Within- and between-population variation for resistance of Daphnia magna to the bacterial endoparasite Pasteuria ramosa

Genetic variation among hosts for resistance to parasites is an important assumption underlying evolutionary theory of host and parasite evolution. Using the castrating bacterial parasite Pasteuria ramosa and its cladoceran host Daphnia magna, we examined both within- and between-population genetic variation for resistance. First, we tested hosts from four populations for genetic variation for resistance to three parasite isolates. Allozyme analysis revealed significant host population divergence and that genetic distance corresponds to geographic distance. Host and parasite fitness components showed strong genetic differences between parasite isolates for host population by parasite interactions and for clones within populations, whereas host population effects were significant for only a few traits. In a second experiment we tested explicitly for within-population differences in variation for resistance by challenging nine host clones from a single population with four different parasite spore doses. Strong clone and dose effects were evident. More susceptible clones also suffered higher costs once infected. The results indicate that within-population variation for resistance is high relative to between-population variation. We speculate that P. ramosa adapts to individual host clones rather than to its host population.     

Differentiating the effects of origin and frequency in reciprocal transplant experiments used to test negative frequency-dependent selection hypotheses

Reciprocal transplant experiments have been used to estimate the probability that negative frequency-dependent selection by natural enemies has occurred in host populations by determining whether pest populations are less adapted to “foreign” (rare) hosts, which originate from a population with which the pests have not coevolved. However, these experiments usually confound the effects of frequency and origin: the rare genotypes are also genotypes that did not originate at a site. When clonal organisms are used, and the clones occur in more than one population, it is possible to separate the effects of origin and frequency. Here I present the results of an experiment in which Arabis clones of known frequency were reciprocally transplanted among sites. Contrary to expectations, clones at their site of origin had less disease, less herbivory, and higher fitness than foreign clones. However, variation within and among sites in herbivory and infection was large, suggesting that the number of sites and clones needed to thoroughly test the hypothesis of negative frequency-dependent selection in this system is very large: thus, these results are suggestive but not conclusive. Received: 20 October 1997 / Accepted: 8 February 1998     

Models of Frequency-Dependent Selection with Mutation from Parental Alleles

Frequency-dependent selection (FDS) remains a common heuristic explanation for the maintenance of genetic variation in natural populations. The pairwise-interaction model (PIM) is a well-studied general model of frequency-dependent selection, which assumes that a genotype’s fitness is a function of within-population intergenotypic interactions. Previous theoretical work indicated that this type of model is able to sustain large numbers of alleles at a single locus when it incorporates recurrent mutation. These studies, however, have ignored the impact of the distribution of fitness effects of new mutations on the dynamics and end results of polymorphism construction. We suggest that a natural way to model mutation would be to assume mutant fitness is related to the fitness of the parental allele, i.e., the existing allele from which the mutant arose. Here we examine the numbers and distributions of fitnesses and alleles produced by construction under the PIM with mutation from parental alleles and the impacts on such measures due to different methods of generating mutant fitnesses. We find that, in comparison with previous results, generating mutants from existing alleles lowers the average number of alleles likely to be observed in a system subject to FDS, but produces polymorphisms that are highly stable and have realistic allele-frequency distributions.     

Constraints on polyploid evolution: a test of the minority cytotype exclusion principle

Polyploid evolution is often considered a mechanism of instant speciation; yet the establishment of rare tetraploids within diploid populations may be constrained by a frequency-dependent mating disadvantage (minority cytotype exclusion principle). I tested this hypothesis using experimental populations of Chamerion angustifolium (Onagraceae) that contained different proportions of tetraploids and diploids. Fitness, measured as total seed production over the entire flowering season, was calculated from a census of flower number and estimates of ovule number per flower and proportion of seed set per fruit. The fitness of tetraploids relative to diploids was frequency dependent, increasing from 0.4, when tetraploids were rare, to 0.7 when at 50% and 1.15 when they were in the majority (67%). This pattern exists because of a negative relationship between tetraploid frequency and seed set per fruit in diploids. Seed set in tetraploids was independent of cytotype frequency. The frequency-independent effect in tetraploids reflects higher assortative mating, partly because of non-random patterns of bee visitation. Bees visited a disproportionately high number of diploid inflorescences; however, the proportion of successive flights between tetraploids increased above random expectations as the frequency of tetraploids decreased. These results provide the first experimental test of frequency-dependent fitness in diploid-polyploid mixtures and suggest an important role for more gradual, population processes governing the evolution of polyploidy in natural populations.     

The nature of nurture in a wild mammal's fitness

Genetic variation in fitness is required for the adaptive evolution of any trait but natural selection is thought to erode genetic variance in fitness. This paradox has motivated the search for mechanisms that might maintain a population''s adaptive potential. Mothers make many contributions to the attributes of their developing offspring and these maternal effects can influence responses to natural selection if maternal effects are themselves heritable. Maternal genetic effects (MGEs) on fitness might, therefore, represent an underappreciated source of adaptive potential in wild populations. Here we used two decades of data from a pedigreed wild population of North American red squirrels to show that MGEs on offspring fitness increased the population''s evolvability by over two orders of magnitude relative to expectations from direct genetic effects alone. MGEs are predicted to maintain more variation than direct genetic effects in the face of selection, but we also found evidence of maternal effect trade-offs. Mothers that raised high-fitness offspring in one environment raised low-fitness offspring in another environment. Such a fitness trade-off is expected to maintain maternal genetic variation in fitness, which provided additional capacity for adaptive evolution beyond that provided by direct genetic effects on fitness.     

Beneficial mutation selection balance and the effect of linkage on positive selection

When beneficial mutations are rare, they accumulate by a series of selective sweeps. But when they are common, many beneficial mutations will occur before any can fix, so there will be many different mutant lineages in the population concurrently. In an asexual population, these different mutant lineages interfere and not all can fix simultaneously. In addition, further beneficial mutations can accumulate in mutant lineages while these are still a minority of the population. In this article, we analyze the dynamics of such multiple mutations and the interplay between multiple mutations and interference between clones. These result in substantial variation in fitness accumulating within a single asexual population. The amount of variation is determined by a balance between selection, which destroys variation, and beneficial mutations, which create more. The behavior depends in a subtle way on the population parameters: the population size, the beneficial mutation rate, and the distribution of the fitness increments of the potential beneficial mutations. The mutation-selection balance leads to a continually evolving population with a steady-state fitness variation. This variation increases logarithmically with both population size and mutation rate and sets the rate at which the population accumulates beneficial mutations, which thus also grows only logarithmically with population size and mutation rate. These results imply that mutator phenotypes are less effective in larger asexual populations. They also have consequences for the advantages (or disadvantages) of sex via the Fisher-Muller effect; these are discussed briefly.     

Frequency-dependent pollinator discrimination acts against female plants in the gynodioecious Geranium maculatum

MethodsTo test the severity and consequences of this type of pollinator discrimination in Geranium maculatum, experimental populations with the range of sex ratios observed in nature were created, ranging from 13 % to 42 % females. Pollinators were observed in order to measure the strength of discrimination, and pollen deposition and seed production of both sexes were measured to determine the fitness consequences of this discrimination. Additionally a comparison was made across the sex ratios to determine whether discrimination was frequency-dependent.ConclusionsThe results suggest that pollinator discrimination negatively affects females'' relative fitness when they are rare. Thus, the initial spread of females in a population, the first step in the evolution of gynodioecy, may be made more difficult due to pollinator discrimination.     

MUTATIONAL MELTDOWN IN LABORATORY YEAST POPULATIONS

Abstract.— In small or repeatedly bottlenecked populations, mutations are expected to accumulate by genetic drift, causing fitness declines. In mutational meltdown models, such fitness declines further reduce population size, thus accelerating additional mutation accumulation and leading to extinction. Because the rate of mutation accumulation is determined partly by the mutation rate, the risk and rate of meltdown are predicted to increase with increasing mutation rate. We established 12 replicate populations of Saccharomyces cerevisiae from each of two isogenic strains whose genomewide mutation rates differ by approximately two orders of magnitude. Each population was transferred daily by a fixed dilution that resulted in an effective population size near 250. Fitness declines that reduce growth rates were expected to reduce the numbers of cells transferred after dilution, thus reducing population size and leading to mutational meltdown. Through 175 daily transfers and approximately 2900 generations, two extinctions occurred, both in populations with elevated mutation rates. For one of these populations there is direct evidence that extinction resulted from mutational meltdown: Extinction immediately followed a major fitness decline, and it recurred consistently in replicate populations reestablished from a sample frozen after this fitness decline, but not in populations founded from a predecline sample. Wild‐type populations showed no trend to decrease in size and, on average, they increased in fitness.     

THE GENETIC STRUCTURE OF HOST PLANT ADAPTATION IN A SPATIAL PATCHWORK: DEMOGRAPHIC VARIABILITY AMONG RECIPROCALLY TRANSPLANTED PEA APHID CLONES

Populations of insect herbivores that feed on several host plant species may experience different selective forces on each host. When the hosts cooccur in a local area, herbivore populations can provide useful models for the study of evolutionary mechanisms in patchy environments. A first step in such a study involves determination of the genetic structure of host adaptation in the region: how is genetic variation for host use structured within and between subpopulations of herbivores on each host? The structure of genetic variation for host use reveals patterns of local adaptation, probable selective consequences of migration between hosts, and the potential for further evolution. To estimate the population structure of host adaptation in a patchwork, 7–11 pea aphid clones were collected at the beginning of the summer from each of two alfalfa and two red clover fields within a very localized area (about 15–20 km²). Using a reciprocal transplant in the field, replicates of these 35 clones were allowed to develop individually on each of the two crops. A complete life table was made for each replicate. Individual fitness was calculated from the life tables as the expected rate of population increase; longevity, age at first reproduction, and total fecundity were also measured for each clonal replicate. Currently, experimental estimates of genetic variation in complete life tables are virtually nonexistent for natural populations, even for single environments (Charlesworth, 1987); field studies are even less common. Because clones from each of two source crops were tested reciprocally on both hosts, variation in relative genotypic fitness on alfalfa and clover could be partitioned among clones within source crops, between fields of the same crop, and between source crops (alfalfa or red clover), providing a view of population structure. Significant clonal variation in relative performance on alfalfa and red clover was found: clones tended to have higher fitness on the crop from which they had been collected (the “home” crop) than they did on the “away” crop, suggesting local adaptation in response to patchy patterns of selection. Clonal variability within collections from the two crops suggests the potential for changes in the genetic constitution of these aphid populations within established fields as a result of clonal selection during the summer season. Significantly negative genetic correlations across crops were found for fitness and its major components. The possibility that these negative cross-environment correlations could act as evolutionary constraints on adaptation to the patchwork is considered.     

Constraints on adaptation of Escherichia coli to mixed‐resource environments increase over time

Can a population evolved in two resources reach the same fitness in both as specialist populations evolved in each of the individual resources? This question is central to theories of ecological specialization, the maintenance of genetic variation, and sympatric speciation, yet relatively few experiments have examined costs of generalism over long‐term adaptation. We tested whether selection in environments containing two resources limits a population's ability to adapt to the individual resources by comparing the fitness of replicate Escherichia coli populations evolved for 6000 generations in the presence of glucose or lactose alone (specialists), or in varying presentations of glucose and lactose together (generalists). We found that all populations had significant fitness increases in both resources, though the magnitude and rate of these increases differed. For the first 4000 generations, most generalist populations increased in fitness as quickly in the individual resources as the corresponding specialist populations. From 5000 generations, however, a widespread cost of adaptation affected all generalists, indicating a growing constraint on their abilities to adapt to two resources simultaneously. Our results indicate that costs of generalism are prevalent, but may influence evolutionary trajectories only after a period of cost‐free adaptation.     

Temperature adaptation in a geographically widespread zooplankter,Daphnia magna

Evidence for temperature adaptation in Daphnia magna was inferred from variation in the shape of temperature reaction norms for somatic growth rate, a fitness‐related trait. Ex‐ephippial clones from eight populations across Europe were grown under standardized conditions after preacclimation at five temperatures (17–29 °C). Significant variation for grand mean growth rates occurred both within populations (among clones) and between populations. Genetic variation for reaction norm shape was found within populations, with temperature‐dependent trade‐offs in clone relative fitness. However, the population average responses to temperature were similar, following approximately parallel reaction norms. The among‐population variation is not evidence for temperature adaptation. Lack of temperature adaptation at the population level may be a feature of intermittent populations where environmentally terminated diapause can entrain the planktonic stage of the life‐history within a similar range of temperatures.     

Mate‐choice copying: A fitness‐enhancing behavior that evolves by indirect selection

A spatially explicit, individual‐based simulation model is used to study the spread of an allele for mate‐choice copying (MCC) through horizontal cultural transmission when female innate preferences do or do not coevolve with a male viability‐increasing trait. Evolution of MCC is unlikely when innate female preferences coevolve with the trait, as copier females cannot express a higher preference than noncopier females for high‐fitness males. However, if a genetic polymorphism for innate preference persists in the population, MCC can evolve by indirect selection through hitchhiking: the copying allele hitchhikes on the male trait. MCC can be an adaptive behavior—that is, a behavior that increases a population's average fitness relative to populations without MCC—even though the copying allele itself may be neutral or mildly deleterious.     

The association between mitochondrial genetic variation and reduced colony fitness in an invasive wasp

Despite the mitochondrion's long‐recognized role in energy production, mitochondrial DNA (mtDNA) variation commonly found in natural populations was assumed to be effectively neutral. However, variation in mtDNA has now been increasingly linked to phenotypic variation in life history traits and fitness. We examined whether the relative fitness in native and invasive common wasp (Vespula vulgaris) populations in Belgium and New Zealand (NZ), respectively, can be linked to mtDNA variation. Social wasp colonies in NZ were smaller with comparatively fewer queen cells, indicating a reduced relative fitness in the invaded range. Interestingly, queen cells in this population were significantly larger leading to larger queen offspring. By sequencing 1,872 bp of the mitochondrial genome, we determined mitochondrial haplotypes and detected reduced genetic diversity in NZ. Three common haplotypes in NZ frequently produced many queens, whereas the four rare haplotypes produced significantly fewer or no queens. The entire mitochondrial genome for each of these haplotypes was sequenced to identify polymorphisms associated with fitness reduction. We found 16 variable sites; however, no nonsynonymous mutation that was clearly causing impaired mitochondrial function was detected. We discuss how detected variants may alter secondary structures, gene expression or mito‐nuclear interactions, or could be associated with nuclear‐encoded variation. Whatever the ultimate mechanism, we show reduced fitness and mtDNA variation in an invasive wasp population as well as specific mtDNA variants associated with fitness variation within this population. Ours is one of only a few studies that confirm fitness impacts of mtDNA variation in wild nonmodel populations.     

Long-Term Experimental Evolution in Escherichia Coli. VI. Environmental Constraints on Adaptation and Divergence

The effect of environment on adaptation and divergence was examined in two sets of populations of Escherichia coli selected for 1000 generations in either maltose- or glucose-limited media. Twelve replicate populations selected in maltose-limited medium improved in fitness in the selected environment, by an average of 22.5%. Statistically significant among-population genetic variation for fitness was observed during the course of the propagation, but this variation was small relative to the fitness improvement. Mean fitness in a novel nutrient environment, glucose-limited medium, improved to the same extent as in the selected environment, with no statistically significant among-population genetic variation. In contrast, 12 replicate populations previously selected for 1000 generations in glucose-limited medium showed no improvement, as a group, in fitness in maltose-limited medium and substantial genetic variation. This asymmetric pattern of correlated responses suggests that small changes in the environment can have profound effects on adaptation and divergence.     

FLAT REACTION NORMS AND “FROZEN” PHENOTYPIC VARIATION IN CLONAL SNAILS (POTAMOPYRGUS ANTIPODARUM)

The Frozen Niche-Variation hypothesis (FNV) suggests that clones randomly sample and “freeze” the genotypes of their ancestral sexual populations. Hence, each clone expresses only a fraction of the total niche-use variation observed in the sexual population, which may lead to selection for ecological specialization and coexistence of clones. A generalized form of the FNV model suggests that the same is true for life-history (as well as other) traits that have important fitness consequences, but do not relate directly to niche use. We refer to the general form of the model as the Frozen Phenotypic Variation (FPV) model. A mixed population of sexual and parthenogenetic snails (Potamopyrgus antipodarum) in a New Zealand lake allowed us to examine the phenotypic variation expressed by coexisting clones in two benthic habitats, and to compare that variation to the sexual population. Three clones were found primarily in an aquatic macrophyte zone composed of Isoetes kirkii (1.5–3.0 m deep), and three additional clones were found in a deeper macrophyte zone composed of Elodea canadensis (4.0–6.0 m deep). These clones showed significant variation between habitats, which mirrored that observed in the sexual population. Specifically, clones and sexuals from the deeper habitat matured at a larger size and had larger broods. There was also significant among-clone variation within habitats; and as expected under the FPV model, the within-clone coefficients of variation for size at maturity were low in both habitats when compared to the sexual population. In addition, we found four clones that were common in both macrophyte zones. The reaction norms of these clones were flat across habitats, suggesting little phenotypic plasticity for morphology or life-history traits. Flat reaction norms, high among-clone variation, and low coefficients of variation (relative to the sexual population) are in accordance with the FPV model for the origin of clonal lineages. We also measured the prevalence of infection by trematode larvae to determine whether clones are inherently more or less infectable, or whether they are freezing phenotypic variation for resistance from the sexual population. We did this in the deep habitats of the lake where recycling of the parasite by the vertebrate host is unlikely, thereby reducing the complications raised by frequency-dependent responses of parasites to host genotypes. We found no indication that clones are either more or less infectable than the resident sexual population. Taken together, our results suggest that phenotypic variation for both life-history traits and resistance to parasites is frozen by clones from the local sexual population.     

Speedy speciation in a bacterial microcosm: new species can arise as frequently as adaptations within a species

Microbiologists are challenged to explain the origins of enormous numbers of bacterial species worldwide. Contributing to this extreme diversity may be a simpler process of speciation in bacteria than in animals and plants, requiring neither sexual nor geographical isolation between nascent species. Here, we propose and test a novel hypothesis for the extreme diversity of bacterial species—that splitting of one population into multiple ecologically distinct populations (cladogenesis) may be as frequent as adaptive improvements within a single population''s lineage (anagenesis). We employed a set of experimental microcosms to address the relative rates of adaptive cladogenesis and anagenesis among the descendants of a Bacillus subtilis clone, in the absence of competing species. Analysis of the evolutionary trajectories of genetic markers indicated that in at least 7 of 10 replicate microcosm communities, the original population founded one or more new, ecologically distinct populations (ecotypes) before a single anagenetic event occurred within the original population. We were able to support this inference by identifying putative ecotypes formed in these communities through differences in genetic marker association, colony morphology and microhabitat association; we then confirmed the ecological distinctness of these putative ecotypes in competition experiments. Adaptive mutations leading to new ecotypes appeared to be about as common as those improving fitness within an existing ecotype. These results suggest near parity of anagenesis and cladogenesis rates in natural populations that are depauperate of bacterial diversity.     

Intraclonal variation in RNA viruses: generation, maintenance and consequences

This paper explores the evolutionary implications of the enormous variability that characterizes populations of RNA viruses and retroviruses. It begins by examining the magnitude of genetic variation in both natural and experimental populations. In natural populations, differences arise even within individual infected patients, with the per-site nucleotide diversity at this level ranging from < 1% to 6%. In laboratory populations, two viruses sampled from the same clone differed by ∼0.7% in their fitness. Three different mechanisms that may be important in maintaining viral genetic variability were tested: (1) Fisher's fundamental theorem, to compare the observed rate of fitness change with the extent of fitness-related variation within the same experimental populations; (2) magnitude of genomic mutation rate, to assess whether it correlated with fitness-related variation, as predicted by the mutation-selection balance hypothesis; (3) frequency-dependent selection, which affords rare genotypes an advantage. The paper concludes with a discussion of two evolutionary consequences of variability: the fixation of deleterious mutations by drift in small populations and the role of clonal interference in large ones.  © 2003 The Linnean Society of London. Biological Journal of the Linnean Society , 2003, 79 , 17–26.     

(S)he who dares, grows! A cross‐population study of growth and behaviour in three‐spined sticklebacks

Three‐spined sticklebacks ( Gasterosteus aculeatus ) exhibit considerable inter‐population variation in behaviour, morphology and life history characteristics. Such population‐level variation can be generated directly by environmental characteristics of the water body they inhabit ( e.g . temperature regimes, which directly influence growth rates) but local genetic adaptation is also important. By performing 'common garden' experiments, in which laboratory‐bred individuals from separate populations are raised under standardized controlled laboratory conditions, it is possible to identify genetically‐based population‐level phenotype variation. Here we present the results of two studies, carried out using juvenile three‐spined sticklebacks bred from parental stock from five geographically isolated UK populations and reared under standard laboratory ('common garden') conditions. Firstly we report the results of a study examining population‐level variation in patterns of early growth, in which we tracked the growth of replicate groups of full‐sibs from all five populations, from hatching to 126d. Secondly we report the results of an experimental behavioural study, designed to examine population‐level variation in the exploratory or 'boldness' behaviour of laboratory‐bred and reared juvenile three‐spined sticklebacks from the same five populations. We discuss how adaptive genetically based patterns of behaviour and growth may co‐vary across populations.     

Subclonal components of consensus fitness in an RNA virus clone.

Most RNA virus populations exhibit extremely high mutation frequencies which generate complex, genetically heterogeneous populations referred to as quasi-species. Previous work has shown that when a large spectrum of the quasi-species is transferred, natural selection operates, leading to elimination of noncompetitive (inferior) genomes and rapid gains in fitness. However, whenever the population is repeatedly reduced to a single virion, variable declines in fitness occur as predicted by the Muller's ratchet hypothesis. Here, we quantitated the fitness of 98 subclones isolated from an RNA virus clonal population. We found a normal distribution around a lower fitness, with the average subclone being less fit than the parental clonal population. This finding demonstrates the phenotypic diversity in RNA virus populations and shows that, as expected, a large fraction of mutations generated during virus replication is deleterious. This clarifies the operation of Muller's ratchet and illustrates why a large number of virions must be transferred for rapid fitness gains to occur. We also found that repeated genetic bottleneck passages can cause irregular stochastic declines in fitness, emphasizing again the phenotypic heterogeneity present in RNA virus populations. Finally, we found that following only 60 h of selection (15 passages in which virus yields were harvested after 4 h), RNA virus populations can undergo a 250% average increase in fitness, even on a host cell type to which they were already well adapted. This is a remarkable ability; in population biology, even a much lower fitness gain (e.g., 1 to 2%) can represent a highly significant reproductive advantage. We discuss the biological implications of these findings for the natural transmission and pathogenesis of RNA viruses.     

PATTERNS OF RUST INFECTION AS A FUNCTION OF HOST GENETIC DIVERSITY AND HOST DENSITY IN NATURAL POPULATIONS OF THE APOMICTIC CRUCIFER,ARABIS HOLBOELLII

It is often assumed that genetic diversity contributes to reduced disease incidence in natural plant populations. However, little is known about the genetic structure of natural populations affected by disease. Here I present data from three apomictic (asexual) populations of Arabis holboellii infected by the rusts Puccinia monoica and P. thlaspeos. An average of 300 host individuals per population were genotyped (using seven variable allozyme loci) and scored for disease presence. Arabis holboellii populations are genetically diverse; the number of clones detected per population ranged from 6 to 27. There was substantial variation in frequency of host clones within and among sites, and significant variation among clones in susceptibility to the different rusts. Contrary to predictions based on frequency-dependent selection theory there was not a consistent positive relationship between clone frequency and disease incidence within any of the populations (Spearman's r = -0.096, P > 0.5). In addition, clonally diverse populations did not necessarily have decreased disease incidence. The population with the lowest overall (both pathogens combined) disease incidence (7.5 ± 1.9%) had the smallest number of clones (6), the lowest spatial variability, and the highest Arabis density. By comparison, another population had 22 clones, high spatial variability, low Arabis density and significantly more disease overall (16.8 ± 2.7%). Although this study does not eliminate the possibility of frequency-dependent pathogen attack in these populations, the results suggest that it is likely to be weak or intermittent.