Natural selection causing microsatellite divergence in wild emmer wheat at the ecologically variable microsite at Ammiad, Israel

Genetic diversity at 28 microsatellite loci was studied in a natural population of Triticum dicoccoides at the Ammiad microsite, north of the Sea of Galilee, Israel. This microsite was subdivided into four major habitats, North, Valley, Ridge and Karst, and further subdivided into nine subhabitats. The units thus defined showed strong and highly significant differentiation in ecological factors; in particular with respect to cover, proximity and height of rocks, and surface soil moisture after early rains. The results showed that allele distributions at microsatellite loci were nonrandom and associated with habitats. Significant genetic differentiation and variation in repeat number were found among subpopulations in the four major habitats and nine subhabitats. Habitat-specific and -unique alleles and linkage disequilibria were observed in the Karst subpopulation. The subpopulations dwelling in drier habitats and subhabitats showed higher genetic diversities at microsatellite loci. These results suggest that natural selection, presumably through aridity stress, acts upon microsatellite divergence predominantly on noncoding sequences, thereby contributing to differences in fitness. Received: 9 September 1999 / Accepted: 16 September 1999     

A HIERARCHICAL ANALYSIS OF GENETIC DIFFERENTIATION IN A MONTANE LEAF BEETLE CHRYSOMELA AENEICOLLIS (COLEOPTERA: CHRYSOMELIDAE)

Herbivorous insects that use the same host plants as larvae and adults can have a subdivided population structure that corresponds to the distribution of their hosts. Having a subdivided population structure favors local adaptation of subpopulations to small-scale environmental differences and it may promote their genetic divergence. In this paper, I present the results of a hierarchical study of population structure in a montane willow leaf beetle, Chrysomela aeneicollis (Coleoptera: Chrysomelidae). This species spends its entire life associated with the larval host (Salix spp.), which occurs in patches along high-elevation streams and in montane bogs. I analyzed the genetic differentiation of C. aeneicollis populations along three drainages in the Sierra Nevada mountains of California at five enzyme loci: ak-1, idh-2, mpi-1, pgi-1, and pgm-1, using recent modifications of Wright's F-statistics. My results demonstrated significant differentiation (F_ST = 0.043) among drainages that are less than 40 kilometers apart. One locus, pgi-1, showed much greater differentiation than the other four (F_ST = 0.412), suggesting that it is under natural selection. C. aeneicollis populations were also subdivided within drainages, with significant differentiation 1) among patches of willows (spanning less than three kilometers) and 2) in some cases, among trees within a willow patch. My results demonstrate that this species has the capacity to adapt to local environmental variation at small spatial scales.     

Population structure and interdemic selection in the cooperative spider Anelosimus eximius

The degree of relatedness among interacting individuals helps determine the fitness consequences of particular behaviors, whereas the partitioning (and amount) of genetic variation among and within groups controls the level at which selection will act most effectively. Three criteria are considered necessary for selection to act at the group or interdemic level: high rate of group initiation/extinction; differential survival and reproduction among groups; and highly subdivided population structure. The first two criteria have been demonstrated by earlier studies of Anelosimus eximius colonies. This study employs hierarchical analysis of allozyme polymorphisms to demonstrate the third criterion, subdivided population structure. Anelosimus eximius were collected from Suriname, Panama, Ecuador, Peru and Trinidad. Seven of 40 scorable enzyme loci revealed variation; 4 of these were polymorphic within colonies or regions. Expected heterozygosities were low, ranging from 0 (Ecuador, Peru) to ～0.03 (Suriname). For each polymorphic locus, hierarchical F -statistics were used to partition overall genetic variation into among-region (or among-population; F _rt ), among-colony ( F _sr ), and within-colony ( F _is ) components. Samples from Suriname (43 colonies, 4 local populations) were the most informative; lack of scorable variation limited the inferences that could be drawn from other regions. A. eximius colonies are highly inbred: negative estimates of F _is imply very small effective colony sizes (～6.5 for Suriname samples). By contrast, estimates of F _sr were very high: the mean for Suriname samples was 0.890, indicating neglibible gene flow among established colonies. Inbreeding within colonies, and genetic differentiation among colonies are consistent with demographic and behavioral observations of A. eximius . We suggest that interdemic selection is probable in this species and other cooperative spiders with this type of social system, and that mutual tolerance and absence of nest-mate recognition, as well as female-biased sex ratios, may have arisen by interdemic selection.     

Quantification and decomposition of environment‐selection relationships

In nature, selection varies across time in most environments, but we lack an understanding of how specific ecological changes drive this variation. Ecological factors can alter phenotypic selection coefficients through changes in trait distributions or individual mean fitness, even when the trait‐absolute fitness relationship remains constant. We apply and extend a regression‐based approach in a population of Soay sheep (Ovis aries) and suggest metrics of environment‐selection relationships that can be compared across studies. We then introduce a novel method that constructs an environmentally structured fitness function. This allows calculation of full (as in existing approaches) and partial (acting separately through the absolute fitness function slope, mean fitness, and phenotype distribution) sensitivities of selection to an ecological variable. Both approaches show positive overall effects of density on viability selection of lamb mass. However, the second approach demonstrates that this relationship is largely driven by effects of density on mean fitness, rather than on the trait‐fitness relationship slope. If such mechanisms of environmental dependence of selection are common, this could have important implications regarding the frequency of fluctuating selection, and how previous selection inferences relate to longer term evolutionary dynamics.     

Correlations between sex rate estimates and fitness across predominantly parthenogenetic flatworm populations

One explanation for the success of sexual reproduction is that sex increases the efficacy of natural selection. Recombination and segregation lead to fitness variance among offspring which then offers a wider target for natural selection. Consequently, adaptation to changing environments is accelerated and population mean fitness will increase. We investigated whether low levels of sex are associated with increased fitness variance and mean in parthenogenetic biotypes of the planarian flatworm Schmidtea polychroa. Parthenogenetic S. polychroa are triploid and reproduce clonally with occasional sexual reproduction. By-products and measures of occasional sex are the local presence of tetraploids and elevated levels of genotypic diversity. We correlated the proportion of tetraploids and genotypic diversity with fitness attributes of six genetically differentiated locations within one meta-population. Results indicate strong, positive correlations with variance and with mean offspring number produced during a 5-week period. The ecological and evolutionary implications for the maintenance of parthenogenetic S. polychroa are discussed.     

Ecosystem engineers as selective agents: the effects of leaf litter on emergence time and early growth in Impatiens capensis

By physically modifying the abiotic environment, ecosystem engineers can have dramatic effects on the distribution and abundance of species in a community. However, ecosystem engineering can also change the selective environment and evolutionary dynamics of affected species, although this remains relatively understudied. Here, we examine the potential for an ecosystem engineer – oak trees – to affect the evolutionary dynamics of the herbaceous, understory annual, Impatiens capensis , through leaf litter deposition. Using a quantitative genetic experimental approach, we found that: (i) the presence of leaf litter significantly affected a suite of germination, growth and phenological traits in I. capensis ; (ii) I. capensis does not exhibit performance trade-offs across litter and bare soil environments in the form of negative across-environment genetic correlations; (iii) the presence or absence of leaf litter significantly alters the pattern of natural selection germination timing and hypocotyl length; and (iv) the frequency of leaf litter environments can dramatically change which combinations of hypocotyl length lead to highest mean fitness across both bare soil and leaf litter environments. More generally, our results demonstrate the potential for ecosystem engineers to alter both the ecological and the evolutionary dynamics of the species they affect.     

Diffusion approximations for one-locus multi-allele kin selection,mutation and random drift in group-structured populations: a unifying approach to selection models in population genetics

Diffusion approximations are ascertained from a two-time-scale argument in the case of a group-structured diploid population with scaled viability parameters depending on the individual genotype and the group type at a single multi-allelic locus under recurrent mutation, and applied to the case of random pairwise interactions within groups. The main step consists in proving global and uniform convergence of the distribution of the group types in an infinite population in the absence of selection and mutation, using a coalescent approach. An inclusive fitness formulation with coefficient of relatedness between a focal individual J affecting the reproductive success of an individual I, defined as the expected fraction of genes in I that are identical by descent to one or more genes in J in a neutral infinite population, given that J is allozygous or autozygous, yields the correct selection drift functions. These are analogous to the selection drift functions obtained with pure viability selection in a population with inbreeding. They give the changes of the allele frequencies in an infinite population without mutation that correspond to the replicator equation with fitness matrix expressed as a linear combination of a symmetric matrix for allozygous individuals and a rank-one matrix for autozygous individuals. In the case of no inbreeding, the mean inclusive fitness is a strict Lyapunov function with respect to this deterministic dynamics. Connections are made between dispersal with exact replacement (proportional dispersal), uniform dispersal, and local extinction and recolonization. The timing of dispersal (before or after selection, before or after mating) is shown to have an effect on group competition and the effective population size. In memory of Sam Karlin.     

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.     

NATURAL SELECTION ON BODY SIZE AND LAYING DATE IN THE TREE SWALLOW

I measured natural selection on body size and laying date in a population of tree swallows (Tachycineta bicolor) from 1986 to 1988. There was little evidence of selection on body size associated with overwinter survival. Disruptive selection on tarsus length, associated with female reproductive success, was detected in one of three years. Both repeatability and mother-daughter regression suggested that laying date was heritable. I found weak evidence of selection on laying date, associated with both overwinter survival and reproduction in females. The ecological implications of both tarsus length and laying date variation in this population could not be identified. Consequently, although I was able to identify the targets of natural selection, the ecological link between trait variation and selection remains unknown.     

PHASE III OF WRIGHT'S SHIFTING BALANCE PROCESS AND THE VARIANCE AMONG DEMES IN MIGRATION RATE

Interdemic selection by the differential migration of individuals out from demes of high fitness and into demes of low fitness (Phase III) is one of the most controversial aspects of Wright's Shifting Balance Theory. I derive a relationship between Phase III migration and the interdemic selection differential, S, and show its potential effect on F_ST. The relationship reveals a diversifying effect of interdemic selection by Phase III migration on the genetic structure of a metapopulation. Using experimental metapopulations, I explored the effect of Phase III migration on F_ST by comparing the genetic variance among demes for two different patterns of migration: (1) island model migration and (2) Wright's Phase III migration. Although mean migration rates were the same, I found that the variance among demes in migration rate was significantly higher with Phase III than with island model migration. As a result, F_ST for the frequency of a neutral marker locus was higher with Phase III than it was with island model migration. By increasing F_ST, Phase III enhanced the genetic differentiation among demes for traits not subject to interdemic selection. This feature makes Wright's process different from individual selection which, by reducing effective population size, decreases the genetic variance within demes for all other traits. I discussed this finding in relation to the efficacy of Phase III and random migration for effecting peak shifts, and the contribution of genes with indirect effects to among‐deme variation.     

THE DISTINCTIVE FOOTPRINTS OF LOCAL HITCHHIKING IN A VARIED ENVIRONMENT AND GLOBAL HITCHHIKING IN A SUBDIVIDED POPULATION

Loci with higher levels of population differentiation than the neutral expectation are traditionally interpreted as evidence of ongoing selection that varies in space. This article emphasizes an alternative explanation that has been largely overlooked to date: in species subdivided into large subpopulations, enhanced differentiation can also be the signature left by the fixation of an unconditionally favorable mutation on its chromosomal neighborhood. This is because the hitchhiking effect is expected to diminish as the favorable mutation spreads from the deme in which it originated to other demes. To discriminate among the two alternative scenarios one needs to investigate how genetic structure varies along the chromosomal region of the locus. Local hitchhiking is shown to generate a single sharp peak of differentiation centered on the adaptive polymorphism and the standard signature of a selective sweep only in those subpopulations in which the allele is favored. Global hitchhiking produces two domes of differentiation on either side of the fixed advantageous mutation and signatures of a selective sweep in every subpopulation, albeit of different magnitude. Investigating population differentiation around a locus that strongly differentiates two otherwise genetically similar populations of the marine mussel Mytilus edulis, plausible evidence for the global hitchhiking hypothesis has been obtained. Global hitchhiking is a neglected phenomenon that might prove to be important in species with large population sizes such as many marine invertebrates.     

The Effects of Background and Interference Selection on Patterns of Genetic Variation in Subdivided Populations

It is well known that most new mutations that affect fitness exert deleterious effects and that natural populations are often composed of subpopulations (demes) connected by gene flow. To gain a better understanding of the joint effects of purifying selection and population structure, we focus on a scenario where an ancestral population splits into multiple demes and study neutral diversity patterns in regions linked to selected sites. In the background selection regime of strong selection, we first derive analytic equations for pairwise coalescent times and F_ST as a function of time after the ancestral population splits into two demes and then construct a flexible coalescent simulator that can generate samples under complex models such as those involving multiple demes or nonconservative migration. We have carried out extensive forward simulations to show that the new methods can accurately predict diversity patterns both in the nonequilibrium phase following the split of the ancestral population and in the equilibrium between mutation, migration, drift, and selection. In the interference selection regime of many tightly linked selected sites, forward simulations provide evidence that neutral diversity patterns obtained from both the nonequilibrium and equilibrium phases may be virtually indistinguishable for models that have identical variance in fitness, but are nonetheless different with respect to the number of selected sites and the strength of purifying selection. This equivalence in neutral diversity patterns suggests that data collected from subdivided populations may have limited power for differentiating among the selective pressures to which closely linked selected sites are subject.     

Migration promotes mutator alleles in subdivided populations

Mutator alleles that elevate the genomic mutation rate may invade nonrecombining populations by hitchhiking with beneficial mutations. Mutators have been repeatedly observed to take over adapting laboratory populations and have been found at high frequencies in both microbial pathogen and cancer populations in nature. Recently, we have shown that mutators are only favored by selection in sufficiently large populations and transition to being disfavored as population size decreases. This population size‐dependent sign inversion in selective effect suggests that population structure may also be an important determinant of mutation rate evolution. Although large populations may favor mutators, subdividing such populations into sufficiently small subpopulations (demes) might effectively inhibit them. On the other hand, migration between small demes that otherwise inhibit hitchhiking may promote mutator fixation in the whole metapopulation. Here, we use stochastic, agent‐based simulations and evolution experiments with the yeast Saccharomyces cerevisiae to show that mutators can, indeed, be favored by selection in subdivided metapopulations composed of small demes connected by sufficient migration. In fact, we show that population structure plays a previously unsuspected role in promoting mutator success in subdivided metapopulations when migration is rare.     

When maladaptive gene flow does not increase selection

Populations receiving high maladaptive gene flow are expected to experience strong directional selection—because gene flow pulls mean phenotypes away from local fitness peaks. We tested this prediction by means of a large and replicated mark‐recapture study of threespine stickleback (Gasterosteus aculeatus) in two stream populations. One of the populations (outlet) experiences high gene flow from the lake population and its morphology is correspondingly poorly adapted. The other population (inlet) experiences very low gene flow from the lake population and its morphology is correspondingly well adapted. Contrary to the above prediction, selection was not stronger in the outlet than in the inlet, a result that forced us to consider potential reasons for why maladaptive gene flow might not increase selection. Of particular interest, we show by means of a simple population genetic model that maladaptive gene flow can—under reasonable conditions—decrease the strength of directional selection. This outcome occurs when immigrants decrease mean fitness in the resident population, which decreases the strength of selection against maladapted phenotypes. We argue that this previously unrecognized effect of gene flow deserves further attention in theoretical and empirical studies.     

Selection, load and inbreeding depression in a large metapopulation

The subdivision of a species into local populations causes its response to selection to change, even if selection is uniform across space. Population structure increases the frequency of homozygotes and therefore makes selection on homozygous effects more effective. However, population subdivision can increase the probability of competition among relatives, which may reduce the efficacy of selection. As a result, the response to selection can be either increased or decreased in a subdivided population relative to an undivided one, depending on the dominance coefficient F(ST) and whether selection is hard or soft. Realistic levels of population structure tend to reduce the mean frequency of deleterious alleles. The mutation load tends to be decreased in a subdivided population for recessive alleles, as does the expected inbreeding depression. The magnitude of the effects of population subdivision tends to be greatest in species with hard selection rather than soft selection. Population structure can play an important role in determining the mean fitness of populations at equilibrium between mutation and selection.     

Lifetime fitness consequences of early‐life ecological hardship in a wild mammal population

Early‐life ecological conditions have major effects on survival and reproduction. Numerous studies in wild systems show fitness benefits of good quality early‐life ecological conditions (“silver‐spoon” effects). Recently, however, some studies have reported that poor‐quality early‐life ecological conditions are associated with later‐life fitness advantages and that the effect of early‐life conditions can be sex‐specific. Furthermore, few studies have investigated the effect of the variability of early‐life ecological conditions on later‐life fitness. Here, we test how the mean and variability of early‐life ecological conditions affect the longevity and reproduction of males and females using 14 years of data on wild banded mongooses (Mungos mungo). Males that experienced highly variable ecological conditions during development lived longer and had greater lifetime fitness, while those that experienced poor early‐life conditions lived longer but at a cost of reduced fertility. In females, there were no such effects. Our study suggests that exposure to more variable environments in early life can result in lifetime fitness benefits, whereas differences in the mean early‐life conditions experienced mediate a life‐history trade‐off between survival and reproduction. It also demonstrates how early‐life ecological conditions can produce different selection pressures on males and females.     

An integrated analysis of phenotypic selection on insect body size and development time

Most studies of phenotypic selection do not estimate selection or fitness surfaces for multiple components of fitness within a unified statistical framework. This makes it difficult or impossible to assess how selection operates on traits through variation in multiple components of fitness. We describe a new generation of aster models that can evaluate phenotypic selection by accounting for timing of life‐history transitions and their effect on population growth rate, in addition to survival and reproductive output. We use this approach to estimate selection on body size and development time for a field population of the herbivorous insect, Manduca sexta (Lepidoptera: Sphingidae). Estimated fitness surfaces revealed strong and significant directional selection favoring both larger adult size (via effects on egg counts) and more rapid rates of early larval development (via effects on larval survival). Incorporating the timing of reproduction and its influence on population growth rate into the analysis resulted in larger values for size in early larval development at which fitness is maximized, and weaker selection on size in early larval development. These results illustrate how the interplay of different components of fitness can influence selection on size and development time. This integrated modeling framework can be readily applied to studies of phenotypic selection via multiple fitness components in other systems.     

THE IMPORTANCE OF FEMALE CHOICE,MALE–MALE COMPETITION,AND SIGNAL TRANSMISSION AS CAUSES OF SELECTION ON MALE MATING SIGNALS

Selection on advertisement signals arises from interacting sources including female choice, male–male competition, and the communication channel (i.e., the signaling environment). To identify the contribution of individual sources of selection, we used previously quantified relationships between signal traits and each putative source to predict relationships between signal variation and fitness in Enchenopa binotata treehoppers (Hemiptera: Membracidae). We then measured phenotypic selection on signals and compared predicted and realized relationships between signal traits and mating success. We recorded male signals, then measured lifetime mating success at two population densities in a realistic environment in which sources of selection could interact. We identified which sources best predicted the relationship between signal variation and mating success using a multiple regression approach. All signal traits were under selection in at least one of the two breeding seasons measured, and in some cases selection was variable between years. Female preference was the strongest source of selection shaping male signals. The E. binotata species complex is a model of ecological speciation initiated by host shifts. Signal and preference divergence contribute to behavioral isolation within the complex, and the finding that female mate preferences drive signal evolution suggests that speciation in this group results from both ecological divergence and sexual selection.     

Refining the conditions for sympatric ecological speciation

Can speciation occur in a single population when different types of resources are available, in the absence of any geographical isolation, or any spatial or temporal variation in selection? The controversial topics of sympatric speciation and ecological speciation have already stimulated many theoretical studies, most of them agreeing on the fact that mechanisms generating disruptive selection, some level of assortment, and enough heterogeneity in the available resources, are critical for sympatric speciation to occur. Few studies, however, have combined the three factors and investigated their interactions. In this article, I analytically derive conditions for sympatric speciation in a general model where the distribution of resources can be uni‐ or bimodal, and where a parameter controls the range of resources that an individual can exploit. This approach bridges the gap between models of a unimodal continuum of resources and Levene‐type models with discrete resources. I then test these conditions against simulation results from a recently published article (Thibert‐Plante & Hendry, 2011, J. Evol. Biol. 24 : 2186–2196) and confirm that sympatric ecological speciation is favoured when (i) selection is disruptive (i.e. individuals with an intermediate trait are at a local fitness minimum), (ii) resources are differentiated enough and (iii) mating is assortative. I also discuss the role of mating preference functions and the need (or lack thereof) for bimodality in resource distributions for diversification.     

Limited indirect fitness benefits of male group membership in a lekking species

In group living species, individuals may gain the indirect fitness benefits characterizing kin selection when groups contain close relatives. However, tests of kin selection have primarily focused on cooperatively breeding and eusocial species, whereas its importance in other forms of group living remains to be fully understood. Lekking is a form of grouping where males display on small aggregated territories, which females then visit to mate. As females prefer larger aggregations, territorial males might gain indirect fitness benefits if their presence increases the fitness of close relatives. Previous studies have tested specific predictions of kin selection models using measures such as group‐level relatedness. However, a full understanding of the contribution of kin selection in the evolution of group living requires estimating individuals' indirect fitness benefits across multiple sites and years. Using behavioural and genetic data from the black grouse (Tetrao tetrix), we show that the indirect fitness benefits of group membership were very small because newcomers joined leks containing few close relatives who had limited mating success. Males' indirect fitness benefits were higher in yearlings during increasing population density but marginally changed the variation in male mating success. Kin selection acting through increasing group size is therefore unlikely to contribute substantially to the evolution and maintenance of lekking in this black grouse population.