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.

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.

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.

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.

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.

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.

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.

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.

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.

Health service and medication use among veterans with persistent postconcussive symptoms.

Persistent postconcussive symptoms (PPCS) are noted when a series of cognitive, emotional, and somatosensory complaints persist for months after a concussion. Clinical management of PPCS can be challenging in the veteran population because of the nonspecific nature of symptoms and co-occurrence with affective disturbances such as posttraumatic stress disorder (PTSD) and chronic pain. In this study, we compared health service and medication use patterns in a sample of 421 veterans with PPCS with an age-matched cohort of case controls. The results suggest that the veterans with PPCS showed high rates of medical and mental health service utilization during a mean treatment period of 2 years. Although chronic pain commonly co-occurs with PPCS in veterans, service use and medication prescribing trends seem to have been influenced more by the presence of PTSD than chronic pain. Our findings reinforce the overlap among PPCS, PTSD, and chronic pain and demonstrate the complexity inherent in treating these conditions in veterans.

Selection gradients, the opportunity for selection, and the coefficient of determination.

Abstract We derive the relationship between R(2) (the coefficient of determination), selection gradients, and the opportunity for selection for univariate and multivariate cases. Our main result is to show that the portion of the opportunity for selection that is caused by variation for any trait is equal to the product of its selection gradient and its selection differential. This relationship is a corollary of the first and second fundamental theorems of natural selection, and it permits one to investigate the portions of the total opportunity for selection that are involved in directional selection, stabilizing (and diversifying) selection, and correlational selection, which is important to morphological integration. It also allows one to determine the fraction of fitness variation not explained by variation in measured phenotypes and therefore attributable to random (or, at least, unknown) influences. We apply our methods to a human data set to show how sex-specific mating success as a component of fitness variance can be decoupled from that owing to prereproductive mortality. By quantifying linear sources of sexual selection and quadratic sources of sexual selection, we illustrate that the former is stronger in males, while the latter is stronger in females.

Evolution of transmission mode in obligate symbionts.

BACKGROUND: A host obtains symbionts by horizontal transmission when infected from the environment or contagiously from other hosts in the same generation. In contrast, vertical transmission occurs when a host obtains its symbionts directly from its parents. Either vertical or horizontal transmission can sustain an association between a host and its symbiont. QUESTIONS: What evolutionary forces are necessary to evolve from an ancestral state of horizontal transmission to a derived state of vertical transmission? MATHEMATICAL METHODS: We explore a general model of fitness interaction, including both additive and epistatic effects, between host and symbiont genes. Recursion equations allow us to analyse the short-term behaviour of the model and to study long-term deterministic effects with numerical iterations. KEY ASSUMPTIONS: Obligate interaction between a symbiont and a single host species with genetically determined horizontal and vertical transmission. No free-living symbionts or uninfected hosts and each host is infected by only a single symbiont genetic lineage (no multiple infections). No population structure. CONCLUSIONS: Epistasis for fitness between host and symbiont genes, like that in a matching alleles model, is a necessary condition for the evolution of vertical from horizontal transmission. Stochastic individual-based simulations show that (1) mutation facilitates the switch to vertical transmission and (2) vertical transmission is a stable evolutionary endpoint for a matching alleles model.

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.

Identification of maternally-loaded RNA transcripts in unfertilized eggs of Tribolium castaneum.

BACKGROUND: Maternal RNAs play a critical role in early development. Variation in the diversity and levels of maternally derived gene transcripts may be central to the origin of phenotypic novelty -- a longstanding problem in evolution and development. By studying maternal transcriptomes within and between divergent species, a better understanding of the evolutionary forces acting on maternal RNA allocation is possible. RESULTS: We present the first maternal transcriptome of the red flour beetle, Tribolium castaneum. Using a tiled whole-genome microarray, we found that 58.2% of T. castaneum genes are maternally loaded into eggs. Comparison of known Drosophila melanogaster maternal genes to our results showed widespread conservation of maternal expression with T. castaneum. Additionally, we found that many genes previously reported as having sex or tissue specific expression in T. castaneum were also maternally loaded. Identification of such pleiotropy is vital for proper modeling and testing of evolutionary theory using empirical data. The microarray design also allowed the detection of 2315 and 4060 novel transcriptionally active regions greater in length than 100 bp in unfertilized and fertilized T. castaneum eggs, respectively. These transcriptionally active regions represent novel exons of potentially unknown genes for future study. CONCLUSIONS: Our results lay a foundation for utilizing T. castaneum as a model for understanding the role of maternal genes in evolution.

Detecting the molecular signature of social conflict: theory and a test with bacterial quorum sensing genes.

Extending social evolution theory to the molecular level opens the door to an unparalleled abundance of data and statistical tools for testing alternative hypotheses about the long-term evolutionary dynamics of cooperation and conflict. To this end, we take a collection of known sociality genes (bacterial quorum sensing [QS] genes), model their evolution in terms of patterns that are detectable using gene sequence data, and then test model predictions using available genetic data sets. Specifically, we test two alternative hypotheses of social conflict: (1) the "adaptive" hypothesis that cheaters are maintained in natural populations by frequency-dependent balancing selection as an evolutionarily stable strategy and (2) the "evolutionary null" hypothesis that cheaters are opposed by purifying kin selection yet exist transiently because of their recurrent introduction into populations by mutation (i.e., kin selection-mutation balance). We find that QS genes have elevated within- and among-species sequence variation, nonsignificant signatures of natural selection, and putatively small effect sizes of mutant alleles, all patterns predicted by our evolutionary null model but not by the stable cheater hypothesis. These empirical findings support our theoretical prediction that QS genes experience relaxed selection due to nonclonality of social groups, conditional expression, and the individual-level advantage enjoyed by cheaters. Furthermore, cheaters are evolutionarily transient, persisting in populations because of their recurrent introduction by mutation and not because they enjoy a frequency-dependent fitness advantage.

Toward a population genetic framework of developmental evolution: the costs, limits, and consequences of phenotypic plasticity.

Adaptive phenotypic plasticity allows organisms to cope with environmental variability, and yet, despite its adaptive significance, phenotypic plasticity is neither ubiquitous nor infinite. In this review, we merge developmental and population genetic perspectives to explore costs and limits on the evolution of plasticity. Specifically, we focus on the role of modularity in developmental genetic networks as a mechanism underlying phenotypic plasticity, and apply to it lessons learned from population genetic theory on the interplay between relaxed selection and mutation accumulation. We argue that the environmental specificity of gene expression and the associated reduction in pleiotropic constraints drive a fundamental tradeoff between the range of plasticity that can be accommodated and mutation accumulation in alternative developmental networks. This tradeoff has broad implications for understanding the origin and maintenance of plasticity and may contribute to a better understanding of the role of plasticity in the origin, diversification, and loss of phenotypic diversity.

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.