Does urbanisation lead to parallel demographic shifts across the world in a cosmopolitan plant?

Urbanisation is occurring globally, leading to dramatic environmental changes that are altering the ecology and evolution of species. In particular, the expansion of human infrastructure and the loss and fragmentation of natural habitats in cities is predicted to increase genetic drift and reduce gene flow by reducing the size and connectivity of populations. Alternatively, the 'urban facilitation model' suggests that some species will have greater gene flow into and within cities leading to higher diversity and lower differentiation in urban populations. These alternative hypotheses have not been contrasted across multiple cities. Here, we used the genomic data from the GLobal Urban Evolution project (GLUE), to study the effects of urbanisation on non-adaptive evolutionary processes of white clover (Trifolium repens) at a global scale. We found that white clover populations presented high genetic diversity and no evidence of reduced Ne linked to urbanisation. On the contrary, we found that urban populations were less likely to experience a recent decrease in effective population size than rural ones. In addition, we found little genetic structure among populations both globally and between urban and rural populations, which showed extensive gene flow between habitats. Interestingly, white clover displayed overall higher gene flow within urban areas than within rural habitats. Our study provides the largest comprehensive test of the demographic effects of urbanisation. Our results contrast with the common perception that heavily altered and fragmented urban environments will reduce the effective population size and genetic diversity of populations and contribute to their isolation.

The seed morphospace, a new contribution towards the multidimensional study of angiosperm sexual reproductive biology.

BACKGROUND: The evolutionary success of flowering plants is associated with the vast diversity of their reproductive structures. Despite recent progress in understanding angiosperm-wide trends of floral structure and evolution, a synthetic view of the diversity in seed form and function across angiosperms is lacking. SCOPE: Here we present a roadmap to synthesise the diversity of seed forms in extant angiosperms, relying on the morphospace concept, i.e. a mathematical representation which relates multiple traits and describes the realised morphologies. We provide recommendations on how to broaden the range of measurable traits beyond mass, by using key morphological traits representative of the embryo, endosperm, and seed coat but also fruit attributes (e.g., dehiscence, fleshiness). These key traits were used to construct and analyse a morphospace to detect evolutionary trends and gain insight into how morphological traits relate to seed functions. Finally, we outline challenges and future research directions, combining the morphospace with macroevolutionary comparative methods to underline the drivers that gave rise to the diversity of observed seed forms. CONCLUSIONS: We conclude that this multidimensional approach has the potential, although still untapped, to improve our understanding of covariation among reproductive traits, and further elucidate angiosperm reproductive biology as a whole.

The great escape: patterns of enemy release are not explained by time, space or climate.

When a plant is introduced to a new ecosystem it may escape from some of its coevolved herbivores. Reduced herbivore damage, and the ability of introduced plants to allocate resources from defence to growth and reproduction can increase the success of introduced species. This mechanism is known as enemy release and is known to occur in some species and situations, but not in others. Understanding the conditions under which enemy release is most likely to occur is important, as this will help us to identify which species and habitats may be most at risk of invasion. We compared in situ measurements of herbivory on 16 plant species at 12 locations within their native European and introduced Australian ranges to quantify their level of enemy release and understand the relationship between enemy release and time, space and climate. Overall, plants experienced approximately seven times more herbivore damage in their native range than in their introduced range. We found no evidence that enemy release was related to time since introduction, introduced range size, temperature, precipitation, humidity or elevation. From here, we can explore whether traits, such as leaf defences or phylogenetic relatedness to neighbouring plants, are stronger indicators of enemy release across species.

Terrestrial ecosystem restoration increases biodiversity and reduces its variability, but not to reference levels: A global meta-analysis.

Ecological restoration projects often have variable and unpredictable outcomes, and these can limit the overall impact on biodiversity. Previous syntheses have investigated restoration effectiveness by comparing average restored conditions to average conditions in unrestored or reference systems. Here, we provide the first quantification of the extent to which restoration affects both the mean and variability of biodiversity outcomes, through a global meta-analysis of 83 terrestrial restoration studies. We found that, relative to unrestored (degraded) sites, restoration actions increased biodiversity by an average of 20%, while decreasing the variability of biodiversity (quantified by the coefficient of variation) by an average of 14%. As restorations aged, mean biodiversity increased and variability decreased relative to unrestored sites. However, restoration sites remained, on average, 13% below the biodiversity of reference (target) ecosystems, and were characterised by higher (20%) variability. The lower mean and higher variability in biodiversity at restored sites relative to reference sites remained consistent over time, suggesting that sources of variation (e.g. prior land use, restoration practices) have an enduring influence on restoration outcomes. Our results point to the need for new research confronting the causes of variability in restoration outcomes, and close variability and biodiversity gaps between restored and reference conditions.

Global analysis of floral longevity reveals latitudinal gradients and biotic and abiotic correlates.

The length of time a flower remains open and functional - floral longevity - governs important reproductive processes influencing pollination and mating and varies considerably among angiosperm species. However, little is known about large-scale biogeographic patterns and the correlates of floral longevity. Using published data on floral longevity from 818 angiosperm species in 134 families and 472 locations world-wide, we present the first global quantification of the latitudinal pattern of floral longevity and the relationships between floral longevity and a range of biotic and abiotic factors. Floral longevity exhibited a significant phylogenetic signal and was longer at higher latitudes in both northern and southern hemispheres, even after accounting for elevation. This latitudinal variation was associated with several biotic and abiotic variables. The mean temperature of the flowering season had the highest predictive power for floral longevity, followed by pollen number per flower. Surprisingly, compatibility status, flower size, pollination mode, and growth form had no significant effects on flower longevity. Our results suggest that physiological processes associated with floral maintenance play a key role in explaining latitudinal variation in floral longevity across global ecosystems, with potential implications for floral longevity under global climate change and species distributions.

Advancing the missed mutualist hypothesis, the under-appreciated twin of the enemy release hypothesis.

Introduced species often benefit from escaping their enemies when they are transported to a new range, an idea commonly expressed as the enemy release hypothesis. However, species might shed mutualists as well as enemies when they colonize a new range. Loss of mutualists might reduce the success of introduced populations, or even cause failure to establish. We provide the first quantitative synthesis testing this natural but often overlooked parallel of the enemy release hypothesis, which is known as the missed mutualist hypothesis. Meta-analysis showed that plants interact with 1.9 times more mutualist species, and have 2.3 times more interactions with mutualists per unit time in their native range than in their introduced range. Species may mitigate the negative effects of missed mutualists. For instance, selection arising from missed mutualists could cause introduced species to evolve either to facilitate interactions with a new suite of species or to exist without mutualisms. Just as enemy release can allow introduced populations to redirect energy from defence to growth, potentially evolving increased competitive ability, species that shift to strategies without mutualists may be able to reallocate energy from mutualism toward increased competitive ability or seed production. The missed mutualist hypothesis advances understanding of the selective forces and filters that act on plant species in the early stages of introduction and establishment and thus could inform the management of introduced species.

The global spectrum of plant form and function.

Earth is home to a remarkable diversity of plant forms and life histories, yet comparatively few essential trait combinations have proved evolutionarily viable in today's terrestrial biosphere. By analysing worldwide variation in six major traits critical to growth, survival and reproduction within the largest sample of vascular plant species ever compiled, we found that occupancy of six-dimensional trait space is strongly concentrated, indicating coordination and trade-offs. Three-quarters of trait variation is captured in a two-dimensional global spectrum of plant form and function. One major dimension within this plane reflects the size of whole plants and their parts; the other represents the leaf economics spectrum, which balances leaf construction costs against growth potential. The global plant trait spectrum provides a backdrop for elucidating constraints on evolution, for functionally qualifying species and ecosystems, and for improving models that predict future vegetation based on continuous variation in plant form and function.

Exposure time is an important variable in quantifying post-dispersal seed removal.

A literature synthesis concluded that small mammals have the greatest impact on post-dispersal removal of intermediate-sized seeds (Dylewski et al. 2020). However, this study failed to consider the duration of seed exposure to predators. Re-analyses of the corrected dataset revealed only a weak effect of seed mass on seed removal.

Macroecological patterns in flower colour are shaped by both biotic and abiotic factors.

There is a wealth of research on the way interactions with pollinators shape flower traits. However, we have much more to learn about influences of the abiotic environment on flower colour. We combine quantitative flower colour data for 339 species from a broad spatial range covering tropical, temperate, arid, montane and coastal environments from 9.25ºS to 43.75ºS with 11 environmental variables to test hypotheses about how macroecological patterns in flower colouration relate to biotic and abiotic conditions. Both biotic community and abiotic conditions are important in explaining variation of flower colour traits on a broad scale. The diversity of pollinating insects and the plant community have the highest predictive power for flower colouration, followed by mean annual precipitation and solar radiation. On average, flower colours are more chromatic where there are fewer pollinators, solar radiation is high, precipitation and net primary production are low, and growing seasons are short, providing support for the hypothesis that higher chromatic contrast of flower colours may be related to stressful conditions. To fully understand the ecology and evolution of flower colour, we should incorporate the broad selective context that plants experience into research, rather than focusing primarily on effects of plant-pollinator interactions.

The sex with the reduced sex chromosome dies earlier: a comparison across the tree of life.

Many taxa show substantial differences in lifespan between the sexes. However, these differences are not always in the same direction. In mammals, females tend to live longer than males, while in birds, males tend to live longer than females. One possible explanation for these differences in lifespan is the unguarded X hypothesis, which suggests that the reduced or absent chromosome in the heterogametic sex (e.g. the Y chromosome in mammals and the W chromosome in birds) exposes recessive deleterious mutations on the other sex chromosome. While the unguarded X hypothesis is intuitively appealing, it had never been subject to a broad test. We compiled male and female longevity data for 229 species spanning 99 families, 38 orders and eight classes across the tree of life. Consistent with the unguarded X hypothesis, a meta-analysis showed that the homogametic sex, on average, lives 17.6% longer than the heterogametic sex. Surprisingly, we found substantial differences in lifespan dimorphism between female heterogametic species (in which the homogametic sex lives 7.1% longer) and male heterogametic species (in which the homogametic sex lives 20.9% longer). Our findings demonstrate the importance of considering chromosome morphology in addition to sexual selection and environment as potential drivers of sexual dimorphism, and advance our fundamental understanding of the mechanisms that shape an organism's lifespan.

Three keys to the radiation of angiosperms into freezing environments.

Early flowering plants are thought to have been woody species restricted to warm habitats. This lineage has since radiated into almost every climate, with manifold growth forms. As angiosperms spread and climate changed, they evolved mechanisms to cope with episodic freezing. To explore the evolution of traits underpinning the ability to persist in freezing conditions, we assembled a large species-level database of growth habit (woody or herbaceous; 49,064 species), as well as leaf phenology (evergreen or deciduous), diameter of hydraulic conduits (that is, xylem vessels and tracheids) and climate occupancies (exposure to freezing). To model the evolution of species' traits and climate occupancies, we combined these data with an unparalleled dated molecular phylogeny (32,223 species) for land plants. Here we show that woody clades successfully moved into freezing-prone environments by either possessing transport networks of small safe conduits and/or shutting down hydraulic function by dropping leaves during freezing. Herbaceous species largely avoided freezing periods by senescing cheaply constructed aboveground tissue. Growth habit has long been considered labile, but we find that growth habit was less labile than climate occupancy. Additionally, freezing environments were largely filled by lineages that had already become herbs or, when remaining woody, already had small conduits (that is, the trait evolved before the climate occupancy). By contrast, most deciduous woody lineages had an evolutionary shift to seasonally shedding their leaves only after exposure to freezing (that is, the climate occupancy evolved before the trait). For angiosperms to inhabit novel cold environments they had to gain new structural and functional trait solutions; our results suggest that many of these solutions were probably acquired before their foray into the cold.

Seeds tend to disperse further in the tropics.

Despite the importance of seed dispersal in a plant's life cycle, global patterns in seed dispersal distance have seldom been studied. This paper presents the first geographically and taxonomically broad quantification of the latitudinal gradient in seed dispersal distance. Although there is substantial variation in the seed dispersal distances of different species at a given latitude, seeds disperse on average more than an order of magnitude further at the equator than towards the poles. This pattern is partially explained by plant life-history traits that simultaneously associate with seed dispersal distance and latitude, including dispersal mode and plant height. The extended seed shadow of tropical plants could increase the distance between conspecific individuals. This could facilitate species coexistence and contribute to the maintenance of high plant diversity in tropical communities. The latitudinal gradient in dispersal distance also has implications for species' persistence in the face of habitat fragmentation and climate change.

Rapid evolution of leaf physiology in an introduced beach daisy.

Photosynthesis is a key biological process. However, we know little about whether plants change their photosynthetic strategy when introduced to a new range. We located the most likely source population for the South African beach daisy Arctotheca populifolia introduced to Australia in the 1930s, and ran a common-garden experiment measuring 10 physiological and morphological leaf traits associated with photosynthesis. Based on predictions from theory, and higher rainfall in the introduced range, we hypothesized that introduced plants would have a (i) higher photosynthetic rate, (ii) lower water-use efficiency (WUE) and (iii) higher nitrogen-use efficiency. However, we found that introduced A. populifolia had a lower photosynthetic rate, higher WUE and lower nitrogen-use efficiency than did plants from Arniston, South Africa. Subsequent site visits suggested that plants in Arniston may be able to access moisture on a rocky shelf, while introduced plants grow on sandy beaches where water can quickly dissipate. Our unexpected findings highlight that: (1) it is important to compare introduced species to their source population for an accurate assessment of evolutionary change; (2) rainfall is not always a suitable proxy for water availability and (3) introduced species often undergo evolutionary changes, but without detailed ecological information we may not be able to accurately predict the direction of these changes.

Rapid reshaping: the evolution of morphological changes in an introduced beach daisy.

Thousands of species have been introduced to new ranges worldwide. These introductions provide opportunities for researchers to study evolutionary changes in form and function in response to new environmental conditions. However, almost all previous studies of morphological change in introduced species have compared introduced populations to populations from across the species' native range, so variation within native ranges probably confounds estimates of evolutionary change. In this study, we used microsatellites to locate the source population for the beach daisy Arctotheca populifolia that had been introduced to eastern Australia. We then compared four introduced populations from Australia with their original South African source population in a common-environment experiment. Despite being separated for less than 100 years, source and introduced populations of A. populifolia display substantial heritable morphological differences. Contrary to the evolution of increased competitive ability hypothesis, introduced plants were shorter than source plants, and introduced and source plants did not differ in total biomass. Contrary to predictions based on higher rainfall in the introduced range, introduced plants had smaller, thicker leaves than source plants. Finally, while source plants develop lobed adult leaves, introduced plants retain their spathulate juvenile leaf shape into adulthood. These changes indicate that rapid evolution in introduced species happens, but not always in the direction predicted by theory.

Can dispersal investment explain why tall plant species achieve longer dispersal distances than short plant species?

Tall plant species disperse further distances than do short species, within and across dispersal syndromes, yet the driver underpinning this relationship is unclear. The ability of taller plants to invest more in dispersal structures may explain the positive relationship between plant height and dispersal distance. Here, we quantify the cross-species relationships between presence of dispersal structures, dispersal investment plant height and dispersal distance. Plant height, dispersal syndrome and dispersal investment data were collated for 1613 species from the literature, with dispersal distance data collated for 114 species. We find that species with high dispersal investment disperse further than do species with low dispersal investment. Tall species have a greater probability of having dispersal structures on their seeds compared with short species. For species with dispersal structures on their seeds, plant height is very weakly related to dispersal investment. Our results provide the first global confirmation of the dispersal investment-distance hypothesis, and show dispersal investment can be used for predicting species dispersal distances. However, our results and those of previous studies indicate plant height is still the best proxy for estimating species dispersal distances due to it being such a readily available plant trait.

Leaf morphological traits show greater responses to changes in climate than leaf physiological traits and gas exchange variables.

Adaptation to changing conditions is one of the strategies plants may use to survive in the face of climate change. We aimed to determine whether plants' leaf morphological and physiological traits/gas exchange variables have changed in response to recent, anthropogenic climate change. We grew seedlings from resurrected historic seeds from ex-situ seed banks and paired modern seeds in a common-garden experiment. Species pairs were collected from regions that had undergone differing levels of climate change using an emerging framework-Climate Contrast Resurrection Ecology, allowing us to hypothesise that regions with greater changes in climate (including temperature, precipitation, climate variability and climatic extremes) would be greater trait responses in leaf morphology and physiology over time. Our study found that in regions where there were greater changes in climate, there were greater changes in average leaf area, leaf margin complexity, leaf thickness and leaf intrinsic water use efficiency. Changes in leaf roundness, photosynthetic rate, stomatal density and the leaf economic strategy of our species were not correlated with changes in climate. Our results show that leaves do have the ability to respond to changes in climate, however, there are greater inherited responses in morphological leaf traits than in physiological traits/variables and greater responses to extreme measures of climate than gradual changes in climatic means. It is vital for accurate predictions of species' responses to impending climate change to ensure that future climate change ecology studies utilise knowledge about the difference in both leaf trait and gas exchange responses and the climate variables that they respond to.

Introduced species shed friends as well as enemies.

Many studies seeking to understand the success of biological invasions focus on species' escape from negative interactions, such as damage from herbivores, pathogens, or predators in their introduced range (enemy release). However, much less work has been done to assess the possibility that introduced species might shed mutualists such as pollinators, seed dispersers, and mycorrhizae when they are transported to a new range. We ran a cross-continental field study and found that plants were being visited by 2.6 times more potential pollinators with 1.8 times greater richness in their native range than in their introduced range. Understanding both the positive and negative consequences of introduction to a new range can help us predict, monitor, and manage future invasion events.

Correlations between physical and chemical defences in plants: tradeoffs, syndromes, or just many different ways to skin a herbivorous cat?

Most plant species have a range of traits that deter herbivores. However, understanding of how different defences are related to one another is surprisingly weak. Many authors argue that defence traits trade off against one another, while others argue that they form coordinated defence syndromes. We collected a dataset of unprecedented taxonomic and geographic scope (261 species spanning 80 families, from 75 sites across the globe) to investigate relationships among four chemical and six physical defences. Five of the 45 pairwise correlations between defence traits were significant and three of these were tradeoffs. The relationship between species' overall chemical and physical defence levels was marginally nonsignificant (P = 0.08), and remained nonsignificant after accounting for phylogeny, growth form and abundance. Neither categorical principal component analysis (PCA) nor hierarchical cluster analysis supported the idea that species displayed defence syndromes. Our results do not support arguments for tradeoffs or for coordinated defence syndromes. Rather, plants display a range of combinations of defence traits. We suggest this lack of consistent defence syndromes may be adaptive, resulting from selective pressure to deploy a different combination of defences to coexisting species.