Quantifying the effect of genetic, environmental and individual demographic stochastic variability for population dynamics in Plantago lanceolata.

Simple demographic events, the survival and reproduction of individuals, drive population dynamics. These demographic events are influenced by genetic and environmental parameters, and are the focus of many evolutionary and ecological investigations that aim to predict and understand population change. However, such a focus often neglects the stochastic events that individuals experience throughout their lives. These stochastic events also influence survival and reproduction and thereby evolutionary and ecological dynamics. Here, we illustrate the influence of such non-selective demographic variability on population dynamics using population projection models of an experimental population of Plantago lanceolata. Our analysis shows that the variability in survival and reproduction among individuals is largely due to demographic stochastic variation with only modest effects of differences in environment, genes, and their interaction. Common expectations of population growth, based on expected lifetime reproduction and generation time, can be misleading when demographic stochastic variation is large. Large demographic stochastic variation exhibited within genotypes can lower population growth and slow evolutionary adaptive dynamics. Our results accompany recent investigations that call for more focus on stochastic variation in fitness components, such as survival, reproduction, and functional traits, rather than dismissal of this variation as uninformative noise.

Phenotypic plasticity masks range-wide genetic differentiation for vegetative but not reproductive traits in a short-lived plant.

Genetic differentiation and phenotypic plasticity jointly shape intraspecific trait variation, but their roles differ among traits. In short-lived plants, reproductive traits may be more genetically determined due to their impact on fitness, whereas vegetative traits may show higher plasticity to buffer short-term perturbations. Combining a multi-treatment greenhouse experiment with observational field data throughout the range of a widespread short-lived herb, Plantago lanceolata, we (1) disentangled genetic and plastic responses of functional traits to a set of environmental drivers and (2) assessed how genetic differentiation and plasticity shape observational trait-environment relationships. Reproductive traits showed distinct genetic differentiation that largely determined observational patterns, but only when correcting traits for differences in biomass. Vegetative traits showed higher plasticity and opposite genetic and plastic responses, masking the genetic component underlying field-observed trait variation. Our study suggests that genetic differentiation may be inferred from observational data only for the traits most closely related to fitness.

Interactions between artificial light at night, soil moisture, and plant density affect the growth of a perennial wildflower.

Artificial light at night (ALAN) has been shown to alter aspects of plant growth, but we are not aware of any studies that have examined whether the effects of ALAN on plants depend upon the backdrop of variation in other abiotic factors that plants encounter in field populations. We conducted a field experiment to investigate whether ALAN affects the growth and anti-herbivore defenses of common milkweed, Asclepias syriaca, and whether the effects of ALAN are influenced by plant density or soil moisture content. Artificial light at night, soil moisture, and plant density were manipulated according to a split-plot factorial design. Although increasing soil moisture by watering had no significant effects on latex exudation, attributes of plant growth generally responded positively to watering. The basal stem diameter (BSD) and height of plants were affected by ALAN × soil moisture interactions. For both of these variables, the positive effects of ALAN were greater for plants that were not watered than for plants that were. Basal stem diameter was also affected by an ALAN × plant density interaction, and the positive effect of ALAN on BSD was greater in the low-density treatment than in the high-density treatment. Our results demonstrate that the effects of ALAN on plant growth can be altered by soil moisture and plant density. Consequently, the effects of ALAN on plants in nature may not be consistent with existing frameworks that do not account for critical abiotic variables such as water availability or biotic interactions between plants such as competition.

Global gene flow releases invasive plants from environmental constraints on genetic diversity.

When plants establish outside their native range, their ability to adapt to the new environment is influenced by both demography and dispersal. However, the relative importance of these two factors is poorly understood. To quantify the influence of demography and dispersal on patterns of genetic diversity underlying adaptation, we used data from a globally distributed demographic research network comprising 35 native and 18 nonnative populations of Plantago lanceolata Species-specific simulation experiments showed that dispersal would dilute demographic influences on genetic diversity at local scales. Populations in the native European range had strong spatial genetic structure associated with geographic distance and precipitation seasonality. In contrast, nonnative populations had weaker spatial genetic structure that was not associated with environmental gradients but with higher within-population genetic diversity. Our findings show that dispersal caused by repeated, long-distance, human-mediated introductions has allowed invasive plant populations to overcome environmental constraints on genetic diversity, even without strong demographic changes. The impact of invasive plants may, therefore, increase with repeated introductions, highlighting the need to constrain future introductions of species even if they already exist in an area.

Death and Plasticity in Clones Influence Invasion Success.

Although invasion processes have been intensely studied, the mechanisms underlying the success of some invasive clonal species remain a mystery. Using the specific example of Carpobrotus edulis, we illustrate how invasion success can be facilitated by a unique spatiotemporal regulation of growth and senescence of plant parts.

Potential impacts of tolerance to herbivory on population dynamics of a monocarpic herb.

PREMISE OF THE STUDY: Mammalian herbivores, particularly white-tailed deer, can have a major impact on plant abundance and distribution. However, plants can tolerate herbivory by increasing seed production or seed quality. We used the monocarpic perennial Prenanthes roanensis to examine tolerance to mammalian herbivory through seed quality and modeled the effects of tolerance on population growth rate. METHODS: We examined seed quality (proportion of viable seeds, seed mass, germination, and seedling size) on damaged and undamaged plants to determine the extent to which plants tolerate herbivory. We then varied seed quality parameters over a range of values in population models to compare population growth rates under "no-tolerance" conditions (herbivory, but no tolerance) to those under "tolerance" conditions. KEY RESULTS: In most populations, plants damaged by herbivores had a greater proportion of viable seeds per plant or a greater probability of seed germination. Incorporating observed tolerance into population models did not significantly increase population growth rate. However, at low germination rates, increased germination of seeds from damaged plants has the potential to significantly increase population growth rate. CONCLUSIONS: Damaged plants can compensate for loss of reproductive heads by increasing seed viability and germination rates in the remaining seeds. This study is one of the first to demonstrate that tolerance through seed quality has the potential to affect population growth rate. Our results suggest that incorporating tolerance into population models may help elucidate mechanisms by which plant populations persist despite herbivory.

An invasive plant alters phenotypic selection on the vegetative growth of a native congener.

PREMISE OF THE STUDY: The ecological consequences of plant competition have frequently been tested, but the evolutionary outcomes of these interactions have gone largely unexplored. The study of species invasions can make an important contribution to this field of research by allowing us to watch ecological and evolutionary processes unfold as a novel species is integrated into a plant community. We explored the ecological and evolutionary impact of an invasive jewelweed, Impatiens glandulifera, on a closely related native congener, I. capensis and asked: (1) Does the presence of the invasive jewelweed alter the fitness of native jewelweed populations? (2) Does the invasive jewelweed affect the vegetative growth of the native congener? and (3) Does the invasive jewelweed alter phenotypic selection on the vegetative traits of the native congener? METHODS: We used a greenhouse competition experiment, an invasive species removal field experiment, and a survey of natural populations. KEY RESULTS: We show that when the invasive jewelweed is present, phenotypic selection favors native jewelweed individuals investing less in rapid upward growth and more in branching and fruiting potential through the production of nodes. CONCLUSIONS: This research demonstrates that invasive plants have the potential to greatly alter natural selection on native competitors. Studies investigating altered selection in invaded communities can reveal the potential evolutionary impact of invasive competitors, while deepening our understanding of the more general role of competition in driving plant evolution and permitting species coexistence.

An invasive plant alters pollinator-mediated phenotypic selection on a native congener.

UNLABELLED: • PREMISE OF STUDY: Recent studies suggest that invasive plants compete reproductively with native plants by reducing the quantity or quality of pollinator visits. Although these studies have revealed ecological consequences of pollinator-mediated competition between invasive and native plants, the evolutionary outcomes of these interactions remain largely unexplored.• METHODS: We studied the ecological and evolutionary impact of pollinator-mediated competition with an invasive jewelweed, Impatiens glandulifera, on a co-occurring native congener, I. capensis. Using a pollinator choice experiment, a hand pollination experiment, and a selection analysis, we addressed the following questions: (1) Do native pollinators show preference for the invasive or native jewelweed, and do they move between the two species? (2) Does invasive jewelweed pollen inhibit seed production in the native plant? (3) Does the invasive jewelweed alter phenotypic selection on the native plant's floral traits?• KEY RESULTS: The pollinator choice experiment showed that pollinators strongly preferred the invasive jewelweed. The hand pollination experiment demonstrated that invasive pollen inhibited seed production in the native plant. The selection analysis showed that the presence of the invasive jewelweed altered phenotypic selection on corolla height in the native plant.• CONCLUSIONS: Invasive plants have the potential to alter phenotypic selection on floral traits in native plant populations. If native plants can evolve in response to this altered selection pressure, the evolution of floral traits may play an important role in permitting long-term coexistence of native and invasive plants.

Population dynamics in central and edge populations of a narrowly endemic plant.

Species' range limits can be caused by environmental gradients, and in such cases, abundance is thought to be highest in the center of a species range and decline towards the edge (the abundant-center model). Although in theory decreased abundance is caused by a decline in performance at the edge, it has been shown that performance and abundance are not necessarily related. Few studies have compared abundance and performance in center and edge populations of endemic species, whose ranges may be restricted by the availability of specialized habitat rather than environmental gradients across their range. Additionally, range-wide studies that examine both northern and southern edge populations are rare. We used Roan Mountain rattlesnake-root (Prenanthes roanensis), a perennial plant endemic to the Southern Appalachians (USA), to compare abundance and performance between central populations and populations at the northern and southern edges of the range. To account for multiple fitness components across the life cycle, we measured performance of edge populations as vital-rate contributions to population growth rate compared to the center. Abundance did not decline at the range edge, but some vital-rate contributions were lower in edge populations compared to central populations. However, each edge population differed in which vital-rate contributions were lower compared to the center. Our results do not support the abundant-center model, and it appears that local factors are important in structuring the range of this endemic species. It is important to recognize that when implementing conservation or management plans, populations in close proximity may have substantial variation in demographic rates due to differences in the local environment.

Longitudinal analysis in Plantago: strength of selection and reverse-age analysis reveal age-indeterminate senescence.

1. Senescence is usually viewed as increased age-specific mortality or decreased age-specific fecundity due to the declining ability of natural selection to remove deleterious age-specific mutations with age. In herbaceous perennial plants, trends in age-specific mortality are often confounded by size. Age-indeterminate senescence, where accumulated physiological damage varies strongly with environment, may be a better model of senescence in these species. 2. We analysed trends in size and fertility in Plantago lanceolata, using a long-term demographic census involving >10 years and >8,000 individuals in 4 cohorts. We used elasticity and pairwise invasion analysis of life history function-parameterized age × stage matrices to assess whether the force of natural selection declined with age. Then, we used reverse age analysis of size and fertility to assess whether age-indeterminate senescence occurred. Reverse age analysis uses longitudinal data for individuals that have died to look at trait patterns as a function of both age and remaining time to death. We hypothesized that i) the strength of natural selection would decline strongly with age, and ii) physiological condition would deteriorate for several years prior to death. 3. Both elasticity and invasion analyses suggested that the strength of natural selection through mortality declined strongly with age once size was accounted for. Further, reverse age analyses showed that individuals shrank for ~3yrs prior to death, suggesting physiological decline. Inflorescence production declined with age, and also declined in the 3 years prior to death regardless of overall age. 4 SYNTHESIS: The hypothesis that plants escape senescence generally assumes that plants can continue to grow larger and increase reproduction as they get older. The results here show that size and reproduction decline with age and the rates of these declines toward death are lifespan- and age-dependent. Further research is needed to delineate the importance of age-determinate vs. age-indeterminate factors in senescence patterns across species.

The triple helix of Plantago lanceolata: genetics and the environment interact to determine population dynamics.

The theory of evolution via natural selection predicts that the genetic composition of wild populations changes over time in response to the environment. Different genotypes should exhibit different demographic patterns, but genetic variation in demography is often impossible to separate from environmental variation. Here, we asked if genetic variation is important in determining demographic patterns. We answer this question using a long-term field experiment combined with general linear modeling of deterministic population growth rates (lambda), deterministic life table response experiment (LTRE) analysis, and stochastic simulation of demography by paternal lineage in a short-lived perennial plant, Plantago lanceolata, in which we replicated genotypes across four cohorts using a standard breeding design. General linear modeling showed that growth rate varied significantly with year, spatial block, and sire. In LTRE analysis of all cohorts, the strongest influences on growth rate were from year x spatial block, and cohort x year x spatial block interactions. In analysis of genetics vs. temporal environmental variation, the strongest impacts on growth rate were from year and year x sire. Finally, stochastic simulation suggested different genetic composition among cohorts after 100 years, and different population growth rates when genetic differences were accounted for than when they were not. We argue that genetic variation, genotype x environment interactions, natural selection, and cohort effects should be better integrated into population ecological studies, as these processes should result in deviations from projected deterministic and stochastic population parameters.

Longitudinal analysis of Plantago: adaptive benefits of iteroparity in a short-lived, herbaceous perennial.

Theory suggests that iteroparity may confer greater fitness than semelparity in situations in which temporal environmental variation is high and unpredictable. Variable age-specific mortality, density dependence, and other factors may also favor iteroparity over semelparity. Here, we empirically test the adaptive benefits of greater numbers of reproductive years in a study of reproductive schedules in an experimental population of a short-lived polycarpic perennial, Plantago lanceolata. A large experimental population was established that included four cohorts with similar genetic structure. Individuals were censused for mortality, size, and reproduction for seven years. Plants experienced variable numbers of reproductive years, but one or two years were most common (approximately 46.7% of the population reproduced only once). The probability of flowering at least once prior to death was determined strongly by extrinsic, environmental or intrinsic but environmentally influenced variables, including early-life size, cohort, and block, but also varied with a number of interactions involving paternal lineage. Maternal effects explained small but significant components of the variance in the number of reproductive years among individuals in each cohort, while paternal effects were significant in only two cohorts. Number of reproductive years contributed significantly to fitness in this system, more so than all other variables tested, although most of the variation in relative fitness may be attributed ultimately to environmental influences. We suggest that the high proportion of each cohort composed of plants reproducing only once may be due to environmental constraints on either growth or size. Such environmental influences, particularly on early life size, may result in small but important indirect effects on fitness.

Longitudinal analysis of Plantago: age-by-environment interactions reveal aging.

We know very little about aging (senescence) in natural populations, and even less about plant aging. Demographic aging is identified by an increasing rate of mortality following reproductive maturity. In natural populations, quantifying aging is often confounded because changes in mortality may be influenced by both short- and long-term environmental fluctuations as well as age-dependent changes in performance. Plants can be easily marked and monitored longitudinally in natural populations yet the age-dependent dynamics of mortality are not known. This study was designed to determine whether a plant species, Plantago lanceolata, shows demographic aging in its natural environment. A large, multiple-cohort design was used to separate age-independent and age-dependent processes. Seven years of results show environmental influences on mortality as evidenced by synchronous changes in mortality across four cohorts over time. Age-dependent mortality was found through an age-by-environment interaction when the oldest cohorts had significantly higher mortality relative to the younger cohorts during times of stress. Neither size nor quantity of reproduction could explain this variation in mortality across cohorts. These results demonstrate demographic senescence in a natural population of plants.

Mating frequency and inclusive fitness in Drosophila melanogaster.

In many species, increased mating frequency reduces maternal survival and reproduction. In order to understand the evolution of mating frequency, we need to determine the consequences of increased mating frequency for offspring. We conducted an experiment in Drosophila melanogaster in which we manipulated the mating frequency of mothers and examined the survival and fecundity of the mothers and their daughters. We found that mothers with the highest mating frequency had accelerated mortality and more rapid reproductive senescence. On average, they had 50% shorter lives and 30% lower lifetime reproductive success (LRS) than did mothers with the lowest mating frequency. However, mothers with the highest mating frequency produced daughters with 28% greater LRS. This finding implies that frequent mating stimulates cross-generational fitness trade-offs such that maternal fitness is reduced while offspring fitness is enhanced. We evaluate these results using a demographic metric of inclusive fitness. We show that the costs and benefits of mating frequency depend on the growth rate of the population. In an inclusive fitness context, there was no evidence that increased mating frequency results in fitness costs for mothers. These results indicate that cross-generational fitness trade-offs have an important role in sexual selection and life-history evolution.

Cross-generational fitness benefits of mating and male seminal fluid.

In many species, the physical act of mating and exposure to accessory gland proteins (Acps) in male seminal fluid reduces female survival and offspring production. It is not clear what males gain from harming their sexual partners or why females mate frequently despite being harmed. Using sterile strains of Drosophila melanogaster that differ in their production of Acps, we found that both the physical act of mating and exposure to male seminal fluid in mothers increase the fitness of daughters. We show that the changes in daughter fitness are mediated by parental effects, not by sexual selection involving good genes or owing to variation in maternal egg production. These results support the idea that male harm of females might partly evolve through cross-generational fitness benefits.

Mating-induced recombination in fruit flies.

In traditional deterministic models the conditions for the evolution of sex and sexual behavior are limited because their benefits are context dependent. In novel and adverse environments both multiple mating and recombination can help generate gene combinations that allow for rapid adaptation. Mating frequency often increases in conditions in which recombination might be beneficial; therefore, increased sexual behavior might evolve to act as a cue that stimulates recombination. We conducted two experiments in the fruit fly, Drosophila melanogaster, using linked phenotypic markers to determine how recent bouts of additional mating affect female recombination rate. The first experiment examined the effect of additional mating, mating history, and age on female recombination rate. The second experiment assessed the effect of recent mating events on recombination rate. Together, the experiments suggest that each additional bout of mating temporarily increases female recombination rate. These findings imply that the conditions favoring the evolution of sexual reproduction and multiple mating behaviors are broader than currently appreciated.

Age-specific demography in Plantago: uncovering age-dependent mortality in a natural population.

Accurate measures of age-dependent mortality are critical to life-history analysis and measures of fitness, yet these measures are difficult to obtain in natural populations. Age-dependent mortality patterns can be obscured not only by seasonal variation in environmental conditions and reproduction but also by changes in the heterogeneity among individuals in the population over time due to selection. This study of Plantago lanceolata uses longitudinal data from a field study with a large number of individuals to develop a model to estimate the shape of the baseline hazard function that represents the age-dependent risk of mortality. The model developed here uses both constant (genetics, spatial location) and time-varying (temperature, rainfall, reproduction, size) covariates not only to estimate the underlying mortality pattern but also to demonstrate that the risk of mortality associated with fitness components can change with time/age. Moreover, this analysis suggests that increasing size after reproductive maturity may allow this plant species to escape from demographic senescence.

The case for negative senescence.

Negative senescence is characterized by a decline in mortality with age after reproductive maturity, generally accompanied by an increase in fecundity. Hamilton (1966) ruled out negative senescence: we adumbrate the deficiencies of his model. We review empirical studies of various plants and some kinds of animals that may experience negative senescence and conclude that negative senescence may be widespread, especially in indeterminate-growth species for which size and fertility increase with age. We develop optimization models of life-history strategies that demonstrate that negative senescence is theoretically possible. More generally, our models contribute to understanding of the evolutionary and demographic forces that mold the age-trajectories of mortality, fertility and growth.

Pathogen frequency in an age-structured population of Plantago lanceolata.

Life-history traits can play important roles in determining the course of ecological species interactions. We explored the consequences of host age on a host-pathogen interaction by quantifying pathogen frequency in an age-structured host population. Our project was motivated by an interest in whether the demographic structure of a host population has consequences for species interactions. In 2 successive years, we planted large cohorts of the perennial herb Plantago lanceolata in its natural environment and observed infection by Fusarium moniliforme, a non-lethal floral fungal pathogen, over 3 years. We documented substantial variation of pathogen frequency across years and between cohorts. Logistic regression revealed that pathogen frequency increased with the number of inflorescences produced and with evidence of prior pathogen presence, whereas it decreased with increasing plant longevity. In addition, interannual variation and an age-year interaction contributed to the observed pathogen frequencies. There was a significant positive effect of age on pathogen frequency overall, but this was not consistent over all ages. Pathogen frequency was higher in 2-year-old plants than in 1-year-olds, suggesting that age-structure can influence the host-pathogen interaction. This pattern did not continue into 3-year-old plants. A possible explanation for this is that selective mortality allows only generally robust plants, and consequently the most resistant plants, to survive to the oldest ages.