Margaret E. K. Evans

Climate, Niche Evolution, and Diversification of the “Bird‐Cage” Evening Primroses (Oenothera, Sections Anogra and Kleinia)

We integrate climatic niche models and dated phylogenies to characterize the evolution of climatic niches in Oenothera sections Anogra and Kleinia (Onagraceae), and from that we make inferences on diversification in relation to climate. The evolution of climatic tolerances in Anogra + Kleinia has been heterogeneous, across phylogenetic groups and across different dimensions of climate. All the extant taxa occur in semiarid to arid conditions (annual precipitation of 10.1–49.1 cm and high temperatures in the warmest month of 28.5°–40.1°C), but there is striking variation among taxa in their climatic tolerances, especially temperature (minimum temperatures in the coldest month of −14.0° to 5.3°C) and summer versus winter precipitation (precipitation in the warmest quarter of 0.6–19.4 cm). Climatic disparity is especially pronounced in two subclades (californica, deltoides) that radiated in the southwestern United States and California, apparently including both divergent and convergent evolution of climatic tolerances. This niche evolution is remarkable, given the probable timescale of the radiation (∼1 million years). We suggest that the spatiotemporal climatic heterogeneity of western North America has served as a driver of diversification. Our data are also consistent with Axelrod’s hypothesis that the spread of arid conditions in western North America stimulated diversification of arid‐adapted lineages.

GERM BANKING: BET-HEDGING AND VARIABLE RELEASE FROM EGG AND SEED DORMANCY

Many species produce eggs or seeds that refrain from hatching despite developmental preparedness and favorable environmental conditions. Instead, these propagules hatch in intervals over long periods. Such variable hatch or germination tactics may represent bet‐hedging against future catastrophes. Empiricists have independently recognized these approaches in diverse species. Terms such as seed banking, delayed egg hatching, and embryonic diapause have been used to describe these tactics, but connections between fields of study have been rare. Here we suggest a general term, germ banking, to incorporate all previous terms, unifying many seemingly disparate biological strategies under a single definition. We define the phenomenon of germ banking and use several biological examples to illustrate it. We then discuss the different causes of variation in emergence timing, delineate which constitute germ banking, and distinguish between germ banking and optimal timing of diapause. The wide‐ranging consequences of germ banking are discussed, including modification of the age structure of a population, the alteration of microevolutionary dynamics, the migration of alleles from the past, the maintenance of genetic and species diversity, and the promotion of species coexistence. We end by posing questions to direct future research.

Advancing population ecology with integral projection models: a practical guide

Summary 1. Integral projection models (IPMs) use information on how an individual’s state influences its vital rates – survival, growth and reproduction – to make population projections. IPMs are constructed from regression models predicting vital rates from state variables (e.g. size or age) and covariates (e.g. environment). By combining regressions of vital rates, an IPM provides mechanistic insight into emergent ecological patterns such as population dynamics, species geographic distributions or life-history strategies. 2. Here, we review important resources for building IPMs and provide a comprehensive guide, with extensive R code, for their construction. IPMs can be applied to any stage-structured population; here, we illustrate IPMs for a series of plant life histories of increasing complexity and biological realism, highlighting the utility of various regression methods for capturing biological patterns. We also present case studies illustrating how IPMs can be used to predict species’ geographic distributions and life-history strategies. 3. IPMs can represent a wide range of life histories at any desired level of biological detail. Much of the strength of IPMs lies in the strength of regression models. Many subtleties arise when scaling from vital rate regressions to population-level patterns, so we provide a set of diagnostics and guidelines to ensure that models are biologically plausible. Moreover, IPMs can exploit a large existing suite of analytical tools developed for matrix projection models.

Bet Hedging via Seed Banking in Desert Evening Primroses (Oenothera, Onagraceae): Demographic Evidence from Natural Populations

Bet hedging is one solution to the problem of an unpredictably variable environment: fitness in the average environment is sacrificed in favor of lower variation in fitness if this leads to higher long‐run stochastic mean fitness. While bet hedging is an important concept in evolutionary ecology, empirical evidence that it occurs is scant. Here we evaluate whether bet hedging occurs via seed banking in natural populations of two species of desert evening primroses (Oenothera, Onagraceae), one annual and one perennial. Four years of data on plants and 3 years of data on seeds yielded two transitions for the entire life cycle. One year was exceptionally dry, leading to reproductive failure in the sample areas, and the other was above average in precipitation, leading to reproductive success in four of five populations. Stochastic simulations of population growth revealed patterns indicative of bet hedging via seed banking, particularly in the annual populations: variance in fitness and fitness in the average environment were lower with seed banking than without, whereas long‐run stochastic mean fitness was higher with seed banking than without across a wide range of probabilities of the wet year. This represents a novel, unusually rigorous demonstration of bet hedging from field data.

Reproductive biology of three sympatric endangered plants endemic to Florida scrub

We investigated the reproductive biology of three plants endemic to rosemary scrub habitats on the Lake Wales Ridge of Florida, USA. We used hand-pollination experiments and observations of flowers and their insect visitors to determine their mating systems and pollination. Fruit or seed set after self pollination was 94, 97, and 8% of fruit or seed set after cross pollination in Eryngium cuneifolium (Apiaceae), Hypericum cumulicola (Hypericaceae), and Liatris ohlingerae (Asteraceae) respectively, indicating that the first two are self-compatible and the last is obligately outcrossing. All three depend on insects for seed production (4–7% fruit or seed set without insects). Diverse insects visit flowers of E. cuneifolium (101 species recorded), whereas L. ohlingerae is visited predominantly by butterflies and H. cumulicola by one genus of bees (Dialictus, Halictidae). Our data indicate pollinator visitation does not currently limit seed production in E. cuneifolium or H. cumulicola, but does in L. ohlingerae. Despite the features they share (habit, habitat, disturbance regime), we found unique aspects of these species’ reproductive biology yielding unique risks to population viability. We suggest that multispecies recovery plans must consider several aspects of the biology of species with superficial similarities to be successful. # 2003 Elsevier Science Ltd. All rights reserved.

CLIMATE AND LIFE-HISTORY EVOLUTION IN EVENING PRIMROSES (OENOTHERA, ONAGRACEAE): A PHYLOGENETIC COMPARATIVE ANALYSIS

Abstract Evolutionary ecologists have long sought to understand the conditions under which perennial (iteroparous) versus annual (semelparous) plant life histories are favored. We evaluated the idea that aridity and variation in the length of droughts should favor the evolution of an annual life history, both by decreasing adult survival and by increasing the potential for high seedling survival via reduced plant cover. We calculated phylogenetically independent contrasts of climate with respect to life history in a clade of winter‐establishing evening primroses (sections Anogra and Kleinia; Oenothera; Onagraceae), which includes seven annuals, 12 perennials, and two variable taxa. Climate variables were quantified from long‐term records at weather stations near collection localities. To explicitly account for phylogenetic uncertainty, contrasts were calculated on a random sample of phylogenetic trees from the posterior distribution of a Bayesian analysis of DNA sequence data. Statements of association are based on comparing the pertree mean contrast, which has a null expectation of zero, to a set of per‐tree mean contrasts calculated on the same trees, after randomizing the climate data. As predicted, increased annual aridity, increased annual potential evapotranspiration, and decreased annual precipitation were associated with transitions to the annual habit, but these trends were not significantly different from the null pattern. Transitions to the annual habit were not significantly associated with increases in one measure of aridity in summer nor with increased summer drought, but they were associated with significantly increased maximum summer temperatures. In winter, increased aridity and decreased precipitation were significantly associated with transitions to the annual habit. Changes in life history were not significantly associated with changes in the coefficient of variation of precipitation, either on an annual or seasonal (summer vs. winter) basis. Though we cannot attribute causality on the basis of a correlational, historical study, our results are consistent with the idea that increased heat and drought at certain times of the year favor the evolution of the annual habit. Increased heat in summer may cause adult survival to decline, while increased aridity and decreased precipitation in the season of seedling recruitment (winter) may favor a drought‐avoiding, short‐lived annual strategy. Not all of the predicted patterns were observed: the capability for drought‐induced dormancy may preclude change in habit in response to summer drought in our study group.

Ecological Conditions Affect Evolutionary Trajectory in a Predator-Prey System

The arms race of adaptation and counter adaptation in predator-prey interactions is a fascinating evolutionary dynamic with many consequences, including local adaptation and the promotion or maintenance of diversity. Although such antagonistic coevolution is suspected to be widespread in nature, experimental documentation of the process remains scant, and we have little understanding of the impact of ecological conditions. Here, we present evidence of predator-prey coevolution in a long-term experiment involving the predatory bacterium Bdellovibrio bacteriovorus and the prey Pseudomonas fluorescens, which has three morphs (SM, FS, and WS). Depending on experimentally applied disturbance regimes, the predator-prey system followed two distinct evolutionary trajectories, where the prey evolved to be either super-resistant to predation (SM morph) without counter-adaptation by the predator, or moderately resistant (FS morph), specialized to and coevolving with the predator. Although predation-resistant FS morphs suffer a cost of resistance, the evolution of extreme resistance to predation by the SM morph was apparently unconstrained by other traits (carrying capacity, growth rate). Thus we demonstrate empirically that ecological conditions can shape the evolutionary trajectory of a predator-prey system.

Insights on the Evolution of Plant Succulence from a Remarkable Radiation in Madagascar (Euphorbia)

Patterns of adaptation in response to environmental variation are central to our understanding of biodiversity, but predictions of how and when broad-scale environmental conditions such as climate affect organismal form and function remain incomplete. Succulent plants have evolved in response to arid conditions repeatedly, with various plant organs such as leaves, stems, and roots physically modified to increase water storage. Here, we investigate the role played by climate conditions in shaping the evolution of succulent forms in a plant clade endemic to Madagascar and the surrounding islands, part of the hyper-diverse genus Euphorbia (Euphorbiaceae). We used multivariate ordination of 19 climate variables to identify links between particular climate variables and three major forms of succulence-succulent leaves, cactiform stem succulence, and tubers. We then tested the relationship between climatic conditions and succulence, using comparative methods that account for shared evolutionary history. We confirm that plant water storage is associated with the two components of aridity, temperature, and precipitation. Cactiform stem succulence, however, is not prevalent in the driest environments, countering the widely held view of cactiforms as desert icons. Instead, leaf succulence and tubers are significantly associated with the lowest levels of precipitation. Our findings provide a clear link between broad-scale climatic conditions and adaptation in land plants, and new insights into the climatic conditions favoring different forms of succulence. This evidence for adaptation to climate raises concern over the evolutionary future of succulent plants as they, along with other organisms, face anthropogenic climate change.

Mating systems and limits to seed production in two Dicerandra mints endemic to Florida scrub

We used hand-pollination experiments to test the mating systems of and evaluate limits to seed production in two federally listed endangered plants endemic to the Lake Wales Ridge in Florida, USA: Dicerandra frutescens Shinners ssp. frutescens Huck and D. christmanii Huck and Judd (Lamiaceae). Both are nonclonal, short-lived perennials found in gaps created by disturbance (e.g., fire, roads) in Florida scrub. We found that both species require pollen and insect visitation to produce seeds. We detected pollinator limitation of seed production in D. christmanii but not D. frutescens ssp. frutescens, which we suggest is a function of time-since-disturbance or gap size rather than intrinsic differences between the two species. Both species are self-compatible. Inbreeding depression reduced seed set by 60% in D. frutescens ssp. frutescens but did not occur in D. christmanii. We conclude that pollinator limitation (in fire-suppressed populations of both species) and inbreeding depression (in D. frutescens ssp. frutescens) have the potential to limit seed production in these seed-dependent, rare species. Appropriate fire management should mitigate both of these risks, by maintaining large populations and conditions attractive to pollinators. Although these two species are very similar in reproductive biology, comparisons with other Florida scrub endemics and with rare plants in general suggest that potential threats to conservation via reproductive biology are difficult to predict, depending on combinations of ecology, life-history, and phylogenetic history.

Extreme environments select for reproductive assurance: evidence from evening primroses (Oenothera)

Competing evolutionary forces shape plant breeding systems (e.g. inbreeding depression, reproductive assurance). Which of these forces prevails in a given population or species is predicted to depend upon such factors as life history, ecological conditions, and geographical context. Here, we examined two such predictions: that self-compatibility should be associated with the annual life history or extreme climatic conditions. We analyzed data from a clade of plants remarkable for variation in breeding system, life history and climatic conditions (Oenothera, sections Anogra and Kleinia, Onagraceae). We used a phylogenetic comparative approach and Bayesian or hybrid Bayesian tests to account for phylogenetic uncertainty. Geographic information system (GIS)-based climate data and ecological niche modeling allowed us to quantify climatic conditions. Breeding system and reproductive life span are not correlated in Anogra and Kleinia. Instead, self-compatibility is associated with the extremes of temperature in the coldest part of the year and precipitation in the driest part of the year. In the 60 yr since this pattern was anticipated, this is the first demonstration of a relationship between the evolution of self-compatibility and climatic extremes. We discuss possible explanations for this pattern and possible implications with respect to anthropogenic climate change.