A quantitative genetic model of altruistic selection

Summary A quantitative genetic model for evolution by altruistic selection based on family selection models used in agricultural genetics is presented. A quantitative genetic version of Hamilton's rule is derived which indicates that evolution will proceed in an altruistic direction whenever the ratic of between-to within-family (or group) heritability exceeds the absolute value of the within-to between-family selection differential ratio. This ratio of heritabilities is equal to a ratio which includes only the phenotypic and genetic intraclass correlation coefficients, thus no heritabilities actually need to be estimated in determining the possibility of altruistic evolution. The phenotypic intraclass correlation can be estimated with standard analysis of variance methods. The genetic intraclass correlation may be estimated by the average within-group coefficient of relationship using genealogical data, by Wright's F-statistics using allele frequency data, or by a theoretical model based on a knowledge of interaction and mating patterns. Selection differentials may be measured by the regression of relative fitness, or one of its major components, on the phenotype of interest. Selection can be considered altruistic only if within-and between-family selection differentials have opposite signs. Consideration of empirical data on genetic and phenotypic intraclass correlations indicates that evolution may proceed in an altruistic direction even if the within-family selection differential exceeds the one between families, especially in situations in which pertinent environmental factors are randomly distributed among families.     

How nepotistic is the brain worm?

Summary The evolution of altruism does not necessarily require an extreme amount of kinship. This point is illustrated with an analysis of altruistic behavior in the Trematode parasite Dicrocoelium dendriticum, which apparently can evolve even when the parasites of the host are derived from as many as five different parents.     

Altruism between in-laws: Some predictions from kin-selection theory

Summary Kin-selection theory predicts that an individual's inclusive fitness should be affected by any interaction involving a relative. This may sometimes lead to the evolution of altruistic or tolerant behaviour towards non-relatives who can influence the fitness of relatives. Selective pressure for non-relatives to behave altruistically towards each other in such situations may not be reciprocal.     

The evolutionary consequences of mate copying on male traits

In some species, a female's mating preference can be influenced by the matings she observes. Mate copying occurs when a female alters her mating preference in favor of the type of males she has observed mating with other females. Here I present a model that explores the consequences of mate copying on the evolution of male traits. In contrast to previous work, I show that mate copying can have diverse evolutionary consequences. Mate copying can cause (positive or negative) directional selection on male traits or (positive or negative) frequency-dependent selection on male traits. The type of selection generated by mate copying depends on the details of how females are influenced by the matings that they observe. I discuss my results in relation to previous theoretical work that posits that mate copying can only hamper the spread of novel male traits.     

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.     

Ecological and evolutionary mechanisms for low seed: ovule ratios: need for a pluralistic approach?

Central to the ecology and evolution of a broad range of plants is understanding why they routinely have submaximal reproduction manifested as low seed : ovule and fruit : flower ratios. We know much less about the processes responsible for low seed : ovule ratios than we do for fruit : flower ratios. Current hypotheses for low seed : ovule ratios are largely drawn from those for fruit : flower ratios, including proximate (ecological) causes of pollen limitation, resource limitation, and pollen quality, as well as the ultimate (evolutionary) hypothesis of "bet hedging" on stochastic pollination. Yet, such mechanisms operating on fruit : flower ratios at the whole-plant level may not best explain low seed : ovule ratios at the individual-flower level. We tested each of these proximate and ultimate causes for low seed : ovule ratios using the specialized pollination mutualism between senita cacti (Pachycereus schottii) and senita moths (Upiga virescens). Seed : ovule ratios were consistently low (approximately 0.61). Such excess ovule production by senita likely has a strong genetic component given the significant differences among plants in ovule number and the consistency in ovule production by plants within and among flowering seasons. Excess ovule production and low seed : ovule ratios could not be explained by pollen limitation, resource limitation, pollen quality, or bet hedging. Nevertheless, phenotypic selection analyses did show significant selection gradients for increased ovule number, suggesting that other evolutionary processes may be responsible for excess ovule production and low seed : ovule ratios. In contrast, low fruit : flower ratios at the whole-plant level were explained by an apparent equilibrium between pollen and resource limitation. Thus, mechanisms responsible for low fruit : flower ratios at the whole-plant level are not necessarily in accord with those of low seed : ovule ratios at the individual-flower level. This suggests that we may need to adopt a more pluralistic approach to seed : ovule ratios and consider alternative hypotheses, including a greater array of proximate and ultimate causes. Initial results of this study suggest that floral allometry, selection on correlated floral traits, stigma clogging with pollen grains, and style clogging with pollen tubes may provide promising avenues for understanding low seed : ovule ratios.     

Revealing how species loss affects ecosystem function: the trait-based Price Equation partition

Species loss can alter ecosystem function. Recent work proposes a general theoretical framework, the "Price Equation partition," for understanding how species loss affects ecosystem functions that comprise the summed contributions of individual species (e.g., primary production). The Price Equation partition shows how the difference in function between a pre-species-loss site and a post-loss site can be partitioned into effects of random loss of species richness (species-richness effect; SRE), nonrandom loss of high- or low-functioning species (species-composition effect; SCE), and post-loss changes in the functional contributions of the remaining species (context-dependence effect; CDE). However, the Price Equation partition is silent on the underlying determinants of species' functional contributions. Here we extend the Price Equation partition by using multiple regression to describe how species' functional contributions depend on species' traits. This allows us to reexpress the SCE and CDE in terms of nonrandom loss of species with particular traits (trait-based SCE), and post-loss changes in species' traits and in the relationship between species' traits and species' functional contributions (trait-based CDE). We apply this new trait-based Price Equation partition to studies of species loss from grassland plant communities and protist microcosm food webs. In both studies, post-loss changes in the relationship between species' traits and their functional contributions alter ecosystem function more than nonrandom loss of species with particular traits. The protist microcosm data also illustrate how the trait-based Price Equation partition can be applied when species' functional contributions depend in part on the traits of other species. To do this, we define "synecological" traits that quantify how unique species are (e.g., in diet) compared to other species. Context dependence in the protist microcosm experiment arises in part because species loss alters the diet uniqueness of the remaining species.     

The evolution of cheating and selfish behavior

Summary We examine the necessary conditions for the spread of genes that determine selfish and cheating behaviors and the rate of spread of these genes through structured populations, in order to address the question of the invadability of altruistic systems by anti-social mutations. We find that, although cheaters always have a higher relative fitness than altruists within groups, population structures which permit the evolution of altruism also preclude invasion by anti-social mutations. These results are related to a discussion by Hamilton (1971) concerning the limits to the evolution of altruistic and selfish behaviors.     

The hunting handicap: costly signaling in human foraging strategies

Humans sometimes forage or distribute the products of foraging in ways that do not maximize individual energetic return rates. As an alternative to hypotheses that rely on reciprocal altruism to counter the costs of inefficiency, we suggest that the cost itself could be recouped through signal benefit. Costly signaling theory predicts that signals can provide fitness benefits when costs are honestly linked to signaler quality, and this information is broadcast to potential mates and competitors. Here, we test some predictions of costly signaling theory against empirical data on human food acquisition and sharing patterns. We show that at least two types of marine foraging, turtle hunting and spearfishing, as practiced among the Meriam (a Melanesian people of Torres Strait, Australia) meet key criteria for costly signaling: signal traits are (1) differentially costly or beneficial in ways that are (2) honestly linked to signaler quality, and (3) designed to effectively broadcast the signal. We conclude that relatively inefficient hunting or sharing choices may be maintained in a population if they serve as costly and reliable signals designed to reveal the signaler's qualities to observers.     

Benefits of memory for the evolution of tag-based cooperation in structured populations

We study the effects of working memory capacity and network rewiring probability on the evolution of cooperation in the standard and modified versions of an agent-based model of tag-mediated altruism. In our evolutionary model, computational agents populate a large complex network, engage into multiplayer Prisoner’s Dilemma-like interactions, and reproduce sexually. Agents carry discernible phenotypic traits subject to mutation, memorize their own experiences, and employ different strategies when interacting with different types of co-players. Choices made are selected from a pool of two conditional and two unconditional strategies, depending on the available memory contents and phenotypic similarity among interactors. For the dominating strategy in our standard model version, we found a strong dependence of cooperation on network structure and a weak one on memory, whereas in the modified version, the structural effect was weaker than that of memory. Most importantly, we found that the previously reported decline of cooperation in memory-based models, typically observed at a high memory capacity, is now prevented with the help of tags. This suggests that the evolutionary advantages of memory capacity limits may be far more complex than previously assumed. For much smaller systems, we observed a quasi-symmetric alternation of the two winning groups of strategists. This result provides an example of ingroup biased interactions that are characterized by bursts of intra-tag cooperation interspersed with periods of unconditional transient altruism. Such switches of strategies may represent a boosting mechanism necessary for the emergence and stability of global altruism in its early evolutionary stages.     

Female fitness, sperm traits and patterns of paternity in an Australian polyandrous mouse

Multiple mating is a common reproductive strategy among mammals, and rodents living in communal, mixed sex social groups are predisposed to a polygamous existence. The sandy inland mouse is a naturally polyandrous species that occurs across most of Australia’s arid region. Females typically have greater reproductive restrictions compared with males and are therefore expected to acquire substantial fitness benefits from copulating with more than one male. Here, I show that the reproductive output of female sandy inland mice did not differ between females mated monandrously (single male) or polyandrously (two males). Paternity data obtained from the polyandrous litters revealed that in most cases, there was a first male-to-mate advantage. I discuss this result in relation to the chastity enforcement hypothesis for the evolution of the copulatory plug. Finally, I compared ejaculate traits of competing males and found that the paternity loss of males that mated first was attributable to their own sperm density and sperm quality, and not to that of their rivals. The sperm data also revealed that second males gained greater paternity representation when sperm velocities and motilities were higher in first-mated males. This investigation indicates that mating position is a critical determinant of male fitness in mammalian sperm competition.     

Niche and fitness differences relate the maintenance of diversity to ecosystem function

The frequently observed positive correlation between species diversity and community biomass is thought to depend on both the degree of resource partitioning and on competitive dominance between consumers, two properties that are also central to theories of species coexistence. To make an explicit link between theory on the causes and consequences of biodiversity, we define in a precise way two kinds of differences among species: niche differences, which promote coexistence, and relative fitness differences, which promote competitive exclusion. In a classic model of exploitative competition, promoting coexistence by increasing niche differences typically, although not universally, increases the "relative yield total", a measure of diversity's effect on the biomass of competitors. In addition, however, we show that promoting coexistence by decreasing relative fitness differences also increases the relative yield total. Thus, two fundamentally different mechanisms of species coexistence both strengthen the influence of diversity on biomass yield. The model and our analysis also yield insight on the interpretation of experimental diversity manipulations. Specifically, the frequently reported "complementarity effect" appears to give a largely skewed estimate of resource partitioning. Likewise, the "selection effect" does not seem to isolate biomass changes attributable to species composition rather than species richness, as is commonly presumed. We conclude that past inferences about the cause of observed diversity-function relationships may be unreliable, and that new empirical estimates of niche and relative fitness differences are necessary to uncover the ecological mechanisms responsible for diversity-function relationships.     

A chemical trait creates a genetic trade-off between intra- and interspecific competitive ability

The importance of non-resource-based mechanisms of competition between plant species has been increasingly recognized, but little is known about how genetic variation and evolutionary changes in the underlying competitive traits might affect species coexistence. I found that genetic variation in sinigrin concentration, a putative allelopathic agent in Brassica nigra, affected the fitness of three heterospecific neighbor species but did not affect neighboring B. nigra individuals. Investment in sinigrin led to a negative genetic correlation between intra- and interspecific competitive ability, which over many generations could provide a strong stabilizing force maintaining both species and genetic diversity in this system.     

Reconciling empirical ecology with neutral community models

Neutral community models embody the idea that individuals are ecologically equivalent, having equal fitness over all environmental conditions, and describe how the spatial dynamics and speciation of such individuals can produce a wide range of patterns of distribution, diversity, and abundance. Neutral models have been controversial, provoking a rush of tests and comments. The debate has been spurred by the suggestion that we should test mechanisms. However, the mechanisms and the spatial scales of interest have never clearly been described, and consequently, the tests have often been only peripherally relevant. At least two mechanisms are present in spatially structured neutral models. Dispersal limitation causes clumping of a species, which increases the strength of intraspecific competition and reduces the strength of interspecific competition. This may prolong coexistence and enhance local and regional diversity. Speciation is present in some neutral models and gives a donor-controlled input of new species, many of which remain rare or are short lived, but which directly add to species diversity. Spatial scale is an important consideration in neutral models. Ecological equivalence and equal fitness have implicit spatial scales because dispersal limitation and its emergent effects operate at population levels, and populations and communities are defined at a chosen spatial scale in recent neutral models; equality is measured relative to a metacommunity, and this necessitates defining the spatial scale of that metacommunity. Furthermore, dispersal has its own scales. Thorough empirical tests of neutral models will require both tests of mechanisms and pattern-producing ability, and will involve coupling theoretical models and experiments.     

Testing the evolution of increased competitive ability (EICA) hypothesis in a novel framework

The "evolution of increased competitive ability" (EICA) hypothesis proposes that escape from natural enemies, e.g., after transcontinental introductions, alters the selection regime because costly defenses no longer enhance fitness. Such an evolutionary loss of defenses enables resources to be directed toward growth or other traits improving performance. We tested the EICA hypothesis in a novel framework in which the natural enemy is the traveler that follows its widespread host by accidental or deliberate (biocontrol) introductions. In a greenhouse experiment we used populations of Senecio vulgaris from North America, Europe, and Australia that differ in the history of exposure to the rust fungus Puccinia lagenophorae. Contrary to what is predicted by EICA, we found no evidence for increased levels of resistance to the rust fungus in plant populations with a longer history of rust exposure (Australia). Similarly, there was no evidence for reduced fecundity in these populations, although vegetative vigor, measured as secondary branching and growth rate, was lower. The maintenance of high rust resistance in populations with no (North America) or only a short history (Europe) of rust exposure is surprising given that resistance seems to incur considerable fitness costs, as indicated by the negative association between family mean resistance and fitness in the absence of disease observed for all three continents. The comparison of population differentiation in quantitative traits with estimates of differentiation in amplified fragment length polymorphic (AFLP) markers suggests that a number of fitness-related traits are under divergent selection among the studied populations. The proposed framework to test changes in the evolutionary trajectory underlying EICA can be employed in an expanded range of systems. These may include investigations on a cosmopolitan weed or crop when an antagonist is expanding its geographic range (such as our study), studies along a chronosequence of introduction time with expected increasing accumulation of natural enemies over time, or comparisons between introduced plant populations that differ in exposure time to biocontrol organisms.     

Female lizards discriminate between potential reproductive partners using multiple male traits when territory cues are absent

Female choice can powerfully influence the evolution of male phenotypes. In territorial species, it is challenging to determine the targets of female choice because male traits (e.g., behavior and morphology) are often correlated with territory. We sought to elucidate if and how females specifically evaluate male traits in a territorial species. In this study, we presented female fence lizards, Sceloporus undulatus, with two potential mates to examine mate choice in the absence of territory cues. Females associated more with males possessing better body condition, longer heads, and wider throat badges, and that performed more shudder behavior, which females responded to by approaching shuddering males and performing push-ups. A post hoc decision tree analysis suggests that the strongest predictor of female association was an overall quality index that incorporates all of these traits, rather than individual traits. Male snout–vent length, head width, abdominal badge width, and push-up behavior did not affect female association. Further research on why these traits, which are known to correlate with fitness, do not appear to be used by females when selecting mates would improve our understanding of the evolution of male traits. Our study reveals that females of this territorial species possess the ability to use multiple male traits interactively to make fitness-relevant mate choice decisions in the absence of direct territory cues.     

Worker senescence and the sociobiology of aging in ants

Senescence, the decline in physiological and behavioral function with increasing age, has been the focus of significant theoretical and empirical research in a broad array of animal taxa. Preeminent among invertebrate social models of aging are ants, a diverse and ecologically dominant clade of eusocial insects characterized by reproductive and sterile phenotypes. In this review, we critically examine selection for worker life span in ants and discuss the relationship between functional senescence, longevity, task performance, and colony fitness. We did not find strong or consistent support for the hypothesis that demographic senescence in ants is programmed, or its corollary prediction that workers that do not experience extrinsic mortality die at an age approximating their life span in nature. We present seven hypotheses concerning how selection could favor extended worker life span through its positive relationship to colony size and predict that large colony size, under some conditions, should confer multiple and significant fitness advantages. Fitness benefits derived from long worker life span could be mediated by increased resource acquisition, efficient division of labor, accuracy of collective decision-making, enhanced allomaternal care and colony defense, lower infection risk, and decreased energetic costs of workforce maintenance. We suggest future avenues of research to examine the evolution of worker life span and its relationship to colony fitness and conclude that an innovative fusion of sociobiology, senescence theory, and mechanistic studies of aging can improve our understanding of the adaptive nature of worker life span in ants.     

Sex linkage among genes controlling sexually selected traits

Using literature data on reciprocal crosses I estimated the influence of sex-chromosomal genes on morphological and behavioral traits. To determine a special role of the sex chromosomes for sexually selected traits, I compared the estimated influence of X-chromosomal genes on sexually selected traits with their estimated influence on traits not under sexual selection. About one-third of the phenotypic variation in sexually selected traits is caused by X-chromosomal genes. There was, in contrast, no significant influence of X-chromosomal genes on traits that were classified as not sexually selected. Sexually selected traits thus seem to be influenced significantly more by X-chromosomal genes than traits not under sexual selection. Though this differential influence of X-chromosomal genes cannot readily be explained with current theoretical knowledge, it may shed some light on X-linked hybrid sterility and on the discussion between arbitrary and good-gene models for the evolution of female choice. Received: 30 January 1998 / Accepted after revision: 20 June 1998     

Testing hypotheses in evolutionary ecology with imperfect detection: capture-recapture structural equation modeling

Studying evolutionary mechanisms in natural populations often requires testing multifactorial scenarios of causality involving direct and indirect relationships among individual and environmental variables. It is also essential to account for the imperfect detection of individuals to provide unbiased demographic parameter estimates. To cope with these issues, we developed a new approach combining structural equation models with capture-recapture models (CR-SEM) that allows the investigation of competing hypotheses about individual and environmental variability observed in demographic parameters. We employ Markov chain Monte Carlo sampling in a Bayesian framework to (1) estimate model parameters, (2) implement a model selection procedure to evaluate competing hypotheses about causal mechanisms, and (3) assess the fit of models to data using posterior predictive checks. We illustrate the value of our approach using two case studies on wild bird populations. We first show that CR-SEM can be useful to quantify the action of selection on a set of phenotypic traits with an analysis of selection gradients on morphological traits in Common Blackbirds (Turdus merula). In a second case study on Blue Tits (Cyanistes caeruleus), we illustrate the use of CR-SEM to study evolutionary trade-offs in the wild, while accounting for varying environmental conditions.     

Patterns of growth and fluctuating asymmetry: the effects of asymmetrical investment in traits with determinate growth

Fluctuating asymmetry (FA, small and random deviations from perfect symmetry in otherwise bilaterally symmetrical traits) is assumed to depend directly on developmental stability (DS). However, since the processes related to DS operate at a microscopic level, the translation of microscopic errors to the macroscopic character asymmetries (i.e. the DS-FA relation) could be mediated by the cost of growth. To investigate the consequences of this hypothesis, I constructed a model with the following assumptions: the degree of development of a trait depends on the amount of resources allocated to growth, which may differ between individuals and between traits; the cost of growth increases with development, and developmental noise causes random asymmetries in biosynthesis in the two sides of the body. The model predicts that FA follows a parabolic trajectory as growth investment levels increase, regardless of DS. However, depending on the range of variation of investment levels, different relationships (positive, negative or flat) between trait size and asymmetry could be expected. This model may also explain why FA is correlated with the degree of stress in some traits but not in others, and why some traits present a higher level of FA than others. The model also suggests that FA measured on growing traits, at a certain size, could be a more reliable indicator of DS than FA measured on fully grown traits. A study analysing FA patterns of developing and fully grown feathers in the house sparrow (Passer domesticus) corroborates that the levels of FA, and the relationship between asymmetry and feather length, depend on the degree of feather development.