Ecological Genetic Conflict: Genetic Architecture Can Shift the Balance between Local Adaptation and Plasticity.

Genetic polymorphism can contribute to local adaptation in heterogeneous habitats, for instance, as a single locus with alleles adapted to different habitats. Phenotypic plasticity can also contribute to trait variation across habitats, through developmental responses to habitat-specific cues. We show that the genetic architecture of genetically polymorphic and plasticity loci may influence the balance between local adaptation and phenotypic plasticity. These effects of genetic architecture are instances of ecological genetic conflict. A reduced effective migration rate for genes tightly linked to a genetic polymorphism provides an explanation for the effects, and they can occur both for a single trait and for a syndrome of coadapted traits. Using individual-based simulations and numerical analysis, we investigate how among-habitat genetic polymorphism and phenotypic plasticity depend on genetic architecture. We also study the evolution of genetic architecture itself, in the form of rates of recombination between genetically polymorphic loci and plasticity loci. Our main result is that for plasticity genes that are unlinked to loci with between-habitat genetic polymorphism, the slope of a reaction norm is steeper in comparison with the slope favored by plasticity genes that are tightly linked to genes for local adaptation.

Evolution of reproductive parasites with direct fitness benefits.

Maternally inherited symbionts such as Wolbachia have long been seen mainly as reproductive parasites, with deleterious effects on host fitness. It is becoming clear, however, that, frequently, these symbionts also have beneficial effects on host fitness, either along with reproductive parasitism or not. Using the examples of cytoplasmic incompatibility (CI) and male-killing (MK), we here analyze the effect of direct fitness benefits on the evolution of reproductive parasites. By means of a simple theoretical framework, we synthesize and extend earlier modeling approaches for CI and MK, which usually ignore fitness benefits. Moreover, our framework is not restricted to a particular mechanism underlying the fitness benefit (e.g., protection against pathogens). We derive invasion conditions and equilibrium frequencies for the different infection scenarios. Our results demonstrate the importance of a symbiont's "effective fecundity" (i.e., the product of the relative fecundity of an infected female and her transmission efficiency) for a symbiont's invasion success. In particular, we adopt the concept of effective fecundity to scenarios where CI and MK co-occur in one host population. We confirm that direct fitness benefits substantially facilitate the invasion and spread of infections (for example, by lowering or removing the invasion threshold) or even make invasion possible in the first place (for example, if reproductive parasitism is weak or absent). Finally, we discuss the role of direct fitness benefits in long-term evolutionary dynamics of reproductive phenotypes and highlight their potential to resolve genetic conflicts between maternally inherited symbionts and their hosts.

Genes as Cues of Relatedness and Social Evolution in Heterogeneous Environments.

There are many situations where relatives interact while at the same time there is genetic polymorphism in traits influencing survival and reproduction. Examples include cheater-cooperator polymorphism and polymorphic microbial pathogens. Environmental heterogeneity, favoring different traits in nearby habitats, with dispersal between them, is one general reason to expect polymorphism. Currently, there is no formal framework of social evolution that encompasses genetic polymorphism. We develop such a framework, thus integrating theories of social evolution into the evolutionary ecology of heterogeneous environments. We allow for adaptively maintained genetic polymorphism by applying the concept of genetic cues. We analyze a model of social evolution in a two-habitat situation with limited dispersal between habitats, in which the average relatedness at the time of helping and other benefits of helping can differ between habitats. An important result from the analysis is that alleles at a polymorphic locus play the role of genetic cues, in the sense that the presence of a cue allele contains statistical information for an organism about its current environment, including information about relatedness. We show that epistatic modifiers of the cue polymorphism can evolve to make optimal use of the information in the genetic cue, in analogy with a Bayesian decision maker. Another important result is that the genetic linkage between a cue locus and modifier loci influences the evolutionary interest of modifiers, with tighter linkage leading to greater divergence between social traits induced by different cue alleles, and this can be understood in terms of genetic conflict.

Evolution of microbial markets.

Biological market theory has been used successfully to explain cooperative behavior in many animal species. Microbes also engage in cooperative behaviors, both with hosts and other microbes, that can be described in economic terms. However, a market approach is not traditionally used to analyze these interactions. Here, we extend the biological market framework to ask whether this theory is of use to evolutionary biologists studying microbes. We consider six economic strategies used by microbes to optimize their success in markets. We argue that an economic market framework is a useful tool to generate specific and interesting predictions about microbial interactions, including the evolution of partner discrimination, hoarding strategies, specialized versus diversified mutualistic services, and the role of spatial structures, such as flocks and consortia. There is untapped potential for studying the evolutionary dynamics of microbial systems. Market theory can help structure this potential by characterizing strategic investment of microbes across a diversity of conditions.

Detection vs. selection: integration of genetic, epigenetic and environmental cues in fluctuating environments.

There are many inputs during development that influence an organism's fit to current or upcoming environments. These include genetic effects, transgenerational epigenetic influences, environmental cues and developmental noise, which are rarely investigated in the same formal framework. We study an analytically tractable evolutionary model, in which cues are integrated to determine mature phenotypes in fluctuating environments. Environmental cues received during development and by the mother as an adult act as detection-based (individually observed) cues. The mother's phenotype and a quantitative genetic effect act as selection-based cues (they correlate with environmental states after selection). We specify when such cues are complementary and tend to be used together, and when using the most informative cue will predominate. Thus, we extend recent analyses of the evolutionary implications of subsets of these effects by providing a general diagnosis of the conditions under which detection and selection-based influences on development are likely to evolve and coexist.

We were all young once: an intragenomic perspective on parent-offspring conflict.

Parent-offspring conflict (POC) describes the evolutionary conflict between offspring and their parents over parental resource allocation. Offspring are expected to demand more resources than their parents are willing to supply because these offspring are more related to their own than to their siblings' offspring. Kin selection acts to limit these divergent interests. Our model departs from previous models by describing POC as an intragenomic conflict between genes determining life-history traits during infancy or parenthood. We explain why a direct fitness approach that measures the total fitness effect during exactly one generation is required to correctly assess POC in interbrood rivalry. We find that incorrect assumptions in previous models led to an overestimation of the scope of POC. Moreover, we show why the degree of monogamy is more important for POC than previously thought. Overall, we demonstrate that a life-history-centred intragenomic approach is necessary to correctly interpret POCs. We further discuss how our work relates to the current debate about the usefulness of inclusive fitness theory.

A helminth immunomodulator exploits host signaling events to regulate cytokine production in macrophages.

Parasitic worms alter their host's immune system to diminish the inflammatory responses directed against them, using very efficient immunomodulating molecules. We have previously shown that the helminth immunomodulator cystatin (AvCystatin) profoundly reduces the progression of inflammatory diseases via modulation of macrophages. Here we elucidate the signaling events in macrophages triggered by AvCystatin. Labeled AvCystatin was predominantly taken up by macrophages and subsequently induced the phosphorylation of the mitogen-activated protein kinases (MAPK) ERK1/2 and p38. IL-10 expression induced by AvCystatin in macrophages was tyrosine kinase sensitive and dependent on activation of both MAP kinases, in clear contrast to expression of IL-12/23p40. In addition, phosphorylation of the transcription factors CREB and STAT3 was induced by AvCystatin and regulated by phospho-ERK. Chemical inhibition of phosphoinositide 3-kinase (PI3K) reduced AvCystatin-induced cytokine release; however, AKT, the downstream target of PI3K, was not activated following AvCystatin exposure. To characterize signaling elements involved in alteration of the macrophage phenotype we applied mathematical modeling. Experimental testing of the in silico generated hypotheses identified dual specificity phosphatase (DUSP) 1 and 2, as regulators in AvCystatin triggered macrophages in vitro and in vivo. In particular, DUSP1 was subsequently found to be responsible for regulation of ERK- and p38-phosphorylation and controlled the IL-10 expression in macrophages by AvCystatin. Thus, we show that AvCystatin exploits activation and deactivation pathways of MAP kinases to induce regulatory macrophages. This study provides insights into molecular mechanisms of macrophage manipulation by parasites and highlights the utility of mathematical modeling for the elucidation of regulatory circuits of immune cells.

A biological employment model of reproductive inequality.

Continuing the centuries-long exchange between economics and biology, our model of reproductive skew is an adaptation of the principal-agent relationship between an employer and an employee. Inspired by the case of purple martins (Progne subis) and lazuli buntings (Passerina amoena), we model a dominant male whose fitness can be advanced not only by coercing a subordinate male but, where coercion is impossible or not cost-effective, also by providing positive fitness incentives for the subordinate that induce him to behave in ways that contribute to the dominant's fitness. We model a situation in which a dominant and subordinate contest over a variable amount of joint total fitness, both the level and division of which result from the strategies adopted by both. Thus there is not some given amount of potential fitness (or 'pie') that is to be divided between the two (or wasted in costly contests). The fitness incentives that in evolutionary equilibrium are conceded to the subordinate by the dominant maximize the dominant's own fitness. The reason is that the larger pie resulting from the subordinate's increased helping more than compensates for the dominant's reduced fitness share. But the conflict over fitness shares nonetheless limits the size of the pie. This article is part of the theme issue 'Evolutionary ecology of inequality'.

Community structure of domesticated pigs in livestock facilities.

The social structure of animal groups is considered to have an impact on their health and welfare. This could also be true for animals under commercial conditions, but research in this area has been limited. Pigs for example are known to be very social animals, but information about their grouping behavior is mostly derived from wild boars and a limited number of studies in seminatural and commercial conditions. Specifically under commercial conditions it is still unclear to what extent pig herds organize themselves in subgroups and how such group patterns emerge. To answer these questions, we tracked the positions of about 200 sows inside a barn during ongoing production over a period of five weeks and used these data to construct and analyze the animal contact networks. Our analysis showed a very high contact density and only little variation in the number of other animals that a specific animal is in contact with. Nevertheless, in each week we consistently detected three subgroups inside the barn, which also showed a clear spatial separation. Our results show that even in the high density environment of a commercial pig farm, the behavior of pigs to form differentiated groups is consistent with their behavior under seminatural conditions. Furthermore, our findings also imply that the barn layout could play an important role in the formation of the grouping pattern. These insights could be used to monitor and understand the spread of infectious diseases inside the barn better. In addition, our insights could potentially be used to improve the welfare of pigs.

The evolution of social learning as phenotypic cue integration.

Most analyses of the origins of cultural evolution focus on when and where social learning prevails over individual learning, overlooking the fact that there are other developmental inputs that influence phenotypic fit to the selective environment. This raises the question of how the presence of other cue 'channels' affects the scope for social learning. Here, we present a model that considers the simultaneous evolution of (i) multiple forms of social learning (involving vertical or horizontal learning based on either prestige or conformity biases) within the broader context of other evolving inputs on phenotype determination, including (ii) heritable epigenetic factors, (iii) individual learning, (iv) environmental and cascading maternal effects, (v) conservative bet-hedging, and (vi) genetic cues. In fluctuating environments that are autocorrelated (and hence predictable), we find that social learning from members of the same generation (horizontal social learning) explains the large majority of phenotypic variation, whereas other cues are much less important. Moreover, social learning based on prestige biases typically prevails in positively autocorrelated environments, whereas conformity biases prevail in negatively autocorrelated environments. Only when environments are unpredictable or horizontal social learning is characterized by an intrinsically low information content, other cues such as conservative bet-hedging or vertical prestige biases prevail. This article is part of the theme issue 'Foundations of cultural evolution'.

Underappreciated features of cultural evolution.

Cultural evolution theory has long been inspired by evolutionary biology. Conceptual analogies between biological and cultural evolution have led to the adoption of a range of formal theoretical approaches from population dynamics and genetics. However, this has resulted in a research programme with a strong focus on cultural transmission. Here, we contrast biological with cultural evolution, and highlight aspects of cultural evolution that have not received sufficient attention previously. We outline possible implications for evolutionary dynamics and argue that not taking them into account will limit our understanding of cultural systems. We propose 12 key questions for future research, among which are calls to improve our understanding of the combinatorial properties of cultural innovation, and the role of development and life history in cultural dynamics. Finally, we discuss how this vibrant research field can make progress by embracing its multidisciplinary nature. This article is part of the theme issue 'Foundations of cultural evolution'.

Sociocultural heterogeneity in a common pool resource dilemma.

Collective action of resource users is essential for sustainability. Yet, often user groups are socioculturally heterogeneous, which requires cooperation to be established across salient group boundaries. We explore the effect of this type of heterogeneity on resource extraction in lab-in-the-field Common Pool Resource (CPR) experiments in Zanzibar, Tanzania. We create heterogeneous groups by mixing fishers from two neighbouring fishing villages which have distinct social identities, a history of conflict and diverging resource use practices and institutions. Additionally, we analyse between-village differences in extraction behaviour in the heterogeneous setting to assess if out-group cooperation in a CPR dilemma is associated with a community's institutional scope in the economic realm (e.g., degree of market integration). We find no aggregate effect of heterogeneity on extraction. However, this is because fishers from the two villages behave differently in the heterogeneity treatment. We find support for the hypothesis that cooperation under sociocultural heterogeneity is higher for fishers from the village with larger institutional scope. In line with this explanation, cooperation under heterogeneity also correlates with a survey measure of individual fishers' radius of trust. We discuss implications for resource governance and collective action research.

Revealing the paradox of drug reward in human evolution.

Neurobiological models of drug abuse propose that drug use is initiated and maintained by rewarding feedback mechanisms. However, the most commonly used drugs are plant neurotoxins that evolved to punish, not reward, consumption by animal herbivores. Reward models therefore implicitly assume an evolutionary mismatch between recent drug-profligate environments and a relatively drug-free past in which a reward centre, incidentally vulnerable to neurotoxins, could evolve. By contrast, emerging insights from plant evolutionary ecology and the genetics of hepatic enzymes, particularly cytochrome P450, indicate that animal and hominid taxa have been exposed to plant toxins throughout their evolution. Specifically, evidence of conserved function, stabilizing selection, and population-specific selection of human cytochrome P450 genes indicate recent evolutionary exposure to plant toxins, including those that affect animal nervous systems. Thus, the human propensity to seek out and consume plant neurotoxins is a paradox with far-reaching implications for current drug-reward theory. We sketch some potential resolutions of the paradox, including the possibility that humans may have evolved to counter-exploit plant neurotoxins. Resolving the paradox of drug reward will require a synthesis of ecological and neurobiological perspectives of drug seeking and use.

The neutral effective migration rate in a mainland-island context.

Genetic influx into a population often does not correspond to the real migration rate (m) of individuals, due to class structure within the population. The effective migration rate (m(e)) is a concept to measure gene flow in such a situation. The ratio of the effective migration rate to the real migration rate (m(e)/m) is called the gene flow factor, and represents the degree of gene flow modification. Prior authors proposed different definitions of the effective migration rate. These may be categorized into two groups: the neutral effective migration rate and the selective effective migration rate. In this article, we construct a general model of a class-structured population with a mainland-island structure. Using the model, we prove that the gene flow factor of the neutral effective migration rate converges to the mean reproductive value of immigrants if the limit is taken with the real migration rate converging to zero. This limit theorem provides a novel interpretation of gene flow and can be used to derive approximation formulae of the neutral effective migration rate. We illustrate this method analyzing two examples, sex ratio distortion due to extrinsic factors and hybrid zones with underdominance.

How many species are infected with Wolbachia?--A statistical analysis of current data.

Wolbachia are intracellular bacteria found in many species of arthropods and nematodes. They manipulate the reproduction of their arthropod hosts in various ways, may play a role in host speciation and have potential applications in biological pest control. Estimates suggest that at least 20% of all insect species are infected with Wolbachia. These estimates result from several Wolbachia screenings in which numerous species were tested for infection; however, tests were mostly performed on only one to two individuals per species. The actual percent of species infected will depend on the distribution of infection frequencies among species. We present a meta-analysis that estimates percentage of infected species based on data on the distribution of infection levels among species. We used a beta-binomial model that describes the distribution of infection frequencies of Wolbachia, shedding light on the overall infection rate as well as on the infection frequency within species. Our main findings are that (1) the proportion of Wolbachia-infected species is estimated to be 66%, and that (2) within species the infection frequency follows a 'most-or-few' infection pattern in a sense that the Wolbachia infection frequency within one species is typically either very high (>90%) or very low (<10%).

A new perspective on developmental plasticity and the principles of adaptive morph determination.

Organisms can have divergent paths of development leading to alternative phenotypes, or morphs. The choice of developmental path may be set by environmental cues, the individual's genotype, or a combination of the two. Using individual-based simulation and analytical investigation, we explore the idea that from the viewpoint of a developmental switch, genetic morph determination can sometimes be regarded as adaptive developmental plasticity. We compare the possibilities for the evolution of environmental and genetic morph determination and combinations of the two in situations with spatial variation in conditions. We find that the accuracy of environmental cues in predicting coming selective conditions is important for environmental morph determination, in accordance with previous results, and that genetic morph determination is favored in a similar way by the accuracy of genetic cues, in the form of selectively maintained gene frequency differences between local populations. Restricted gene flow and strong selection acting on the phenotypic alternatives produce clearer gene frequency differences and lead to greater accuracy of genetic cues. For combined environmental and genetic morph determination, we show that the developmental machinery can evolve toward efficiently combining information in environmental and genetic cues for the purpose of predicting coming selective conditions.

On the relevance of mitochondrial fusions for the accumulation of mitochondrial deletion mutants: a modelling study.

The molecular mechanisms underlying the aging process are still unclear, but the clonal accumulation of mitochondrial deletion mutants is one of the prime candidates. An important question for the mitochondrial theory of aging is to discover how defective organelles might be selected at the expense of wild-type mitochondria. We propose that mitochondrial fission and fusion events are of critical importance for resolving this apparent contradiction. We show that the occurrence of fusions removes the problems associated with the idea that smaller DNA molecules accumulate because they replicate in a shorter time--the survival of the tiny (SOT) hypothesis. Furthermore, stochastic simulations of mitochondrial replication, mutation and degradation show that two important experimental findings, namely the overall low mosaic pattern of oxidative phosphorylation (OXPHOS) impaired cells in old organisms and the distribution of deletion sizes, can be reproduced and explained by this hypothesis. Finally, we make predictions that can be tested experimentally to further verify our explanation for the age-related accumulation of mitochondrial deletion mutants.

Biological trade and markets.

Cooperation between organisms can often be understood, like trade between merchants, as a mutually beneficial exchange of services, resources or other 'commodities'. Mutual benefits alone, however, are not sufficient to explain the evolution of trade-based cooperation. First, organisms may reject a particular trade if another partner offers a better deal. Second, while human trade often entails binding contracts, non-human trade requires unwritten 'terms of contract' that 'self-stabilize' trade and prevent cheating even if all traders strive to maximize fitness. Whenever trading partners can be chosen, market-like situations arise in nature that biologists studying cooperation need to account for. The mere possibility of exerting partner choice stabilizes many forms of otherwise cheatable trade, induces competition, facilitates the evolution of specialization and often leads to intricate forms of cooperation. We discuss selected examples to illustrate these general points and review basic conceptual approaches that are important in the theory of biological trade and markets. Comparing these approaches with theory in economics, it turns out that conventional models-often called 'Walrasian' markets-are of limited relevance to biology. In contrast, early approaches to trade and markets, as found in the works of Ricardo and Cournot, contain elements of thought that have inspired useful models in biology. For example, the concept of comparative advantage has biological applications in trade, signalling and ecological competition. We also see convergence between post-Walrasian economics and biological markets. For example, both economists and biologists are studying 'principal-agent' problems with principals offering jobs to agents without being sure that the agents will do a proper job. Finally, we show that mating markets have many peculiarities not shared with conventional economic markets. Ideas from economics are useful for biologists studying cooperation but need to be taken with caution.