Ultimate causes and the evolution of altruism

Reconciling the evolution of altruism with Darwinian natural selection is frequently presented as a fundamental problem in biology. In addition to an exponentially increasing literature on specific mechanisms that can permit altruism to evolve, there has been a recent trend to establish general principles to explain altruism in populations undergoing natural selection. This paper reviews and extends one approach to understanding the ultimate causes underlying the evolution of altruism and mechanisms that can realise them, based on the Price equation. From the Price equation, we can see that such ultimate causes equate to the different ways in which the frequency of an altruistic allele in a population can increase. Under this approach, the ultimate causes underlying the evolution of altruism, given some positive fitness costs and benefits, are positive assortment of altruistic alleles with the altruistic behaviour of others, positive deviations from additive fitness effects when multiple altruists interact or bias in the inheritance of altruistic traits. In some cases, one cause can be interpreted in terms of another. The ultimate causes thus identified can be realised by a number of different mechanisms, and to demonstrate its general applicability, I use the Price equation approach to analyse a number of classical mechanisms known to support the evolution of altruism (or cooperation): repeated interaction, ‘greenbeard’ traits, games played on graphs and payoff synergism. I also briefly comment on other important points for the evolution of altruism, such as the ongoing debate over the predominant status of inclusive fitness as the best way to understand its evolution. I conclude by arguing that analysing the evolution of altruism in terms of its ultimate causes is the logical way to approach the problem and that, despite some of its technical limitations, the Price equation approach is a particularly powerful way of doing so.     

Effect of Migration or Inbreeding Followed by Selection on Low-Founder-Number Populations: Implications for Captive Breeding Programs

Using the housefly, Musca domestica (L), as a model system, we tested the ability of two extremes in the range of possible captive breeding protocols to yield sustainable populations following founding with low founder numbers. The protocols tested included two levels of migration as well as inbreeding followed by selection, each with appropriate controls. Each low-founder-number population was founded with two pairs of flies. The maximum migration scheme had 50% migration per generation, and the minimum migration populations experienced a migration rate of 2.5% per generation. The control level of migration was 0%. A fourth low-founder-number treatment was designed to test the effect of inbreeding followed by selection. Two sets of high-founder-number control groups were also derived from the stock population. Two fitness measures, viability and productivity of the populations, were recorded at the fifth generation. Populations in the minimum-migration and zero migration treatment groups had lower fitness than populations in any other treatment for both measures. Populations that experienced inbreeding and selection for high fitness levels, high levels of migration, or large high-founder-number populations were equally fit. These results demonstrate that a captive-breeding scheme that contains substantial levels of migration or inbreeding followed by selection can yield highly adapted populations.     

A model for the evolution of communal foraging in hierarchically structured populations

A kin selection model is described for populations in which groups of interacting individuals (trait groups, sensu Wilson 1975) are spatially situated within larger aggregations. The model predicts the optimal foraging strategy when resources are shared with other trait group members and there is an individual risk in foraging. The ecological mechanism of variation in group fitness, differential resource accumulation, is explicitly incorporated into the model. The optimal foraging rate obtained from this model depends on the product of a benefit-to-cost ratio and a relatedness parameter. The appropriate definition of relatedness for the evolution of communal foraging is determined by the details of the ecological interaction between consumers and resources. When competition is purely intra-specific, the genetic correlation among interactants relative to other members of the local aggregation defines the relatedness parameter applicable to selection on foraging propensity. When competition is primarily inter-specific, the genetic correlation among trait group members relative to the entire population defines relatedness.     

SIZE DOESN'T MATTER: MICROBIAL SELECTION EXPERIMENTS ADDRESS ECOLOGICAL PHENOMENA

Experimental evolution is relevant to ecology because it can connect physiology, and in particular metabolism, to questions in ecology. The investigation of the linkage between the environment and the evolution of metabolism is tractable because these experiments manipulate a very simple environment to produce predictable evolutionary outcomes. In doing so, microbial selection experiments can examine the causal elements of natural selection: how specific traits in varying environments will yield different fitnesses. Here, we review the methodology of microbial evolution experiments and address three issues that are relevant to ecologists: genotype-by-environment interactions, ecological diversification due to specialization, and negative frequency-dependent selection. First, we expect that genotype-by-environment interactions will be ubiquitous in biological systems. Second, while antagonistic pleiotropy is implicated in some cases of ecological specialization, other mechanisms also seem to be at work. Third, while negative frequency-dependent selection can maintain ecological diversity in laboratory systems, a mechanistic (biochemical) analysis of these systems suggests that negative frequency dependence may only apply within a narrow range of environments if resources are substitutable. Finally, we conclude that microbial experimental evolution needs to avail itself of molecular techniques that could enable a mechanistic understanding of ecological diversification in these simple systems.     

Adaptive speciation theory: a conceptual review

Speciation—the origin of new species—is the source of the diversity of life. A theory of speciation is essential to link poorly understood macro-evolutionary processes, such as the origin of biodiversity and adaptive radiation, to well understood micro-evolutionary processes, such as allele frequency change due to natural or sexual selection. An important question is whether, and to what extent, the process of speciation is ‘adaptive’, i.e., driven by natural and/or sexual selection. Here, we discuss two main modelling approaches in adaptive speciation theory. Ecological models of speciation focus on the evolution of ecological differentiation through divergent natural selection. These models can explain the stable coexistence of the resulting daughter species in the face of interspecific competition, but they are often vague about the evolution of reproductive isolation. Most sexual selection models of speciation focus on the diversification of mating strategies through divergent sexual selection. These models can explain the evolution of prezygotic reproductive isolation, but they are typically vague on questions like ecological coexistence. By means of an integrated model, incorporating both ecological interactions and sexual selection, we demonstrate that disruptive selection on both ecological and mating strategies is necessary, but not sufficient, for speciation to occur. To achieve speciation, mating must at least partly reflect ecological characteristics. The interaction of natural and sexual selection is also pivotal in a model where sexual selection facilitates ecological speciation even in the absence of diverging female preferences. In view of these results, it is counterproductive to consider ecological and sexual selection models as contrasting and incompatible views on speciation, one being dominant over the other. Instead, an integrative perspective is needed to achieve a thorough and coherent understanding of adaptive speciation.     

Guppies and the TIT FOR TAT strategy: preference based on past interaction

Summary The evolution of cooperation requires either (a) nonrandom interactions, such that cooperators preferentially interact with other cooperators, or (b) conditional behaviors, such that individuals act cooperatively primarily towards other cooperators. Although these conditions can be met without assuming sophisticated animal cognition, they are more likely to be met if animals can remember individuals with whom they have interacted, associate past interactions with these individuals, and base future behavior on this information. Here we show that guppies (Poecilia reticulata), in the context of predator inspection behavior, can identify and remember (for at least 4 h) the more cooperative among two conspecifics and subsequently choose to be near these individuals in future encounters. Offprint requests to: L.A. Dugatkin     

Intergroup conflict,ostracism, and the evolution of cooperation under free migration

Theoretical investigations and quasi-experimental evidence from modern conflict areas suggest that intergroup conflict and ostracism play a pivotal role in the evolution of cooperation. However, there is little direct evidence about the influence of intergroup conflict on human social behavior in the presence of endogenous group formation and unrestricted migration. This study introduces an experiment to examine the impact of intergroup conflict and ostracism on group formation, and human cooperation in a dynamic environment where group size, the occurrence of intergroup hostility and the threat of ostracism are endogenously determined. Here, we show that intergroup conflict may inhibit merging into single large human coalitions. The threat of ostracism is shown to increase the average group size and cooperation within the society. In addition, we find that competitive pressure between groups decreases the likelihood of social exclusion. Our results suggest that free migration between groups suppresses the impact of between-group competition on within-group cooperation. Moreover, our results stress the role of ostracism as a means to repress competition within groups and enhance group success in competition against other groups.     

Estimates of Natural Selection in a Salmon Population in Captive and Natural Environments

Abstract:  Captive breeding is a commonly used strategy for species conservation. One risk of captive breeding is domestication selection—selection for traits that are advantageous in captivity but deleterious in the wild. Domestication selection is of particular concern for species that are bred in captivity for many generations and that have a high potential to interbreed with wild populations. Domestication is understood conceptually at a broad level, but relatively little is known about how natural selection differs empirically between wild and captive environments. We used genetic parentage analysis to measure natural selection on time of migration, weight, and morphology for a coho salmon ( Oncorhynchus kisutch ) population that was subdivided into captive and natural components. Our goal was to determine whether natural selection acting on the traits we measured differed significantly between the captive and natural environments. For males, larger individuals were favored in both the captive and natural environments in all years of the study, indicating that selection on these traits in captivity was similar to that in the wild. For females, selection on weight was significantly stronger in the natural environment than in the captive environment in 1 year and similar in the 2 environments in 2 other years. In both environments, there was evidence of selection for later time of return for both males and females. Selection on measured traits other than weight and run timing was relatively weak. Our results are a concrete example of how estimates of natural selection during captivity can be used to evaluate this common risk of captive breeding programs.     

Selection on social traits in greater spear-nosed bats, Phyllostomus hastatus

Many studies assume that selection molds social traits and have investigated the manner in which this occurs, yet very few studies have measured the strength of selection on social traits in natural populations. In this paper, I report results of phenotypic selection analyses on two social traits – the size of social groups and the frequency of group foraging – in Phyllostomus hastatus, the greater spear-nosed bat. I found significant positive directional selection on individual group foraging frequency, but no directional selection on individuals in different-sized social groups. These results have implications for the structure of social groups, cooperative behavior among group mates, and maternal investment strategies. I argue that combining studies of natural selection on wild populations with experiments to identify the agents and mechanisms of selection can do much to increase our understanding of social evolution.     

Tardy females,impatient males: protandry and divergent selection on arrival date in the two sexes of the barn swallow

Protandry reflects the earlier arrival of males than females to the site of reproduction. Such protandry is hypothesised to arise from sex differences in costs and benefits of early arrival. I investigated temporal patterns of arrival date of male and female barn swallows Hirundo rustica and temporal patterns of selection to test the hypothesis that sex differences in selection account for sex differences in arrival date. Mean arrival date of male barn swallows but not of females advanced during the last 33 years, giving rise to an increasing sex difference in arrival date. Early arrival was favoured by increasingly better survival in males, while females showed an opposite pattern that did not reach significance, although the effect differed between sexes. Early arrival increased fecundity in both sexes equally.The sex difference in viability selection in relation to arrival date changed from positive to negative as the degree of protandry increased in recent years, although there was no similar significant relationship for fecundity selection. Furthermore, sex differences in viability selection in a given year affected the degree of protandry in the following year through differential survival of certain phenotypes over others. Finally, temporal changes in sex difference in viability selection and protandry were related to an increase in the interval between first and second clutches, as the duration of the breeding season increased because of climatic amelioration. These findings suggest that arrival date is under divergent selection in the two sexes, providing a mechanism for the evolution of protandry.     

Ecological applications of multilevel analysis of variance

A Bayesian representation of the analysis of variance by A. Gelman is introduced with ecological examples. These examples demonstrate typical situations encountered in ecological studies. Compared to conventional methods, the multilevel approach is more flexible in model formulation, easier to set up, and easier to present. Because the emphasis is on estimation, multilevel models are more informative than the results from a significance test. The improved capacity is largely due to the changed computation methods. In our examples, we show that (1) the multilevel model is able to discern a treatment effect that is smaller than the conventional approach can detect, (2) the graphical presentation associated with the multilevel method is more informative, and (3) the multilevel model can incorporate all sources of uncertainty to accurately describe the true relationship between the outcome and potential predictors.     

Coping with complex and dynamic systems. An approach to a transdisciplinary understanding of coastal zone developments

Complexity and uncertainty play important roles in coastal management. Economic development may push the coastal system beyond its resilience thresholds as a result of interactions between environmental and socio-economic processes. The concepts in this paper link processes of system change, natural evolutionary processes observed in coastal zones, to processes of social evolution. An indicator based on calculating an ecological footprint for coastal zones is presented to guide decision-making in spatial and economic planning. The suggested indicator may support a range of methods linking economic valuation and environmental impact analysis.     

Mutualistic stability in the arbuscular mycorrhizal symbiosis: exploring hypotheses of evolutionary cooperation

The 450-million-year-old symbiosis between the majority of land plants and arbuscular mycorrhizal fungi (AMF) is one of the most ancient, abundant, and ecologically important mutualisms on Earth. Yet, the evolutionary stability of mycorrhizal associations is still poorly understood, as it follows none of the constraints thought to stabilize cooperation in other well-known mutualisms. The capacity of both host and symbiont to simultaneously interact with several partners introduces a unique dilemma; detecting and punishing those exploiting the mutualism becomes increasingly difficult if these individuals can continue to access resources from alternative sources. Here, we explore four hypotheses to explain evolutionary cooperation in the arbuscular mycorrhizal symbiosis: (1) pseudo-vertical transmission and spatial structuring of plant and fungal populations leading to local adaptation of partners; (2) luxury resource exchange in which plants trade surplus carbon for excess fungal nutrients; (3) partner choice allowing partners to associate with better cooperators; and (4) host and symbiont sanctions which actively reward good partners and punish less cooperative ones. We propose that mycorrhizal cooperation is promoted by an exchange of surplus resources between partners and enforced through sanctions by one or both partners. These mechanisms may allow plant and fungal genotypes to discriminate against individuals employing exploitative strategies, promoting patterns of partner choice. Together these selection pressures provide a framework for understanding the stabilization of mycorrhizal cooperation over evolutionary time.     

Behavioural trait assortment in a social network: patterns and implications

The social fine structure of a population plays a central role in ecological and evolutionary processes. Whilst many studies have investigated how morphological traits such as size affect social structure of populations, comparatively little is known about the influence of behaviours such as boldness and shyness. Using information on social interactions in a wild population of Trinidadian guppies (Poecilia reticulata), we construct a social network. For each individual in the network, we quantify its behavioural phenotype using two measures of boldness, predator inspection tendency, a repeatable and reliably measured behaviour well studied in the context of co-operation, and shoaling tendency. We observe striking heterogeneity in contact patterns, with strong ties being positively assorted and weak ties negatively assorted by our measured behavioural traits. Moreover, shy fish had more network connections than bold fish and these were on average stronger. In other words, social fine structure is strongly influenced by behavioural trait. We assert that such structure will have implications for the outcome of selection on behavioural traits and we speculate that the observed positive assortment may act as an amplifier of selection contributing to the maintenance of co-operation during predator inspection.     

Nonrandom, Size- and Timing-Biased Breeding in a Hatchery Population of Steelhead Trout

Abstract:  Hatcheries have been built and operated to buffer salmon and trout populations from overfishing and to compensate for habitat lost or degraded by human activities. These facilities are now so prevalent that in some cases hatchery-produced salmon outnumber salmon produced in the wild. By default, this makes them an important component in the current ecology and evolution of salmonids. Hatcheries differ from natural environments in many ways, and among the most fundamental is the necessity that humans select fish for breeding instead of allowing natural processes of mate choice and competition. We examined the mating system for steelhead trout ( Oncorhynchus mykiss ) at Forks Creek Hatchery in southwest Washington and investigated factors affecting selection of individual steelhead for spawning by the hatchery staff. Despite efforts by the staff to not spawn selectively, data on steelhead spawned over 7 years revealed selection for large adult body size and early reproductive timing and a tendency for size-assortative mating (i.e., large with large). Selection on size was related to selection on reproductive timing because early returning fish tended to be larger than those returning later. To improve the fitness of both hatchery fish destined to spawn in the wild and hatchery fish designated to be spawned in the hatchery, a better understanding of factors associated with the range of reproductive success and mate-choice mechanisms in the wild is vital. This knowledge may then be applied to artificial propagation programs designed for conservation or enhancement.     

Geographic variation and behavioral evolution in marine plankton: the case of<Emphasis Type="Italic"> Mastigias</Emphasis> (Scyphozoa,Rhizostomeae)

Although complex behavior in marine zooplankton has been considered strong evidence of adaptation, ethological studies of marine zooplankton generally have not employed either the comparative approach or evolutionary perspective necessary to distinguish adaptation from any alternative. Consequently, the potential for intra-specific variation in the behavior of marine zooplankton has received insufficient attention and conclusions of adaptation remain poorly substantiated. Intra-specific comparison of patterns of migration and behavior for seven populations of golden jellyfish, Mastigias (Scyphozoa: Rhizostomeae), inhabiting isolated marine lakes and semi-enclosed lagoon coves in Palau document population specific differences in patterns of horizontal migration, vertical migration, pulse rate, swimming speed, and turning behavior. Evidence was found for symplesiomorphic behaviors, canalization, exaptation, adaptation, and probably once-deleterious traits. Behavioral evolution likely proceeded via, at least, relaxation of selection, trade-offs with morphology, and natural selection effected by predation. Behavioral patterns also may change with ontogeny. Geographic variation in the behavior of marine plankton therefore can be substantial and patterns of evolution complex. Behavioral evolution can rapidly generate coastal biodiversity. Thus, geographic variation in marine plankton is of potential interest to ethologists, evolutionary biologists, biogeographers, and conservation biologists.Electronic Supplementary Supplementary material is available in the online version of this article at Communicated by G.F. Humphrey, Sydney     

The roles of sensory traps in the origin, maintenance, and breakdown of mutualism

Sensory traps are signal mimics that elicit out-of-context behaviors by exploiting the adaptive, neural responses of signal receivers. Sensory traps have long been invoked in studies of mate and prey attraction, but the possible roles of sensory traps in mutualisms (cooperation between species) have yet to be thoroughly examined. Our review identifies four candidate roles for sensory traps in the evolution of mutualistic interactions: reassembly, error reduction, enforcement, and cost reduction. A key consequence of sensory traps is that they limit the applicability of partner choice and biological market models of mutualism. We conclude by suggesting that an important research topic in the evolution of cooperation should be to identify any mechanisms that increase the truthfulness of communication between cooperating species.     

Effects of kinship on territorial conflicts among groups of lions,<Emphasis Type="Italic"> Panthera leo</Emphasis>

Inclusive fitness theory predicts that cost of tolerant behaviour during competitive interactions is lower for relatives than for nonrelatives. Many studies have examined the effect of relatedness on behaviour within social groups. In contrast, kin selection acting among groups has received less attention. The genetic structure of African lion (Panthera leo) populations creates a strong possibility that kin selection among groups modifies behaviour during group conflicts. We used playback experiments and genetic data to investigate the importance of relatedness during simulated territorial disputes in lions. However, we found no effect of relatedness on territorial behaviour. Degree of relatedness did not affect the decision to approach simulated intrusions, nor did it affect the behaviour during approaches. The decision to approach was instead affected by position within the territory and consecutive playback number (a measure of habituation). For playbacks that did elicit an approach, the speed of response was not detectably affected by relatedness, but was affected by odds (the ratio of residents to intruders), number of intruders, number of bouts, presence of cubs, position within the territory, temperature and playback number. Although responses were unaffected by relatedness, it remains possible that other aspects of behaviour during natural encounters among prides are affected by kin selection.Communicated by L. Sterck     

Rapid cultural adaptation can facilitate the evolution of large-scale cooperation

Over the past several decades, we have argued that cultural evolution can facilitate the evolution of large-scale cooperation because it often leads to more rapid adaptation than genetic evolution, and, when multiple stable equilibria exist, rapid adaptation leads to variation among groups. Recently, Lehmann, Feldman, and colleagues have published several papers questioning this argument. They analyze models showing that cultural evolution can actually reduce the range of conditions under which cooperation can evolve and interpret these models as indicating that we were wrong to conclude that culture facilitated the evolution of human cooperation. In the main, their models assume that rates of cultural adaption are not strong enough compared to migration to maintain persistent variation among groups when payoffs create multiple stable equilibria. We show that Lehmann et al. reach different conclusions because they have made different assumptions. We argue that the assumptions that underlie our models are more consistent with the empirical data on large-scale cultural variation in humans than those of Lehmann et al., and thus, our models provide a more plausible account of the cultural evolution of human cooperation in large groups.     

Levels of selection in a social insect: a review of conflict and cooperation during honey bee (<Emphasis Type="Italic">Apis mellifera</Emphasis>) queen replacement

The extended phenotype of a social insect colony enables selection to act at both the individual level (within-colony selection) and the colony level (between-colony selection). Whether a particular trait persists over time depends on the relative within- and between-colony selection pressures. Queen replacement in honey bee colonies exemplifies how selection may act at these different levels in opposing directions. Normally, a honey bee colony has only one queen, but a colony rears many new queens during the process of colony reproduction. The replacement of the mother queen has two distinct phases: queen rearing, where many queens develop and emerge from their cells, and queen elimination, where most queens die in a series of fatal duels. Which queens are reared to adulthood and which queens ultimately survive the elimination process depends on the strength and direction of selection at both the individual and colony levels. If within-colony selection is predominant, then conflict is expected to occur among nestmates over which queens are produced. If between-colony selection is predominant, then cooperation is expected among nestmates. We review the current evidence for conflict and cooperation during queen replacement in honey bees during both the queen rearing and queen elimination phases. In particular, we examine whether workers of different subfamilies exhibit conflict by acting nepotistically toward queens before and after they have emerged from their cells, and whether workers exhibit cooperation by collectively producing queens of high reproductive quality. We conclude that although workers may weakly compete through nepotism during queen rearing, workers largely cooperate to raise queens of similar reproductive potential so that any queen is suitable to inherit the nest. Thus it appears that potential conflict over queen replacement in honey bees has not translated into actual conflict, suggesting that between-colony selection predominates during these important events in a colonys life cycle.Communicated by A. Cockburn