Simon G. Innes

Assisted gene flow, the human-facilitated movement of species within its range, has the potential to increase genetic diversity and facilitate adaptation for climate-threatened populations. However, concerns regarding outbreeding depression and gene swamping have limited the application of assisted gene flow, and experimental tests have been largely confined to simulations and laboratories. We conducted a landscape-scale manipulation, planting seeds and seedlings from historically hotter and drier source populations into climate-threatened populations of the common yellow monkeyflower ( Mimulus guttatus ) and tracked change in genomes, phenotypes, and fitness. Within three generations, source alleles introgressed into half of the target populations. Assisted gene flow increased fitness in one experimental block of populations and slightly decreased fitness in a second block. Fitness increases were associated with flowering earlier and producing fewer trichomes. Greater fitness changes occurred in populations where seeds rather than seedlings were introduced. Both the amount of introgression and fitness changes were heterogeneous between years, suggesting that temporal fluctuations in climate likely impact initial introgression and success of assisted gene flow. Initial introgression from source populations was low across the genome, limiting concerns of gene swamping. Our results are generally consistent with theoretical models, and provide cautious optimism for an often-maligned conservation strategy.

Secondary metabolites are critical to plant defenses and frequently exhibit variation among populations associated with heterogeneous climatic factors and/or herbivore communities. We examined genetic-based geographic and ontogenetic variation in phenylpropanoid glycoside (PPG) concentrations and arsenals in Mimulus moschatus, a perennial monkeyflower native to western North America. We conducted a greenhouse common garden with maternal lines collected from three populations sampled along a latitudinal gradient paralleling spatial sampling from a previous study in the closely related congener, Mimulus guttatus. We assessed PPG arsenals as well as concentrations of individual and total PPGs within leaf tissue from two developmental stages. Populations differed in total concentration and arsenal composition of PPGs, with the populations from intermediate latitudes exhibiting higher concentrations than higher and lower latitude populations. Leaves from earlier developmental stages had higher overall PPG concentrations than leaves from later developmental stages across all populations, suggesting juvenile tissue is better defended than more mature tissue. Spatial patterns in relative PPG concentrations and arsenal composition tightly paralleled those in the closely related M. guttatus across space despite consistently lower total PPG concentrations in M. moschatus. Because we did not measure herbivory and our sample size is limited, these results should be interpreted cautiously. Nonetheless, they provide baseline data for understanding geographic and developmental variation in chemical defenses and generate hypotheses about environmental influences and potential convergence in defenses among closely related species.

Premise: The increasing frequency and severity of heat waves across the globe is well known. However, few longitudinal studies have tracked demographic change and fitness within natural populations, and fewer still have spanned multiple extreme events. Determining how organisms tolerate, respond, and potentially adapt to extreme events is key for assessing long‐term population viability.Methods: We examined how mortality, fecundity, seed provisioning, and offspring germination differed across 12 populations of annual common monkeyflower (Mimulus guttatus) over 5 years.Results: Two heat waves occurred within the study: a heat wave within the first 10 days of the growing season in 2019 and a heat dome event nearly a month into the growing season in 2021. Mortality was high, and fecundity decreased in a population‐specific manner following each heat wave. However, the 2021 heat dome caused declines of 34.5% in seed size and 22.1% in the ability to germinate, while the 2019 heat wave did not significantly affect either. Structural equation models indicated that similar climatic factors—including early‐season maximum temperatures and late‐season precipitation—are associated with declines in fecundity and slower germination.Conclusions: These results suggest that the consequences of heat waves will depend on the relative severity and timing of the heat wave in the growing season, and further suggest that this timing may have amplified longer‐term impacts because offspring have less provisioning. Specifically, with growing seasons shifting earlier into the spring, later or slower germination could exacerbate population extirpation risk.

Rapid adaptation during invasion has historically been considered limited and unpredictable. We leverage whole-genome sequencing of >2600 plants across six continents to investigate the relative roles of colonization history and adaptation during the worldwide invasion of Trifolium repens. Introduced populations contain high levels of genetic variation with independent colonization histories evident on different continents. Five large structural variants on three chromosomes exist as standing genetic variation within the native range, and exhibit strong signatures of parallel climate-associated adaptation across continents. Common gardens in the native and introduced ranges demonstrate that three structural variants exhibit patterns of selection consistent with local adaptation across each range. Our results provide strong evidence that rapid and parallel adaptation during invasion is caused by large-effect structural variants introduced throughout the world. Significance Statement Biological invasions occur over short timescales and introductions are often hypothesized to include limited genetic diversity, making the role of adaptation in invasion success controversial. We demonstrate that the invasion of a human-commensal species, Trifolium repens, likely stems from multiple, diverse introductions with significant evidence of climate-associated adaptation following introduction. The genetic basis of adaptation is most strongly linked to five chromosomal rearrangements that each span hundreds of genes – matching theoretical predictions that large-effect variants are key to the initial stages of adaptation to novel environments. Chromosomal rearrangements have remarkably parallel signatures of adaptation across different introductions despite initial colonization from different areas of Europe. Our study highlights the impact of globalization and rapid adaptation for the invasion success of human commensal species.

The extent to which species can adapt to spatiotemporal climatic variation in their native and introduced ranges remains unresolved. To address this, we examined how clines in cyanogenesis (hydrogen cyanide [HCN] production-an antiherbivore defense associated with decreased tolerance to freezing) have shifted in response to climatic variation in space and time over a 60-year period in both the native and introduced ranges of Trifolium repens. HCN production is a polymorphic trait controlled by variation at two Mendelian loci (Ac and Li). Using phenotypic assays, we estimated within-population frequencies of HCN production and dominant alleles at both loci (i.e., Ac and Li) from 10,575 plants sampled from 131 populations on five continents, and then compared these frequencies to those from historical data collected in the 1950s. There were no clear relationships between changes in the frequency of HCN production, Ac, or Li and changes in temperature between contemporary and historical samples. We did detect evidence of continued evolution to temperature gradients in the introduced range, whereby the slope of contemporary clines for HCN and Ac in relation to winter temperature became steeper than historical clines and more similar to native clines. These results suggest that cyanogenesis clines show no clear changes through time in response to global warming, but introduced populations continue to adapt to their contemporary environments.

Urbanization transforms environments in ways that alter biological evolution. We examined whether urban environmental change drives parallel evolution by sampling 110,019 white clover plants from 6169 populations in 160 cities globally. Plants were assayed for a Mendelian antiherbivore defense that also affects tolerance to abiotic stressors. Urban-rural gradients were associated with the evolution of clines in defense in 47% of cities throughout the world. Variation in the strength of clines was explained by environmental changes in drought stress and vegetation cover that varied among cities. Sequencing 2074 genomes from 26 cities revealed that the evolution of urban-rural clines was best explained by adaptive evolution, but the degree of parallel adaptation varied among cities. Our results demonstrate that urbanization leads to adaptation at a global scale.