Comparing the Predicted versus Realized Rate of Adaptation of Chamaecrista fasciculata to Climate Change.

AbstractFisher's fundamental theorem of natural selection (FTNS) can be used in a quantitative genetics framework to predict the rate of adaptation in populations. Here, we estimated the capacity for a wild population of the annual legume Chamaecrista fasciculata to adapt to future environments and compared predicted and realized rates of adaptation. We planted pedigreed seeds from one population into three prairie reconstructions along an east-to-west decreasing precipitation gradient. The FTNS predicted adaptation at all sites, but we found a response to selection that was smaller at the home and westernmost sites and maladaptive at the middle site because of changes in the selective environment between generations. However, mean fitness of the progeny generation at the home and westernmost sites exceeded population replacement, which suggests that the environment was sufficiently favorable to promote population persistence. More studies employing the FTNS are needed to clarify the degree to which predictions of the rate of adaptation are realized and its utility in the conservation of populations at risk of extinction from climate change.

High Juvenile Mortality Overwhelms Benefits of Mating Potential for Reproductive Fitness.

AbstractAn individual's access to mates (i.e., its "mating potential") can constrain its reproduction but may also influence its fitness through effects on offspring survival. For instance, mate proximity may correspond with relatedness and lead to inbreeding depression in offspring. While offspring production and survival might respond differently to mating potential, previous studies have not considered the simultaneous effects of mating potential on these fitness components. We investigated the relationship of mating potential with both production and survival of offspring in populations of a long-lived herbaceous perennial, Echinacea angustifolia. Across 7 years and 14 sites, we quantified the mating potential of maternal plants in 1,278 mating bouts and followed the offspring from these bouts over 8 years. We used aster models to evaluate the relationship of mating potential with the number of offspring that emerged and that were alive after 8 years. Seedling emergence increased with mating potential. Despite this, the number of offspring surviving after 8 years showed no relationship to mating potential. Our results support the broader conclusion that the effect of mating potential on fitness erodes over time because of demographic stochasticity at the maternal level.

The conservation value of small population remnants: variability in inbreeding depression and heterosis of a perennial herb, the narrow-leaved purple coneflower (Echinacea angustifolia).

Anthropogenically fragmented populations may have reduced fitness due to loss of genetic diversity and inbreeding. The extent of such fitness losses due to fragmentation and potential gains from conservation actions are infrequently assessed together empirically. Controlled crosses within and among populations can identify whether populations are at risk of inbreeding depression and whether interpopulation crossing alleviates fitness loss. Because fitness depends on environment and life stage, studies quantifying cumulative fitness over a large portion of the lifecycle in conditions that mimic natural environments are most informative. To assess fitness consequences of habitat fragmentation, we leveraged controlled within-family, within-population, and between-population crosses to quantify inbreeding depression and heterosis in seven populations of Echinacea angustifolia within a 6400-hectare area. We then assessed cumulative offspring fitness after 14 years of growth in a natural experimental plot (N = 1136). Mean fitness of progeny from within-population crosses varied considerably, indicating genetic differentiation among source populations, even though these sites are all less than 9 km apart. The fitness consequences of within-family and between-population crosses varied in magnitude and direction. Only one of the seven populations showed inbreeding depression of high effect, while four populations showed substantial heterosis. Outbreeding depression was rare and slight. Our findings indicate that local crossings between isolated populations yield unpredictable fitness consequences ranging from slight decreases to substantial increases. Interestingly, inbreeding depression and heterosis did not relate closely to population size, suggesting that all fragmented populations could contribute to conservation goals as either pollen recipients or donors.

Do Interactions among Microbial Symbionts Cause Selection for Greater Pathogen Virulence?

AbstractThe ecological and evolutionary consequences of microbiome treatments aimed at protecting plants and animals against infectious disease are not well understood, even as such biological control measures become more common in agriculture and medicine. Notably, we lack information on the impacts of symbionts on pathogen fitness with which to project the consequences of competition for the evolution of virulence. To address this gap, we estimated fitness consequences for a common plant pathogen, Ustilago maydis, over differing virulence levels and when the host plant (Zea mays) is coinfected with a defensive symbiont (Fusarium verticillioides) and compared these fitness estimates to those obtained when the symbiont is absent. Here, virulence is measured as the reduction in the growth of the host caused by pathogen infection. Results of aster statistical models demonstrate that the defensive symbiont most negatively affects pathogen infection and that these effects propagate through subsequent stages of disease development to cause lower pathogen fitness across all virulence levels. Moreover, the virulence level at which pathogen fitness is maximal is higher in the presence of the defensive symbiont than in its absence. Thus, as expected from theory for multiple parasites, competition from the defensive symbiont may cause selection for increased pathogen virulence. More broadly, we consider that the evolutionary impacts of interactions between pathogens and microbial symbionts will depend critically on biological context and environment and that interactions among diverse microbial symbionts in spatially heterogeneous communities contribute to the maintenance of the highly diverse symbiotic functions observed in these communities.

Genetic variation in reproductive timing in a long-lived herbaceous perennial.

PREMISE: Reproductive fitness of individual plants depends on the timing of flowering, especially in mate-limited populations, such as those in fragmented habitats. When flowering time traits are associated with differential reproductive success, the narrow-sense heritability (h2 ) of traits will determine how rapidly trait means evolve in response to selection. Heritability of flowering time is documented in many annual plants. However, estimating h2 of flowering time in perennials presents additional methodological challenges, often including paternity assignment and trait expression over multiple years. METHODS: We evaluated the h2 of onset and duration of flowering using offspring-midparent regressions and restricted maximum likelihood methods in an experimental population of an iterocarpic, perennial, herbaceous plant, Echinacea angustifolia, growing in natural conditions. We assessed the flowering time of the parental cohort in 2005 and 2006; the offspring in 2014 through 2017. We also examined the effects of the paternity assignment from Cervus and MasterBayes on estimates of h2 . RESULTS: We found substantial h2 for onset and duration of flowering. We also observed variation in estimates among years. The most reliable estimates for both traits fell in the range of 0.1-0.17. We found evidence of a genotype by year interaction for onset of flowering and strong evidence that genotypes are consistent in their duration of flowering across years. CONCLUSIONS: Substantial heritabilities in this population imply the capacity for a response to natural selection, while also suggesting the potential for differential contributions to adaptive evolution among seasons.

Lifetime Fitness through Female and Male Function: Influences of Genetically Effective Population Size and Density.

AbstractAn individual's lifetime fitness and patterns of mating between individuals are interdependent features of sexual organisms. Mating systems (outcrossing vs. selfing or mating between close relatives) can affect the distribution of offspring fitness, which generally declines with inbreeding, which in turn is related to a population's genetically effective size (Ne). Fitness and mating patterns are also expected to vary with proximity of mates (i.e., population density). Consequently, density and Ne may influence demographic and genetic changes over generations and interact in their effects. Here, we report an experiment designed to assess the influence of these two population-level properties on mating system and lifetime fitness. In experimental arrays under quasi-natural conditions, we varied the density and Ne of the hermaphroditic annual legume Chamaecrista fasciculata. We recorded components of fitness for each individual and employed microsatellite markers to estimate outcrossing and assign paternity. We used aster analyses to estimate lifetime fitness for genetic families using female (seeds set) and male (seeds sired) reproduction as fitness measures. With estimates from these analyses, we assessed the evidence for a trade-off between fitness attained through female versus male function, but we found none. Lifetime fitness increased with density, especially under high Ne. Outcrossing rates increased with density under high Ne but declined modestly with density under low Ne. Our results show that density and Ne have strong direct effects on fitness and mating systems, with negative fitness effects of low Ne limiting the positive effects of increasing density. These findings highlight the importance of the interactive effects of density and Ne on lifetime fitness.

From the Past to the Future: Considering the Value and Limits of Evolutionary Prediction.

The complex interplay of the multiple genetic processes of evolution and the ecological contexts in which they proceed frustrates detailed identification of many of the states of populations, both past and future, that may be of interest. Prediction of rates of adaptation, in the sense of change in mean fitness, into the future would, however, valuably inform expectations for persistence of populations, especially in our era of rapid environmental change. Heavy investment in genomics and other molecular tools has fueled belief that those approaches can effectively predict adaptation into the future. I contest this view. Genome scans display the genomic footprints of the effects of natural selection and the other evolutionary processes over past generations, but it remains problematic to predict future change in mean fitness via genomic approaches. Here, I advocate for a direct approach to prediction of rates of ongoing adaptation. Following an overview of relevant quantitative genetic approaches, I outline the promise of the fundamental theorem of natural selection for the study of the adaptive process. Empirical implementation of this concept can productively guide efforts both to deepen scientific insight into the process of adaptation and to inform measures for conserving the biota in the face of rapid environmental change.

Phenotypic selection on growth rhythm in whitebark pine under climatic conditions warmer than seed origins.

Growth rhythm that is well synchronized with seasonal changes in local climatic conditions is understood to enhance fitness; however, rapid ongoing climate change threatens to disrupt this synchrony. To evaluate phenotypic selection on growth rhythm under expected warmer and drier future climate, seedlings from 49 populations of whitebark pine (Pinus albicaulis Engelm.) were grown and measured over more than 10 years in two common garden field experiments on sites that approximate the projected future climate of the seed origins. Selection on growth rhythm was assessed by relating individual plant fitness to timing and rate of shoot elongation. Differential survival clearly evidenced selection on growth rhythm. We detected directional and stabilizing selection that varied in magnitude between experimental sites and among years. The observed phenotypic selection supports the interpretation of clinal variation among populations within tree species as reflecting adaptive variation in response to past natural selection mediated by climate. To the extent that growth rhythm is heritable, results of the present study suggest evolution of whitebark pine toward a more distinct timing of shoot elongation and generally more rapid elongation in the immediate next generation under ongoing climate change in environments similar to the study sites.

Plant community response to switchgrass (Panicum virgatum) population source in establishing prairies.

Ecological restoration and revegetation efforts entail the translocation of native plant populations. Risks associated with these efforts include failure of translocated populations to establish or, conversely, such strong establishment that they excessively dominate the recipient community. The role that selective breeding plays in mediating these risks is unclear but of increasing importance as efforts to restore and establish multifunctional grasslands also increase. In a three-year, spatially replicated study, we seeded experimental prairie communities with either domesticated (cultivar) or undomesticated strains of Panicum virgatum (switchgrass), a North American C4 species under development as a biomass crop. We evaluated the composition, performance, and diversity of the recipient plant communities and compared the performance of cultivar and undomesticated switchgrass in those communities. We found little evidence that switchgrass population source affected community response. Switchgrass cultivars modestly exceeded undomesticated strains with respect to stand establishment, third-year stand density, and aboveground biomass; effect size and significance differed among sites. Our results suggest that including cultivars in ecological restorations and multifunctional grasslands may enhance success of switchgrass establishment with little risk of impairing the composition or diversity of plant communities for up to three years, as reflected in the measures used here. However, the incorporation of undomesticated switchgrass into multifunctional grasslands may enhance landscape-scale genetic variation and mitigate risks associated with gene flow between translocated and local wild switchgrass populations; more research on these dynamics is needed.

Detrimental effects of rhizobial inoculum early in the life of partridge pea, Chamaecrista fasciculata.

PREMISE OF THE STUDY: Mutualistic relationships with microbes may aid plants in overcoming environmental stressors and increase the range of abiotic environments where plants can persist. Rhizobia, nitrogen-fixing bacteria associated with legumes, often confer fitness benefits to their host plants by increasing access to nitrogen in nitrogen-limited soils, but effects of rhizobia on host fitness under other stresses, such as drought, remain unclear. METHODS: In this greenhouse study, we varied the application of rhizobia (Bradyrhizobium sp.) inoculum and drought to examine whether the fitness benefits of rhizobia to their host, partridge pea (Chamaecrista fasciculata), would differ between drought and well-watered conditions. Plants were harvested 9 weeks after seeds were sown. KEY RESULTS: Young C. fasciculata plants that had been inoculated had lower biomass, leaf relative growth rate, and stem relative growth rate compared to young uninoculated plants in both drought and well-watered environments. CONCLUSIONS: Under the conditions of this study, the rhizobial interaction imposed a net cost to their hosts early in development. Potential reasons for this cost include allocating more carbon to nodule and root development than to aboveground growth and a geographic mismatch between the source populations of host plants and rhizobia. If developing plants incur such costs from rhizobia in nature, they may suffer an early disadvantage relative to other plants, whether conspecifics lacking rhizobia or heterospecifics.

Rate, spectrum, and evolutionary dynamics of spontaneous epimutations.

Stochastic changes in cytosine methylation are a source of heritable epigenetic and phenotypic diversity in plants. Using the model plant Arabidopsis thaliana, we derive robust estimates of the rate at which methylation is spontaneously gained (forward epimutation) or lost (backward epimutation) at individual cytosines and construct a comprehensive picture of the epimutation landscape in this species. We demonstrate that the dynamic interplay between forward and backward epimutations is modulated by genomic context and show that subtle contextual differences have profoundly shaped patterns of methylation diversity in A. thaliana natural populations over evolutionary timescales. Theoretical arguments indicate that the epimutation rates reported here are high enough to rapidly uncouple genetic from epigenetic variation, but low enough for new epialleles to sustain long-term selection responses. Our results provide new insights into methylome evolution and its population-level consequences.

Climate-related genetic variation in a threatened tree species, Pinus albicaulis.

PREMISE OF THE STUDY: With ongoing climate change, understanding of intraspecific adaptive variation is critical for conservation and restoration of plant species. Such information is especially scarce for threatened and endangered tree species, such as Pinus albicaulis Engelm. Therefore, our principal aims were to assess adaptive variation and characterize its relationship with climate of seed origin. METHODS: We grew seedlings from 49 P. albicaulis populations representative of the interior northwestern United States in two common garden field experiments under warm-dry conditions that mimic climatic conditions predicted in the current century for areas within the species' range. Differences among populations were assessed for growth and survival. We then used regression to describe clines of apparent adaptive variation in relation to climate variation among the populations' origins. KEY RESULTS: We detected genetic divergence for growth and survival among populations of P. albicaulis. These differences corresponded to distinct climatic clines. Populations originating from locations with lower spring precipitation exhibited greater survival in response to natural drought. Populations originating from increasingly milder climates exhibited greater height growth under relatively limited stress in early years and greater fitness after 12 yr. CONCLUSIONS: The results suggest that P. albicaulis exhibits adaptive variation for drought tolerance and growth in response to selection pressures associated with variation in moisture availability and temperature, respectively. Even so, clinal variation was relatively gentle. Thus, apparent differences in local adaptation to climate among populations appears to be relatively low.

Project Baseline: An unprecedented resource to study plant evolution across space and time.

PREMISE OF THE STUDY: Project Baseline is a seed bank that offers an unprecedented opportunity to examine spatial and temporal dimensions of microevolution during an era of rapid environmental change. Over the upcoming 50 years, biologists will withdraw genetically representative samples of past populations from this time capsule of seeds and grow them contemporaneously with modern samples to detect any phenotypic and molecular evolution that has occurred during the intervening time. METHODS: We carefully developed this living genome bank using protocols to enhance its experimental value by collecting from multiple populations and species across a broad geographical range in sites that are likely to be preserved into the future. Seeds are accessioned with site and population data and are stored by maternal line under conditions that maximize seed longevity. This open-access resource will be available to researchers at regular intervals to evaluate contemporary evolution. KEY RESULTS: To date, the Project Baseline collection includes 100-200 maternal lines of each of 61 species collected from over 831 populations on sites that are likely to be preserved into the future across the United States (∼78,000 maternal lines). Our strategically designed collection circumvents some problems that can cloud the results of "resurrection" studies involving naturally preserved or existing seed collections that are available fortuitously. CONCLUSIONS: The resurrection approach can be coupled with long-established and newer techniques over the next five decades to elucidate genetic change and thereby vastly improve our understanding of temporal and spatial changes in phenotype and the evolutionary processes underlying it.

How functional traits, herbivory, and genetic diversity interact in Echinacea: implications for fragmented populations.

Habitat fragmentation produces small, spatially isolated populations that promote inbreeding. Remnant populations often contain inbred and outbred individuals, but it is unclear how inbreeding relative to outbreeding affects the expression of functional traits and biotic interactions such as herbivory. We measured a suite of 12 functional traits and herbivore damage on three genotypic cross types in the prairie forb, Echinacea angustifolia: inbred, and outbred crosses resulting from matings within and between remnant populations. Inbreeding significantly affected the expression of all 12 functional traits that influence resource capture. Inbred individuals had consistently lower photosynthetic rates, water use efficiencies, specific leaf areas, and had higher trichome numbers, percent C, and percent N than outbred individuals. However, herbivore damage did not differ significantly among the cross types and was not correlated with other leaf functional traits. Leaf architecture and low physiological rates of the inbred compared to outbred individuals imply poorer capture or use of resources. Inbred plants also had lower survival and fitness relative to outbred plants. Our results show that inbreeding, a phenomenon predicted and observed to occur in fragmented populations, influences key functional traits such as plant structure, physiology and elemental composition. Because of their likely role in fitness of individuals and ecological dynamics plant functional traits can serve as a bridge between evolution and community or ecosystem ecology.

Indirect effects drive evolutionary responses to global change.

Anthropogenic environmental changes pose significant threats to plant and animal populations. These changes also may affect the evolution of natural populations either directly or indirectly by altering the outcome of species interactions that are important drivers of evolution. This latter indirect pathway may be especially important for evolutionary responses to elevated atmospheric CO2 concentrations (eCO2), which appear to have minimal direct effects on plant evolution but have large effects on interspecific interactions, such as competition. We manipulated competitive and CO2 environments of experimental Arabidopsis thaliana populations to test whether eCO2 alters evolutionary trajectories indirectly by altering selection imposed by competitors. We found that interspecific competition increased selection on growth traits, reduced heritabilities, and altered genetic covariances between traits and that the magnitude of these effects depended upon the CO2 environment. Although eCO2 had minimal direct effects on evolutionary processes, eCO2 typically reduced the strength of selection imposed by competitors and, therefore, relaxed selection on plant traits when competitors were present. Our results indicate that global changes may affect plant evolution indirectly by altering competitive interactions and underscore the importance of conducting research in natural communities when attempting to predict population responses to global change.

Juvenile survival increases with dispersal distance and varies across years: 15 years of evidence in a prairie perennial.

Juvenile survival is critical to population persistence and evolutionary change. However, the survival of juvenile plants from emergence to reproductive maturity is rarely quantified. This is especially true for long-lived perennials with extended pre-reproductive periods. Furthermore, studies rarely have the replication necessary to account for variation among populations and cohorts. We estimated juvenile survival and its relationship to population size, density of conspecifics, distance to the maternal plant, age, year, and cohort for Echinacea angustifolia, a long-lived herbaceous perennial. In 14 remnant prairie populations over seven sampling years, 2007-2013, we identified 886 seedlings. We then monitored these individuals annually until 2021 (8-15 years). Overall, juvenile mortality was very high; for almost all cohorts fewer than 10% of seedlings survived to age 8 or to year 2021. Only two of the seedlings reached reproductive maturity within the study period. Juvenile survival increased with distance from the maternal plant and varied more among the study years than it did by age or cohort. Juvenile survival did not vary with population size or local density of conspecific neighbors. Our results suggest that low juvenile survival could contribute to projected population declines.

Insights from population genetics for range limits of a widely distributed native plant.

PREMISE OF THE STUDY: Species' range limits are determined by a combination of history, ecology, and genetics. While much of our understanding of range limits comes from ecological studies, molecular population genetic methods can provide insight into the contribution of historical range shifts and gene flow to current range limits. METHODS: We sequenced nine nuclear loci in 68 individuals from four populations (two within the range interior, one at the western range edge, and one at northern range edge) of the native annual legume Chamaecrista fasciculata in the Upper Midwest of North America. KEY RESULTS: Molecular diversity was greatest in an interior population and significantly reduced at both the western and northern range edges. We found no molecular genetic evidence for historical demographic expansion or contraction in any of the populations. Coalescent simulations indicate that the absence of a genetic signal for expansion or contraction could be due to inadequate statistical power or to a bottleneck that was weak and old. Populations were significantly differentiated and clustered into three demes, with the fourth population containing individuals that were assigned to the two nearest populations. We found evidence that recent migration between the northern edge and the most proximate interior population has been slight, within the distribution of values that theoretical models predict would alleviate genetic load without impeding adaptation. CONCLUSIONS: When coupled with results from transplant experiments, these results suggest that ecological-genetic factors other than gene flow currently limit range expansion of C. fasciculata. Further, they highlight challenges in using molecular data to make inferences about species' distributions that have complex demographic histories.

and the Persistence of Hereditarian Fallacies.

Clark (2023) considers the similarity in socioeconomic status between relatives, drawing on records spanning four centuries in England. The paper adapts a classic quantitative genetics model in order to argue the fit of the model to the data suggests that: (1) variation in socioeconomic status is largely determined by additive genetic variation; (2) contemporary English people "remain correlated in outcomes with their lineage relatives in exactly the same way as in preindustrial England"; and (3) social mobility has remained static over this time period due to strong assortative mating on a "social genotype." These conclusions are based on a misconstrual of model parameters, which conflates genetic and non-genetic transmission (e.g. of wealth) within families. As we show, there is strong confounding of genetic and non-genetic sources of similarity in these data. Inconsistent with claims (2) and (3), we show that familial correlations in status are variable-generally decreasing-through the time period analyzed. Lastly, we find that statistical artifacts substantially bias estimates of familial correlations in the paper. Overall, Clark (2023) provides no information about the relative contribution of genetic and non-genetic factors to social status.

Rapid climate change and the rate of adaptation: insight from experimental quantitative genetics.

Evolution proceeds unceasingly in all biological populations. It is clear that climate-driven evolution has molded plants in deep time and within extant populations. However, it is less certain whether adaptive evolution can proceed sufficiently rapidly to maintain the fitness and demographic stability of populations subjected to exceptionally rapid contemporary climate change. Here, we consider this question, drawing on current evidence on the rate of plant range shifts and the potential for an adaptive evolutionary response. We emphasize advances in understanding based on theoretical studies that model interacting evolutionary processes, and we provide an overview of quantitative genetic approaches that can parameterize these models to provide more meaningful predictions of the dynamic interplay between genetics, demography and evolution. We outline further research that can clarify both the adaptive potential of plant populations as climate continues to change and the role played by ongoing adaptation in their persistence.

Role of climate and competitors in limiting fitness across range edges of an annual plant.

It is often assumed that the geographic distributions of species match their climatic tolerances, but this assumption is not frequently tested. Moreover, few studies examine the relative importance of abiotic and biotic factors for limiting species ranges. We combined multiple approaches to assess the extent to which fitness of a widespread native annual legume, Chamaecrista fasciculata, decreases at and beyond its northern and western range edges, and how this is influenced by the presence of neighbors. First, we examined plant fitness and the effect of neighbors in natural populations at different geographic range locations for three years. Fitness decreased toward the northern range edge, but not the western edge. Neighbor removal had a consistently positive effect on seedpod production across all years and sites. Second, we established experimental populations at sites within the range, and at and beyond the northern and western range edges. We tracked individual fitness and recorded seedling recruitment in the following year (a complete generation) to estimate population growth rate. Individual fitness and population growth declined to near zero beyond both range edges, indicating that C. fasciculata with its present genetic composition will not establish in these regions, given conditions currently. We also carried out a neighbor removal treatment. Consistent with the natural populations, neighbors reduced seedpod production of reproductive adults. However, neighbors also increased early-season survival, and this positive effect early in life history resulted in a net positive effect of neighbors on lifetime fitness at most range locations. Our data show that the population growth rate of C. fasciculata includes values above replacement, and populations are well adapted to conditions up to the edge of the range, whereas the severely compromised fitness at sites beyond the edge precludes immediate establishment of populations and thereby impedes adaptation to these conditions.