Spatial environmental variation can select for evolvability

Previous studies have shown that temporally fluctuating environments can create indirect selection for modifiers of evolvability. Here, we use a simple computational model to investigate whether spatially varying environments (multiple demes with limited migration among them, and a different, static selective optimum in each) can also create indirect selection for increased evolvability. The answer is surprisingly complicated. Spatial variation in the environment can sharply reduce the survival rate of migrants, because migrants may be maladapted to their new deme, relative to incumbents. The incumbent advantage can be removed by occasional extinctions in single demes. After all incumbents in a particular deme die, incoming migrants from other demes will, on average, be similarly maladapted to the new environment. This sets off a race to adapt rapidly. Over many extinction events, and the subsequent invasions by maladapted immigrants into a new environment, indirect selection for the ability to adapt rapidly, also known as high evolvability, may result.     

Phenotypic variability can promote the evolution of adaptive plasticity by reducing the stringency of natural selection

Adaptive phenotypic plasticity is a potent but not ubiquitous solution to environmental heterogeneity, driving interest in what factors promote and limit its evolution. Here, a novel computational model representing stochastic information flow in development is used to explore evolution from a constitutive phenotype to an adaptively plastic response. Results show that populations tend to evolve robustness to developmental stochasticity, but that this evolved robustness limits evolvability; specifically, robust genotypes have less ability to evolve adaptive plasticity when presented with a mix of both the ancestral environment and a new environment. Analytic calculations and computational experiments confirm that this constraint occurs when the initial mutational steps towards plasticity are pleiotropic, such that mutant fitnesses decline in the environment to which their parents are well‐adapted. Greater phenotypic variability improves evolvability in the model by lessening this decline as well as by improving the fitness of partial adaptations to the new environment. By making initial plastic mutations more palatable to natural selection, phenotypic variability can increase the evolvability of an innovative, plastic response without improving evolvability to simpler challenges such as a shifted optimum in a single environment. Populations that evolved robustness by negative feedback between the trait and its rate of change show a particularly strong constraining effect on the evolvability of plasticity, revealing another mechanism by which evolutionary history can limit later innovation. These results document a novel mechanism by which weakening selection could actually stimulate the evolution of a major innovation.     

Evolvability of the Primate Pelvic Girdle

The ilium and ischiopubic bones of the pelvis arise from different regulatory pathways, and as a result, they may be modular in their organization such that features on one bone may be morphologically integrated with each other, but not with features on the other pelvic bone. Modularity at this gross level of organization can act to increase the ability of these structures to respond to selection pressures (i.e., their evolvability). Furthermore, recent work has suggested that the evolution of the human pelvis was facilitated by low levels of integration and high levels of evolvability relative to other African apes. However, the extent of morphological integration and modularity of the bones of the pelvic girdle is not well understood, especially across the entire order of primates. Therefore, the hypothesis that the ilium and ischiopubis constitute separate modules was tested using three-dimensional landmark data that were collected from 752 pelves from 35 primate species. In addition, the hypothesis that the human pelvis demonstrates greatest evolvability was tested by comparing it to all other primates. The results demonstrate that regardless of phylogeny and locomotor function, the primate pelvis as a whole is characterized by low levels of overall integration and high levels of evolvability. In addition, the results support the developmental hypothesis of separate ilium and ischiopubis modular units. Finally, all primates, including humans, apparently share a common pattern of integration, modularity, and evolvability in the pelvis.     

Local evolvability of statistically neutral GasNet robot controllers

In this paper we introduce and apply the concept of local evolvability to investigate the behaviour of populations during evolutionary search. We focus on the evolution of GasNet neural network controllers for a robotic visual discrimination problem, showing that the evolutionary process undergoes long neutral fitness epochs. We show that the local evolvability properties of the search space surrounding a group of statistically neutral solutions do vary across the course of an evolutionary run, especially during periods of population takeover. However, once takeover is complete there is no evidence for further increase in local evolvability across fitness epochs. We also see no evidence for the neutral evolution of increased solution robustness, but show that this may be due to the ability of evolutionary algorithms to focus search on volumes of the fitness landscape with above average robustness.     

Predicting evolutionary potential: A numerical test of evolvability measures

Despite sophisticated mathematical models, the theory of microevolution is mostly treated as a qualitative rather than a quantitative tool. Numerical measures of selection, constraints, and evolutionary potential are often too loosely connected to theory to provide operational predictions of the response to selection. In this paper, we study the ability of a set of operational measures of evolvability and constraint to predict short‐term selection responses generated by individual‐based simulations. We focus on the effects of selective constraints under which the response in one trait is impeded by stabilizing selection on other traits. The conditional evolvability is a measure of evolutionary potential explicitly developed for this situation. We show that the conditional evolvability successfully predicts rates of evolution in an equilibrium situation, and further that these equilibria are reached with characteristic times that are inversely proportional to the fitness load generated by the constraining characters. Overall, we find that evolvabilities and conditional evolvabilities bracket responses to selection, and that they together can be used to quantify evolutionary potential on time scales where the G‐matrix remains relatively constant.     

Complex Adaptations Can Drive the Evolution of the Capacitor [PSI +], Even with Realistic Rates of Yeast Sex

The [PSI⁺] prion may enhance evolvability by revealing previously cryptic genetic variation, but it is unclear whether such evolvability properties could be favored by natural selection. Sex inhibits the evolution of other putative evolvability mechanisms, such as mutator alleles. This paper explores whether sex also prevents natural selection from favoring modifier alleles that facilitate [PSI⁺] formation. Sex may permit the spread of “cheater” alleles that acquire the benefits of [PSI⁺] through mating without incurring the cost of producing [PSI⁺] at times when it is not adaptive. Using recent quantitative estimates of the frequency of sex in Saccharomyces paradoxus, we calculate that natural selection for evolvability can drive the evolution of the [PSI⁺] system, so long as yeast populations occasionally require complex adaptations involving synergistic epistasis between two loci. If adaptations are always simple and require substitution at only a single locus, then the [PSI⁺] system is not favored by natural selection. Obligate sex might inhibit the evolution of [PSI⁺]-like systems in other species.     

Survivability is more fundamental than evolvability

For a lineage to survive over long time periods, it must sometimes change. This has given rise to the term evolvability, meaning the tendency to produce adaptive variation. One lineage may be superior to another in terms of its current standing variation, or it may tend to produce more adaptive variation. However, evolutionary outcomes depend on more than standing variation and produced adaptive variation: deleterious variation also matters. Evolvability, as most commonly interpreted, is not predictive of evolutionary outcomes. Here, we define a predictive measure of the evolutionary success of a lineage that we call the k-survivability, defined as the probability that the lineage avoids extinction for k generations. We estimate the k-survivability using multiple experimental replicates. Because we measure evolutionary outcomes, the initial standing variation, the full spectrum of generated variation, and the heritability of that variation are all incorporated. Survivability also accounts for the decreased joint likelihood of extinction of sub-lineages when they 1) disperse in space, or 2) diversify in lifestyle. We illustrate measurement of survivability with in silico models, and suggest that it may also be measured in vivo using multiple longitudinal replicates. The k-survivability is a metric that enables the quantitative study of, for example, the evolution of 1) mutation rates, 2) dispersal mechanisms, 3) the genotype-phenotype map, and 4) sexual reproduction, in temporally and spatially fluctuating environments. Although these disparate phenomena evolve by well-understood microevolutionary rules, they are also subject to the macroevolutionary constraint of long-term survivability.     

Genetic constraints predict evolutionary divergence in Dalechampia blossoms

If genetic constraints are important, then rates and direction of evolution should be related to trait evolvability. Here we use recently developed measures of evolvability to test the genetic constraint hypothesis with quantitative genetic data on floral morphology from the Neotropical vine Dalechampia scandens (Euphorbiaceae). These measures were compared against rates of evolution and patterns of divergence among 24 populations in two species in the D. scandens species complex. We found clear evidence for genetic constraints, particularly among traits that were tightly phenotypically integrated. This relationship between evolvability and evolutionary divergence is puzzling, because the estimated evolvabilities seem too large to constitute real constraints. We suggest that this paradox can be explained by a combination of weak stabilizing selection around moving adaptive optima and small realized evolvabilities relative to the observed additive genetic variance.     

Complex Adaptations Can Drive the Evolution of the Capacitor [PSI+], Even with Realistic Rates of Yeast Sex

The [PSI⁺] prion may enhance evolvability by revealing previously cryptic genetic variation, but it is unclear whether such evolvability properties could be favored by natural selection. Sex inhibits the evolution of other putative evolvability mechanisms, such as mutator alleles. This paper explores whether sex also prevents natural selection from favoring modifier alleles that facilitate [PSI⁺] formation. Sex may permit the spread of “cheater” alleles that acquire the benefits of [PSI⁺] through mating without incurring the cost of producing [PSI⁺] at times when it is not adaptive. Using recent quantitative estimates of the frequency of sex in Saccharomyces paradoxus, we calculate that natural selection for evolvability can drive the evolution of the [PSI⁺] system, so long as yeast populations occasionally require complex adaptations involving synergistic epistasis between two loci. If adaptations are always simple and require substitution at only a single locus, then the [PSI⁺] system is not favored by natural selection. Obligate sex might inhibit the evolution of [PSI⁺]-like systems in other species.     

Biological hierarchies and the nature of extinction

Hierarchy theory recognises that ecological and evolutionary units occur in a nested and interconnected hierarchical system, with cascading effects occurring between hierarchical levels. Different biological disciplines have routinely come into conflict over the primacy of different forcing mechanisms behind evolutionary and ecological change. These disconnects arise partly from differences in perspective (with some researchers favouring ecological forcing mechanisms while others favour developmental/historical mechanisms), as well as differences in the temporal framework in which workers operate. In particular, long‐term palaeontological data often show that large‐scale (macro) patterns of evolution are predominantly dictated by shifts in the abiotic environment, while short‐term (micro) modern biological studies stress the importance of biotic interactions. We propose that thinking about ecological and evolutionary interactions in a hierarchical framework is a fruitful way to resolve these conflicts. Hierarchy theory suggests that changes occurring at lower hierarchical levels can have unexpected, complex effects at higher scales due to emergent interactions between simple systems. In this way, patterns occurring on short‐ and long‐term time scales are equally valid, as changes that are driven from lower levels will manifest in different forms at higher levels. We propose that the dual hierarchy framework fits well with our current understanding of evolutionary and ecological theory. Furthermore, we describe how this framework can be used to understand major extinction events better. Multi‐generational attritional loss of reproductive fitness (MALF) has recently been proposed as the primary mechanism behind extinction events, whereby extinction is explainable solely through processes that result in extirpation of populations through a shutdown of reproduction. While not necessarily explicit, the push to explain extinction through solely population‐level dynamics could be used to suggest that environmentally mediated patterns of extinction or slowed speciation across geological time are largely artefacts of poor preservation or a coarse temporal scale. We demonstrate how MALF fits into a hierarchical framework, showing that MALF can be a primary forcing mechanism at lower scales that still results in differential survivorship patterns at the species and clade level which vary depending upon the initial environmental forcing mechanism. Thus, even if MALF is the primary mechanism of extinction across all mass extinction events, the primary environmental cause of these events will still affect the system and result in differential responses. Therefore, patterns at both temporal scales are relevant.     

Evolution of evolvability in a developmental model

Evolvability, the ability of populations to adapt, can evolve through changes in the mechanisms determining genetic variation and in the processes of development. Here we construct and evolve a simple developmental model in which the pleiotropic effects of genes can evolve. We demonstrate that selection in a changing environment favors a specific pattern of variability, and that this favored pattern maximizes evolvability. Our analysis shows that mutant genotypes with higher evolvability are more likely to increase to fixation. We also show that populations of highly evolvable genotypes are much less likely to be invaded by mutants with lower evolvability, and that this dynamic primarily shapes evolvability. We examine several theoretical objections to the evolution of evolvability in light of this result. We also show that this result is robust to the presence or absence of recombination, and explore how nonrandom environmental change can select for a modular pattern of variability.     

The evolutionary dynamics of evolvability in a gene network model

Evolvability, the ability of populations to adapt, has recently emerged as a major unifying concept in biology. Although the study of evolvability offers new insights into many important biological questions, the conceptual bases of evolvability, and the mechanisms of its evolution, remain controversial. We used simulated evolution of a model of gene network dynamics to test the contentious hypothesis that natural selection can favour high evolvability, in particular in sexual populations. Our results conclusively demonstrate that fluctuating natural selection can increase the capacity of model gene networks to adapt to new environments. Detailed studies of the evolutionary dynamics of these networks establish a broad range of validity for this result and quantify the evolutionary forces responsible for changes in evolvability. Analysis of the genotype–phenotype map of these networks also reveals mechanisms connecting evolvability, genetic architecture and robustness. Our results suggest that the evolution of evolvability can have a pervasive influence on many aspects of organisms.     

Metabolic networks of Sodalis glossinidius: a systems biology approach to reductive evolution

Background

Genome reduction is a common evolutionary process affecting bacterial lineages that establish symbiotic or pathogenic associations with eukaryotic hosts. Such associations yield highly reduced genomes with greatly streamlined metabolic abilities shaped by the type of ecological association with the host. Sodalis glossinidius, the secondary endosymbiont of tsetse flies, represents one of the few complete genomes available of a bacterium at the initial stages of this process. In the present study, genome reduction is studied from a systems biology perspective through the reconstruction and functional analysis of genome-scale metabolic networks of S. glossinidius.

Results

The functional profile of ancestral and extant metabolic networks sheds light on the evolutionary events underlying transition to a host-dependent lifestyle. Meanwhile, reductive evolution simulations on the extant metabolic network can predict possible future evolution of S. glossinidius in the context of genome reduction. Finally, knockout simulations in different metabolic systems reveal a gradual decrease in network robustness to different mutational events for bacterial endosymbionts at different stages of the symbiotic association.

Conclusions

Stoichiometric analysis reveals few gene inactivation events whose effects on the functionality of S. glossinidius metabolic systems are drastic enough to account for the ecological transition from a free-living to host-dependent lifestyle. The decrease in network robustness across different metabolic systems may be associated with the progressive integration in the more stable environment provided by the insect host. Finally, reductive evolution simulations reveal the strong influence that external conditions exert on the evolvability of metabolic systems.     

Mate Familiarity Affects Pairing Behaviour in a Long‐Term Monogamous Lizard: Evidence from Detailed Bio‐Logging and a 31‐Year Field Study

Long‐term monogamy is most prevalent in birds but is also found in lizards. We combined a 31‐year field study of the long‐lived, monogamous Australian sleepy lizard, Tiliqua rugosa, with continuous behavioural observations through GPS data logging, in 1 yr, to investigate the duration of pair bonds, rates of partner change and whether either the reproductive performance hypothesis or the mate familiarity hypothesis could explain this remarkable long‐term monogamy. The reproductive performance hypothesis predicts higher reproductive success in more experienced parents, whereas the mate familiarity hypothesis suggests that effects of partner familiarity select for partner retention and long‐term monogamy. Rates of partner change were below 34% over a 5‐yr period and most sleepy lizards formed long‐term pair bonds: 31 partnerships lasted for more than 15 yr, 110 for more than 10 yr, and the recorded maximum was 27 yr (ongoing). In the year when we conducted detailed observations, familiar pairs mated significantly earlier than unfamiliar pairs. Previous pairing experience (total number of years paired with previous partners) had no significant effect. Early mating often equates to higher reproductive success, and we infer that is the case in sleepy lizards. Early mating of familiar pairs was not due to better body condition. We propose two suggestions about the proximate mechanisms that may allow familiar pair partners to mate earlier than unfamiliar partners. First, they may have improved coordination of their reproductive sexual cycles to reach receptivity earlier and thereby maximise fertilisation success. Second, they may forage more efficiently, benefiting from effective information transfer and/or cooperative predator detection. Those ideas need empirical testing in the future. Regardless of the mechanism, our observations of sleepy lizard pairing behaviour support the mate familiarity hypothesis, but not the reproductive performance hypothesis, as an explanation for its long‐term monogamous mating system.     

Robustness and evolvability: a paradox resolved

Understanding the relationship between robustness and evolvability is key to understand how living things can withstand mutations, while producing ample variation that leads to evolutionary innovations. Mutational robustness and evolvability, a system's ability to produce heritable variation, harbour a paradoxical tension. On one hand, high robustness implies low production of heritable phenotypic variation. On the other hand, both experimental and computational analyses of neutral networks indicate that robustness enhances evolvability. I here resolve this tension using RNA genotypes and their secondary structure phenotypes as a study system. To resolve the tension, one must distinguish between robustness of a genotype and a phenotype. I confirm that genotype (sequence) robustness and evolvability share an antagonistic relationship. In stark contrast, phenotype (structure) robustness promotes structure evolvability. A consequence is that finite populations of sequences with a robust phenotype can access large amounts of phenotypic variation while spreading through a neutral network. Population-level processes and phenotypes rather than individual sequences are key to understand the relationship between robustness and evolvability. My observations may apply to other genetic systems where many connected genotypes produce the same phenotypes.     

Mass extinction: a commentary

Four neocatastrophist claims about mass extinction are currently being debated; they are that: 1, the late Cretaceous mass extinction was caused by large body impact; 2, as many as five other major extinctions were caused by impact; 3, the timing of extinction events since the Permian is uniformly periodic; and 4, the ages of impact craters on Earth are also periodic and in phase with the extinctions. Although strongly interconnected the four claims are independent in the sense that none depends on the others. Evidence for a link between impact and extinction is strong but still needs more confirmation through bed-by-bed and laboratory studies. An important area for future research is the question of whether extinction is a continuous process, with the rate increasing at times of mass extinctions, or whether it is episodic at all scales. If the latter is shown to be generally true, then species are at risk of extinction only rarely during their existence and catastrophism, in the sense of isolated events of extreme stress, is indicated. This is line of reasoning can only be considered an hypothesis for testing. In a larger context, paleontologists may benefit from a research strategy that looks to known Solar System and Galactic phenomena for predictions about environmental effects on earth. The recent success in the recognition of Milankovitch Cycles in the late Pleistocene record is an example of the potential of this research area.     

Emergence of robust regulatory motifs from in silico evolution of sustained oscillation

The relationship between robustness and evolvability (easiness to evolve), and the evolutionary emergence of robust genetic circuits in biology have attracted much attention in systems biology. This paper investigates in silico the influence of the cis-regulation logic and the coupling of feedback loops on the evolvability and robustness of gene regulatory motifs that can generate sustained oscillation. Our simulation results indicate that both evolvability and robustness of the considered regulatory motifs depend on the cis-regulation logic and the way in which positive and negative feedback loops are coupled. Most interestingly, our findings suggest that robust regulatory motifs can emerge from evolution without an explicit selection pressure on robustness and adding noise in the parameters during the evolution is likely to promote the evolution of sustained oscillation.     

The return of the Red Queen, or the law of the growth in the mean duration of the existence of genera during evolution

Phanerozoic marine genera apparently do not become less extinction-prone with age. Higher extinction probability in "young" cohorts of genera is better explained by initially different levels of extinction-tolerance of genera in the cohort. This fact agrees with one of the two basic statements of the "Red Queen" hypothesis (Van Valen, 1973). In the second statement (the idea that the increase in fitness lowers extinction probability) the term "fitness" should be changed to "adaptability". The increase of extinction-tolerance, that can be interpreted as the increase of adaptability to unpredictable changes of environment, is found in succession of "generations" of genera that replace one another through time. This increase reveals itself, firstly, in the growth of mean duration of genera, as well as in the decrease of extinction/origination rates, gradual accumulation of long-lived genera and origination of genera with higher duration. The increase of adaptability may be caused by selective extinction of stenotopic, ecologically specialized forms; Cope's law; evolution of ecosystems that involves development of more effective mechanisms of sustaining homeostasis which may stimulate the recovery of a genus after partial extinction.     

Evolvability Is Inevitable: Increasing Evolvability without the Pressure to Adapt

Why evolvability appears to have increased over evolutionary time is an important unresolved biological question. Unlike most candidate explanations, this paper proposes that increasing evolvability can result without any pressure to adapt. The insight is that if evolvability is heritable, then an unbiased drifting process across genotypes can still create a distribution of phenotypes biased towards evolvability, because evolvable organisms diffuse more quickly through the space of possible phenotypes. Furthermore, because phenotypic divergence often correlates with founding niches, niche founders may on average be more evolvable, which through population growth provides a genotypic bias towards evolvability. Interestingly, the combination of these two mechanisms can lead to increasing evolvability without any pressure to out-compete other organisms, as demonstrated through experiments with a series of simulated models. Thus rather than from pressure to adapt, evolvability may inevitably result from any drift through genotypic space combined with evolution''s passive tendency to accumulate niches.