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1. Evidence of fruit syndromes in the recently diverged wild tomato clade opens new possibilities for the study of fleshy fruit evolution

   https://doi.org/10.1002/ppp3.10399  

   Barnett, Jacob R. ; Sharma, Rovin ; Buonauro, Gina ; Gillis, Ian M. ; Rashidzade, Maryam ; Caicedo, Ana L. ( June 2023 , PLANTS, PEOPLE, PLANET)

   Fleshy fruits provide humans with many flavorful and nutritious crops. Understanding the diversity of these plants is fundamental to managing agriculture and food security in a changing world. This study surveyed fruit trait variation across species of tomato wild relatives and explored associations among color, size, shape, sugars, and acids. These wild tomato species native to South America can be interbred with the economically important cultivated tomato. Beyond its application to tomatoes, deepening our knowledge of how fruit traits evolve together is valuable to crop improvement efforts aimed at breeding more nutritious and appealing varieties of fruits.

   Fleshy fruits display a striking diversity of traits, many of which are important for agriculture. The evolutionary drivers of this variation are not well understood, and most studies have relied on variation found in the wild. Few studies have explored this question on a fine‐grained scale with a group of recently diverged species while controlling for environmental effects.

   We developed the tomato clade as a novel system for fruit trait evolution research by presenting the first common garden‐based systematic survey of variation and phylogenetic signal in color, nutrition, and morphology traits across all 13 species of tomato wild relatives (Solanum sect.Lycopersicon). We laid the groundwork for further testing of potential evolutionary drivers by assessing patterns of clustering and correlation among disperser‐relevant fruit traits as well as historical climate variables.

   We found evidence of two distinct clusters of associated fruit traits defined by color, sugar type, and malic acid concentration. We also observed correlations between a fruit's external appearance and internal nutrient content that could function as honest signals to dispersers. Analyses of historical climate and soil variables revealed an association between red/orange/yellow fruits and high annual average temperature.

   Our results establish the tomato clade as a promising system for testing hypotheses on the drivers of divergence behind early‐stage fleshy fruit evolution, particularly selective pressure from frugivores.

    

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2. Flowering time responses to warming drive reproductive fitness in a changing Arctic

   https://doi.org/10.1093/aob/mcae007  

   Collins, Courtney G. ; Angert, Amy L. ; Clark, Karin ; Elmendorf, Sarah C. ; Elphinstone, Cassandra ; Henry, Greg H. R. ( January 2024 , Annals of Botany)

   The Arctic is warming at an alarming rate, leading to earlier spring conditions and plant phenology. It is often unclear to what degree changes in reproductive fitness (flower, fruit and seed production) are a direct response to warming versus an indirect response through shifting phenology. The aim of this study was to quantify the relative importance of these direct and indirect pathways and project the net effects of warming on plant phenology and reproductive fitness under current and future climate scenarios.

   We used two long-term datasets on 12 tundra species in the Canadian Arctic as part of the International Tundra Experiment (ITEX). Phenology and reproductive fitness were recorded annually on tagged individual plants at both Daring Lake, Northwest Territories (64° 52' N, - 111° 35' W) and Alexandra Fiord, Nunavut (78° 49' N, - 75° 48' W). The plant species encompassed a wide taxonomic diversity across a range of plant functional types with circumpolar/boreal distributions. We used hierarchical Bayesian structural equation models to compare the direct and indirect effects of climate warming on phenology and reproductive fitness across species, sites and years.

   We found that warming, both experimental and ambient, drove earlier flowering across species, which led to higher numbers of flowers and fruits produced, reflecting directional phenotypic selection for earlier flowering phenology. Furthermore, this indirect effect of climate warming mediated through phenology was generally about two to three times stronger than the direct effect of climate on reproductive fitness. Under future climate predictions, individual plants showed a ~2- to 4.5-fold increase in their reproductive fitness (flower counts) with advanced flowering phenology.

   Our results suggest that, on average, the benefits of early flowering, such as increased development time and subsequent enhanced reproductive fitness, might outweigh its risks. Overall, this work provides important insights into population-level consequences of phenological shifts in a warming Arctic over multi-decadal time scales.

    

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3. Water availability drives population divergence and sex‐specific responses in a dioecious plant

   https://doi.org/10.1002/ajb2.1359  

   Delph, Lynda F. ( September 2019 , American Journal of Botany)

   Water availability is an important abiotic factor, resulting in differences between plant species growing in xeric and mesic habitats. Species with populations occurring in both habitat types allow examination of whether water availability has acted as a selective force at the intraspecific level. Investigating responses to water availability with a dioecious species allows determination of whether males and females, which often have different physiologies and life histories, respond differently.

   An experiment varying water availability was performed under an outdoor rain‐out shelter using plants from two mesic and two xeric populations of the dioecious plantSilene latifolia. Early growth rate, flowering propensity, flower size, and specific leaf area were measured. At the end of the season, the plants were harvested, aboveground and root biomass were measured, and the total number of flowers and fruit produced were counted.

   Compared to the two mesic populations, plants from the two xeric populations grew more slowly, were less likely to flower, took longer to flower, had thicker leaves, invested less in aboveground biomass and more in root biomass, produced fewer flowers and fruit, but were more likely to live. Many traits exhibited significant habitat type × treatment interactions. Compared to the xeric populations, males—but not females—from mesic populations had less root biomass and greatly reduced their flower production in response to low water availability.

   Mesic and xeric populations responded in ways congruent with water availability being a selective force for among‐population divergence, especially for males.

    

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4. Adaptation to hummingbird pollination is associated with reduced diversification in Penstemon

   https://doi.org/10.1002/evl3.130  

   Wessinger, Carolyn A. ; Rausher, Mark D. ; Hileman, Lena C. ( October 2019 , Evolution Letters)

   A striking characteristic of the Western North American flora is the repeated evolution of hummingbird pollination from insect-pollinated ancestors. This pattern has received extensive attention as an opportunity to study repeated trait evolution as well as potential constraints on evolutionary reversibility, with little attention focused on the impact of these transitions on species diversification rates. Yet traits conferring adaptation to divergent pollinators potentially impact speciation and extinction rates, because pollinators facilitate plant reproduction and specify mating patterns between flowering plants. Here, we examine macroevolutionary processes affecting floral pollination syndrome diversity in the largest North American genus of flowering plants, Penstemon. Within Penstemon, transitions from ancestral bee-adapted flowers to hummingbird-adapted flowers have frequently occurred, although hummingbird-adapted species are rare overall within the genus. We inferred macroevolutionary transition and state-dependent diversification rates and found that transitions from ancestral bee-adapted flowers to hummingbird-adapted flowers are associated with reduced net diversification rate, a finding based on an estimated 17 origins of hummingbird pollination in our sample. Although this finding is congruent with hypotheses that hummingbird adaptation in North American Flora is associated with reduced species diversification rates, it contrasts with studies of neotropical plant families where hummingbird pollination has been associated with increased species diversification. We further used the estimated macroevolutionary rates to predict the expected pattern of floral diversity within Penstemon over time, assuming stable diversification and transition rates. Under these assumptions, we find that hummingbird-adapted species are expected to remain rare due to their reduced diversification rates. In fact, current floral diversity in the sampled Penstemon lineage, where less than one-fifth of species are hummingbird adapted, is consistent with predicted levels of diversity under stable macroevolutionary rates.

    

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5. Fruit traits of pioneer trees structure seed dispersal across distances on tropical deforested landscapes: Implications for restoration

   https://doi.org/10.1111/1365-2664.13697  

   Camargo, Paulo H. S. A. ; Pizo, Marco A. ; Brancalion, Pedro H. S. ; Carlo, Tomás A. ; Hampe, ed., Arndt ( July 2020 , Journal of Applied Ecology)

   Pioneer trees with fleshy fruits are typically planted in restoration projects to attract frugivores as a mean to increase dispersal and accelerate forest regeneration. However, differences in fruit traits of pioneer trees can potentially influence dispersal and their restoration outcomes.

   Here we investigated the effects of bird and plant traits, and distance to forest fragments, on the seed rain using a tree‐planting experiment replicated in 12 deforested sites in Brazil. Factors were fruit traits of pioneer trees (wind‐dispersed, bird‐dispersed with lipids or with carbohydrates and controls) and distance (10, 50, 300 m) from forest fragments.

   We found that density and richness of birds and seeds decreased exponentially with distance from fragments, yet these effects were minor compared to the effects of fruit traits on the structure of the seed rain.

   Overall, plots with fleshy fruited pioneers attracted much greater bird activity and seed dispersal than plots with wind‐dispersal pioneers and the controls. For instance, plots with carbohydrate‐rich fruits received more than twice the average species richness and density of birds and seeds of plots with lipid‐rich pioneer trees, surpassing wind‐dispersed pioneers by more than 80%, and controls by over 90%. Furthermore, the fruit trait treatments resulted in morphological shifts in the average traits of visiting birds. Significant differences in bill gape and flight capacities (wing‐loading) were associated with the differences in the seed rain associated with each treatment.

   Synthesis and applications. Understanding how trait‐matching processes mediating mutualistic seed dispersal by frugivores interact with distance‐dependent dispersal limitation on deforested tropical landscapes is critical for improving forest restoration efforts. This is especially relevant in the context of applied nucleation. As shown here, avian seed dispersal can thus be manipulated in restoration projects in order to increase connectivity and speed up forest recovery and the provision of the multiple ecosystem services that follow forest succession.

    

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