Site-specific group selection drives locally adapted group compositions.

Group selection may be defined as selection caused by the differential extinction or proliferation of groups. The socially polymorphic spider Anelosimus studiosus exhibits a behavioural polymorphism in which females exhibit either a 'docile' or 'aggressive' behavioural phenotype. Natural colonies are composed of a mixture of related docile and aggressive individuals, and populations differ in colonies' characteristic docile:aggressive ratios. Using experimentally constructed colonies of known composition, here we demonstrate that population-level divergence in docile:aggressive ratios is driven by site-specific selection at the group level--certain ratios yield high survivorship at some sites but not others. Our data also indicate that colonies responded to the risk of extinction: perturbed colonies tended to adjust their composition over two generations to match the ratio characteristic of their native site, thus promoting their long-term survival in their natal habitat. However, colonies of displaced individuals continued to shift their compositions towards mixtures that would have promoted their survival had they remained at their home sites, regardless of their contemporary environment. Thus, the regulatory mechanisms that colonies use to adjust their composition appear to be locally adapted. Our data provide experimental evidence of group selection driving collective traits in wild populations.

Multilevel and kin selection in a connected world.

Wild et al. argue that the evolution of reduced virulence can be understood from the perspective of inclusive fitness, obviating the need to evoke group selection as a contributing causal factor. Although they acknowledge the mathematical equivalence of the inclusive fitness and multilevel selection approaches, they conclude that reduced virulence can be viewed entirely as an individual-level adaptation by the parasite. Here we show that their model is a well-known special case of the more general theory of multilevel selection, and that the cause of reduced virulence resides in the opposition of two processes: within-group and among-group selection. This distinction is important in light of the current controversy among evolutionary biologists in which some continue to affirm that natural selection centres only and always at the level of the individual organism or gene, despite mathematical demonstrations that evolutionary dynamics must be described by selection at various levels in the hierarchy of biological organization.

On the effectiveness of multilevel selection.

Experimental studies of group selection show that higher levels of selection act on indirect genetic effects, making the response to group and community selection qualitatively different from that of individual selection. This suggests that multilevel selection plays a key role in the evolution of supersocial societies. Experiments showing the effectiveness of community selection indicate that we should consider the possibility that selection among communities may be important in the evolution of supersocial species.

Cyto-nuclear epistasis: two-locus random genetic drift in hermaphroditic and dioecious species.

We report the findings of our theoretical investigation of the effect of random genetic drift on the covariance of identity-by-descent (ibd) of nuclear and cytoplasmic genes. The covariance in ibd measures of the degree to which cyto-nuclear gene combinations are heritable, that is, transmitted together from parents to offspring. We show how the mating system affects the covariance of ibd, a potentially important aspect of host-pathogen or host-symbiont coevolution. The magnitude of this covariance influences the degree to which the evolution of apparently neutral cytoplasmic genes, often used in molecular phylogenetics, might be influenced by selection acting on unlinked nuclear genes. To the extent that cyto-nuclear gene combinations are inherited together, genomic conflict is mitigated and intergenomic transfer it facilitated, because genes in both organelle and nuclear genomes share the same evolutionary fate. The covariance of ibd also affects the rate at which cyto-nuclear epistatic variance is converted to additive variance necessary for a response to selection. We find that conversion is biased in species with separate sexes, so that the increment of additive variance added to the nuclear genome exceeds that added to the cytoplasmic genome. As a result, the host might have an adaptive advantage in a coevolutionary arms race with vertically (maternally) transmitted pathogens. Similarly, the nuclear genome could be a source of compensatory mutations for its organellar genomes, as occurs in cytoplasmic male sterility in some plant species. We also discuss the possibility that adaptive cytoplasmic elements, such as favorable mitochondrial mutations or endosymbionts (e.g., Wolbachia), have the potential to release heritable nuclear variation as they sweep through a host population, supporting the view that cytoplasmic introgression plays an important role in adaptation and speciation.

Getting the Hologenome Concept Right: an Eco-Evolutionary Framework for Hosts and Their Microbiomes.

Given the complexity of host-microbiota symbioses, scientists and philosophers are asking questions at new biological levels of hierarchical organization-what is a holobiont and hologenome? When should this vocabulary be applied? Are these concepts a null hypothesis for host-microbe systems or limited to a certain spectrum of symbiotic interactions such as host-microbial coevolution? Critical discourse is necessary in this nascent area, but productive discourse requires that skeptics and proponents use the same lexicon. For instance, critiquing the hologenome concept is not synonymous with critiquing coevolution, and arguing that an entity is not a primary unit of selection dismisses the fact that the hologenome concept has always embraced multilevel selection. Holobionts and hologenomes are incontrovertible, multipartite entities that result from ecological, evolutionary, and genetic processes at various levels. They are not restricted to one special process but constitute a wider vocabulary and framework for host biology in light of the microbiome.

Long-term selection experiments: epistasis and the response to selection.

Two common features of long-term selection experiments are that, first, there is typically no evidence for selection limits due to exhaustion of genetic variation, and second, selection plateaus are frequently observed that last multiple generations before a response to selection is resumed. These features are usually attributed to the high mutation rates of quantitative traits, and the effects of linkage disequilibrium. Using previously published theoretical results and a simple deterministic model I explore the potential role of gene interaction in generating these patterns seen in the response to long-term selection experiments. I show that epistasis provides a pool of variation that can contribute to an extended response to selection, but that this extended response will, at least under some circumstances, result in intermediate selection plateaus.

On multilevel selection and kin selection: contextual analysis meets direct fitness.

When Hamilton defined the concept of inclusive fitness, he specifically was looking to define the fitness of an individual in terms of that individual's behavior, and the effects of its' behavior on other related individuals. Although an intuitively attractive concept, issues of accounting for fitness, and correctly assigning it to the appropriate individual make this approach difficult to implement. The direct fitness approach has been suggested as a means of modeling kin selection while avoiding these issues. Whereas Hamilton's inclusive fitness approach assigns to the focal individual the fitness effects of its behavior on other related individuals, the direct fitness approach assigns the fitness effects of other actors to the focal individual. Contextual analysis was independently developed as a quantitative genetic approach for measuring multilevel selection in natural populations. Although the direct fitness approach and contextual analysis come from very different traditions, both methods rely on the same underlying equation, with the primary difference between the two approaches being that the direct fitness approach uses fitness optimization modeling, whereas with contextual analysis, the same equation is used to solve for the change in fitness associated with a change in phenotype when the population is away from the optimal phenotype.

Genetic variation and evolution of secondary compounds in native and introduced populations of the invasive plant Melaleuca quinquenervia.

We examined multivariate evolution of 20 leaf terpenoids in the invasive plant Melaleuca quinquenervia in a common garden experiment. Although most compounds, including 1,8-Cineole and Viridiflorol, were reduced in home compared with invaded range genotypes, consistent with an evolutionary decrease in defense, one compound (E-Nerolidol) was greater in invaded than home range genotypes. Nerolidol was negatively genetically correlated with Cineole and Viridiflorol, and the increase in this compound in the new range may have been driven by this negative correlation. There was positive selection on all three focal compounds, and a loss of genetic variation in introduced range genotypes. Selection skewers analysis predicted an increase in Cineole and Viridiflorol and a decrease or no change in Nerolidol, in direct contrast to the observed changes in the new range. This discrepancy could be due to differences in patterns of selection, genetic correlations, or the herbivore communities in the home versus introduced ranges. Although evolutionary changes in most compounds were consistent with the evolution of increased competitive ability hypothesis, changes in other compounds as well as selection patterns were not, indicating that it is important to understand selection and the nature of genetic correlations to predict evolutionary change in invasive species.

Evolution in metacommunities.

A metacommunity can be defined as a set of communities that are linked by migration, and extinction and recolonization. In metacommunities, evolution can occur not only by processes that occur within communities such as drift and individual selection, but also by among-community processes, such as divergent selection owing to random differences among communities in species composition, and group and community-level selection. The effect of these among-community-level processes depends on the pattern of migration among communities. Migrating units may be individuals (migrant pool model), groups of individuals (single-species propagule pool model) or multi-species associations (multi-species propagule pool model). The most interesting case is the multi-species propagule pool model. Although this pattern of migration may a priori seem rare, it becomes more plausible in small well-defined 'communities' such as symbiotic associations between two or a few species. Theoretical models and experimental studies show that community selection is potentially an effective evolutionary force. Such evolution can occur either through genetic changes within species or through changes in the species composition of the communities. Although laboratory studies show that community selection can be important, little is known about how important it is in natural populations.

Horizontal transmission rapidly erodes disequilibria between organelle and symbiont genomes.

We investigate the generation and decay of interspecific disequilibrium (ID) between organelle and symbiont genomes as a function of the rate of horizontal transmission. We show that rare horizontal transmission greatly diminishes the covariance between organelle and symbiont genomes. This result has two important implications. First, a low level of ID does not indicate low levels of vertical transmission. Second, even with low levels of horizontal transmission, the additive effects of host and symbiont loci will determine the response to selection, while epistatic effects will not be selectable.

Empirical comparison of G matrix test statistics: finding biologically relevant change.

A central assumption of quantitative genetic theory is that the breeder's equation (R=GP(-1)S) accurately predicts the evolutionary response to selection. Recent studies highlight the fact that the additive genetic variance-covariance matrix (G) may change over time, rendering the breeder's equation incapable of predicting evolutionary change over more than a few generations. Although some consensus on whether G changes over time has been reached, multiple, often-incompatible methods for comparing G matrices are currently used. A major challenge of G matrix comparison is determining the biological relevance of observed change. Here, we develop a "selection skewers"G matrix comparison statistic that uses the breeder's equation to compare the response to selection given two G matrices while holding selection intensity constant. We present a bootstrap algorithm that determines the significance of G matrix differences using the selection skewers method, random skewers, Mantel's and Bartlett's tests, and eigenanalysis. We then compare these methods by applying the bootstrap to a dataset of laboratory populations of Tribolium castaneum. We find that the results of matrix comparison statistics are inconsistent based on differing a priori goals of each test, and that the selection skewers method is useful for identifying biologically relevant G matrix differences.

THE INFLUENCE OF ENVIRONMENTAL VARIATION ON GROUP AND INDIVIDUAL SELECTION IN A CRESS.

An experimental study of group and individual selection for leaf area under different patterns of environmental variation is presented. This study, which uses the cress Arabidopsis thaliana, demonstrates that group selection can occur in plants. The response to group selection was always in the expected direction, but surprisingly, the response to individual selection was not. Furthermore the interaction between group and individual selection was significant. Individual selection interfered with the response to group selection whether the two forces were acting in concert or were opposed. The effects of the environmental variation treatments were detected mainly as three-way interactions with group and individual selection. Group selection was more effective in environments that interfered with individual selection, as well as in environments that did not interfere with group selection. These results suggest that the ability of a character to respond to group selection, individual selection, or both will depend on a great many factors and that the relative importance of the different levels of selection can only be determined empirically.

EXPERIMENTAL STUDIES OF COMMUNITY EVOLUTION II: THE ECOLOGICAL BASIS OF THE RESPONSE TO COMMUNITY SELECTION.

Community selection, defined as the differential proliferation and/or extinction of communities, can bring about a response that may be qualitatively different from the response to selection acting at lower levels. This is because community selection can result in genetic changes in all of the species within the community by acting on the interaction among species. In the experiment presented here, a series of one generation assays were performed on the coevolved communities of two species of flour beetles, Tribolium castaneum and T. confusum, discussed by Goodnight (1990). Two community assays and one single-species assay were performed. Taken together, these provide insights into the genetic basis of the response to community selection. The first community assay involved measuring the selected traits on the original coevolved communities that had been subjected to community selection. This assay indicated that all of the selection treatments resulted in a significant response to selection in the original coevolved communities. The single-species assay involved separating the coevolved communities into their constituent single-species populations and again measuring the selected traits on these populations. None of the single-species populations exhibited a significant response to selection; thus the responses to community selection observed in the first community assay are expressed only in a community context. The second community assay again involved separating the coevolved communities into their constituent single-species populations; however, in this assay a competitor of the opposite species that had never been exposed to community selection was added to each population to form a "reconstructed" community. The results of this assay were that for two traits, emigration rate in T. castaneum and emigration rate in T. confusum, the genetic identity of the competing species did not affect the response to selection. This indicates that the competing species was acting like a nonevolving part of the environment. For the other two traits measured, population size in T. castaneum and population size in T. confusum, the results were very different. For these traits there was no detectable response to selection in the reconstructed communities. This indicates that for these traits the response to selection cannot be attributed to a genetic change in either species independently of the other species in the community. Rather it resides in the interaction between the two species.

EXPERIMENTAL STUDIES OF COMMUNITY EVOLUTION I: THE RESPONSE TO SELECTION AT THE COMMUNITY LEVEL.

Coevolution generally refers to the process of two or more organisms adapting to each other as a result of individual selection. Another possibility, however, is that coevolution may result from selection acting directly at the community level. Certain types of multispecies associations, such as lichens, which are a symbiotic association between an alga and a fungus, are examples of simple two species communities that may be units of selection. The study presented here uses two species communities of Tribolium castaneum and T. confusum in an investigation of selection acting at the community level. Selection at the community level is performed on one trait measured in one species and correlated responses in other traits measured both within species and among species are monitored. I demonstrate that community selection, defined as the differential survival and or reproduction of communities, can result in significant changes in the phenotype of a community. The observed changes in the phenotype of a community as a result of community selection included changes in the trait under selection (direct effects of selection), as well as changes in traits that are not under selection (correlated responses to selection). Furthermore, two types of correlated responses to selection were observed. The first, within-species correlated responses to selection, are changes in a trait measured in one species as a result of community selection acting on another trait measured in the same species. The second, between-species correlated responses to selection, are changes in a trait measured in one species as a result of community selection acting on a trait measured in another species. Between species correlated responses to selection are of particular interest because they cannot be mediated by pathways of gene action that are internal to an individual, rather they can be mediated only through ecological pathways. In other words, between-species correlated responses to selection suggest that genetically based interactions among individuals are contributing to the response to community selection. These among species ecological pathways of gene action cannot contribute to a response to selection at a lower level; thus community selection may be able to bring about a response to selection that is qualitatively different from the response selection that would occur as a result of selection acting at a lower level.

ON THE EFFECT OF FOUNDER EVENTS ON EPISTATIC GENETIC VARIANCE.

Mayr (1963) proposed that small isolated propagules from a large panmictic population would occasionally undergo a genetic revolution due to loss of genetic variability. More recently Templeton (1980a) has suggested that founder events may be much more important in systems that have strong epistasis. Because of the work of these and other authors it becomes an interesting theoretical problem to study the distribution of epistatic variance in a population following a founder event. In the model presented here measures of coancestry (Cockerham, 1967, 1984; Cockerham and Weir, 1973; Weir and Cockerham, 1973, 1977; Tachida and Cockerham, unpubl.) are used to examine the effect of founder events on additive-by-additive epistasis. Using this approach, the coancestries, or intraclass correlations, within individuals and within demes, together with the genetic variance components in the ancestral population are used to obtain the variance within and among demes following a founder event. Examples are analyzed for single founder events of 1-25 individuals and multiple founder events of two individuals. Following a single founder event, the contribution of the additive variance to the variance within demes relative to the additive variance in the ancestral population is always less than one. However, the contribution of epistatic variance to the variance within demes relative to the epistatic variance in the ancestral population is always greater than one. Thus, while a founder event decreases the contribution of additive variance to the variance within demes, it increases the contribution of epistatic variance to the variance within demes. The contribution of epistatic variance to the variance among demes following a single founder event is not qualitatively different from the contribution of additive variance to the variance among demes. These results indicate that epistatic variance is less likely than additive variance to cause a genetic revolution following a single founder event. When populations undergo multiple founder events the situation changes considerably. Epistatic variance may contribute as much as four times its original value to the variance among demes, while additive variance can contribute maximally twice its original value to the variance among demes. Thus, epistasis, which is relatively unimportant following a single founder event, may have major evolutionary implications if drift is allowed to continue for several generations.

EPISTASIS AND THE EFFECT OF FOUNDER EVENTS ON THE ADDITIVE GENETIC VARIANCE.

Models of founder events have focused on the reduction in the genetic variation following a founder event. However, recent work (Bryant et al., 1986; Goodnight, 1987) suggests that when there is epistatic genetic variance in a population, the total genetic variance within demes may actually increase following a founder event. Since the additive genetic variance is a statistical property of a population and can change with the level of inbreeding, some of the epistatic genetic variance may be converted to additive genetic variance during a founder event. The model presented here demonstrates that some of the additive-by-additive epistatic genetic variance is converted to additive genetic variance following a founder event. Furthermore, the amount of epistasis converted to additive genetic variance is a function of the recombination rate and the propagule size. For a single founder event of two individuals, as much as 75% of the epistatic variance in the ancestral population may become additive genetic variance following the founder event. For founder events involving two individuals with free recombination, the relative contribution of epistasis to the additive genetic variance following a founder event is equal to its proportion of the total genetic variance prior to the founder event. Traits closely related to fitness are expected to have relatively little additive genetic variance but may have substantial nonadditive genetic variance. Founder events may be important in the evolution of fitness traits, not because they lead to a reduction in the genetic variance, but rather because they lead to an increase in the additive genetic variance.

EPISTASIS AND THE INCREASE IN ADDITIVE GENETIC VARIANCE: IMPLICATIONS FOR PHASE 1 OF WRIGHT'S SHIFTING-BALANCE PROCESS.

Central to Wright's shifting-balance theory is the idea that genetic drift and selection in systems with gene interaction can lead to the formation of "adaptive gene complexes." The theory of genetic drift has been well developed over the last 60 years; however, nearly all of this theory is based on the assumption that only additive gene effects are acting. Wright's theory was developed recognizing that there was a "universality of interaction effects," which implies that additive theory may not be adequate to describe the process of differentiation that Wright was considering. The concept of an adaptive gene complex implies that an allele that is favored by individual selection in one deme may be removed by selection in another deme. In quantitative genetic terms, the average effects of an allele relative to other alleles changes from deme to deme. The model presented here examines the variance in local breeding values (LBVs) of a single individual and the covariance in the LBVs of a pair of individuals mated in the same deme relative to when they are mated in different demes. Local breeding value is a measure of the average effects of the alleles that make up that individual in a particular deme. I show that when there are only additive effects the covariance between the LBVs of individuals equals the variance in the LBV of an individual. As the amount of epistasis in the ancestral population increases, the variance in the LBV of an individual increases and the covariance between the LBVs of a pair of individuals decreases. The divergence in these two values is a measure of the extent to which the LBV of an individual varies independently of the LBVs of other individuals. When this value is large, it means that the relative ordering of the average effects of alleles will change from deme to deme. These results confirm an important component of Wright's shifting-balance theory: When there is gene interaction, genetic drift can lead to the reordering of the average effects of alleles and when coupled with selection this will lead to the formation of the adaptive gene complexes.