Capacity of soil bacteria to reach the phyllosphere and convergence of floral communities despite soil microbiota variation

Leaves and flowers are colonized by diverse bacteria that impact plant fitness and evolution. Although the structure of these microbial communities is becoming well-characterized, various aspects of their environmental origin and selection by plants remain uncertain, such as the relative proportion of soilborne bacteria in phyllosphere communities. Here, to address this issue and to provide experimental support for bacteria being filtered by flowers, we conducted common-garden experiments outside and under gnotobiotic conditions. We grew Arabidopsis thaliana in a soil substitute and added two microbial communities from natural soils. We estimated that at least 25% of the phyllosphere bacteria collected from the plants grown in the open environment were also detected in the controlled conditions, in which bacteria could reach leaves and flowers only from the soil. These taxa represented more than 40% of the communities based on amplicon sequencing. Unsupervised hierarchical clustering approaches supported the convergence of all floral microbiota, and 24 of the 28 bacteria responsible for this pattern belonged to the Burkholderiaceae family, which includes known plant pathogens and plant growth-promoting members. We anticipate that our study will foster future investigations regarding the routes used by soil microbes to reach leaves and flowers, the ubiquity of the environmental filtering of Burkholderiaceae across plant species and environments, and the potential functional effects of the accumulation of these bacteria in the reproductive organs of flowering plants.

Urbanization extends flight phenology and leads to local adaptation of seasonal plasticity in Lepidoptera

Urbanization is gaining force globally, which challenges biodiversity, and it has recently also emerged as an agent of evolutionary change. Seasonal phenology and life cycle regulation are essential processes that urbanization is likely to alter through both the urban heat island effect (UHI) and artificial light at night (ALAN). However, how UHI and ALAN affect the evolution of seasonal adaptations has received little attention. Here, we test for the urban evolution of seasonal life-history plasticity, specifically changes in the photoperiodic induction of diapause in two lepidopterans, Pieris napi (Pieridae) and Chiasmia clathrata (Geometridae). We used long-term data from standardized monitoring and citizen science observation schemes to compare yearly phenological flight curves in six cities in Finland and Sweden to those of adjacent rural populations. This analysis showed for both species that flight seasons are longer and end later in most cities, suggesting a difference in the timing of diapause induction. Then, we used common garden experiments to test whether the evolution of the photoperiodic reaction norm for diapause could explain these phenological changes for a subset of these cities. These experiments demonstrated a genetic shift for both species in urban areas toward a lower daylength threshold for direct development, consistent with predictions based on the UHI but not ALAN. The correspondence of this genetic change to the results of our larger-scale observational analysis of in situ flight phenology indicates that it may be widespread. These findings suggest that seasonal life cycle regulation evolves in urban ectotherms and may contribute to ecoevolutionary dynamics in cities.

Introduction to the Special Issue: The ecology and genetics of population differentiation in plants

Population differentiation is a pervasive process in nature. At present, evolutionary studies on plant population differentiation address key questions by undertaking joint ecological and genetic approaches and employing a combination of molecular and experimental means. In this special issue, we gathered a collection of papers dealing with various ecological and genetic aspects of population differentiation in plants. In particular, this special issue encompasses eight research articles and two reviews covering a wide array of worldwide environments, plant functional types, genetic and genomic approaches, and common garden experiments to quantify molecular and/or quantitative trait differentiation in plant populations. Overall, this special issue stresses the validity of traditional evolutionary studies focused on plant populations, whilst emphasizing the integration of classical biological disciplines and state-of-the-art molecular techniques into a unique toolkit for evolutionary plant research.

Increases in multiple resources promote plant invasion

Invasion by alien plants is frequently attributed to increased resource availabilities. Still, our understanding is mainly based on effect of single resource. Despite the fact that plants rely on many resources, little is known about how multiple resources affect success of alien plants. Here, with two common garden experiments, one in China and one in Germany, we tested whether nutrient and light availabilities affected the competitive outcomes between alien and native plants. We found that under low resource availabilities or with addition of only one type of resources aliens were not more competitive than natives. However, with a joint increase of nutrients and light intensity, aliens outcompeted natives. Our finding indicates that addition of multiple resources could greatly reduce the number of limiting factors (i.e. niche dimensionality), and that this favors the dominance of alien species. It also indicates that habitats experiencing multiple global changes might be more vulnerable to plant invasion.

Environment and phenology shape local adaptation in thermal performance

Populations within species often exhibit variation in traits that reflect local adaptation and further shape existing adaptive potential for species to respond to climate change. However, our mechanistic understanding of how the environment shapes trait variation remains poor. Here, we used common garden experiments to quantify thermal performance in eight populations of the marine snail Urosalpinx cinerea across thermal gradients on the Atlantic and the Pacific coasts of North America. We then evaluated the relationship between thermal performance and environmental metrics derived from time-series data. Our results reveal a novel pattern of ‘mixed’ trait performance adaptation, where thermal optima were positively correlated with spawning temperature (cogradient variation), while maximum trait performance was negatively correlated with season length (countergradient variation). This counterintuitive pattern probably arises because of phenological shifts in the spawning season, whereby ‘cold’ populations delay spawning until later in the year when temperatures are warmer compared to ‘warm’ populations that spawn earlier in the year when temperatures are cooler. Our results show that variation in thermal performance can be shaped by multiple facets of the environment and are linked to organismal phenology and natural history. Understanding the impacts of climate change on organisms, therefore, requires the knowledge of how climate change will alter different aspects of the thermal environment.

Shifting chemical defence or novel weapons? A review of defence traits in Agarophyton vermiculophyllum and other invasive seaweeds

Seaweed bioinvasions increasingly affect coastal environments around the world, which increases the need for predictive models and mitigation strategies. The biotic interactions between seaweed invaders and invaded communities are often considered a key determinant of invasion success and failure and we here revise the current evidence that the capacity of seaweed invaders to deter enemies in newly reached environments correlates with their invasion success. Particularly efficient chemical defences have been described for several of the more problematic seaweed invaders during the last decades. However, confirmed cases in which seaweed invaders confronted un-adapted enemies in newly gained environments with deterrents that were absent from these environments prior to the invasion (so-called “novel weapons”) are scarce, although an increasing number of invasive and non-invasive seaweeds are screened for defence compounds. More evidence exists that seaweeds may adapt defence intensities to changing pressure by biological enemies in newly invaded habitats. However, most of this evidence of shifting defence was gathered with only one particular model seaweed, the Asia-endemic red alga Agarophyton vermiculophyllum, which is particularly accessible for direct comparisons of native and non-native populations in common garden experiments. A. vermiculophyllum interacts with consumers, epibionts and bacterial pathogens and in most of these interactions, non-native populations have rather gained than lost defensive capacity relative to native conspecifics. The increases in the few examined cases were due to an increased production of broad-spectrum deterrents and the relative scarcity of specialized deterrents perhaps reflects the circumstance that seaweed consumers and epibionts are overwhelmingly generalists.

Striking between-population floral divergences in a habitat specialized plant

When the habitat occupied by a specialist species is patchily distributed, limited gene flow between the fragmented populations may allow population differentiation and eventual speciation. ‘Sky islands’—montane habitats that form terrestrial islands—have been shown to promote diversification in many taxa through this mechanism. We investigate floral variation in Impatiens lawii, a plant specialized on laterite rich rocky plateaus that form sky islands in the northern Western Ghats mountains of India. We focus on three plateaus separated from each other by ca. 7 to 17 km, and show that floral traits have diverged strongly between these populations. In contrast, floral traits have not diverged in the congeneric I. oppositifolia, which co-occurs with I. lawii in the plateaus, but is a habitat generalist that is also found in the intervening valleys. We conducted common garden experiments to test whether the differences in I. lawii are due to genetic differentiation or phenotypic plasticity. There were strong differences in floral morphology between experimental plants sourced from the three populations, and the relative divergences between population pairs mirrored that seen in the wild, indicating that the populations are genetically differentiated. Common garden experiments confirmed that there was no differentiation in I. oppositifolia. Field floral visitation surveys indicated that the observed differences in floral traits have consequences for I. lawii populations, by reducing the number of visitors and changing the relative abundance of different floral visitor groups. Our results highlight the role of habitat specialization in diversification, and corroborates the importance of sky islands as centres of diversification.