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.

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.

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.

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.

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.

Additive genetic variance for lifetime fitness and the capacity for adaptation in an annual plant.

The immediate capacity for adaptation under current environmental conditions is directly proportional to the additive genetic variance for fitness, VA (W). Mean absolute fitness, W¯ , is predicted to change at the rate VA(W)W¯ , according to Fisher's Fundamental Theorem of Natural Selection. Despite ample research evaluating degree of local adaptation, direct assessment of VA (W) and the capacity for ongoing adaptation is exceedingly rare. We estimated VA (W) and W¯ in three pedigreed populations of annual Chamaecrista fasciculata, over three years in the wild. Contrasting with common expectations, we found significant VA (W) in all populations and years, predicting increased mean fitness in subsequent generations (0.83 to 6.12 seeds per individual). Further, we detected two cases predicting "evolutionary rescue," where selection on standing VA (W) was expected to increase fitness of declining populations ( W¯ < 1.0) to levels consistent with population sustainability and growth. Within populations, inter-annual differences in genetic expression of fitness were striking. Significant genotype-by-year interactions reflected modest correlations between breeding values across years, indicating temporally variable selection at the genotypic level that could contribute to maintaining VA (W). By directly estimating VA (W) and total lifetime W¯ , our study presents an experimental approach for studies of adaptive capacity in the wild.

Phenotypic selection on ponderosa pine seed and seedling traits in the field under three experimentally manipulated drought treatments.

Drought-related selection during seedling emergence and early development may play a strong role in adaptation. Yet this process is poorly understood and particularly so in relation to ongoing climate change. To evaluate drought-induced differences in selection during early life stages, a total of 50 maternal families sampled from three climatically disparate ponderosa pine (Pinus ponderosa Doug.) populations were grown from seed in two common garden field experiments at a location that was warmer and drier than seed origins. Three drought treatments were imposed experimentally. Phenotypic selection was assessed by relating plant fitness measured as survival or unconditional expected height at age 3 to seed density (mass per unit volume), date of emergence, and timing of shoot elongation. In the year of emergence from seed, differential mortality was particularly strong and clearly indicated selection. In contrast, selection in subsequent years was far less pronounced. Phenotypes with high seed density, an intermediate but relatively early emergence date, and high 2nd-year early-season shoot elongation exhibited the greatest estimated fitness under drought. The form of selection varied among seed sources in relation to drought treatment. Selection was generally more acute in the cases of greatest difference between drought treatment and climatic patterns of precipitation at the site of seed origin. These results suggest that populations of ponderosa pine are differentially adapted to drought patterns associated with the climate of their origin. To the extent that the phenotypic traits examined are heritable or correlated with heritable traits, our results provide insight into how tree populations may evolve in response to drought.

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.

Fine-Grained Analysis of Spontaneous Mutation Spectrum and Frequency in Arabidopsis thaliana.

Mutations are the ultimate source of all genetic variation. However, few direct estimates of the contribution of mutation to molecular genetic variation are available. To address this issue, we first analyzed the rate and spectrum of mutations in the Arabidopsis thaliana reference accession after 25 generations of single-seed descent. We then compared the mutation profile in these mutation accumulation (MA) lines against genetic variation observed in the 1001 Genomes Project. The estimated haploid single nucleotide mutation (SNM) rate for A. thaliana is 6.95 × 10-9 (SE ± 2.68 × 10-10) per site per generation, with SNMs having higher frequency in transposable elements (TEs) and centromeric regions. The estimated indel mutation rate is 1.30 × 10-9 (±1.07 × 10-10) per site per generation, with deletions being more frequent and larger than insertions. Among the 1694 unique SNMs identified in the MA lines, the positions of 389 SNMs (23%) coincide with biallelic SNPs from the 1001 Genomes population, and in 289 (17%) cases the changes are identical. Of the 329 unique indels identified in the MA lines, 96 (29%) overlap with indels from the 1001 Genomes dataset, and 16 indels (5% of the total) are identical. These overlap frequencies are significantly higher than expected, suggesting that de novo mutations are not uniformly distributed and arise at polymorphic sites more frequently than assumed. These results suggest that high mutation rate potentially contributes to high polymorphism and low mutation rate to reduced polymorphism in natural populations providing insights of mutational inputs in generating natural genetic diversity.

Expression of additive genetic variance for fitness in a population of partridge pea in two field sites.

Despite the importance of adaptation in shaping biological diversity over many generations, little is known about populations' capacities to adapt at any particular time. Theory predicts that a population's rate of ongoing adaptation is the ratio of its additive genetic variance for fitness, VA(W) , to its mean absolute fitness, W¯ . We conducted a transplant study to quantify W¯ and standing VA(W) for a population of the annual legume Chamaecrista fasciculata in one field site from which we initially sampled it and another site where it does not currently occur naturally. We also examined genotype-by-environment interactions, G × E, as well as its components, differences between sites in VA(W) and in rank of breeding values for fitness. The mean fitness indicated population persistence in both sites, and there was substantial VA(W) for ongoing adaptation at both sites. Statistically significant G × E indicated that the adaptive process would differ between sites. We found a positive correlation between fitness of genotypes in the "home" and "away" environments, and G × E was more pronounced as the life-cycle proceeds. This study exemplifies an approach to assessing whether there is sufficient VA(W) to support evolutionary rescue in populations that are declining.

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.

Multivariate phenotypic selection on a complex sexual signal.

Animal signals are complex, comprising multiple components that receivers may use to inform their decisions. Components may carry information of differing value to receivers, and selection on one component could modulate or reverse selection on another, necessitating a multivariate approach to estimating selection gradients. However, surprisingly few empirical studies have estimated the strength of phenotypic selection on complex signals with appropriate design and adequate power to detect nonlinear selection. We used phonotaxis assays to measure sexual selection on the advertisement signal of Cope's gray tree frog, Hyla chrysoscelis. Female preferences were assessed for five signal components using single- and two-stimulus behavioral assays. Linear, quadratic, and correlational selection gradients were estimated from the single-stimulus data. Significant directional selection is acting on call duration, call rate, pulse rate, and relative amplitude; stabilizing selection is acting on call duration and call rate. Under the two-stimulus paradigm, conclusions were qualitatively different, revealing nonlinear selection on all components except call duration. For individual subjects, the outcomes of single- and two-stimulus trials were frequently discordant, suggesting that the choice of testing paradigm may affect conclusions drawn from experiments.

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.