Molecular Evolutionary Dynamics of Energy Limited Microorganisms

Microorganisms have the unique ability to survive extended periods of time in environments with extremely low levels of exploitable energy. To determine the extent that energy limitation affects microbial evolution, we examined the molecular evolutionary dynamics of a phylogenetically diverse set of taxa over the course of 1,000 days. We found that periodic exposure to energy limitation affected the rate of molecular evolution, the accumulation of genetic diversity, and the rate of extinction. We then determined the degree that energy limitation affected the spectrum of mutations as well as the direction of evolution at the gene level. Our results suggest that the initial depletion of energy altered the direction and rate of molecular evolution within each taxon, though after the initial depletion the rate and direction did not substantially change. However, this consistent pattern became diminished when comparisons were performed across phylogenetically distant taxa, suggesting that although the dynamics of molecular evolution under energy limitation are highly generalizable across the microbial tree of life, the targets of adaptation are specific to a given taxon.     

Microbial seed banks: the ecological and evolutionary implications of dormancy

Dormancy is a bet-hedging strategy used by a wide range of taxa, including microorganisms. It refers to an organism's ability to enter a reversible state of low metabolic activity when faced with unfavourable environmental conditions. Dormant microorganisms generate a seed bank, which comprises individuals that are capable of being resuscitated following environmental change. In this Review, we highlight mechanisms that have evolved in microorganisms to allow them to successfully enter and exit a dormant state, and discuss the implications of microbial seed banks for evolutionary dynamics, population persistence, maintenance of biodiversity, and the stability of ecosystem processes.     

Temporal genetic stability in natural populations of the waterflea Daphnia magna in response to strong selection pressure

Studies monitoring changes in genetic diversity and composition through time allow a unique understanding of evolutionary dynamics and persistence of natural populations. However, such studies are often limited to species with short generation times that can be propagated in the laboratory or few exceptional cases in the wild. Species that produce dormant stages provide powerful models for the reconstruction of evolutionary dynamics in the natural environment. A remaining open question is to what extent dormant egg banks are an unbiased representation of populations and hence of the species’ evolutionary potential, especially in the presence of strong environmental selection. We address this key question using the water flea Daphnia magna, which produces dormant stages that accumulate in biological archives over time. We assess temporal genetic stability in three biological archives, previously used in resurrection ecology studies showing adaptive evolutionary responses to rapid environmental change. We show that neutral genetic diversity does not decline with the age of the population and it is maintained in the presence of strong selection. In addition, by comparing temporal genetic stability in hatched and unhatched populations from the same biological archive, we show that dormant egg banks can be consulted to obtain a reliable measure of genetic diversity over time, at least in the multidecadal time frame studied here. The stability of neutral genetic diversity through time is likely mediated by the buffering effect of the resting egg bank.     

The implications of rapid eco‐evolutionary processes for biological control ‐ a review

Novel environmental conditions experienced by introduced species can drive rapid evolution of diverse traits. In turn, rapid evolution, both adaptive and non‐adaptive, can influence population size, growth rate, and other important ecological characteristics of populations. In addition, spatial evolutionary processes that arise from a combination of assortative mating between highly dispersive individuals at the expanding edge of populations and altered reproductive rates of those individuals can accelerate expansion speed. Growing experimental evidence shows that the effects of rapid evolution on ecological dynamics can be quite large, and thus it can affect establishment, persistence, and the distribution of populations. We review the experimental and theoretical literature on such eco‐evolutionary feedbacks and evaluate the implications of these processes for biological control. Experiments show that evolving populations can establish at higher rates and grow larger than non‐evolving populations. However, non‐adaptive processes, such as genetic drift and inbreeding depression can also lead to reduced fitness and declines in population size. Spatial evolutionary processes can increase spread rates and change the fitness of individuals at the expansion front. These examples demonstrate the power of eco‐evolutionary dynamics and indicate that evolution is likely more important in biocontrol programs than previously realized. We discuss how this knowledge can be used to enhance efficacy of biological control.     

土壤种子库的研究进展及若干研究热点

 土壤种子库是指存在于表层土壤（包括凋落物）中的有生命的种子。土壤种子库的研究已是植物生态学研究不可缺少的一部分,现已成为植物种群生态学中比较活跃的领域。土壤种子库时期是植物种群生活史的一个重要阶段,有人称之为潜种群阶段。土壤种子库对一年生植物来说尤其重要。土壤种子库简单地可分为瞬时土壤种子库和长久土壤种子库,即使给予理想的萌发条件如季节、温度、湿度等,土壤种子库中也仍有部分种子保持休眠状态,休眠的种子组成了土壤长久种子库的成分。时空异质性是土壤种子库的基本特性之一,不仅不同植被类型的土壤种子库具有不同的组成、大小和多样性,而且微环境也影响土壤种子库的分布格局。由于萌发、捕食和衰老等原因,土壤种子库具有季节动态,一般在旧种子萌发之后,新种子散布之前达到最低点。在高等植物占据的大多数生境中,以休眠繁殖体形式存在的个体远远超过地上植株的数量;土壤种子库、幼苗库和成年植被相互联系相互影响。由于各种原因如群落类型的差异、群落的演替阶段、取样的时间等,地上植被和土壤种子库之间关系大体上可分为两种情况,即相似性和差异性;研究土壤种子库的方法通常有萌发法和物理分离法。土壤种子库能部分反应群落的历史,对退化生态系统的恢复起着重要的作用。目前土壤种子库的主要研究热点问题可分为以下几个方面：1）土壤种子库的研究方法,2）土壤种子库的分类问题,3）土壤种子库分布的时空格局,4）地上植被和土壤种子库的关系,5）土壤种子库的动态等。     

种子雨研究进展

种子雨是指在特定的时间和特定的空间从母株上散落的种子量。种子雨的组成和大小具有时空异质性。种子雨的空间异质性表现在种子雨的组成和大小因群落而异,种群间的种子雨因种群而异,种群内部的种子雨因个体而异;种子雨的时间异质性表现在不管是群落、种群还是种群内部的个体,其种子雨既具有季节动态,又具有年际变化。种子雨、种子库、幼苗库和地上植被相互联系、相互作用。种子雨的研究对更好地了解种群和群落动态等具有重要意义。应用现代的分子遗传标记技术、同位素标记法和荧光染料法等研究种子雨的散布过程和种子命运将是未来种子雨研究的热点,种子雨和种子库的结合研究及其与动植物关系的研究尚需加强。     

Seed bank persistence of clonal weeds in contrasting habitats: implications for control

The ability of weeds to form a seed bank is important for their population dynamics and management because it provides a refuge enabling reinvasion after established target plants have died. However, knowledge of the differential seed behaviour of individual species over multiple years and varying environmental conditions is surprisingly rare but necessary for effective control of diverse weed populations. We established a seed burial experiment in alpine habitats differing in management regime (i.e., forest, hay meadow and pasture) to determine whether seeds of the unpalatable perennial weeds, Veratrum album (white hellebore) and Gentiana lutea (yellow gentian) were able to delay germination and remain viable over 3 years. Our study shows that both species formed a short-term persistent seed bank; in the third-year, the soil seed banks of both species were nearly depleted, having declined to <5% of their original size. Both species had strikingly different germination strategies: G. lutea seeds mainly germinated in their first-year, whilst the majority of V. album seeds germinated in their second-year. The fraction of dormant G. lutea seeds increased with seed age, indicating that seeds remained viable after forgoing germination in the previous year. Habitat-specific differences in seed germination increased with seed age, with germination fractions being lowest in moist hay meadows. This suggests that the negative effects of anoxic conditions became more pronounced as seeds aged in hay meadows. Conversely, seed dormancy was equal among habitats. The absence of a long-term persistent seed bank has important implications for the management of both nuisance and endangered-plant populations. In the case of V. album and G. lutea, re-colonization of habitats from the seed bank is unlikely after established plants have been removed.     

Global asymptotic stability of plant-seed bank models

Many plant populations have persistent seed banks, which consist of viable seeds that remain dormant in the soil for many years. Seed banks are important for plant population dynamics because they buffer against environmental perturbations and reduce the probability of extinction. Viability of the seeds in the seed bank can depend on the seed’s age, hence it is important to keep track of the age distribution of seeds in the seed bank. In this paper we construct a general density-dependent plant-seed bank model where the seed bank is age-structured. We consider density dependence in both seedling establishment and seed production, since previous work has highlighted that overcrowding can suppress both of these processes. Under certain assumptions on the density dependence, we prove that there is a globally stable equilibrium population vector which is independent of the initial state. We derive an analytical formula for the equilibrium population using methods from feedback control theory. We apply these results to a model for the plant species Cirsium palustre and its seed bank.     

A resurrection experiment finds evidence of both reduced genetic diversity and potential adaptive evolution in the agricultural weed Ipomoea purpurea

Despite the negative economic and ecological impact of weeds, relatively little is known about the evolutionary mechanisms that influence their persistence in agricultural fields. Here, we use a resurrection approach to examine the potential for genotypic and phenotypic evolution in Ipomoea purpurea, an agricultural weed that is resistant to glyphosate, the most widely used herbicide in current‐day agriculture. We found striking reductions in allelic diversity between cohorts sampled nine years apart (2003 vs. 2012), suggesting that populations of this species sampled from agricultural fields have experienced genetic bottleneck events that have led to lower neutral genetic diversity. Heterozygosity excess tests indicate that these bottlenecks may have occurred prior to 2003. A greenhouse assay of individuals sampled from the field as seed found that populations of this species, on average, exhibited modest increases in herbicide resistance over time. However, populations differed significantly between sampling years for resistance: some populations maintained high resistance between the sampling years whereas others exhibited increased or decreased resistance. Our results show that populations of this noxious weed, capable of adapting to strong selection imparted by herbicide application, may lose genetic variation as a result of this or other environmental factors. We probably uncovered only modest increases in resistance on average between sampling cohorts due to a strong and previously identified fitness cost of resistance in this species, along with the potential that nonresistant migrants germinate from the seed bank.     

Evidence that implicit assumptions of ‘no evolution’ of disease vectors in changing environments can be violated on a rapid timescale

Projected impacts of climate change on vector-borne disease dynamics must consider many variables relevant to hosts, vectors and pathogens, including how altered environmental characteristics might affect the spatial distributions of vector species. However, many predictive models for vector distributions consider their habitat requirements to be fixed over relevant time-scales, when they may actually be capable of rapid evolutionary change and even adaptation. We examine the genetic signature of a spatial expansion by an invasive vector into locations with novel temperature conditions compared to its native range as a proxy for how existing vector populations may respond to temporally changing habitat. Specifically, we compare invasions into different climate ranges and characterize the importance of selection from the invaded habitat. We demonstrate that vector species can exhibit evolutionary responses (altered allelic frequencies) to a temperature gradient in as little as 7–10 years even in the presence of high gene flow, and further, that this response varies depending on the strength of selection. We interpret these findings in the context of climate change predictions for vector populations and emphasize the importance of incorporating vector evolution into models of future vector-borne disease dynamics.     

Thermal tolerance in the keystone species Daphnia magna—a candidate gene and an outlier analysis approach

Changes in temperature have occurred throughout Earth's history. However, current warming trends exacerbated by human activities impose severe and rapid loss of biodiversity. Although understanding the mechanisms orchestrating organismal response to climate change is important, remarkably few studies document their role in nature. This is because only few systems enable the combined analysis of genetic and plastic responses to environmental change over long time spans. Here, we characterize genetic and plastic responses to temperature increase in the aquatic keystone grazer Daphnia magna combining a candidate gene and an outlier analysis approach. We capitalize on the short generation time of our species, facilitating experimental evolution, and the production of dormant eggs enabling the analysis of long‐term response to environmental change through a resurrection ecology approach. We quantify plasticity in the expression of 35 candidate genes in D. magna populations resurrected from a lake that experienced changes in average temperature over the past century and from experimental populations differing in thermal tolerance isolated from a selection experiment. By measuring expression in multiple genotypes from each of these populations in control and heat treatments, we assess plastic responses to extreme temperature events. By measuring evolutionary changes in gene expression between warm‐ and cold‐adapted populations, we assess evolutionary response to temperature changes. Evolutionary response to temperature increase is also assessed via an outlier analysis using EST‐linked microsatellite loci. This study provides the first insights into the role of plasticity and genetic adaptation in orchestrating adaptive responses to environmental change in D. magna.     

How phenotypic convergence arises in experimental evolution

Evolutionary convergence is a core issue in the study of adaptive evolution, as well as a highly debated topic at present. Few studies have analyzed this issue using a “real‐time” or evolutionary trajectory approach. Do populations that are initially differentiated converge to a similar adaptive state when experiencing a common novel environment? Drosophila subobscura populations founded from different locations and years showed initial differences and variation in evolutionary rates in several traits during short‐term (～20 generations) laboratory adaptation. Here, we extend that analysis to 40 more generations to analyze (1) how differences in evolutionary dynamics among populations change between shorter and longer time spans, and (2) whether evolutionary convergence occurs after 60 generations of evolution in a common environment. We found substantial variation in longer term evolutionary trajectories and differences between short‐ and longer term evolutionary dynamics. Although we observed pervasive patterns of convergence toward the character values of long‐established populations, populations still remain differentiated for several traits at the final generations analyzed. This pattern might involve transient divergence, as we report in some cases, indicating that more generations should lead to final convergence. These findings highlight the importance of longer term studies for understanding convergent evolution.     

Algebraic determination of the evolutionary stable germination fraction

In this article, we consider a bet-hedging model with density dependence for germination behavior of dormant seeds. We show how to compute accurate values of the evolutionary stable germination fraction using a method based on expansion around the average seed bank size. The expansion is made up to the fourth order and is expressed in terms of the first four moments of the distribution of the year-to-year variation in the average yield per adult plant. This method leads to a simple algebraic equation, which can be solved without recurring to simulations of the seed bank dynamics. We first show the analytical derivation under general assumptions about the effect of density dependence. We then test our results with a numerical analysis where an explicit form of the density dependence has been taken.     

Balancing selection and drift in a polymorphic salamander metapopulation

Understanding how genetic variation is maintained in a metapopulation is a longstanding problem in evolutionary biology. Historical resurveys of polymorphisms have offered efficient insights about evolutionary mechanisms, but are often conducted on single, large populations, neglecting the more comprehensive view afforded by considering all populations in a metapopulation. Here, we resurveyed a metapopulation of spotted salamanders (Ambystoma maculatum) to understand the evolutionary drivers of frequency variation in an egg mass colour polymorphism. We found that this metapopulation was demographically, phenotypically and environmentally stable over the last three decades. However, further analysis revealed evidence for two modes of evolution in this metapopulation—genetic drift and balancing selection. Although we cannot identify the balancing mechanism from these data, our findings present a clear view of contemporary evolution in colour morph frequency and demonstrate the importance of metapopulation-scale studies for capturing a broad range of evolutionary dynamics.     

CONVERGENT AND CORRELATED EVOLUTION OF MAJOR LIFE‐HISTORY TRAITS IN THE ANGIOSPERM GENUS LEUCADENDRON (PROTEACEAE)

Natural selection is expected to cause convergence of life histories among taxa as well as correlated evolution of different life‐history traits. Here, we quantify the extent of convergence of five key life‐history traits (adult fire survival, seed storage, degree of sexual dimorphism, pollination mode, and seed‐dispersal mode) and test hypotheses about their correlated evolution in the genus Leucadendron (Proteaceae) from the fire‐prone South African fynbos. We reconstructed a new molecular phylogeny of this highly diverse genus that involves more taxa and molecular markers than previously. This reconstruction identifies new clades that were not detected by previous molecular study and morphological classifications. Using this new phylogeny and robust methods that account for phylogenetic uncertainty, we show that the five life‐history traits studied were labile during the evolutionary history of the genus. This diversity allowed us to tackle major questions about the correlated evolution of life‐history strategies. We found that species with longer seed‐dispersal distances tended to evolve lower pollen‐dispersal distance, that insect‐pollinated species evolved decreased sexual dimorphism, and that species with a persistent soil seed‐bank evolved toward reduced fire‐survival ability of adults.     

Modelling compensatory regrowth with bud dormancy and gradual activation of buds

Many plants show compensatory regrowth after herbivory and dormant buds often have an important role in compensatory responses. Theoretical models have shown that herbivore damage may select for a bud bank, i.e., a pool of dormant buds that are protected from herbivory and that are activated after herbivore damage. Earlier models assumed that undamaged plants cannot activate their dormant buds without damage, although they apparently have sufficient resources for successful seed production through the additional shoots dormant buds could produce. However, many plants are able to gradually activate buds over an extended period of time without any cue from damage. The aim of this study was to analyze how herbivory imposes selection for gradual mobilization of the bud bank. I assume that selection pressures that affect the fraction of buds active at each time point include damage by herbivores, time left to the end of season, and the opportunity costs of dormant buds. I modelled bud dynamics with gradual activation when there is a single damage event and (i) when the seed set of a shoot is not dependent on the time it is active, or (ii) when the seed set of a shoot diminishes with later activation. In addition, I analyzed how (iii) risk of repeated herbivory affects selection for gradual activation. Under these models, gradual activation is optimal over a wide range of herbivory pressures. Selection appears to favour activation of all buds at the beginning of the season only when herbivore pressure is weak and when early shoots have a higher seed set than late shoots. Alternatively, strong herbivore pressure and late damage may select for a large bud bank throughout the growing season, without gradual activation; the bud bank is only mobilized after damage. In this case, damaged plants can overcompensate, i.e. they have a higher seed set than undamaged plants with the same bud activation pattern. Selection for overcompensation demands a stronger herbivore pressure in this current model than in earlier bud bank models. The model never predicts selection for overcompensation when there is a risk of repeated herbivory. This revised version was published online in July 2006 with corrections to the Cover Date.     

The Dynamics of Genetic Draft in Rapidly Adapting Populations

The accumulation of beneficial mutations on competing genetic backgrounds in rapidly adapting populations has a striking impact on evolutionary dynamics. This effect, known as clonal interference, causes erratic fluctuations in the frequencies of observed mutations, randomizes the fixation times of successful mutations, and leaves distinct signatures on patterns of genetic variation. Here, we show how this form of “genetic draft” affects the forward-time dynamics of site frequencies in rapidly adapting asexual populations. We calculate the probability that mutations at individual sites shift in frequency over a characteristic timescale, extending Gillespie’s original model of draft to the case where many strongly selected beneficial mutations segregate simultaneously. We then derive the sojourn time of mutant alleles, the expected fixation time of successful mutants, and the site frequency spectrum of beneficial and neutral mutations. Finally, we show how this form of draft affects inferences in the McDonald–Kreitman test and how it relates to recent observations that some aspects of genetic diversity are described by the Bolthausen–Sznitman coalescent in the limit of very rapid adaptation.     

Soil seed bank contributes significantly to genetic variation of Hypericum sinaicum in a changing environment

The contribution of soil seed bank of a desert endemic plant species in maintaining genetic diversity has been addressed in this paper through investigating the differences in genetic diversity and structure (using AFLP markers) between plants grown from soil seed bank and standing crop plants within and among five populations of H. sinaicum growing at St. Katherine Protectorate, southern Sinai, Egypt. Standard genetic diversity measures showed that the molecular variation within and among populations was highly significantly different between standing crop and soil seed bank. While soil seed bank had lower genetic diversity than standing crop populations, pooling soil seed bank with standing crop samples resulted in higher diversity. The results revealed also that soil seed bank had lower differentiation (7 %) than among populations of the standing crop (18 %). Results of neighbor-joining, Bayesian clustering and principal coordinate analysis showed that soil seed banks had a separate gene pool different from standing crop. The study came to the conclusion that the genetic variation of the soil seed bank contributes significantly to the genetic variation of the species. This also stresses the importance of elucidating the genetic diversity and structure of the soil seed bank for any sound and long-term conservation efforts for desert species. These have been growing in small-size populations for a long time that any estimates gained only from aboveground sampling of populations may be ambiguous.     

Is the population turnover of patchy‐distributed annuals determined by dormancy dynamics or dispersal processes?

In species with fragmented distribution, regional turnover dynamics is given by the processes of local population extinction and patch (re)colonization by migrants spreading from neighboring occupied patches. In plants with dormant stages (e.g. seeds) and limited dispersal capacity, regional dynamics based on dispersal processes can be overridden by pseudo-turnover determined by signals inducing or breaking dormancy (e.g. due to changes in habitat quality) resulting in a low importance of habitat configuration and size.
In this study, I investigated the turnover dynamics of 5 annual plant species growing on ant mounds of Lasius flavus over three years. I analyzed whether the grassland-scale dynamics of these annuals is influenced by dispersal processes, or alternatively, by pseudo-turnover of soil seed populations. For that purpose I 1) searched for populations formed from soil seeds only, 2) compared the relative contribution of the soil seed bank and seed rain for population restoration after disappearance from the vegetation and 3) investigated whether colonization and extinction events are affected by patch isolation. I assumed if population turnover was rather a result of the soil seed bank dynamics then spatial effects would be hard to detect.
In spite of the presence of populations formed from soil seed and the relatively more important soil seed bank for potential population reestablishment, turnover dynamics followed the predictions of metapopulation theory. Population appearance was more probable in larger and less isolated patches. Probability of disappearance increased with decrease of population size that was negatively influenced by the patch size and its isolation. These findings indicate dispersal processes to be important in the turnover dynamics and only limited contribution of soil seed populations. Their small effectiveness is probably related to the low chance of recurrent disturbance on the mound surface.