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Cozzolino, S.

Publications and source records attributed to Cozzolino, S..

10 recordsLinked to original sources

Evidence from the field that multiple processes maintain hidden adaptive capacity to a novel environment in a wild daisy

Populations often persist in novel environments despite predictions that adaptive capacity to such conditions should be limited by a lack of genetic variation. A leading hypothesis is that genetic variation for adapting to novel environments is maintained but remains hidden under native conditions. However, direct evidence for the mechanisms that maintain this adaptive potential in natural populations is scarce. Here, we integrate data from four large-scale field experiments to test whether variation in selection across life history and environments, together with genetic architecture, maintains genetic variation important for adapting to novel environments. Using a quantitative genetic breeding design, we generated families of the Sicilian daisy, Senecio chrysanthemifolius (Asteraceae), and planted seeds and cuttings across native and novel elevations on Mount Etna. We tracked fitness across elevations, life stages, seasons and generations. Genotypes with higher survival and flowering success at the novel elevation increased adaptive potential, but were only weakly selected against in the native environment where they had slightly lower fitness at a later life-history stage. A negative genetic correlation in seedling survival across seasons indicated that different genotypes were favoured across temporal variation in native environments. Crosses between genotypes with low and high fitness in the novel environment revealed that genotypes that increased adaptive potential had heritable effects on plasticity and fitness across generations, but were recessive and therefore largely hidden in heterozygotes. Together, these results provide rare field-based evidence that weak selection in native environments, temporal variation in selection and dominance effects act together to maintain cryptic adaptive potential in natural populations.

evolutionary biology↗

Are dumbbell stomata unique? Diversified developmental trajectories in sedges and grasses result in partially convergent stomata

Dumbbell-shaped stomata in grasses represent an evolutionary novelty, as their distinctive guard cell morphology is absent from most plant lineages. Stomata exhibit two major morphological forms: the kidney-shaped type found in most plants, and the dumbbell-shaped type that evolved in grasses. Dumbbell-like forms occur in sedges (Cyperaceae), providing an opportunity to examine how changes in developmental trajectories contribute to morphological evolution. By integrating analyses of cellulose microfibril organization, guard cell length to width ratio, and nuclear morphology, we demonstrate partial convergence between sedge and grass stomatal development. Specifically, cellulose microfibril organization in sedges represents an intermediate developmental state between kidney-shaped stomata and the grass dumbbell-shaped stomata. We further document differences in nuclear architecture: in contrast to kidney-shaped stomata, which have rounded nuclei in central guard cell regions, sedge nuclei are partially elongated and localize within bulbous regions, whereas grass nuclei exhibit fully elongated shapes along the cell axis. Notably, we identified secondary plasmodesmata between guard cells in one sedge species, suggesting a convergent route to symplastic communication achieved through secondary plasmodesmata formation rather than the incomplete cytokinesis characteristic of grasses. Together, these findings reveal convergent developmental solutions underlying similar stomatal morphologies.

plant biology↗

Genetic differences in plasticity across environmental scales determine fitness along an ecological gradient

When populations suffer reduced fitness in novel environments, genotypes that better adjust their phenotype to cope with environmental change can aid persistence by reducing the severity of fitness declines. However, we know little about how plastic changes in phenotype allow different genotypes to track environmental variation across ecological gradients, particularly as environments become novel. We transplanted numerous clones of 19 genotypes of a Sicilian daisy, Senecio chrysanthemifolius, at four elevations on Mt Etna. We assessed fitness at native and novel elevations and quantified leaf plasticity among and within elevations. Genotypes with higher fitness at novel elevations showed lower variance in fitness, lower plasticity across elevations, but higher plasticity within elevations compared to those with higher fitness in the native range. Our results suggest that there are genotypes hidden in a population whose plasticity better tracks novel environmental variation at multiple scales, which will be crucial for population persistence under rapid environmental change.

evolutionary biology↗

The evolutionary history of the common bean (Phaseolus vulgaris) revealed by chloroplast and nuclear genomes.

The remarkable evolutionary history of the common bean (Phaseolus vulgaris L.) has led to the emergence of three wild main genepools corresponding to three different ecogeographic areas: Mesoamerica, the Andes and northern Peru/Ecuador. Recent works proposed novel scenarios and the northern Peru/Ecuador population has been described as a new species called P. debouckii, rekindling the debate about the origin of P. vulgaris. Here we shed light on the origin of P. vulgaris by analysing the chloroplast and nuclear genomes of a large varietal collection representing the entire geographical distribution of wild forms. We assembled 37 chloroplast genomes de novo and used them to construct a time frame for the divergence of the genotypes under investigation, revealing that the separation of the Mesoamerican and northern Peru/Ecuador genepools occurred [~]0.15 Mya. Our results clearly support a Mesoamerican origin of the common bean and reject the recent P. deboukii hypothesis. These results also imply two independent migratory events from Mesoamerica to the North and South Andes, probably facilitated by birds. Our work represents a paradigmatic example of the importance of taking into account recombination events when investigating phylogeny and of the analysis of wild forms when studying the evolutionary history of a crop species.

genetics↗

Mimicking orchids lure bees from afar with exaggerated ultraviolet signals

O_LIFlowers have many sensory traits to appeal to pollinators, including ultraviolet (UV) absorbing markings, which are well known for attracting bees at close proximity (e.g. < 1 m). While striking UV signals have been thought to attract pollinators also at greater distances of meters, how the signals impact the plant pollination success over distance remains unknown. Here we report the case of the Australian orchid Diuris brumalis, a non-rewarding species, pollinated by bees via mimicry of rewarding pea plant Daviesia decurrens. When distant from the pea plant, Diuris brumalis was hypothesized to enhance pollinator attraction by exaggerately mimicking the floral ultraviolet (UV) reflecting patterns of its model. C_LIO_LIBy experimentally modulating floral UV reflectance with a UV screening solution, we quantified the orchid pollination success at variable distance from the model plants. C_LIO_LIWe demonstrate that the deceptive orchid Diuris brumalis attracts bee pollinators by emphasizing the visual stimuli, which mimic the floral UV signalling of the rewarding model D. decurrens. Moreover, the exaggerated UV reflectance of D. brumalis flowers impacted pollinators visitation at an optimal distance from D. decurrens, and the effect decreased when orchids were too close or too far away from the model. C_LIO_LIOur findings show that salient UV flower signalling plays a functional role in visual floral mimicry, likely exploiting perceptual gaps in bee neural coding, and mediates the plant pollination success at much greater spatial scales than previously expected. C_LI

ecology↗

Trick or Treat? Pollinator attraction in Vanilla pompona (Orchidaceae)

Natural pollination of species belonging to the pantropical orchid genus Vanilla remains poorly understood. Based on sporadic records, euglossine bees have been observed visiting flowers of Neotropical Vanilla species. Our research aimed at better understanding the pollinator attraction mechanism of the Neotropical species Vanilla pompona, a crop wild relative with valuable traits for vanilla crop improvement programs. Using video footage, we identified floral visitors and examined their behavior. The flowers of V. pompona attracted Eulaema cingulata males, which distinctively displayed two behaviors: floral scent collection and nectar search; with the latter leading to pollen removal. Morphological measurements of floral and visitor traits showed that other Eulaema species may also act as potential pollinators. Additionally, we recorded natural fruit set in three populations and over a period of two years, tested for nectar presence and analyzed floral fragrances through gas chromatography - mass spectrometry. We observed a low natural fruit set (2.42%) and did not detect nectar. Twenty floral volatile compounds were identified, with the dominant compound trans-carvone oxide previously found to attract Eulaema cingulata males. We hypothesize a dual attraction of Eulaema cingulata males to V. pompona flowers, based on floral fragrance reward as the primary long-distance attraction, and food deception for successful pollen removal. Further research confirming this hypothesis is recommended to develop appropriate conservation policies for Vanilla crop wild relatives, which are the primary reserves of this crops genetic variation.

plant biology↗

Plasticity in novel environments induces larger changes in genetic variance than adaptive divergence

Adaptive plasticity allows populations to cope with environmental variation but is expected to fail as conditions become unfamiliar. In novel conditions, populations may instead rely on rapid adaptation to increase fitness and avoid extinction. Adaptation should be fastest when both plasticity and selection occur in directions of the multivariate phenotype that contain abundant genetic variation. However, tests of this prediction from field experiments are rare. Here, we quantify how additive genetic variance in a multivariate phenotype changes across an elevational gradient, and test whether plasticity and selection align with genetic variation. We do so using two closely related, but ecologically distinct, sister species of Sicilian daisy (Senecio, Asteraceae) adapted to high and low elevations on Mount Etna. Using a paternal half-sibling breeding design, we generated and then reciprocally planted c.19,000 seeds of both species, across an elevational gradient spanning each species native elevation, and then quantified mortality and five leaf traits of emergent seedlings. We found that genetic variance in leaf traits changed more across elevations than between species. The high-elevation species at novel lower elevations showed changes in the distribution of genetic variance among the leaf traits, which reduced the amount of genetic variance in the directions of selection and the native phenotype. By contrast, the low-elevation species mainly showed changes in the amount of genetic variance at the novel high elevation, and genetic variance was concentrated in the direction of the native phenotype. For both species, leaf trait plasticity across elevations was in a direction of the multivariate phenotype that contained a moderate amount of genetic variance. Together, these data suggest that where plasticity is adaptive, selection on genetic variance for an initially plastic response could promote adaptation. However, large environmental effects on genetic variance are likely to reduce adaptive potential in novel environments.

evolutionary biology↗

Adaptive maternal effects in early life history traits help to maintain ecological resilience in novel environments for two contrasting Senecio species

While many organisms shift their development plastically to maintain fitness as environments change, such plasticity has limits. Population mean fitness is expected to decline when novel environments exceed the limits to plasticity, but the level of fitness costs is expected to vary among genotypes that can increase adaptive potential. We lack fundamental insights into how and when changes in early development traits increase adaptive potential in novel environments, which limits our ability to predict the response of natural populations to global change. To test whether genetic variation in development time is associated with increased adaptive potential in novel environments, we used a breeding design to generate c.20,000 seeds of two ecologically contrasting Sicilian species of daisies (Senecio, Asteraceae) adapted to high and low elevations on Mount Etna. We planted the seeds across four elevations that included the native range of each species, and a novel elevation. We tracked seedling mortality and measured development time as the number of days it took seedlings to establish. As predicted, genetic variance in survival increased at novel elevations. However, genetic variance in development time showed the opposite trend, decreasing at novel elevations. A strong negative genetic correlation between development time in the native range and survival at novel elevations suggested that genotypes with faster development in native environments survived better in novel environments. These results were consistent across the two ecologically contrasting species, suggesting that genetic variance in early development in native environments could be used to predict population responses to novel environments.

evolutionary biology↗

Hidden genetic variation in plasticity increases the potential to adapt to novel environments

Rapid environmental change is forcing populations into novel environments where plasticity will no longer maintain fitness. When populations are exposed to novel environments, evolutionary theory predicts that genetic variation in fitness will increase and should be associated with genetic differences in plasticity. If true, then genetic variation in plasticity can increase adaptive potential in novel environments, and population persistence via rapid adaptation is more likely. To test whether genetic variation in fitness increases in novel environments and is associated with plasticity, we transplanted 8,149 clones of 314 genotypes of a Sicilian daisy (Senecio chrysanthemifolius) within and outside its native range, and quantified genetic variation in fitness, and plasticity in leaf traits and gene expression. Although mean fitness declined by 87% in the novel environment, genetic variance in fitness increased threefold and was correlated with plasticity in leaf traits. High fitness genotypes showed greater plasticity in gene expression, but lower plasticity in most leaf traits. Interestingly, genotypes with greater fitness in the novel environment had the lowest fitness at the native site. These results suggest that standing genetic variation in plasticity could help populations to persist and adapt to novel environments, despite remaining hidden in native environments.

evolutionary biology↗

Ecology and evolutionary history determine plastic responses to environmental variation in two closely related species

The evolution of plastic responses to external cues allows species to track the environmental variation they regularly experience. However, it remains unclear how plasticity evolves during adaptation. To test whether distinct patterns of plasticity is associated with recent adaptive divergence, we quantified plasticity for two closely related but ecologically divergent Sicilian daisy species (Senecio, Asteraceae). We sampled c.40 genotypes of each species from natural populations on and around Mt Etna and then reciprocally transplanted multiple clones of each genotype into four field sites along an elevational gradient representing each species native range, the edge of their range, and conditions outside their native range. At each elevation we quantified survival and measured leaf traits that included investment (specific leaf area), morphology, chlorophyll fluorescence, pigment content and gene expression. As evidence of adaptive divergence, both species performed better at their native site and better than the species from the other habitat. Traits and differentially expressed genes that changed with elevation in one species often showed little change in the other species, or changed in the opposite direction. Adaptive divergence is therefore associated with the evolution of distinct plastic responses to environmental variation, despite these two species sharing a recent common ancestor.

evolutionary biology↗