Genetic structure in patchy populations of a candidate foundation plant: a case study of Leymus chinensis using genetic and clonal diversity.

PREMISE: The distribution of genetic diversity on the landscape has critical ecological and evolutionary implications. This may be especially the case on a local scale for foundation plant species because they create and define ecological communities, contributing disproportionately to ecosystem function. METHODS: We examined the distribution of genetic diversity and clones, which we defined first as unique multilocus genotypes (MLG), and then by grouping similar MLGs into multilocus lineages. We used 186 markers from inter-simple sequence repeats (ISSR) across 358 ramets from 13 patches of the foundation grass Leymus chinensis. We examined the relationship between genetic and clonal diversities, their variation with patch size, and the effect of the number of markers used to evaluate genetic diversity and structure in this species. RESULTS: Every ramet had a unique MLG. Almost all patches consisted of individuals belonging to a single multilocus lineages. We confirmed this with a clustering algorithm to group related genotypes. The predominance of a single lineage within each patch could be the result of the accumulation of somatic mutations, limited dispersal, some sexual reproduction with partners mainly restricted to the same patch, or a combination of all three. CONCLUSIONS: We found strong genetic structure among patches of L. chinensis. Consistent with previous work on the species, the clustering of similar genotypes within patches suggests that clonal reproduction combined with somatic mutation, limited dispersal, and some degree of sexual reproduction among neighbors causes individuals within a patch to be more closely related than among patches.

Inheritance of DNA methylation differences in the mangrove Rhizophora mangle.

The capacity to respond to environmental challenges ultimately relies on phenotypic variation which manifests from complex interactions of genetic and nongenetic mechanisms through development. While we know something about genetic variation and structure of many species of conservation importance, we know very little about the nongenetic contributions to variation. Rhizophora mangle is a foundation species that occurs in coastal estuarine habitats throughout the neotropics where it provides critical ecosystem functions and is potentially threatened by anthropogenic environmental changes. Several studies have documented landscape-level patterns of genetic variation in this species, but we know virtually nothing about the inheritance of nongenetic variation. To assess one type of nongenetic variation, we examined the patterns of DNA sequence and DNA methylation in maternal plants and offspring from natural populations of R. mangle from the Gulf Coast of Florida. We used a reduced representation bisulfite sequencing approach (epi-genotyping by sequencing; epiGBS) to address the following questions: (a) What are the levels of genetic and epigenetic diversity in natural populations of R. mangle? (b) How are genetic and epigenetic variation structured within and among populations? (c) How faithfully is epigenetic variation inherited? We found low genetic diversity but high epigenetic diversity from natural populations of maternal plants in the field. In addition, a large portion (up to ~25%) of epigenetic differences among offspring grown in common garden was explained by maternal family. Therefore, epigenetic variation could be an important source of response to challenging environments in the genetically depauperate populations of this foundation species.

Scale-dependent portfolio effects explain growth inflation and volatility reduction in landscape demography.

Population demography is central to fundamental ecology and for predicting range shifts, decline of threatened species, and spread of invasive organisms. There is a mismatch between most demographic work, carried out on few populations and at local scales, and the need to predict dynamics at landscape and regional scales. Inspired by concepts from landscape ecology and Markowitz's portfolio theory, we develop a landscape portfolio platform to quantify and predict the behavior of multiple populations, scaling up the expectation and variance of the dynamics of an ensemble of populations. We illustrate this framework using a 35-y time series on gypsy moth populations. We demonstrate the demography accumulation curve in which the collective growth of the ensemble depends on the number of local populations included, highlighting a minimum but adequate number of populations for both regional-scale persistence and cross-scale inference. The attainable set of landscape portfolios further suggests tools for regional population management for both threatened and invasive species.

Landscape Demography: Population Change and its Drivers Across Spatial Scales.

Demographic studies of plants and animals have a rich history and literature in ecology, and are important for both fundamental and applied ecology and conservation biology. Almost all demographic work has focused on intensive studies in which births, deaths, growth of individuals, and related measures are quantified in a single population or a few populations. This has been for practical reasons due to the high demands of labor required for this work, and because the questions addressed in these studies have been asked at the level of individual populations, with implicit assumptions about generalizing from the results. We introduce the concept of landscape demography, the study of the demographic properties of populations and their drivers at multiple spatial scales, and of how the relationships among populations and their drivers at any one scale influence demographic outcomes at other scales. We explore the ways in which considering the dynamics of ensembles of populations at different spatial scales can advance progress in thinking about ecological issues of high current interest such as biological invasions, range expansions and contractions due to climate change, and the decline of threatened species, as well as fundamental ecological and evolutionary questions.

Variation among individuals in cone production in Pinus palustris (Pinaceae).

PREMISE OF THE STUDY: Reproductive output varies considerably among individuals within plant populations, and this is especially so in cone production of conifers. While this variation can have substantial effects on populations, little is known about its magnitude or causes. METHODS: We studied variation in cone production for 2 years within a population of Pinus palustris Mill. (longleaf pine; Pinaceae). Using hurdle models, we evaluated the importance of burn treatments, tree size (dbh), canopy status (open, dominant, subordinate), and number of conspecific neighbors within 4 m (N(4)). KEY RESULTS: Cone production of individuals-even after accounting for other variables-was strongly correlated between years. Trees in plots burned every 1, 2, or 5 years produced more cones than those burned every 7 years, or unburned. Larger trees tend to produce more cones, but the large effects of the other factors studied caused substantial scatter in the dbh-cone number relationship. Among trees in the open, dbh had little explanatory power. Subordinate trees with three neighbors produced no cones. CONCLUSIONS: Tree size alone was a weak predictor of cone production. Interactions with neighbors play an important role in generating reproductive heterogeneity, and must be accounted for when relating cone production to size. The strong between-year correlation, together with the large variance in cone production among trees without neighbors, suggests that still more of the variance may be explainable, but requires factors outside of our study.

Demographic heterogeneity, cohort selection, and population growth.

Demographic heterogeneity--variation among individuals in survival and reproduction--is ubiquitous in natural populations. Structured population models address heterogeneity due to age, size, or major developmental stages. However, other important sources of demographic heterogeneity, such as genetic variation, spatial heterogeneity in the environment, maternal effects, and differential exposure to stressors, are often not easily measured and hence are modeled as stochasticity. Recent research has elucidated the role of demographic heterogeneity in changing the magnitude of demographic stochasticity in small populations. Here we demonstrate a previously unrecognized effect: heterogeneous survival in long-lived species can increase the long-term growth rate in populations of any size. We illustrate this result using simple models in which each individual's annual survival rate is independent of age but survival may differ among individuals within a cohort. Similar models, but with nonoverlapping generations, have been extensively studied by demographers, who showed that, because the more "frail" individuals are more likely to die at a young age, the average survival rate of the cohort increases with age. Within ecology and evolution, this phenomenon of "cohort selection" is increasingly appreciated as a confounding factor in studies of senescence. We show that, when placed in a population model with overlapping generations, this heterogeneity also causes the asymptotic population growth rate lambda to increase, relative to a homogeneous population with the same mean survival rate at birth. The increase occurs because, even integrating over all the cohorts in the population, the population becomes increasingly dominated by the more robust individuals. The growth rate increases monotonically with the variance in survival rates, and the effect can be substantial, easily doubling the growth rate of slow-growing populations. Correlations between parent and offspring phenotype change the magnitude of the increase in lambda, but the increase occurs even for negative parent-offspring correlations. The effect of heterogeneity in reproductive rate on lambda is quite different: growth rate increases with reproductive heterogeneity for positive parent-offspring correlation but decreases for negative parent-offspring correlation. These effects of demographic heterogeneity on lambda have important implications for population dynamics, population viability analysis, and evolution.

Inferring microhabitat preferences of Lilium catesbaei (Liliaceae).

PREMISE OF THE STUDY: Microhabitat studies use varied statistical methods, some treating site occupancy as a dependent and others as an independent variable. Using the rare Lilium catesbaei as an example, we show why approaches to testing hypotheses of differences between occupied and unoccupied sites can lead to erroneous conclusions about habitat preferences. Predictive approaches like logistic regression can better lead to understanding of habitat requirements. METHODS: Using 32 lily locations and 30 random locations >2 m from a lily (complete data: 31 lily and 28 random spots), we measured physical conditions--photosynthetically active radiation (PAR), canopy cover, litter depth, distance to and height of nearest shrub, and soil moisture--and number and identity of neighboring plants. Twelve lilies were used to estimate a photosynthetic assimilation curve. Analyses used logistic regression, discriminant function analysis (DFA), (multivariate) analysis of variance, and resampled Wilcoxon tests. KEY RESULTS: Logistic regression and DFA found identical predictors of presence (PAR, canopy cover, distance to shrub, litter), but hypothesis tests pointed to a different set (PAR, litter, canopy cover, height of nearest shrub). Lilies are mainly in high-PAR spots, often close to light saturation. By contrast, PAR in random spots was often near the lily light compensation point. Lilies were near Serenoa repens less than at random; otherwise, neighbor identity had no significant effect. CONCLUSIONS: Predictive methods are more useful in this context than the hypothesis tests. Light availability plays a big role in lily presence, which may help to explain increases in flowering and emergence after fire and roller-chopping.

The statistical mechanics of community assembly and species distribution.

• Theoretically, communities at or near their equilibrium species number resist entry of new species. Such 'biotic resistance' recently has been questioned because of successful entry of alien species into diverse natural communities. • Data on 10,409 naturalizations of 5350 plant species over 16 sites dispersed globally show exponential distributions both for species over sites and for sites over number of species shared. These exponentials signal a statistical mechanics of species distribution, assuming two conditions. First, species and sites are equivalent, either identical ('neutral') or so complex that the chance a species is in the right place at the right time is vanishingly small ('idiosyncratic'); the range of species and sites in our data disallows a neutral explanation. Secondly, the total number of naturalizations is fixed in any era by a 'regulator'. • Previous correlation of species naturalization rates with net primary productivity over time suggests that the regulator is related to productivity. • We conclude that biotic resistance is a moving ceiling, with resistance controlled by productivity. The general observation that the majority of species occur naturally at only a few sites, and only a few species occur at many sites, now has a quantitative (exponential) character, offering the study of species' distributions a previously unavailable rigor.

Consequences of heterogeneity in survival probability in a population of Florida scrub-jays.

1. Using data on breeding birds from a 35-year study of Florida scrub-jays Aphelocoma coerulescens (Bosc 1795), we show that survival probabilities are structured by age, birth cohort, and maternal family, but not by sex. Using both accelerated failure time (AFT) and Cox proportional hazard models, the data are best described by models incorporating variation among birth cohorts and greater mortality hazard with increasing age. AFT models using Weibull distributions with the shape parameter > 1 were always the best-fitting models. 2. Shared frailty models allowing for family structure greatly reduce model deviance. The best-fitting models included a term for frailty shared by maternal families. 3. To ask how long a data set must be to reach qualitatively the same conclusions, we repeated the analyses for all possible truncated data sets of 2 years in length or greater. Length of the data set affects the parameter estimates, but not the qualitative conclusions. In all but three of 337 truncated data sets the best-fitting models pointed to same conclusions as the full data set. Shared frailty models appear to be quite robust. 4. The data are not adequate for testing hypotheses as to whether variation in frailty is heritable. 5. Substantial structured heterogeneity for survival exists in this population. Such structured heterogeneity has been shown to have substantial effects in reducing demographic stochasticity.

Sources of variation in growth, form, and survival in dwarf and normal-stature pitch pines (Pinus rigida, Pinaceae) in long-term transplant experiments.

Determining the relative contributions of genetic and environmental factors to phenotypic variation is critical for understanding the evolutionary ecology of plant species, but few studies have examined the sources of phenotypic differentiation between nearby populations of woody plants. We conducted reciprocal transplant experiments to examine sources of variation in growth rate, form, survival, and maturation in a globally rare dwarf population of pitch pine (Pinus rigida) and in surrounding populations of normal-stature pitch pines on Long Island, New York. Transplants were monitored over a 6-yr period. The influence of seedling origin on height, growth rate, survival, and form (single-stemmed vs. multi-stemmed growth habit) was much smaller than the effect of transplanting location. Both planting site and seed origin were important factors in determining time to reproduction; seedlings originating from dwarf populations and seedlings planted at the normal-stature site reproduced earliest. These results suggest that many of the differences between dwarf and normal-stature pitch pines may be due more to plastic responses to environmental factors than to genetic differentiation among populations. Therefore, preservation of the dwarf pine habitat is essential for preserving dwarf pine communities; the dwarf pines cannot be preserved ex situ.

Limiting relationships between selection and recombination.

It is difficult to directly observe processes like natural selection at the genetic level, but relatively easy to estimate genetic frequencies in populations. As a result, genetic frequency data are widely used to make inferences about the underlying evolutionary processes. However, multiple processes can generate the same patterns of frequency data, making such inferences weak. By studying the limits to the underlying processes, one can make inferences from frequency data by asking how strong selection (or some other process of interest) would have to be to generate the observed pattern. Here we present results of a study of the limits to the relationship between selection and recombination in two-locus, two-allele systems in which we found the limiting relationships for over 30000 sets of parameters, effectively covering the range of two-locus, two-allele problems. Our analysis relates T(min)--the minimum time for a population to evolve from the initial to the final conditions--to the strengths of selection and recombination, the amount of linkage disequilibrium, and the Nei distance between the initial and final conditions. T(min) can be large with either large disequilibrium and small Nei distance, or the reverse. The behavior of T(min) provides information about the limiting relationships between selection and recombination. Our methods allow evolutionary inferences from frequency data when deterministic processes like selection and recombination are operating; in this sense they complement methods based entirely on drift.

Variation among Individuals and Reduced Demographic Stochasticity.

Population viability analysis ( PVA) is a technique that employs stochastic demographic models to predict extinction risk. All else being equal, higher variance in a demographic rate leads to a greater extinction risk. Demographic stochasticity represents variance due to differences among individuals. Current implementations of PVAs, however, assume that the expected fates of all individuals are identical. For example, demographic stochasticity in survival is modeled as a random draw from a binomial distribution. We developed a simple conceptual model showing that if there is variation among individuals in expected survival, then existing PVA models overestimate the variance due to demographic stochasticity in survival. This is a consequence of Jensen's inequality and the fact that the binomial demographic variance is a concave function of mean survival. The effect of variation among individuals on demographic stochasticity in fecundity depends on the mean-variance relationship for individual reproductive success, which is not presently known. If fecundity patterns mirror those of survival, then variation among individuals will reduce the extinction risk of small populations.

RESUMEN: El análisis de viabilidad poblacional (AVP) es un técnica que emplea modelos demográficos estocásticos para predecir el riesgo de extinción. Todo lo demás siendo igual, mayor variación en la tendencia demográfica conduce a un mayor riesgo de extinción. La estocasticidad demográfica representa variación debido a diferencias entre individuos. Sin embargo, los AVP actualmente asumen que el destino esperado para cada individuo es idéntico. Por ejemplo, la estocasticidad demográfica en la supervivencia es modelada como una muestra aleatoria de una distribución binomial. Desarrollamos un modelo conceptual simple que muestra que si hay variación entre individuos en la supervivencia esperada, entonces los modelos de AVP existentes sobrestiman la variación debida a la estocasticidad demográfica en la supervivencia. Esto es una consecuencia de la desigualdad de Jensen y del hecho de que la variación demográfica binomial es una función cóncava de la supervivencia promedio. El efecto de la variación entre individuos sobre la estocasticidad demográfica en la fecundidad depende de la relación media-varianza del éxito reproductivo individual, que actualmente es desconocida. Si los patrones de fecundidad son un reflejo de los de supervivencia, entonces la variación entre individuos reducirá el riesgo de extinción de poblaciones pequeñas.

Population Numbers Count: Tools for Near-Term Demographic Analysis.

How do unit or proportional changes in vital rates affect populations in the short term? We present a new extension to standard methods of matrix model analysis that allows us to answer this question for the first time. By using the sensitivities of all the eigenvalues/vectors, rather than just the leading eigenvalue/vector pair, we can predict the consequences of unit or proportional changes in vital rates to population size and structure at any arbitrary time, not just when populations have neared their stable distribution. These extensions are particularly important in studying populations subject to frequent disturbance, where stable growth rate and stable distribution do not provide sufficient information about the effects of changes in the vital rates; managed populations in which short-term goals are defined; and the adequacy of the underlying matrix model for either short- or long-term understanding. We use analysis of empirical data on the cactus Coryphantha robbinsorum to demonstrate this approach and show that short-term predictions can differ substantially from those based on standard, asymptotic, analysis.

COMPONENTS OF FLOWERING TIME VARIATION IN A DESERT ANNUAL.

How much of the variation seen in life histories is consistent with adaptive hypotheses, and how much requires other kinds of explanation? Differences in flowering time between Sonoran (earlier flowering) and Chihuahuan Desert (later flowering) populations of the desert annual Eriogonum abertianum Torr. (Polygonaceae) are significant, repeatable between greenhouse experiments, and persist into a second greenhouse generation. These apparent genetic differences are consistent with a hypothesis of local adaptation: field demographic studies (Fox, 1989b) show that many fewer Sonoran than Chihuahuan Desert plants survive to the summer rainy season, suggesting selection for earlier flowering in the Sonoran Desert. Within natural populations there is considerable phenological complexity: time of first flowering varies by up to six months, and individuals may have zero, one, or several reproductive episodes. Greenhouse sib analyses revealed only marginal among-family genetic variation for flowering size. The resemblance between parents and offspring for size and time of flowering varied with growth conditions, suggesting that this marginal variation among families may be at least partly due to factors other than additive genetic variance. On the other hand, moisture limitation significantly delayed the onset of flowering in two independent experiments. Variation in moisture availability in both time and space is characteristic of desert environments. The phenological complexity in natural populations may thus be generated by random variation in moisture availability, possibly in conjunction with variation in germination date and plant size. The results call into question the claim that drought generally induces flowering in desert annuals.