Niche construction and the environmental term of the price equation: How natural selection changes when organisms alter their environments.

Organisms construct their own environments and phenotypes through the adaptive processes of habitat choice, habitat construction, and phenotypic plasticity. We examine how these processes affect the dynamics of mean fitness change through the environmental change term of the Price Equation. This tends to be ignored in evolutionary theory, owing to the emphasis on the first term describing the effect of natural selection on mean fitness (the additive genetic variance for fitness of Fisher's Fundamental Theorem). Using population genetic models and the Price Equation, we show how adaptive niche constructing traits favorably alter the distribution of environments that organisms encounter and thereby increase population mean fitness. Because niche-constructing traits increase the frequency of higher-fitness environments, selection favors their evolution. Furthermore, their alteration of the actual or experienced environmental distribution creates selective feedback between niche constructing traits and other traits, especially those with genotype-by-environment interaction for fitness. By altering the distribution of experienced environments, niche constructing traits can increase the additive genetic variance for such traits. This effect accelerates the process of overall adaption to the niche-constructed environmental distribution and can contribute to the rapid refinement of alternative phenotypic adaptations to different environments. Our findings suggest that evolutionary biologists revisit and reevaluate the environmental term of the Price Equation: owing to adaptive niche construction, it contributes directly to positive change in mean fitness; its magnitude can be comparable to that of natural selection; and, when there is fitness G × E, it increases the additive genetic variance for fitness, the much-celebrated first term.

Relative rates of evolution of male-beneficial nuclear compensatory mutations and male-harming Mother's Curse mitochondrial alleles.

Mother's Curse alleles represent a significant source of potential male fitness defects. The maternal inheritance of mutations with the pattern of sex-specific fitness effects, s♀>0>s♂, allows Mother's Curse alleles to spread through a population even though they reduce male fitness. Although the mitochondrial genomes of animals contain only a handful of protein-coding genes, mutations in many of these genes have been shown to have a direct effect on male fertility. The evolutionary process of nuclear compensation is hypothesized to counteract the male-limited mitochondrial defects that spread via Mother's Curse. Here we use population genetic models to investigate the evolution of compensatory autosomal nuclear mutations that act to restore the loss of fitness caused by mitochondrial mutation pressures. We derive the rate of male fitness deterioration by Mother's Curse and the rate of restoration by nuclear compensatory evolution. We find that the rate of nuclear gene compensation is many times slower than that of its deterioration by cytoplasmic mutation pressure, resulting in a significant lag in the recovery of male fitness. Thus, the numbers of nuclear genes capable of restoring male mitochondrial fitness defects must be large in order to sustain male fitness in the face of mutation pressures.

Maternal inheritance, such as that of the mitochondrial genome, allows genetic variants that benefit female survival and reproduction to spread even when they negatively impact male fitness, referred to as Mother's Curse alleles. The maintenance of male fitness in spite of such alleles is predominantly attributed to the spread of variants in the nuclear genome that compensate for the male harming effects. However, the relative rate of nuclear compensatory evolution has not been derived. Here we show that many features of nuclear compensatory mutations slow their rate of evolution many-fold relative to the rapid spread of Mother's Curse alleles. Thus, the pool of nuclear genes capable of compensating for mitochondria-associated male harm must be very large to maintain male fitness, especially in light of the potential contribution of male-harming effects from the maternally inherited microbiome.

Host-parasite coevolution: Partitioning the effects of natural selection and environmental change using coupled Price equations.

George Price showed how the effects of natural selection and environmental change could be mathematically partitioned. This partitioning may be especially useful for understanding host-parasite coevolution, where each species represents the environment for the other species. Here, we use coupled Price equations to study this kind of antagonistic coevolution. We made the common assumption that parasites must genetically match their host's genotype to avoid detection by the host's self/nonself recognition system, but we allowed for the possibility that non-matching parasites have some fitness. Our results show how natural selection on one species results in environmental change for the other species. Numerical iterations of the model show that these environmental changes can periodically exceed the changes in mean fitness due to natural selection, as suggested by R.A. Fisher. Taken together, the results give an algebraic dissection of the eco-evolutionary feedbacks created during host-parasite coevolution.

Niche construction in quantitative traits: heritability and response to selection.

A central tenet of niche construction (NC) theory is that organisms can alter their environments in heritable and evolutionarily important ways, often altering selection pressures. We suggest that the physical changes niche constructors make to their environments may also alter trait heritability and the response of phenotypes to selection. This effect might change evolution, over and above the effect of NC acting via selection alone. We develop models of trait evolution that allow us to partition the effects of NC on trait heritability from those on selection to better investigate their distinct effects. We show that the response of a phenotype to selection and so the pace of phenotypic change can be considerably altered in the presence of NC and that this effect is compounded when trans-generational interactions are included. We argue that novel mathematical approaches are needed to describe the simultaneous effects of NC on trait evolution via selection and heritability. Just as indirect genetic effects have been shown to significantly increase trait heritability, the effects of NC on heritability in our model suggest a need for further theoretical development of the concept of heritability.

Generating and testing the efficacy of transgenic Cas9 in Tribolium castaneum.

CRISPR/Cas9 genome editing has now expanded to many insect species, including Tribolium castaneum. However, compared to Drosophila melanogaster, the CRISPR toolkit of T. castaneum is limited. A particularly apparent gap is the lack of Cas9 transgenic animals, which generally offer higher editing efficiency. We address this by creating and testing transgenic beetles expressing Cas9. We generated two different constructs bearing basal heat shock promoter-driven Cas9, two distinct 3' UTRs, and one containing Cas9 fused to EGFP by a T2A peptide. Analyses of Cas9 activity in each transgenic line demonstrated that both designs are capable of inducing CRISPR- mediated changes in the genome in the absence of heat induction. Overall, these resources enhance the accessibility of CRISPR/Cas9 genome editing for the Tribolium research community and provide a benchmark against which to compare future transgenic Cas9 lines.

Maternal-Offspring Interactions: Reciprocally Coevolving Social Environments.

Maternal-zygotic co-evolution is one of the most common examples of indirect genetic effects. I investigate how maternal-zygotic gene interactions affect rates of evolution and adaptation. Using comparably parameterized population genetic models, I compare evolution to an abiotic environment with genotype-by-environment interaction (G × E) to evolution to a maternal environment with offspring genotype-by-maternal environment interaction (G × Gmaternal). There are strong parallels between the 2 models in the components of fitness variance but they differ in their rates of evolution measured in terms of ∆p, gene frequency change, or of ∆W, change in mean fitness. The Price Equation is used to partition ∆W into 2 components, one owing to the genetic variance in fitness by natural selection and a second owing to change in environment. Adaptive evolution is faster in the 2-locus model with G × Gmaternal with free recombination, than it is in the 1-locus model with G × E, because in the former the maternal genetic environment coevolves with the zygotic phenotype adapting to it. I discuss the relevance of these findings for the evolution of genes with indirect genetic effects.

When is Offspring Viability Fitness a Measure of Paternal Fitness and When is it not?

We use population genetics to model the evolution of a gene with an indirect effect owing to paternal care and with a second pleiotropic, direct effect on offspring viability. We use the model to illustrate how the common empirical practice of considering offspring viability as a component of parent fitness can confound a gene's direct and indirect fitness effects. We investigate when this confounding results in a distorted picture of overall evolution and when it does not. We find that the practice has no effect on mean fitness, W, but it does have an effect on the dynamics of gene frequency change, ∆q. We also find that, for some regions of parameter space associated with fitness trade-offs, the distortion is not only quantitative but also qualitative, obscuring the direction of gene frequency change. Because it affects the evolutionary dynamics, it also affects the expected amount of genetic variation at mutation-selection balance, an important consideration in molecular evolution. We discuss empirical techniques for separating direct from indirect effects and how field studies measuring the value of male paternal care might be improved by using them.

Adaptive co-evolution of mitochondria and the Y-chromosome: A resolution to conflict between evolutionary opponents.

In most species with motile sperm, male fertility depends upon genes located on the Y-chromosome and in the mitochondrial genome. Coordinated adaptive evolution for the function of male fertility between genes on the Y and the mitochondrion is hampered by their uniparental inheritance in opposing sexes: The Y-chromosome is inherited uniparentally, father to son, and the mitochondrion is inherited maternally, mother to offspring. Preserving male fertility is problematic, because maternal inheritance permits mitochondrial mutations advantageous to females, but deleterious to male fertility, to accumulate in a population. Although uniparental inheritance with sex-restricted adaptation also affects genes on the Y-chromosome, females lack a Y-chromosome and escape the potential maladaptive consequences of male-limited selection. Evolutionary models have shown that mitochondrial mutations deleterious to male fertility can be countered by compensatory evolution of Y-linked mutations that restore it. However, direct adaptive coevolution of Y- and mitochondrial gene combinations has not yet been mathematically characterized. We use population genetic models to show that adaptive coevolution of Y and mitochondrial genes are possible when Y-mt gene combinations have positive effects on male fertility and populations are inbred.

The evolutionary genetics of paternal care: How good genes and extrapair copulation affect the trade-off between paternal care and mating success.

We investigate the evolution of a gene for paternal care, with pleiotropic effects on male mating fitness and offspring viability, with and without extrapair copulations (EPCs). We develop a population genetic model to examine how pleiotropic effects of a male mating advantage and paternal care are affected by "good genes" and EPCs. Using this approach, we show that the relative effects of each on fitness do not always predict the evolutionary change. We then find the line of combinations of mating success and paternal care that bisects the plane of possible values into regions of positive or negative gene frequency change. This line shifts when either good genes or EPCs are introduced, thereby expanding or contracting the region of positive gene frequency change and significantly affecting the evolution of paternal care. Predictably, a direct viability effect of "good genes" that enhances offspring viability constrains or expands the parameter space over which paternal care can evolve, depending on whether the viability effect is associated with the paternal care allele or not. In either case, the effect of a "good gene" that enhances offspring viability is substantial; when strong enough, it can even facilitate the evolution of poor paternal care, where males harm their young. When nonrandom mating is followed by random EPCs, the genetic regression between sire and offspring is reduced and, consequently, the relative strengths of selection are skewed away from paternal care and toward the male mating advantage. However, when random mating is followed by nonrandom EPCs, a situation called "trading up" by females, we show that selection is skewed in the opposite direction, away from male mating advantage and toward paternal care across the natural range of EPC frequencies.

Relaxed Selection and the Rapid Evolution of Reproductive Genes.

Evolutionary genomic studies find that reproductive protein genes, those directly involved in reproductive processes, diversify more rapidly than most other gene categories. Strong postcopulatory sexual selection acting within species is the predominant hypothesis proposed to account for the observed pattern. Recently, relaxed selection due to sex-specific gene expression has also been put forward to explain the relatively rapid diversification. We contend that relaxed selection due to sex-limited gene expression is the correct null model for tests of molecular evolution of reproductive genes and argue that it may play a more significant role in the evolutionary diversification of reproductive genes than previously recognized. We advocate for a re-evaluation of adaptive explanations for the rapid diversification of reproductive genes.

When mother knows best: A population genetic model of transgenerational versus intragenerational plasticity.

Many organisms exhibit phenotypic plasticity; producing alternate phenotypes depending on the environment. Individuals can be plastic (intragenerational or direct plasticity), wherein individuals of the same genotype produce different phenotypes in response to the environments they experience. Alternatively, an individual's phenotype may be under the control of its parents, usually the mother (transgenerational or indirect plasticity), so that mother's genotype determines the phenotype produced by a given genotype of her offspring. Under what conditions does plasticity evolve to have intragenerational as opposed to transgenerational genetic control? To explore this question, we present a population genetic model for the evolution of transgenerational and intragenerational plasticity. We hypothesize that the capacity for plasticity incurs a fitness cost, which is borne either by the individual developing the plastic phenotype or by its mother. We also hypothesize that individuals are imperfect predictors of future environments and their capacity for plasticity can lead them occasionally to make a low-fitness phenotype for a particular environment. When the cost, benefit and error parameters are equal, we show that there is no evolutionary advantage to intragenerational over transgenerational plasticity, although the rate of evolution of transgenerational plasticity is half the rate for intragenerational plasticity, as predicted by theory on indirect genetic effects. We find that transgenerational plasticity evolves when mothers are better predictors of future environments than offspring or when the fitness cost of the capacity for plasticity is more readily borne by a mother than by her developing offspring. We discuss different natural systems with either direct intragenerational plasticity or indirect transgenerational plasticity and find a pattern qualitatively in accord with the predictions of our model.

50-year anniversary of Lloyd's "mean crowding": Ideas on patchy distributions.

This year marks the 50th anniversary of Monte B. Lloyd's "Mean Crowding" (1967) paper, in which he introduced a metric that accounts for an individual's experience of conspecific density. Mean crowding allows ecologists to measure the degree of spatial aggregation of individuals in a manner relevant to intraspecific competition for resources. We take the concept of mean crowding a step beyond its most common usage and that it has a mathematical relationship to many of the most important concepts in ecology and evolutionary biology. Mean crowding, a first-order approximation of the degree of nonrandomness in a distribution, can function as a powerful heuristic that can unify concepts across disciplines in a more general way that Lloyd originally envisioned.

Response to Comment on "Precipitation drives global variation in natural selection".

The comment by Myers-Smith and Myers focuses on three main points: (i) the lack of a mechanistic explanation for climate-selection relationships, (ii) the appropriateness of the climate data used in our analysis, and (iii) our focus on estimating climate-selection relationships across (rather than within) taxonomic groups. We address these critiques in our response.

The promise and peril of CRISPR gene drives: Genetic variation and inbreeding may impede the propagation of gene drives based on the CRISPR genome editing technology.

Gene drives are selfish genetic elements that use a variety of mechanisms to ensure they are transmitted to subsequent generations at greater than expected frequencies. Synthetic gene drives based on the clustered regularly interspersed palindromic repeats (CRISPR) genome editing system have been proposed as a way to alter the genetic characteristics of natural populations of organisms relevant to the goals of public health, conservation, and agriculture. Here, we review the principles and potential applications of CRISPR drives, as well as means proposed to prevent their uncontrolled spread. We also focus on recent work suggesting that factors such as natural genetic variation and inbreeding may represent substantial impediments to the propagation of CRISPR drives.

What Are the Environmental Determinants of Phenotypic Selection? A Meta-analysis of Experimental Studies.

Although many selection estimates have been published, the environmental factors that cause selection to vary in space and time have rarely been identified. One way to identify these factors is by experimentally manipulating the environment and measuring selection in each treatment. We compiled and analyzed selection estimates from experimental studies. First, we tested whether the effect of manipulating the environment on selection gradients depends on taxon, trait type, or fitness component. We found that the effect of manipulating the environment was larger when selection was measured on life-history traits or via survival. Second, we tested two predictions about the environmental factors that cause variation in selection. We found support for the prediction that variation in selection is more likely to be caused by environmental factors that have a large effect on mean fitness but not for the prediction that variation is more likely to be caused by biotic factors. Third, we compared selection gradients from experimental and observational studies. We found that selection varied more among treatments in experimental studies than among spatial and temporal replicates in observational studies, suggesting that experimental studies can detect relationships between environmental factors and selection that would not be apparent in observational studies.

CRISPR/Cas9 gene drives in genetically variable and nonrandomly mating wild populations.

Synthetic gene drives based on CRISPR/Cas9 have the potential to control, alter, or suppress populations of crop pests and disease vectors, but it is unclear how they will function in wild populations. Using genetic data from four populations of the flour beetle Tribolium castaneum, we show that most populations harbor genetic variants in Cas9 target sites, some of which would render them immune to drive (ITD). We show that even a rare ITD allele can reduce or eliminate the efficacy of a CRISPR/Cas9-based synthetic gene drive. This effect is equivalent to and accentuated by mild inbreeding, which is a characteristic of many disease-vectoring arthropods. We conclude that designing such drives will require characterization of genetic variability and the mating system within and among targeted populations.

Precipitation drives global variation in natural selection.

Climate change has the potential to affect the ecology and evolution of every species on Earth. Although the ecological consequences of climate change are increasingly well documented, the effects of climate on the key evolutionary process driving adaptation-natural selection-are largely unknown. We report that aspects of precipitation and potential evapotranspiration, along with the North Atlantic Oscillation, predicted variation in selection across plant and animal populations throughout many terrestrial biomes, whereas temperature explained little variation. By showing that selection was influenced by climate variation, our results indicate that climate change may cause widespread alterations in selection regimes, potentially shifting evolutionary trajectories at a global scale.

Nuclear-mitochondrial epistasis: a gene's eye view of genomic conflict.

We use population genetic models to investigate the cooperative and conflicting synergistic fitness effects between genes from the nucleus and the mitochondrion. By varying fitness parameters, we examine the scope for conflict relative to cooperation among genomes and the utility of the "gene's eye view" analytical approach, which is based on the marginal average fitness of specific alleles. Because sexual conflict can maintain polymorphism of mitochondrial haplotypes, we can explore two types of evolutionary conflict (genomic and sexual) with one epistatic model. We find that the nuclear genetic architecture (autosomal, X-linked, or Z-linked) and the mating system change the regions of parameter space corresponding to the evolution by sexual and genomic conflict. For all models, regardless of conflict or cooperation, we find that population mean fitness increases monotonically as evolution proceeds. Moreover, we find that the process of gene frequency change with positive, synergistic fitnesses is self-accelerating, as the success of an allele in one genome or in one sex increases the frequency of the interacting allele upon which its success depends. This results in runaway evolutionary dynamics caused by the positive intergenomic associations generated by selection. An inbreeding mating system tends to further accelerate these runaway dynamics because it maintains favorable host-symbiont or male-female gene combinations. In contrast, where conflict predominates, the success of an allele in one genome or in one sex diminishes the frequency of the corresponding allele in the other, resulting in considerably slower evolutionary dynamics. The rate of change of mean fitness is also much faster with positive, synergistic fitnesses and much slower where conflict is predominant. Consequently, selection rapidly fixes cooperative gene combinations, while leaving behind a slowing evolving residue of conflicting gene combinations at mutation-selection balance. We discuss how an emphasis on marginal fitness averages may obscure the interdependence of allelic fitness across genomes, making the evolutionary trajectories appear independent of one another when they are not.

The effects of temperature, relative humidity, light, and resource quality on flight initiation in the red flour beetle, Tribolium castaneum.

We investigated the environmental conditions that induce a flight response in the red flour beetle, Tribolium castaneum Herbst (Coleoptera: Tenebrionidae), including resource quality, temperature, relative humidity, and light. Over 72-h trial periods, we observed the proportion of individuals emigrating by flight to range from 0.0 in extreme heat or cold to 0.82 with starvation. Resource quality, presence of a light source, and temperature all directly influenced the initiation of the flight response. We did not detect any effect of relative humidity or sudden change in temperature on the incidence of flight. We discuss our findings in the context of Tribolium ecology and evolution.

Evolutionary genetics of maternal effects.

Maternal genetic effects (MGEs), where genes expressed by mothers affect the phenotype of their offspring, are important sources of phenotypic diversity in a myriad of organisms. We use a single-locus model to examine how MGEs contribute patterns of heritable and nonheritable variation and influence evolutionary dynamics in randomly mating and inbreeding populations. We elucidate the influence of MGEs by examining the offspring genotype-phenotype relationship, which determines how MGEs affect evolutionary dynamics in response to selection on offspring phenotypes. This approach reveals important results that are not apparent from classic quantitative genetic treatments of MGEs. We show that additive and dominance MGEs make different contributions to evolutionary dynamics and patterns of variation, which are differentially affected by inbreeding. Dominance MGEs make the offspring genotype-phenotype relationship frequency dependent, resulting in the appearance of negative frequency-dependent selection, while additive MGEs contribute a component of parent-of-origin dependent variation. Inbreeding amplifies the contribution of MGEs to the additive genetic variance and, therefore enhances their evolutionary response. Considering evolutionary dynamics of allele frequency change on an adaptive landscape, we show that this landscape differs from the mean fitness surface, and therefore, under some condition, fitness peaks can exist but not be "available" to the evolving population.