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'.

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'.

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.

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.

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.

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.

"Darwin's corollary" and cytoplasmic incompatibility induced by Cardinium may contribute to speciation in Encarsia wasps (Hymenoptera: Aphelinidae).

The potential importance of cytoplasmic incompatibility (CI)-inducing bacterial symbionts in speciation of their arthropod hosts has been debated. Theoretical advances have led to a consensus that a role is plausible when CI is combined with other isolating barriers. However, the insect model systems Nasonia and Drosophila are the only two experimental examples documented. Here, we analyzed the components of reproductive isolation between the parasitoid wasp Encarsia suzannae, which is infected by the CI-inducing symbiont Cardinium, and its uninfected sibling species Encarsia gennaroi. Laboratory crosses demonstrated that: (1) sexual isolation is incomplete; (2) hybrid offspring production is greatly reduced in the interspecific CI cross; (3) viable hybrids may be produced by curing E. suzannae males of Cardinium with antibiotics; (4) hybrid offspring production in the reciprocal cross is greatly reduced by hybrid inviability due to genetic incompatibilities; (5) hybrid sterility is nearly complete in both directions at the F1 stage. Thus, asymmetrical hybrid incompatibilities and CI act as complementary isolating mechanisms. We propose a new model for contributions of CI symbionts to speciation, with CI reducing gene flow between species in one direction, and in the other, a symbiont sweep resulting in accelerated mtDNA evolution, negative cytonuclear interactions, and hybrid incompatibilities.

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.

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.

Wolbachia and the insect immune system: what reactive oxygen species can tell us about the mechanisms of Wolbachia-host interactions.

Wolbachia are intracellular bacteria that infect a vast range of arthropod species, making them one of the most prevalent endosymbionts in the world. Wolbachia's stunning evolutionary success is mostly due to their reproductive parasitism but also to mutualistic effects such as increased host fecundity or protection against pathogens. However, the mechanisms underlying Wolbachia phenotypes, both parasitic and mutualistic, are only poorly understood. Moreover, it is unclear how the insect immune system is involved in these phenotypes and why it is not more successful in eliminating the bacteria. Here we argue that reactive oxygen species (ROS) are likely to be key in elucidating these issues. ROS are essential players in the insect immune system, and Wolbachia infection can affect ROS levels in the host. Based on recent findings, we elaborate a hypothesis that considers the different effects of Wolbachia on the oxidative environment in novel vs. native hosts. We propose that newly introduced Wolbachia trigger an immune response and cause oxidative stress, whereas in coevolved symbioses, infection is not associated with oxidative stress, but rather with restored redox homeostasis. Redox homeostasis can be restored in different ways, depending on whether Wolbachia or the host is in charge. This hypothesis offers a mechanistic explanation for several of the observed Wolbachia phenotypes.

Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts.

Wolbachia are the most abundant bacterial endosymbionts among arthropods. Although maternally inherited, they do not conform to the widespread view that vertical transmission inevitably selects for beneficial symbionts. Instead, Wolbachia are notorious for their reproductive parasitism which, although lowering host fitness, ensures their spread. However, even for reproductive parasites it can pay to enhance host fitness. Indeed, there is a recent upsurge of reports on Wolbachia-associated fitness benefits. Therefore, the question arises how such instances of mutualism are related to the phenotypes of reproductive parasitism. Here, we review the evidence of Wolbachia mutualisms in arthropods, including both facultative and obligate relationships, and critically assess their biological relevance. Although many studies report anti-pathogenic effects of Wolbachia, few actually prove these effects to be relevant to field conditions. We further show that Wolbachia frequently have beneficial and detrimental effects at the same time, and that reproductive manipulations and obligate mutualisms may share common mechanisms. These findings undermine the idea of a clear-cut distinction between Wolbachia mutualism and parasitism. In general, both facultative and obligate mutualisms can have a strong, and sometimes unforeseen, impact on the ecology and evolution of Wolbachia and their arthropod hosts. Acknowledging this mutualistic potential might be the key to a better understanding of some unresolved issues in the study of Wolbachia-host interactions.

Dobzhansky-muller and wolbachia-induced incompatibilities in a diploid genetic system.

Genetic incompatibilities are supposed to play an important role in speciation. A general (theoretical) problem is to explain the persistence of genetic diversity after secondary contact. Previous theoretical work has pointed out that Dobzhansky-Muller incompatibilities (DMI) are not stable in the face of migration unless local selection acts on the alleles involved in incompatibility. With local selection, genetic variability exists up to a critical migration rate but is lost when migration exceeds this threshold value. Here, we investigate the effect of intracellular bacteria Wolbachia on the stability of hybrid zones formed after the Dobzhansky Muller model. Wolbachia are known to cause a cytoplasmic incompatibility (CI) within and between species. Incorporating intracellular bacteria Wolbachia can lead to a significant increase of critical migration rates and maintenance of divergence, primarily because Wolbachia-induced incompatibility acts to reduce frequencies of F1 hybrids. Wolbachia infect up to two-thirds of all insect species and it is therefore likely that CI co-occurs with DMI in nature. The results indicate that both isolating mechanisms strengthen each other and under some circumstances act synergistically. Thus they can drive speciation processes more forcefully than either when acting alone.

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.

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.

Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected.

Wolbachia are intracellular bacteria that manipulate the reproduction of their arthropod hosts in remarkable ways. They are predominantly transmitted vertically from mother to offspring but also occasionally horizontally between species. In doing so, they infect a huge range of arthropod species worldwide. Recently, a statistical analysis estimated the infection frequency of Wolbachia among arthropod hosts to be 66%. At the same time, the authors of this analysis highlighted some weaknesses of the underlying data and concluded that in order to improve the estimate, a larger number of individuals per species should be assayed and species be chosen more randomly. Here we apply the statistical approach to a more appropriate data set from a recent survey that tested both a broad range of species and a sufficient number of individuals per species. Indeed, we find a substantially different infection frequency: We now estimate the proportion of Wolbachia-infected species to be around 40% which is lower than the previous estimate but still points to a surprisingly high number of arthropods harboring the bacteria. Notwithstanding this difference, we confirm the previous result that, within a given species, typically most or only a few individuals are infected. Moreover, we extend our analysis to include several reproductive parasites other than Wolbachia that were also screened for in the aforementioned empirical survey. For these symbionts we find a large variation in estimated infection frequencies and corroborate the finding that Wolbachia are the most abundant endosymbionts among arthropod species.

A new model and method for understanding Wolbachia-induced cytoplasmic incompatibility.

Wolbachia are intracellular bacteria transmitted almost exclusively vertically through eggs. In response to this mode of transmission, Wolbachia strategically manipulate their insect hosts' reproduction. In the most common manipulation type, cytoplasmic incompatibility, infected males can only mate with infected females, but infected females can mate with all males. The mechanism of cytoplasmic incompatibility is unknown; theoretical and empirical findings need to converge to broaden our understanding of this phenomenon. For this purpose, two prominent models have been proposed: the mistiming-model and the lock-key-model. The former states that Wolbachia manipulate sperm of infected males to induce a fatal delay of the male pronucleus during the first embryonic division, but that the bacteria can compensate the delay by slowing down mitosis in fertilized eggs. The latter states that Wolbachia deposit damaging "locks" on sperm DNA of infected males, but can also provide matching "keys" in infected eggs to undo the damage. The lock-key-model, however, needs to assume a large number of locks and keys to explain all existing incompatibility patterns. The mistiming-model requires fewer assumptions but has been contradicted by empirical results. We therefore expand the mistiming-model by one quantitative dimension to create the new, so-called goalkeeper-model. Using a method based on formal logic, we show that both lock-key- and goalkeeper-model are consistent with existing data. Compared to the lock-key-model, however, the goalkeeper-model assumes only two factors and provides an idea of the evolutionary emergence of cytoplasmic incompatibility. Available cytological evidence suggests that the hypothesized second factor of the goalkeeper-model may indeed exist. Finally, we suggest empirical tests that would allow to distinguish between the models. Generalizing our results might prove interesting for the study of the mechanism and evolution of other host-parasite interactions.