Being John Harper: Using evolutionary ideas to improve understanding of global patterns in plant traits

This review summarizes current understanding of five key plant traits: seed mass, plant height, wood density, leaf mass per unit area and leaf size, emphasizing ways in which our understanding of large-scale patterns in plant traits have improved over the last two decades. Notable advances include: (1) large-seeded species have greater seed dispersal distances than do small-seeded species, (2) leaf mass per unit area is not strongly or consistently related to plant traits outside the leaf economics spectrum, or to broad gradients in environmental conditions, and (3) fleshy fruit could not have first evolved for seed dispersal, as the first fleshy fruit appeared millions of years before the first potential seed dispersers. While quantifying large-scale patterns in plant traits has yielded many important discoveries, it is clear that the next major leap in understanding will not come from simply including ever more variables in our analyses. I suggest that we build upon Harper's “Darwinian approach to plant ecology” and apply evolutionary ideas to large-scale trait ecology. For example, quantifying trait impacts on lifetime fitness rather than on particular stages of plant regeneration can allow us to understand the coordination between seemingly disparate traits. I use this approach to bring seed mass and plant height together as integrated parts of a species’ life-history spectrum. I then point out problems associated with the implicit assumption that selection acts on species’ mean trait values and show how considering the way selection acts can improve our understanding of the effects of climate on plant traits. A goal for the future is to quantify the full suite of biotic and abiotic factors that shape plant strategy in complex, real-world situations. Synthesis. Enormous data availability and ever more powerful computational and statistical tools have given ecologists unprecedented power to quantify large-scale patterns in plant ecology. However, there is a limit to how far big data alone can take us. The time is ripe for a new generation of hypotheses and ecological theory built on strong evolutionary foundations. Let the creativity begin!

Inverted invasions: Native plants can frequently colonise urban and highly disturbed habitats

There is an enormous body of literature on plant invasions, including many investigations of the types of introduced species that are most likely to invade natural ecosystems. In this study we turn invasion biology upside down, and ask what sort of native species colonise novel anthropogenic habitats such as roadside lawns, infrequently tended road shoulders, railway embankments and fire trails. We quantified species richness and cover in roadside lawns and infrequently tended road shoulders in five regions of New South Wales, Australia. The native vegetation in these regions included sclerophyll forest, fertile and infertile Eucalypt-dominated woodlands, rainforest, and semi-arid woodland. We performed a complementary survey of sites spanning five disturbance levels within the region containing sclerophyll forest vegetation. Although many non-native species were present in disturbed, novel habitats, a total of 136 native species were also found. Most of these native species were in sites with low levels of disturbance (fire trails and railway embankments), but 35 native species were found to colonise roadside lawns, our most highly-disturbed vegetation type. There was a significant negative relationship between the disturbance level in novel habitats and the number and cover of native species. Native species that colonised novel habitats were disproportionately likely be generalist species whose natural habitat includes both high and low light and high and low disturbance conditions. The native species colonising novel habitats also tended to have traits associated with a fast life-history, including short stature and small seeds. A surprisingly high number of native plant species are colonising novel, anthropogenic habitats. Our findings highlight the potential importance of urban ecosystems for conservation and restoration biology

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

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

Detecting steps in spatial genetic data: Which diversity measures are best?

Accurately detecting sudden changes, or steps, in genetic diversity across landscapes is important for locating barriers to gene flow, identifying selectively important loci, and defining management units. However, there are many metrics that researchers could use to detect steps and little information on which might be the most robust. Our study aimed to determine the best measure/s for genetic step detection along linear gradients using biallelic single nucleotide polymorphism (SNP) data. We tested the ability to differentiate between linear and step-like gradients in genetic diversity, using a range of diversity measures derived from the q-profile, including allelic richness, Shannon Information, GST, and Jost-D, as well as Bray-Curtis dissimilarity. To determine the properties of each measure, we repeated simulations of different intensities of step and allele proportion ranges, with varying genome sample size, number of loci, and number of localities. We found that alpha diversity (withinlocality) based measures were ineffective at detecting steps. Further, allelic richness-based beta (between-locality) measures (e.g., Jaccard and Sørensen dissimilarity) were not reliable for detecting steps, but instead detected departures from fixation. The beta diversity measures best able to detect steps were: Shannon Information based measures, GST based measures, a Jost-D related measure, and Bray-Curtis dissimilarity. No one measure was best overall, with a trade-off between those measures with high step detection sensitivity (GST and Bray-Curtis) and those that minimised false positives (a variant of Shannon Information). Therefore, when detecting steps, we recommend understanding the differences between measures and using a combination of approaches

Tropical plants do not have narrower temperature tolerances, but are more at risk from warming because they are close to their upper thermal limits

Aim: Tropical species are thought to be more susceptible to climate warming than are higher latitude species. This prediction is largely based on the assumption that tropical species can tolerate a narrower range of temperatures. While this prediction holds for some animal taxa, we do not yet know the latitudinal trends in temperature tolerance for plants. We aim to address this knowledge gap and establish if there is a global trend in plant warming risk. Location: Global. Time period: Present–2070. Major taxa studied: Plants. Methods: We used 9,737 records for 1,312 species from the Kew Gardens’ global germination database to quantify global patterns in germination temperature. Results: We found no evidence for a latitudinal gradient in the breadth of temperatures at which plant species can germinate. However, tropical plants are predicted to face the greatest risk from climate warming, because they experience temperatures closer to their upper germination limits. By 2070, over half (79/142) of tropical plant species are predicted to experience temperatures exceeding their optimum germination temperatures, with some even exceeding their maximum germination temperature (41/190). Conversely, 95% of species at latitudes above 45° are predicted to benefit from warming, with environmental temperatures shifting closer to the species’ optimal germination temperatures. Main conclusions: The prediction that tropical plant species would be most at risk under future climate warming was supported by our data, but through a different mechanism to that generally assumed

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

The ZAX Herbivory Trainer—Free software for training researchers to visually estimate leaf damage

Plants lose a remarkable amount of energy to herbivorous animals, and this damage has substantial impacts on plant fitness and species' distributions. There are many ways ecologists can measure leaf damage, with some methods being more time-consuming than others. Due to a high variance in herbivory, accurate quantification of damage at the population level requires sampling of many leaves. A simple yet effective solution to this problem is to estimate leaf damage visually. Visually estimating leaf damage may be less accurate than scanning methods, but visual estimates of leaf damage are much faster than digital measurements. Using simulations, we show that gathering larger quantities of data at a slightly higher level of inaccuracy gives a more accurate estimate of a population's overall leaf damage than fewer, exact measurements. We then introduce the ZAX Herbivory Trainer, a free online application that teaches researchers to accurately visually estimate leaf damage. On average, users took ~9 min and 48 images to complete our trainer which significantly decreased their estimate inaccuracy from 13.2% to 6%. This low level of inaccuracy can be retained up to 3 months post-training so researchers can use the ZAX Herbivory Trainer once prior to short fieldwork or every 3 months for extensive fieldwork. We also recommend a cut-off point, whereby if a person has not completed the app in 17.5 min or 85 images (90th percentile), they may not be suitable to estimate herbivory for research purposes. The ZAX Herbivory Trainer will allow researchers of any experience level to assess herbivory quickly and accurately in a globally standardised way. International collaborators, students and citizen scientists can all find use in this app, no matter the scale of their projects. From this we can gather better data to address big picture questions in ecology such as patterns in herbivory relating to latitude or climate change

Time-traveling seeds reveal that plant regeneration and growth traits are responding to climate change

Studies assessing the biological impacts of climate change typically rely on long-term, historic data to measure trait responses to climate through time. Here, we overcame the problem of absent historical data by using resurrected seeds to capture historic plant-trait data for a number of plant regeneration and growth traits. We collected seed and seedling trait measurements from resurrected historic seeds and compared these with modern seed and seedling traits collected from the same species in the same geographic location. We found a total of 43 species from southeastern Australia for which modern/historic seed pairs could be located. These species were located in a range of regions that have undergone different amounts of climate change across a range of temperature, precipitation, and extreme measures of climate. There was a correlation between the amount of change in climate metrics, and the amount of change in plant traits. Using stepwise model selection, we found that for all regeneration and growth trait changes (except change in stem density), the most accurate model selected at least two measures of climate change. Changes in extreme measures of climate, such as heat-wave duration and changes in climate variability, were more strongly related to changes in regeneration and growth traits than changes in mean climate metrics. Across our species, for every 5% increase in temperature variability, there was a threefold increase in the probability of seed viability and seed germination success. An increase of 1 d in the maximum duration of dry spells through time led to a 1.5-fold decrease in seed viability and seeds became 30% flatter/thinner. Regions where the maximum heat-wave duration had increased by 10 d saw a 1.35-cm decrease in seedling height and a 1.04-g decrease in seedling biomass. Rapid responses in plant traits to changes in climate may be possible; however, it is not clear whether these changes will be fast enough for plants to keep pace with future climate change