Measurement of concurrent selection episodes

Current methods for measuring selection with longitudinal data have been developed with the assumption that episodes of selection are sequential. However, a number of empirical examinations have demonstrated that natural and sexual selection may act concurrently and in opposing directions. Other recent work has highlighted the difficulty of assigning fitness values for survival when reproduction and mortality within a population temporally overlap. I treat these as facets of a single problem; how to analyze selection where mortality and reproduction are concurrent. To address this problem, I formalize a method to estimate total fitness of individuals over a period of time utilizing longitudinal data. I then show how the fitness may be partitioned to provide two separate estimates of fitness for reproductive opportunity and reproductive success. In addition, another total fitness estimate for the period can be obtained from the two partitioned estimates. This procedure will allow calculation of total fitness where there are some missing datapoints for reproductive success of an individual. A simulation indicates that bias is generally low for the various fitness estimates. These methods should expand our ability to understand the interaction of different selection episodes.     

The population genetics of adaptation: the adaptation of DNA sequences

I describe several patterns characterizing the genetics of adaptation at the DNA level. Following Gillespie (1983, 1984, 1991), I consider a population presently fixed for the ith best allele at a locus and study the sequential substitution of favorable mutations that results in fixation of the fittest DNA sequence locally available. Given a wild type sequence that is less than optimal, I derive the fitness rank of the next allele typically fixed by natural selection as well as the mean and variance of the jump in fitness that results when natural selection drives a substitution. Looking over the whole series of substitutions required to reach the best allele, I show that the mean fitness jumps occurring throughout an adaptive walk are constrained to a twofold window of values, assuming only that adaptation begins from a reasonably fit allele. I also show that the first substitution and the substitution of largest effect account for a large share of the total fitness increase during adaptation. I further show that the distribution of selection coefficients fixed throughout such an adaptive walk is exponential (ignoring mutations of small effect), a finding reminiscent of that seen in Fisher's geometric model of adaptation. Last, I show that adaptation by natural selection behaves in several respects as the average of two idealized forms of adaptation, perfect and random.     

Fitness declines towards range limits and local adaptation to climate affect dispersal evolution during climate‐induced range shifts

Dispersal ability will largely determine whether species track their climatic niches during climate change, a process especially important for populations at contracting (low‐latitude/low‐elevation) range limits that otherwise risk extinction. We investigate whether dispersal evolution at contracting range limits is facilitated by two processes that potentially enable edge populations to experience and adjust to the effects of climate deterioration before they cause extinction: (i) climate‐induced fitness declines towards range limits and (ii) local adaptation to a shifting climate gradient. We simulate a species distributed continuously along a temperature gradient using a spatially explicit, individual‐based model. We compare range‐wide dispersal evolution during climate stability vs. directional climate change, with uniform fitness vs. fitness that declines towards range limits (RLs), and for a single climate genotype vs. multiple genotypes locally adapted to temperature. During climate stability, dispersal decreased towards RLs when fitness was uniform, but increased when fitness declined towards RLs, due to highly dispersive genotypes maintaining sink populations at RLs, increased kin selection in smaller populations, and an emergent fitness asymmetry that favoured dispersal in low‐quality habitat. However, this initial dispersal advantage at low‐fitness RLs did not facilitate climate tracking, as it was outweighed by an increased probability of extinction. Locally adapted genotypes benefited from staying close to their climate optima; this selected against dispersal under stable climates but for increased dispersal throughout shifting ranges, compared to cases without local adaptation. Dispersal increased at expanding RLs in most scenarios, but only increased at the range centre and contracting RLs given local adaptation to climate.     

Fisher’s fundamental theorem of inclusive fitness and the change in fitness due to natural selection when conspecifics interact

Competition and cooperation is fundamental to evolution by natural selection, both in animals and plants. Here, I investigate the consequences of such interactions for response in fitness due to natural selection. I provide quantitative genetic expressions for heritable variance and response in fitness due to natural selection when conspecifics interact. Results show that interactions among conspecifics generate extra heritable variance in fitness, and that interacting with kin is the key to evolutionary success because it translates the extra heritable variance into response in fitness. This work also unifies Fisher’s fundamental theorem of natural selection (FTNS) and Hamilton’s inclusive fitness (IF). The FTNS implies that natural selection maximizes fitness, whereas Hamilton proposed maximization of IF. This work shows that the FTNS describes the increase in IF, rather than direct fitness, at a rate equal to the additive genetic variance in fitness. Thus, Hamilton’s IF and Fisher’s FTNS both describe the maximization of IF.     

Fitness valleys constrain HIV‐1's adaptation to its secondary chemokine coreceptor

Fitness valleys, in which mutations at different loci are singly deleterious but jointly beneficial, arise because of reciprocal sign epistasis. Recent theoretical work provides analytical approximations of times to cross fitness valleys via three mechanisms: sequential fixation, stochastic tunnelling and recombination. These times depend critically on the effective population size (N_e). Human immunodeficiency virus type 1 (HIV‐1) encounters fitness valleys in adapting to its secondary cell‐surface chemokine coreceptor, CXCR4. Adaptation to CXCR4 tends to occur late in infection and only in about 50% of patients and is associated with disease progression. It has been hypothesized that the need to cross fitness valleys may explain the delayed and inconsistent adaptation to CXCR4. We have identified four fitness valleys from a previous study of fitness epistasis in adaptation to CXCR4 and use estimates of the within‐patient variance N_e for different patient treatment statuses and infection stages (conditions) to estimate times to cross the valleys. These valleys may be crossed predominantly by stochastic tunnelling, although mean crossing times are consistently longer than the durations of the conditions for which they are calculated. These results were confirmed with stochastic simulation. Simulations show that crossing times for a given condition are highly variable and that for each condition there is a low probability of crossing each valley. These findings support the hypothesis that fitness valleys constrain the adaptation of HIV‐1 to CXCR4. This study provides the first detailed analysis of the evolutionary dynamics associated with empirical fitness valleys.     

Eco-evolutionary vs. habitat contributions to invasion in salmon: experimental evaluation in the wild

Although trait evolution over contemporary timescales is well documented, its influence on ecological dynamics in the wild has received much less attention particularly compared to traditional ecological and environmental factors. For example, evolution over ecologically relevant timescales is expected in populations that colonize new habitats, where it should theoretically enhance fitness, associated vital rates of survival and reproduction, and population growth potential. Nonetheless, success of exotic species is much more commonly attributed to ecological aspects of habitat quality and 'escape from enemies' in the invaded range. Here, we consider contemporary evolution of vital rates in introduced Chinook salmon (Oncorhynchus tshawytscha) that quickly colonized New Zealand and diverged over c. 26 generations. By using experimental translocations, we partitioned the roles of evolution and habitat quality in modifying geographical patterns of vital rates. Variation in habitat quality within the new range had the greatest influence on broad geographical patterns of vital rates, but locally adapted salmon still exhibited more than double the vital rate performance, and hence fitness, of nonlocal counterparts. The scope of this fitness evolution far exceeds the scale of divergence in trait values for these populations, or even the expected fitness effects of particular traits. These results suggest that contemporary evolution can be an important part of the eco-evolutionary dynamics of invasions and highlight the need for studies of the emergent fitness and ecological consequences of such evolution, rather than just changes in trait values.     

The short‐ and long‐term fitness consequences of natal dispersal in a wild bird population

Dispersal is a key process in population and evolutionary ecology. Individual decisions are affected by fitness consequences of dispersal, but these are difficult to measure in wild populations. A long‐term dataset on a geographically closed bird population, the Mauritius kestrel, offers a rare opportunity to explore fitness consequences. Females dispersed further when the availability of local breeding sites was limited, whereas male dispersal correlated with phenotypic traits. Female but not male fitness was lower when they dispersed longer distances compared to settling close to home. These results suggest a cost of dispersal in females. We found evidence of both short‐ and long‐term fitness consequences of natal dispersal in females, including reduced fecundity in early life and more rapid aging in later life. Taken together, our results indicate that dispersal in early life might shape life history strategies in wild populations.     

Measuring microbial fitness in a field reciprocal transplant experiment

Microbial fitness is easy to measure in the laboratory, but difficult to measure in the field. Laboratory fitness assays make use of controlled conditions and genetically modified organisms, neither of which are available in the field. Among other applications, fitness assays can help researchers detect adaptation to different habitats or locations. We designed a competitive fitness assay to detect adaptation of Saccharomyces paradoxus isolates to the habitat they were isolated from (oak or larch leaf litter). The assay accurately measures relative fitness by tracking genotype frequency changes in the field using digital droplet PCR (DDPCR). We expected locally adapted S. paradoxus strains to increase in frequency over time when growing on the leaf litter type from which they were isolated. The DDPCR assay successfully detected fitness differences among S. paradoxus strains, but did not find a tendency for strains to be adapted to the habitat they were isolated from. Instead, we found that the natural alleles of the hexose transport gene we used to distinguish S. paradoxus strains had significant effects on fitness. The origin of a strain also affected its fitness: strains isolated from oak litter were generally fitter than strains from larch litter. Our results suggest that dispersal limitation and genetic drift shape S. paradoxus populations in the forest more than local selection does, although further research is needed to confirm this. Tracking genotype frequency changes using DDPCR is a practical and accurate microbial fitness assay for natural environments.     

LONG-TERM EXPERIMENTAL EVOLUTION IN ESCHERICHIA COLI. VII. MECHANISMS MAINTAINING GENETIC VARIABILITY WITHIN POPULATIONS

Six replicate populations of the bacterium Escherichia coli were propagated for more than 10,000 generations in a defined environment. We sought to quantify the variation among clones within these populations with respect to their relative fitness, and to evaluate the roles of three distinct population genetic processes in maintaining this variation. On average, a pair of clones from the same population differed from one another in their relative fitness by approximately 4%. This within-population variation was small compared with the average fitness gain relative to the common ancestor, but it was statistically significant. According to one hypothesis, the variation in fitness is transient and reflects the ongoing substitution of beneficial alleles. We used Fisher's fundamental theorem to compare the observed rate of each population's change in mean fitness with the extent of variation for fitness within that population, but we failed to discern any correspondence between these quantities. A second hypothesis supposes that the variation in fitness is maintained by recurrent deleterious mutations that give rise to a mutation-selection balance. To test this hypothesis, we made use of the fact that two of the six replicate populations had evolved mutator phenotypes, which gave them a genomic mutation rate approximately 100-fold higher than that of the other populations. There was a marginally significant correlation between a population's mutation rate and the extent of its within-population variance for fitness, but this correlation was driven by only one population (whereas two of the populations had elevated mutation rates). Under a third hypothesis, this variation is maintained by frequency-dependent selection, whereby genotypes have an advantage when they are rare relative to when they are common. In all six populations, clones were more fit, on average, when they were rare than when they were common, although the magnitude of the advantage when rare was usually small (~1% in five populations and ~5% in the other). These three hypotheses are not mutually exclusive, but frequency-dependent selection appears to be the primary force maintaining the fitness variation within these experimental populations.     

Fitness cost from fluctuating ultraviolet radiation in Daphnia magna

Solar ultraviolet radiation (UVR) is an important environmental threat for organisms in aquatic systems, but its temporally variable nature makes the understanding of its effects ambiguous. The aim of our study was to assess potential fitness costs associated with fluctuating UVR in the aquatic zooplankter Daphnia magna. We investigated individual survival, reproduction and behaviour when exposed to different UVR treatments. Individuals exposed to fluctuating UVR, resembling natural variations in cloud cover, had the lowest fitness (measured as the number of offspring produced during their lifespan). By contrast, individuals exposed to the same, but constant UVR dose had similar fitness to control individuals (not exposed to UVR), but they showed a significant reduction in daily movement. The re-occurring threat response to the fluctuating UVR treatment thus had strong fitness costs for D. magna, and we found no evidence for plastic behavioural responses when continually being exposed to UVR, despite the regular, predictable exposure schedule. In a broader context, our results imply that depending on how variable a stressor is in nature, populations may respond with alternative strategies, a framework that could promote rapid population differentiation and local adaptation.     

Physiological consequences of immune response by Drosophila melanogaster (Diptera: Drosophilidae) against the parasitoid Asobara tabida (Hymenoptera: Braconidae)

Abstract Parasites can exert a wide range of negative effects on their hosts. Consequently, hosts that can resist infection should have a selective advantage over nonresistant conspecifics. Yet, host populations remain susceptible to some parasites. Could genetic heterogeneity in the host's ability to resist parasites reflect costs of mounting an immune response? Previous work on Drosophila melanogaster establishes that maintaining the ability to mount an immune response decreases larval competitive ability. Moreover, mounting an immune response decreases fitness. I report on the impact of mounting an immune response on fitness of D. melanogaster survived parasitism by Asobara tabida. I used isofemale lines to determine whether genotype influences the costs of immune response. I examined fitness consequences both to larvae and adults. Survivors of parasitism show no measurable decrease in larval fitness (development time) but have decreased adult fitness (population growth rates), probably because of their smaller size.     

Many Possible Worlds: Expanding the Ecological Scenarios in Experimental Evolution

Experimental microbial evolution has focused on the particular ecological scenario where a population is placed suddenly in an environment where its fitness is low, and then adapts while the environment remains stable. In line with this, most microbial evolution studies use fitness measures that report how evolved genotypes fare when competed directly against their own distant ancestor while other studies compare life history traits (such as growth rates) of ancestral and evolved genotypes. This standard way of measuring and reporting changes in fitness has resulted in a consistent body of literature that explains adaptation when populations evolve in this “standard ecological scenario.” Here, I suggest that for experimental evolution to investigate adaptation in other ecological scenarios, such as fluctuating or persistently changing environments, measures of fitness must be expanded such that they not only continue to be comparable between experiments, but also account for evolution and demographic effects in all environments that an evolving lineage experiences. I examine two non-standard measures of fitness—fitness flux and the total number of reproductive events—as potential ways to quantify adaptation by integrating historical information about selection over many environments. This approach could allow us to make quantitative and biologically-meaningful comparisons of adaptation across diverse ecological scenarios. I use the case study of understanding how phytoplankton communities may respond to global change, where environmental variables change continuously, to explore concrete ways of using non-standard fitness measures that consider both demographic effects and selection in changing, rather than in changed, environments.     

Parental and developmental temperature effects on the thermal dependence of fitness in Drosophila melanogaster

Cross-generational effects refer to nongenetic influences of the parental phenotype or environment on offspring phenotypes. Such effects are commonly observed, but their adaptive significance is largely unresolved. We examined cross-generational effects of parental temperature on offspring fitness (estimated via a serial-transfer assay) at different temperatures in a laboratory population of Drosophila melanogaster. Parents were reared at 18 degrees C, 25 degrees C, or 29 degrees C (Tpar) and then their offspring were reared at 18 degrees C, 25 degrees C, or 29 degrees C (Toff) to evaluate several competing hypotheses (including an adaptive one) involving interaction effects of parental and offspring temperature on offspring fitness. The results clearly show that hotter parents are better; in other words, the higher the temperature of the parents, the higher the fitness of their offspring, independent of offspring thermal environment. These data contradict the adaptive cross-generational hypothesis, which proposes that offspring fitness is maximal when the offspring thermal regime matches the parental one. Flies with hot parents have high fitness seemingly because their own offspring develop relatively quickly, not because they have higher fecundity early in life.     

Testing for local adaptation in Avena barbata: a classic example of ecotypic divergence

Forty years ago, Robert Allard and colleagues documented that the slender wild oat, Avena barbata , occurred in California as two multi-locus allozyme genotypes, associated with mesic and xeric habitats. This is arguably the first example of ecotypes identified by molecular techniques. Despite widespread citation, however, the inference of local adaptation of these ecotypes rested primarily on the allozyme pattern. This study tests for local adaptation of these ecotypes using reciprocal transplant and quantitative trait locus (QTL) mapping techniques. Both ecotypes and 188 recombinant inbred lines (RILs) derived from a cross between them were grown in common garden plots established at two sites representative of the environments in which the ecotypes were first described. Across four growing seasons at each site, three observations consistently emerged. First, despite significant genotype by environment interaction, the mesic ecotype consistently showed higher lifetime reproductive success across all years and sites. Second, the RILs showed no evidence of a trade-off in performance across sites or years, and fitness was positively correlated across environments. Third, at QTL affecting lifetime reproductive success, selection favoured the same allele in all environments. None of these observations are consistent with local adaptation but suggest that a single genotype is selectively favoured at both moist and dry sites. I propose an alternative hypothesis that A. barbata may be an example of contemporary evolution – whereby the favoured genotype is spreading and increasing in frequency – rather than local adaptation.     

Inference of parasite local adaptation using two different fitness components

Estimating parasite fitness is central to studies aiming to understand parasite evolution. Theoretical models generally use the basic reproductive rate R(0) to express fitness, yet it is very difficult to quantify R(0) empirically and experimental studies often use fitness components such as infection intensity or infectivity as substitutes. These surrogate measures may be biased in several ways. We assessed local adaptation of the microsporidium Ordospora colligata to its host, the crustacean Daphnia magna using two different parasite fitness components: infection persistence over several host generations in experimental populations and infection intensity in individual hosts. We argue that infection persistence is a close estimator of R(0), whereas infection intensity measures only a component of it. Both measures show a pattern that is consistent with parasite local adaptation and they correlate positively. However, several inconsistencies between them suggest that infection intensity may at times provide an inadequate estimate of parasite fitness.     

MULTIDIMENSIONAL ADAPTIVE EVOLUTION OF A FEED‐FORWARD NETWORK AND THE ILLUSION OF COMPENSATION

When multiple substitutions affect a trait in opposing ways, they are often assumed to be compensatory, not only with respect to the trait, but also with respect to fitness. This type of compensatory evolution has been suggested to underlie the evolution of protein structures and interactions, RNA secondary structures, and gene regulatory modules and networks. The possibility for compensatory evolution results from epistasis. Yet if epistasis is widespread, then it is also possible that the opposing substitutions are individually adaptive. I term this possibility an adaptive reversal. Although possible for arbitrary phenotype‐fitness mappings, it has not yet been investigated whether such epistasis is prevalent in a biologically realistic setting. I investigate a particular regulatory circuit, the type I coherent feed‐forward loop, which is ubiquitous in natural systems and is accurately described by a simple mathematical model. I show that such reversals are common during adaptive evolution, can result solely from the topology of the fitness landscape, and can occur even when adaptation follows a modest environmental change and the network was well adapted to the original environment. The possibility of adaptive reversals warrants a systems perspective when interpreting substitution patterns in gene regulatory networks.     

MODELING THE GENETIC BASIS OF HETEROSIS: TESTS OF ALTERNATIVE HYPOTHESES

Houle (1994) showed that marker-associated heterosis due to general inbreeding depression could not be distinguished from direct overdominance at the marker locus by examining mean genotypic fitnesses, in the one-locus case. Indeed, both hypotheses equally fit the same regression model, referred to as the “adaptive distance model” (Smouse 1986). I here extend the analysis to several loci and to the relationship between marker genotype and variance in fitness. Several predictions differ between the overdominance and inbreeding hypotheses: (1) all locus-specific effects are equal under inbreeding, whereas they are not under overdominance; (2) the adaptive distance model has an increasingly low fit when the number of loci increases, under inbreeding, whereas it always explains the whole variance in fitness under overdominance; (3) a negative relationship is predicted between mean fitness and the variance in fitness, under inbreeding, which is not predicted under overdominance. Some statistical tests are derived from these predictions, that help to identify the genetic basis of heterosis. Simulations show that the power of these tests allows their application to real datasets.     

The fitness effect of mutations across environments: Fisher's geometrical model with multiple optima

When are mutations beneficial in one environment and deleterious in another? More generally, what is the relationship between mutation effects across environments? These questions are crucial to predict adaptation in heterogeneous conditions in a broad sense. Empirical evidence documents various patterns of fitness effects across environments but we still lack a framework to analyze these multivariate data. In this article, we extend Fisher's geometrical model to multiple environments determining distinct peaks. We derive the fitness distribution, in one environment, among mutants with a given fitness in another and the bivariate distribution of random mutants’ fitnesses across two or more environments. The geometry of the phenotype‐fitness landscape is naturally interpreted in terms of fitness trade‐offs between environments. These results may be used to fit/predict empirical distributions or to predict the pattern of adaptation across heterogeneous conditions. As an example, we derive the genomic rate of substitution and of adaptation in a metapopulation divided into two distinct habitats in a high migration regime and show that they depend critically on the geometry of the phenotype‐fitness landscape.     

ESS gene expression of X-linked imprinted genes subject to sexual selection

We define ESS (Evolutionary Stable Strategy) conditions for the evolution of genomic imprinting at an X-linked locus. The system analysed is designed for mammalian imprinting in which X-linked genes typically undergo random X-inactivation and lack Y-linked homologues. We consider two models that map cellular gene expression to fitness in females subject to random X-inactivation. In the first model, female fitness is simply a function of the average gene expression across all cells. In the second model, each cell contributes independently to fitness, and female fitness is assessed as the average of these contributions across all cells. In both models, imprinting readily evolves when sexual selection favours different levels of gene expression in the two sexes. Imprinting is beneficial as it improves adaptation in both sexes. There are limits to the improvement in adaptation when sexual selection is strong and favours greater gene expression in males (the heterogametic sex). We also consider the consequences of an active Y-linked homologue on the evolution of imprinting. Our analysis suggests that restrictive conditions apply for the evolution of polymorphic ESSs at an X-linked imprinted loci.     

Costs of predator‐induced morphological defences in Daphnia

1. Inducible defences are advantageous because they protect the prey while limiting associated fitness costs. The presence of these costs is an essential component of this conditional strategy, since their absence would favour constitutive (fixed) defences. In some cases, however, these costs have been difficult to measure because of complex interactions between the defences themselves, resultant life history changes and the organism’s environment. 2. The pond‐dwelling water flea, Daphnia pulex, forms defensive neck spines in response to kairomones released by predatory larvae of the phantom midge, Chaoborus. This predator–prey interaction and the formation of these inducible defences have been well studied, but costs associated with the development of neck spines remain unclear. In this study, I address this problem by analysing the effect of Chaoborus kairomones on the life history responses (and fitness costs associated with these responses) of two clones of D. pulex that are from the same pond population, but differ greatly in their degree of neck spine development. 3. Both D. pulex clones exhibited the same predator‐induced shifts in life history: larger size at birth, reduced juvenile growth rate (producing a smaller size at maturity), delayed reproduction and a reduction in the number of neonates produced after the first clutch. Relative fitness decreased significantly and to the same degree (c. 10% reduction in r) in each clone. This observed fitness cost was not directly related to the neck spines per se since the cost was the same in both clones, despite their considerable differences in neck spine development. Rather, it appears to be indirectly related to this antipredator morphology via a combination of delayed reproduction and a set of life history trade‐offs (decreased growth rate, decreased reproduction after the first clutch) for increased neonate body size, which is necessary for neck spines to be effective defences. This suite of induced responses is probably a result of local adaptation of these two D. pulex clones to their common pond environment. 4. Costs of inducible defences do not always entail direct allocation costs associated with forming and maintaining a defence, but may also involve indirect life history responses that are specific to particular environmental situations. This local adaptation would explain the highly variable life history responses observed among D. pulex clones from different pond environments.