfunctional traits are retained or lost, we investigated short stamens in 16 populations of Arabidopsis thaliana along an elevational cline in northeast Spain. A. thaliana is highly self-pollinating and prior work suggests short stamens do not contribute to self-pollination. We found a cline in short stamen number from retention of short stamens in high-elevation populations to incomplete loss in low-elevation populations. We did not find evidence that limited genetic variation constrains short stamen loss at high elevations, nor evidence for divergent selection on short stamens between high and low elevations. Finally, we identified loci associated with short stamens in northeast Spain that are different from loci associated with variation in short stamens across latitudes from a previous study. Overall, we did not identify the evolutionary mechanisms contributing to an elevational cline in short stamen number so further research is clearly warranted.more » « less
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{"Abstract":["Traits conserved across evolutionary time often provide compelling\n examples of key adaptations for a given taxonomic group. Tetradynamy is\n the presence of four long stamens plus two short stamens within a flower\n and is conserved across most of the roughly 4000 species in the mustard\n family, Brassicaceae. While this differentiation in stamens is\n hypothesized to play a role in pollination efficiency, very little is\n known about the potential function of the two stamen types. The present\n study sheds new light on this mystery using wild radish (Raphanus\n raphanistrum), a widespread and well-studied tetradynamous plant. We used\n data collected from slow-motion videos of pollinators visiting wild radish\n flowers to test three non-mutually exclusive adaptive hypotheses: 1) short\n and long stamens are specialized for either feeding or pollinating, 2)\n short and long stamens are specialized for different pollinator taxa, and\n 3) the presence of short and long stamens increases pollinator movement\n and thus effectiveness. We find evidence consistent with hypothesis three,\n but no evidence for hypotheses one or two. Thus, tetradynamy may be an\n adaptation for generalized pollination, enabling effective visits by the\n variety of pollinators visiting most species of Brassicaceae."],"TechnicalInfo":["# Data from: Testing adaptive hypotheses for an evolutionarily conserved\n trait through slow-motion videos of pollinators The data contained in\n these files was generated from close observation of slow-motion video\n footage by the same experimenter for each variable. ## Description of\n Files ### MainData.csv Data related to slow-motion video analysis,\n including plant information, anther and stigma contact, and number of\n movements Missing data are indicated by "NA" #### Basic Video\n Info in Columns A:F * VideoID: unique individual video identifier *\n PlantID: unique individual plant identifier with the following format -\n "PopulationCode FamilyCode-Replicate" * PopulationCode: BINY =\n natural population, Sep = separation-selected, Exsertion =\n exsertion-selected * FamilyCode: unique 3-5 character code for a given\n maternal seed family * Replicate: individual plant number between 0 and 9,\n where replicate 0 is indicated by the lack of a hyphen and number * Date:\n date of observations * Year: year of observations * Pollinator: taxa of\n visiting pollinator * VideoLength: total length of visit in 1/8 real-time\n seconds #### Feeding Info in Columns G:N * G:K are binary columns in which\n 1 indicates the visit included foraging in the given category, 0 indicates\n lack of foraging, and ? indicates uncertainty ("Short" = short\n stamen anthers, "Long" = long stamen anthers) * L:N summarize\n the info from G:K in different ways * Foraging: whether the visit included\n foraging on nectar, pollen, or both * Feed_All: for visits including\n pollen-foraging, whether foraging was on short stamen anthers, long stamen\n anthers, or both * Feed_Bin: same as Feed_All but groups "Long"\n and "Short" into "One" #### Contact Info in Columns\n O:AM Columns have the following format:\n "ResponseVariable_BodySection_FlowerPart" * ResponseVariable is\n what kind of contact is being recorded and can take three values: * sec:\n duration of contact in 1/8 real-time seconds * bin: binary contact, 1 =\n contacted and 0 = not contacted * n: count of body sections contacted\n (sums binary contact with Legs, Ventral, Side) * BodySection is the part\n of the pollinator body contacted and can take four values: Ventral, Side,\n Legs, or Total (sum of prior 3) * FlowerPart is the part of the flower\n contacted by the pollinator and can take 4 values: S (short stamen\n anthers), L (long stamen anthers), Stigma, or Anthers (both short and long\n stamen anthers) #### Movement Info in Columns AN:AR * Between_Moves: # of\n movements from feeding on one stamen to another * Within_Moves: # of\n movements within stamen types, combining movements from long to long\n stamen ("Long.Long_Moves") and movements from short to short\n stamen ("Short.Short_Moves") * Total_Moves: total # of movements\n from one stamen to another ### DyeSwab.csv Data from small preliminary\n test in which 3 bees were swabbed with gelatin cubes after visiting\n flowers with short and long stamens marked with different colors of\n fluorescent dye. * ID: unique individual bee identifier * BodySection: the\n body section swabbed * NParticles: count of dye particles contained in\n gelatin swab * StamenType: type of stamen matching the color of counted\n particles ### Final_Analysis_Dryad.R R script of all analyses used in the\n paper. * Details provided as comments within script. * The script was run\n in RStudio running R v. 4.4.2."]}more » « less
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