Divergent patterns of integration and reduced constraint in the human hip and the origins of bipedalism

When compared to other hominids--great apes including humans--the human pelvis reveals a fundamental reorganization of bony morphology comprised of multiple trait-level changes, many of which are associated with bipedal locomotion. Establishing how patterns of integration--correlations and covariances among traits--within the pelvis have evolved in concert with morphology is essential to explaining this evolutionary transition because integration may facilitate or constrain morphological evolution. Here, we show that the human hip bone has significantly lower levels of integration and constraint overall when compared to other hominids, that the focus of these changes is on traits hypothesized to play major functional roles in bipedalism, and we provide evidence that the human hip was reintegrated in a pattern distinct from other members of this group. Additionally, the evolutionary transition from a nonhuman great ape-like to human hip bone morphology was significantly easier to traverse using the human integration pattern in each comparison, which suggests hominin patterns may have evolved to facilitate this transition. Our results suggest natural selection for bipedalism broke down earlier hominid integration patterns, allowing relevant traits to respond to separate selection pressures to a greater extent than was previously possible, and reintegrated traits in a way that could have facilitated evolution along the vector specifying ancestral hominid and hominin morphological differences.     

Sperm competition and mate harm unresponsive to male-limited selection in Drosophila: an evolving genetic architecture under domestication

Earlier research by W.R. Rice showed that experimentally limiting gene expression to males in Drosophila melanogaster leads to the rapid evolution of higher fitness. Using a similar male-limited (ML) selection protocol, we confirmed that result and showed that eliminating intralocus sexual conflict results in a comprehensive remodeling of the sexually dimorphic phenotype. However, despite starting from laboratory-evolved descendants of the same founder population used in earlier work, we found no evidence for the increased performance in sperm competition or increased postmating harm to females previously demonstrated. We employed females with both ancestral population genotypes and those of the special "clone generator" females used in ML selection. Despite strong differences in sperm storage or usage patterns between these females, there was no detectable adaptation by males to the specific female stock used in the selection protocol. The lack of evolution of postcopulatory traits suggests either that requisite genetic variation was eliminated by long-term domestication of the base population, or that complex male-by-male-by-female interactions made these traits unavailable to selection. The different evolutionary outcomes produced by two very similar experiments done at different time points underscores the potential for cryptic adaptation in the laboratory to qualitatively affect inferences made using quantitative genetic methodologies.     

FISHER'S GEOMETRIC MODEL WITH A MOVING OPTIMUM

Fisher's geometric model has been widely used to study the effects of pleiotropy and organismic complexity on phenotypic adaptation. Here, we study a version of Fisher's model in which a population adapts to a gradually moving optimum. Key parameters are the rate of environmental change, the dimensionality of phenotype space, and the patterns of mutational and selectional correlations. We focus on the distribution of adaptive substitutions, that is, the multivariate distribution of the phenotypic effects of fixed beneficial mutations. Our main results are based on an “adaptive‐walk approximation,” which is checked against individual‐based simulations. We find that (1) the distribution of adaptive substitutions is strongly affected by the ecological dynamics and largely depends on a single composite parameter γ, which scales the rate of environmental change by the “adaptive potential” of the population; (2) the distribution of adaptive substitution reflects the shape of the fitness landscape if the environment changes slowly, whereas it mirrors the distribution of new mutations if the environment changes fast; (3) in contrast to classical models of adaptation assuming a constant optimum, with a moving optimum, more complex organisms evolve via larger adaptive steps.     

Evolution in response to social selection: the importance of interactive effects of traits on fitness

Social interactions have a powerful effect on the evolutionary process. Recent attempts to synthesize models of social selection with equations for indirect genetic effects (McGlothlin et al. 2010) provide a broad theoretical base from which to study selection and evolutionary response in the context of social interactions. However, this framework concludes that social selection will lead to evolution only if the traits carried by social partners are nonrandomly associated. I suggest this conclusion is incomplete, and that traits that do not covary between social partners can nevertheless lead to evolution via interactive effects on fitness. Such effects occur when there are functional interactions between traits, and as an example I use the interplay in water striders (Gerridae) between grasping appendages carried by males and spines by females. Functional interactive effects between traits can be incorporated into both the equations for social selection and the general model of social evolution proposed by McGlothlin et al. These expanded equations would accommodate adaptive coevolution in social interactions, integrate the quantitative genetic approach to social evolution with game theoretical approaches, and stimulate some new questions about the process of social evolution.     

Ecomorphological specialization leads to loss of evolvability in primate limbs*

Primate limb morphology is often described as either generalized, that is, suited to a range of locomotor and positional behaviors, or specialized for unique locomotor behaviors such as brachiation or bipedalism. The evolution of highly specialized limb morphology may result in loss of evolvability, that is, in a decreased capacity of the locomotor skeleton to evolve in response to selection towards alternative ecomorphological niches. Using evolutionary simulations, I show that the highly specialized limb anatomy of hominoids is associated with a significant loss of evolvability, defined as the number of generations to reach alternative adaptive peaks, and in parallel an increased risk of extinction, particularly in simulated evolution toward generalized quadrupedal limb proportions. Loss of evolvability in apes and humans correlates with three factors: (1) decreased correlation among limb bone lengths (i.e., integration), which slows the rate of change along lines of least evolutionary resistance; (2) limb specialization, which places apes and humans in relatively remote areas of morphospace; and (3) increased skeletal size as a proxy for body size. Thus, locomotor over-specialization can lead to evolutionary dead-ends that significantly increase the probability of hominoid populations going extinct before evolving new adaptive morphologies.     

Conservative coevolution of Müllerian mimicry in a group of rift lake catfish

Biological mimicry has long been viewed as a powerful example of natural selection's ability to drive phenotypic evolution, although continuing debates surround the mechanisms leading to its development and the nature of these mimetic relationships. Müllerian mimicry, in which unpalatable species derive a mutual selective benefit through evolved phenotypic similarity, has alternatively been proposed to evolve through either a two-step process initiated by a large mutational change, or through continuous gradual evolution toward a common aposematic phenotype. I exposed a model predatory fish species to two species of endemic Lake Tanganyikan Synodontis to provide evidence for aposematism and the presence of Müllerian mimicry in these species. Predators quickly became conditioned to avoid the venomous catfish and did not discriminate between the two species when they were switched, supporting a hypothesis of functional Müllerian mimicry in this group of similarly colored fish. Ancestral state reconstructions and statistical comparisons of color pattern divergence in Tanganyikan Synodontis indicate that Müllerian mimicry in these catfish has developed through diversification of an aposematic common ancestor with subsequent conservative mutualistic coevolution among its daughter lineages, rather than advergent evolution of a mimic toward a nonrelated model, as assumed by widely accepted models of Müllerian mimicry evolution.     

The length of adaptive walks is insensitive to starting fitness in Aspergillus nidulans

Adaptation involves the successive substitution of beneficial mutations by selection, a process known as an adaptive walk. Gradualist models of adaptation, which assume that all mutations are small relative to the distance to a fitness optimum, predict that adaptive walks should be longer when the founding genotype is less well adapted. More recent work modeling adaptation as a sequence of moves in phenotype or genotype space predicts, by contrast, much shorter adaptive walks irrespective of the fitness of the founding genotype. Here, we provide what is, to the best of our knowledge, the first direct test of these alternative models, measuring the length of adaptive walks in evolving lineages of fungus that differ initially in fitness. Contrary to the gradualist view, we show that the length of adaptive walks in the fungus Aspergillus nidulans is insensitive to starting fitness and involves just two mutations on average. This arises because poorly adapted populations tend to fix mutations of larger average effect than those of better-adapted populations. Our results suggest that the length of adaptive walks may be independent of the fitness of the founding genotype and, moreover, that poorly adapted populations can quickly adapt to novel environments.     

SELECTION BIASES THE PREVALENCE AND TYPE OF EPISTASIS ALONG ADAPTIVE TRAJECTORIES

The contribution to an organism's phenotype from one genetic locus may depend upon the status of other loci. Such epistatic interactions among loci are now recognized as fundamental to shaping the process of adaptation in evolving populations. Although little is known about the structure of epistasis in most organisms, recent experiments with bacterial populations have concluded that antagonistic interactions abound and tend to deaccelerate the pace of adaptation over time. Here, we use the NK model of fitness landscapes to examine how natural selection biases the mutations that substitute during evolution based on their epistatic interactions. We find that, even when beneficial mutations are rare, these biases are strong and change substantially throughout the course of adaptation. In particular, epistasis is less prevalent than the neutral expectation early in adaptation and much more prevalent later, with a concomitant shift from predominantly antagonistic interactions early in adaptation to synergistic and sign epistasis later in adaptation. We observe the same patterns when reanalyzing data from a recent microbial evolution experiment. These results show that when the order of substitutions is not known, standard methods of analysis may suggest that epistasis retards adaptation when in fact it accelerates it.     

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.     

Robustness to noise in gene expression evolves despite epistatic constraints in a model of gene networks

Stochastic noise in gene expression causes variation in the development of phenotypes, making such noise a potential target of stabilizing selection. Here, we develop a new simulation model of gene networks to study the adaptive landscape underlying the evolution of robustness to noise. We find that epistatic interactions between the determinants of the expression of a gene and its downstream effect impose significant constraints on evolution, but these interactions do allow the gradual evolution of increased robustness. Despite strong sign epistasis, adaptation rarely proceeds via deleterious intermediate steps, but instead occurs primarily through small beneficial mutations. A simple mathematical model captures the relevant features of the single‐gene fitness landscape and explains counterintuitive patterns, such as a correlation between the mean and standard deviation of phenotypes. In more complex networks, mutations in regulatory regions provide evolutionary pathways to increased robustness. These results chart the constraints and possibilities of adaptation to reduce expression noise and demonstrate the potential of a novel modeling framework for gene networks.     

Divergence of Eurosta solidaginis in response to host plant variation and natural enemies

We tested the hypothesis that forest and prairie populations of the gall-inducing fly, Eurosta solidaginis, have diverged in response to variation in selection by its host plant Solidago altissima, and its natural enemies. A reciprocal cross infection design experiment demonstrated that fly populations from the prairie and forest biomes had higher survival on local biome plants compared to foreign biome host plants. Flies from each biome also had an oviposition preference for their local plants. Each fly population induced galls of the size and shape found in their local biome on host plants from both biomes indicating a genetic basis to the differences in gall morphology. Solidago altissima from the prairie and forest biomes retained significant morphological differences in the common garden indicating that they are genetically differentiated, possibly at the subspecies level. The populations are partially reproductively isolated as a result of a combination of prezygotic isolation due to host-associated assortative mating, and postzygotic isolation due to low hybrid survival. We conclude that E. solidaginis is undergoing diversifying selection to adapt to differences between prairie and forest habitats.     

THE COEVOLUTION OF HUMAN HANDS AND FEET

Human hands and feet have longer, more robust first digits, and shorter lateral digits compared to African apes. These similarities are often assumed to be independently evolved adaptations for manipulative activities and bipedalism, respectively. However, hands and feet are serially homologous structures that share virtually identical developmental blueprints, raising the possibility that digital proportions coevolved in human hands and feet because of underlying developmental linkages that increase phenotypic covariation between them. Here we show that phenotypic covariation between serially homologous fingers and toes in Homo and Pan is not only higher than expected, it also causes these digits to evolve along highly parallel trajectories under episodes of simulated directional selection, even when selection pressures push their means in divergent directions. Further, our estimates of the selection pressures required to produce human‐like fingers and toes from an African ape‐like ancestor indicate that selection on the toes was substantially stronger, and likely led to parallel phenotypic changes in the hands. Our data support the hypothesis that human hands and feet coevolved, and suggest that the evolution of long robust big toes and short lateral toes for bipedalism led to changes in hominin fingers that may have facilitated the emergence of stone tool technology.     

Antagonism between sexual and natural selection in experimental populations of Saccharomyces cerevisiae

Trade-offs between life-history components are a central concept of evolution and ecology. Sexual and natural selection seem particularly apt to impose antagonistic selective pressures. When sex is not integrated into reproduction, as in Saccharomyces cerevisiae, natural selection can impair or even eliminate it. In this study, a genetic trade-off between the sexual and asexual phases of the yeast life cycle was suggested by sharp declines in the mating and sporulation abilities of unrelated genotypes that were propagated asexually in minimal growth medium and in mice. When sexual selection was applied to populations that had previously evolved asexually, sexual fitness increased but asexual fitness declined. No such negative correlation was observed when sexual selection was applied to an ancestral strain: sexual and asexual fitness both increased. Thus, evolutionary history affected the evolution of genetic correlations, as fitness increases in a population already well adapted to the environment were more likely to come at the expense of sexual functions.     

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

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

DIFFERENTIAL DOMINANCE OF PLEIOTROPIC LOCI FOR MOUSE SKELETAL TRAITS

The term "differential dominance" describes the situation in which the dominance effects at a pleiotropic locus vary between traits. Directional selection on the phenotype can lead to balancing selection on differentially dominant pleiotropic loci. Even without any individual overdominant traits, some linear combination of traits will display overdominance at a locus displaying differential dominance. Multivariate overdominance may be responsible, in part, for high levels of heterozygosity found in natural populations. We examine differential dominance of 70 mouse skeletal traits at 92 quantitative trait loci (QTL). Our results indicate moderate to strong additive and dominance effects at pleiotropic loci, low levels of individual-trait overdominance, and universal multivariate overdominance. Multivariate overdominance affects a range of 6% to 81% of morphospace, with a mean of 32%. Multivariate overdominance tends to affect a larger percentage of morphospace at pleiotropic loci with antagonistic effects on multiple traits (42%). We conclude that multivariate overdominance is common and should be considered in models and in empirical studies of the role of genetic variation in evolvability.     

A MODULAR FRAMEWORK CHARACTERIZES MICRO‐ AND MACROEVOLUTION OF OLD WORLD MONKEY DENTITIONS

The study of modularity can provide a foundation for integrating development into studies of phenotypic evolution. The dentition is an ideal phenotype for this as it is developmentally relatively simple, adaptively highly significant, and evolutionarily tractable through the fossil record. Here, we use phenotypic variation in the dentition to test a hypothesis about genetic modularity. Quantitative genetic analysis of size variation in the baboon dentition indicates a genetic modular framework corresponding to tooth type categories. We analyzed covariation within the dentitions of six species of Old World monkeys (OWMs) to assess the macroevolutionary extent of this framework: first by estimating variance–covariance matrices of linear tooth size, and second by performing a geometric morphometric (GM) analysis of tooth row shape. For both size and shape, we observe across OWMs a framework of anterior and postcanine modules, as well as submodularity between the molars and premolars. Our results of modularity by tooth type suggest that adult variation in the OWM dentition is influenced by early developmental processes such as odontogenesis and jaw patterning. This study presents a comparison of genotypic modules to phenotypic modules, which can be used to better understand their action across evolutionary time scales.     

Altitudinal divergence in maternal thermoregulatory behaviour may be driven by differences in selection on offspring survival in a viviparous lizard

Plastic responses to temperature during embryonic development are common in ectotherms, but their evolutionary relevance is poorly understood. Using a combination of field and laboratory approaches, we demonstrate altitudinal divergence in the strength of effects of maternal thermal opportunity on offspring birth date and body mass in a live-bearing lizard (Niveoscincus ocellatus). Poor thermal opportunity decreased birth weight at low altitudes where selection on body mass was negligible. In contrast, there was no effect of maternal thermal opportunity on body mass at high altitudes where natural selection favored heavy offspring. The weaker effect of poor maternal thermal opportunity on offspring development at high altitude was accompanied by a more active thermoregulation and higher body temperature in highland females. This may suggest that passive effects of temperature on embryonic development have resulted in evolution of adaptive behavioral compensation for poor thermal opportunity at high altitudes, but that direct effects of maternal thermal environment are maintained at low altitudes because they are not selected against. More generally, we suggest that phenotypic effects of maternal thermal opportunity or incubation temperature in reptiles will most commonly reflect weak selection for canalization or selection on maternal strategies rather than adaptive plasticity to match postnatal environments.     

FISHER'S GEOMETRIC MODEL OF ADAPTATION MEETS THE FUNCTIONAL SYNTHESIS: DATA ON PAIRWISE EPISTASIS FOR FITNESS YIELDS INSIGHTS INTO THE SHAPE AND SIZE OF PHENOTYPE SPACE

The functional synthesis uses experimental methods from molecular biology, biochemistry and structural biology to decompose evolutionarily important mutations into their more proximal mechanistic determinants. However these methods are technically challenging and expensive. Noting strong formal parallels between R.A. Fisher's geometric model of adaptation and a recent model for the phenotypic basis of protein evolution, we sought to use the former to make inferences into the latter using data on pairwise fitness epistasis between mutations. We present an analytic framework for classifying pairs of mutations with respect to similarity of underlying mechanism on this basis, and also show that these data can yield an estimate of the number of mutationally labile phenotypes underlying fitness effects. We use computer simulations to explore the robustness of our approach to violations of analytic assumptions and analyze several recently published datasets. This work provides a theoretical complement to the functional synthesis as well as a novel test of Fisher's geometric model.     

SIZE AS A LINE OF LEAST RESISTANCE II: DIRECT SELECTION ON SIZE OR CORRELATED RESPONSE DUE TO CONSTRAINTS?

Evolutionary change in New World Monkey (NWM) skulls occurred primarily along the line of least resistance defined by size (including allometric) variation ( g_max ). Although the direction of evolution was aligned with this axis, it was not clear whether this macroevolutionary pattern results from the conservation of within population genetic covariance patterns (long‐term constraint) or long‐term selection along a size dimension, or whether both, constraints and selection, were inextricably involved. Furthermore, G ‐matrix stability can also be a consequence of selection, which implies that both, constraints embodied in g_max and evolutionary changes observed on the trait averages, would be influenced by selection. Here, we describe a combination of approaches that allows one to test whether any particular instance of size evolution is a correlated by‐product due to constraints ( g_max ) or is due to direct selection on size and apply it to NWM lineages as a case study. The approach is based on comparing the direction and amount of evolutionary change produced by two different simulated sets of net‐selection gradients ( β ), a size (isometric and allometric size) and a nonsize set. Using this approach it is possible to distinguish between the two hypotheses (indirect size evolution due to constraints or direct selection on size), because although both may produce an evolutionary response aligned with g_max , the amount of change produced by random selection operating through the variance/covariance patterns (constraints hypothesis) will be much smaller than that produced by selection on size (selection hypothesis). Furthermore, the alignment of simulated evolutionary changes with g_max when selection is not on size is not as tight as when selection is actually on size, allowing a statistical test of whether a particular observed case of evolution along the line of least resistance is the result of selection along it or not. Also, with matrix diagonalization (principal components [PC]) it is possible to calculate directly the net‐selection gradient on size alone (first PC [PC1]) by dividing the amount of phenotypic difference between any two populations by the amount of variation in PC1, which allows one to benchmark whether selection was on size or not.     

ALGAE FOR BIOFUEL: WILL THE EVOLUTION OF WEEDS LIMIT THE ENTERPRISE?

Algae hold promise as a source of biofuel. Yet, the manner in which algae are most efficiently propagated and harvested is different from that used in traditional agriculture. In theory, algae can be grown in continuous culture and harvested frequently to maintain high yields with a short turnaround time. However, the maintenance of the population in a state of continuous growth will likely impose selection for fast growth, possibly opposing the maintenance of lipid stores desirable for fuel. Any harvesting that removes a subset of the population and leaves the survivors to establish the next generation may quickly select traits that escape harvesting. An understanding of these problems should help identify methods for retarding the evolution and enhancing biofuel production.