Familial selection and the evolution of social behaviour re-examined

The equation for the fitness requirements for the evolution of altruism by diploid workers in haplodiploid species was derived from the model. of Scudo & Ghiselin (1975). When the benefit to a family is proportional to the number of altruists, the constraints on fitness were found to be the same as for haploid altruists in haplodiploid species and for workers of ether sex in diploid species, in contrast to the equation given by Scudo & Ghiselin (1975). With this correction, their results are now in agreement both with comparable allele frequency models and with kin selection games theory. The general condition for evolution of altruism under this model, when benefits are not necessarily proportional to the number of altruists, was also derived. The result appears to differ from games theory predictions, but this is solely because the basic assumptions are not comparable. Altruism is less likely to arise under these conditions, which are less favorable for altruism at gene frequencies above 0·33.     

Evolution of eusociality by kin selection: the effect of inbreeding between siblings

The effect of sib-sib inbreeding on the evolution of eusocial altruism in Hymenoptera by kin selection is examined by computer simulations. Inbreeding has minor effects on the ratio of relatedness to siblings: relatedness to offspring, but this ratio remains approximately one no matter what the degree of inbreeding. This implies that although inbreeding increases relatedness to siblings, relatedness to offspring increases to the same degree. Hence, inbreeding does not make the evolution of altruism more likely. If all the brothers of (non-mating) altruists outbreed, thereby increasing the frequency of altruism alleles in the outbred fraction of the population especially at low gene frequency, then altruism can be promoted by inbreeding. However, this is an indirect advantage, not attributable to inbreeding per se.     

Effects of brood manipulation costs on optimal sex allocation in social hymenoptera

In eusocial Hymenoptera, queens and workers are in conflict over optimal sex allocation. Sex ratio theory, while generating predictions on the extent of this conflict under a wide range of conditions, has largely neglected the fact that worker control of investment almost certainly requires the manipulation of brood sex ratio. This manipulation is likely to incur costs, for example, if workers eliminate male larvae or rear more females as sexuals rather than workers. In this article, we present a model of sex ratio evolution under worker control that incorporates costs of brood manipulation. We assume cost to be a continuous, increasing function of the magnitude of sex ratio manipulation. We demonstrate that costs counterselect sex ratio biasing, which leads to less female-biased population sex ratios than expected on the basis of relatedness asymmetry. Furthermore, differently shaped cost functions lead to different equilibria of manipulation at the colony level. While linear and accelerating cost functions generate monomorphic equilibria, decelerating costs lead to a process of evolutionary branching and hence split sex ratios.     

Sex-ratio conflict between queens and workers in eusocial Hymenoptera: mechanisms, costs, and the evolution of split colony sex ratios

Because workers in the eusocial Hymenoptera are more closely related to sisters than to brothers, theory predicts that natural selection should act on them to bias (change) sex allocation to favor reproductive females over males. However, selection should also act on queens to prevent worker bias. We use a simulation approach to analyze the coevolution of this conflict in colonies with single, once-mated queens. We assume that queens bias the primary (egg) sex ratio and workers bias the secondary (adult) sex ratio, both at some cost to colony productivity. Workers can bias either by eliminating males or by directly increasing female caste determination. Although variation among colonies in kin structure is absent, simulations often result in bimodal (split) colony sex ratios. This occurs because of the evolution of two alternative queen or two alternative worker biasing strategies, one that biases strongly and another that does not bias at all. Alternative strategies evolve because the mechanisms of biasing result in accelerating benefits per unit cost with increasing bias, resulting in greater fitness for strategies that bias more and bias less than the population equilibrium. Strategies biasing more gain from increased biasing efficiency whereas strategies biasing less gain from decreased biasing cost. Our study predicts that whether queens or workers evolve alternative strategies depends upon the mechanisms that workers use to bias the sex ratio, the relative cost of queen and worker biasing, and the rates at which queen and worker strategies evolve. Our study also predicts that population and colony level sex allocation, as well as colony productivity, will differ diagnostically according to whether queens or workers evolve alternative biasing strategies and according to what mechanism workers use to bias sex allocation.     

Sex ratios and the evolution of eusociality in the hymenoptera

The potential role of sex ratio biassing in the evolution of worker behaviour in male-haploid hymenopteran insects is examined using a deterministic genetic model. The model is based on a bivoltine life cycle with annual colonies and it assumes five gene loci, each of them controlling a specific feature of the life cycle (particularly brood sex ratios). The hypothetical gene controlling worker behaviour is assumed to be expressed either in the mothers (parental manipulation models) or in the female offspring (offspring altruism models). The threshold of the worker efficiency required for the worker behaviour to evolve is 0.5 under parental manipulation and 1.0 under offspring altruism when the sex ratios are not skewed. Worker evolution by offspring altruism can evolve more easily if the first workers initially raise mainly female brood. With such a sex ratio bias, the threshold of worker efficiency allowing eusociality to evolve drops below 1.0, even close to 0.8. Worker evolution is also favoured by the elimination of males from the first of the two annually occurring offspring generations. It is concluded that the male-haploid sex determination can, through the control of sex ratios, play a significant role in the evolution of eusociality in hymenopteran insects.     

Effective population size in eusocial Hymenoptera with worker-produced males

In many eusocial Hymenoptera, a proportion of males are produced by workers. To assess the effect of male production by workers on the effective population size N_e, a general expression of N_e in Hymenoptera with worker-produced males is derived on the basis of the genetic drift in the frequency of a neutral allele. Stochastic simulation verifies that the obtained expression gives a good prediction of N_e under a wide range of conditions. Numerical computation with the expression indicates that worker reproduction generally reduces N_e. The reduction can be serious in populations with a unity or female-biased breeding sex ratio. Worker reproduction may increase N_e in populations with a male-biased breeding sex ratio, only if each laying worker produce a small number of males and the difference of male progeny number among workers is not large. Worker reproduction could be an important cause of the generally lower genetic variation found in Hymenoptera, through its effect on N_e.     

Sex-biased dispersal, haplodiploidy and the evolution of helping in social insects

In his famous haplodiploidy hypothesis, W. D. Hamilton proposed that high sister-sister relatedness facilitates the evolution of kin-selected reproductive altruism among Hymenopteran females. Subsequent analyses, however, suggested that haplodiploidy cannot promote altruism unless altruists capitalize on relatedness asymmetries by helping to raise offspring whose sex ratio is more female-biased than the population at large. Here, we show that haplodiploidy is in fact more favourable than is diploidy to the evolution of reproductive altruism on the part of females, provided only that dispersal is male-biased (no sex-ratio bias or active kin discrimination is required). The effect is strong, and applies to the evolution both of sterile female helpers and of helping among breeding females. Moreover, a review of existing data suggests that female philopatry and non-local mating are widespread among nest-building Hymenoptera. We thus conclude that Hamilton was correct in his claim that 'family relationships in the Hymenoptera are potentially very favourable to the evolution of reproductive altruism'.     

Sex ratios in bumble bees

The median proportion of investment in females among 11 populations of seven bumble bee (Bombus) species was 0.32 (range 0.07 to 0.64). By contrast, two species of workerless social parasites in the related genus Psithyrus had female-biased sex allocation, the reasons for which remain unclear. Male-biased sex allocation in Bombus contradicts the predictions of Trivers and Hare''s sex ratio model for the social Hymenoptera, which are that the population sex investment ratio should be 0.5 (1:1) under queen control and 0.75 (3:1 females:males) under worker control (assuming single, once-mated, outbred queens and non-reproductive workers). Male bias in Bombus does not appear to be either an artefact, or purely the result of symbiotic sex ratio distorters. According to modifications of the Trivers–Hare model, the level of worker male-production in Bombus is insufficient to account for observed levels of male bias. There is also no evidence that male bias arises from either local resource competition (related females compete for resources) or local mate enhancement (related males cooperate in securing mates). Bulmer presented models predicting sexual selection for protandry (males are produced before females) in annual social Hymenoptera and, as a consequence (given some parameter values), male-biased sex allocation. Bumble bees fit the assumptions of Bulmer''s models and are protandrous. These models therefore represent the best current explanation for the bees'' male-biased sex investment ratios. This conclusion suggests that the relative timing of the production of the sexes strongly influences sex allocation in the social Hymenoptera.     

Pleiotropy Can Be Effectively Estimated Without Counting Phenotypes Through the Rank of a Genotype–Phenotype Map

Although pleiotropy, the capability of a gene to affect multiple phenotypes, has been well known as one of the common gene properties, a quantitative estimation remains a great challenge, simply because of the phenotype complexity. Not surprisingly, it is hard for general readers to understand how, without counting phenotypes, gene pleiotropy can be effectively estimated from the genetics data. In this article we extensively discuss the Gu-2007 method that estimated pleiotropy from the protein sequence analysis. We show that this method is actually to estimate the rank (K) of genotype–phenotype mapping that can be concisely written as K = min(r, P_min), where P_min is the minimum pleiotropy among all legitimate measures including the fitness components, and r is the rank of mutational effects of an amino acid site. Together, the effective gene pleiotropy (K_e) estimated by the Gu-2007 method has the following meanings: (i) K_e is an estimate of K = min(r, P_min), the rank of a genotype–phenotype map; (ii) K_e is an estimate for the minimum pleiotropy P_min only if P_min < r; (iii) the Gu-2007 method attempted to estimate the pleiotropy of amino acid sites, a conserved proxy to the true gene pleiotropy; (iv) with a sufficiently large phylogeny such that the rank of mutational effects at an amino acid site is r → 19, one can estimate P_min between 1 and 19; and (v) K_e is a conserved estimate of K because those slightly affected components in fitness have been effectively removed by the estimation procedure. In addition, we conclude that mutational pleiotropy (number of traits affected by a single mutation) cannot be estimated without knowing the phenotypes.     

A comparison of the reproductive ability of <Emphasis Type="Italic">Varroa destructor</Emphasis> (Mesostigmata:Varroidae) in worker and drone brood of Africanized honey bees (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

Colony infestation by the parasitic mite, Varroa destructor is one of the most serious problems for beekeeping worldwide. In order to reproduce varroa females, enter worker or drone brood shortly before the cell is sealed. To test the hypothesis that, due to the preference of mites to invade drone brood to reproduce, a high proportion of the mite reproduction should occur in drone cells, a comparative study of mite reproductive rate in worker and drone brood of Africanized honey bees (AHB) was done for 370 mites. After determining the number, developmental stage and sex of the offspring in worker cells, the foundress female mite was immediately transferred into an uninfested drone cell. Mite fertility in single infested worker and drone brood cells was 76.5 and 79.3%, respectively. There was no difference between the groups (X ² = 0.78, P = 0.37). However, one of the most significant differences in mite reproduction was the higher percentage of mites producing viable offspring (cells that contain one live adult male and at least one adult female mite) in drone cells (38.1%) compared to worker cells (13.8%) (X ² = 55.4, P < 0.01). Furthermore, a high level of immature offspring occurred in worker cells and not in drone cells (X ² = 69, P < 0.01). Although no differences were found in the percentage of non-reproducing mites, more than 74% (n = 85) of the mites that did not reproduce in worker brood, produced offspring when they were transferred to drone brood.     

Colony-level selection in the social insects: Single locus additive and nonadditive models

Genetic models of colony-level selection applicable to diploids (termites) and haplodiploids (social Hymenoptera) are analysed. In the Additive model colony fitnesses are just the arithmetic average of the contribution of the worker genotypes. In the Nonadditive model the fitness of the heterogenotypic colonies (those comprised of more than one worker genotype) may be altered due to interaction between the different worker genotypes. This is modelled by multiplying the additive fitness by the variable, e_i. With additive selection the same equilibrium gene frequency occurs in diploids and in haplodiploids with both once and twice mated queens. In haplodiploids if selection is nonadditive and strong, up to three polymorphic equilibria can exist; however, only a maximum of two are possible with weak selection. Multiple mating by queens increases the number of equilibria possible. Worker-produced males alter the conditions for the existence of a polymorphic equilibrium, and shift the male and female equilibrium gene frequencies.     

The need for sperm selection may explain why termite colonies have kings and queens,whereas those of ants,wasps and bees have only queens

Hymenoptera have haploid males, which produce sperm by cloning. Sperm selection theory predicts that because termites have diploid males that produce genetically diverse sperm, they may profit from a high sperm surplus (large K), whereas Hymenoptera (ants, bees and wasps) should produce few sperm per fertilization (low Κ). Male reproductive “kings”, which continuously provide spermatozoa during the whole life of the queen, allow for a large K. Available empirical evidence confirms the existence of a large difference in K between diploid insects, especially Blattodea (Isoptera) (K > 1,000), and haplo-diploids such as Hymenoptera (K < 10). The available data suggest that sperm selection may be an important evolutionary force for species with diploid, but not haploid males.     

Response of foster Asian honeybee (Apis cerana Fabr.) colonies to the brood of European honeybee (Apis mellifera L.) infested with parasitic mite,Varroa jacobsoni oudemans

The response of Asian honeybee (Apis cerana Fabr.) colonies toward the introduced worker brood of the European honeybee (Apis mellifera L.) infested with the parasitic mite Varroa jacobsoni Oudemans was investigated. When no mites were present, 40% of the healthy open brood and 3% of the healthy capped brood of the European honeybees were rejected by the Asian honeybee colonies. When the brood was infested, brood rejection was significantly higher for open (P < 0.05) and capped broods (P < 0.01). The brood removal activity decreased with time. The quantity of brood removed was also correlated with mite infestation level for open (r² = 0.933) and sealed broods (r² = 0.918). The feasibility of using heterospecific colonies to control Varroa mite is unclear and is discussed from behavioral and ecological points of view.     

Sex allocation in the ant Camponotus (Colobopsis) nipponicus (Wheeler): II. The effect of resource availability on sex-ratio variability

Sex-ratio studies have played a prominent role in tests of kin selection theory in the eusocial Hymenoptera. The winner in sex-ratio conflict between queens and workers must control the ratio through proximate mechanisms. To determine how a colony adjusts its sex ratio, the mechanism of sex-ratio determination was analyzed in the field in colonies of the ant Camponotus (Colobopsis) nipponicus. A path model including five colony characteristics showed that the resource availability of the colony (quantified as the amount of stored fat in the bodies of the workers) has a large positive effect on the proportion of new queens in the female larvae, but has little effect on male production. The results indicated that a colony adjusts the sex ratio by altering the proportion of new queens obtained from a diploid brood in response to resource availability rather than by eliminating male larvae.     

Selective pressures for accurate altruism targeting: evidence from digital evolution for difficult-to-test aspects of inclusive fitness theory

Inclusive fitness theory predicts that natural selection will favour altruist genes that are more accurate in targeting altruism only to copies of themselves. In this paper, we provide evidence from digital evolution in support of this prediction by competing multiple altruist-targeting mechanisms that vary in their accuracy in determining whether a potential target for altruism carries a copy of the altruist gene. We compete altruism-targeting mechanisms based on (i) kinship (kin targeting), (ii) genetic similarity at a level greater than that expected of kin (similarity targeting), and (iii) perfect knowledge of the presence of an altruist gene (green beard targeting). Natural selection always favoured the most accurate targeting mechanism available. Our investigations also revealed that evolution did not increase the altruism level when all green beard altruists used the same phenotypic marker. The green beard altruism levels stably increased only when mutations that changed the altruism level also changed the marker (e.g. beard colour), such that beard colour reliably indicated the altruism level. For kin- and similarity-targeting mechanisms, we found that evolution was able to stably adjust altruism levels. Our results confirm that natural selection favours altruist genes that are increasingly accurate in targeting altruism to only their copies. Our work also emphasizes that the concept of targeting accuracy must include both the presence of an altruist gene and the level of altruism it produces.     

Effects of Intracellular Adenosine-5''-diphosphate and Orthophosphate on the Sensitivity of Sodium Efflux from Squid Axon to External Sodium and Potassium

A study was made of sodium efflux from squid giant axon, and its sensitivity to external K and Na. When sodium efflux from untreated axons was strongly stimulated by K_o, Na_o was inhibitory; when dependence on K_o was low, Na_o had a stimulatory effect. Incipient CN poisoning or apyrase injection, which produces high intracellular levels of ADP¹ and P_i, rendered sodium efflux less dependent on external K and more dependent on external Na. Injection of ADP, AMP, arginine, or creatine + creatine phosphokinase, all of which raise ADP levels without raising P_i levels, had the same effect as incipient CN poisoning. P_i injection had no effect on the K sensitivity of sodium efflux. Axons depleted of arginine and phosphoarginine by injection of arginase still lost their K sensitivity when the ATP:ADP ratio was lowered and regained it partially when the ratio was raised. Rough calculations show that sodium efflux is maximally K_o-dependent when the ATP:ADP ratio is about 10:1, becomes insensitive to K_o when the ratio is about 1:2, and is inhibited by K_o when the ratio is about 1:10. Deoxy-ATP mimicked ADP when injected into intact axons. Excess Mg, as well as P_i, inhibited both strophanthidin-sensitive and strophanthidin-insensitive sodium efflux. An outline is presented for a model which might explain the effects of ADP, P_i and deoxy-ATP.     

Sex investment ratios in eusocial Hymenoptera support inclusive fitness theory

Inclusive fitness theory predicts that sex investment ratios in eusocial Hymenoptera are a function of the relatedness asymmetry (relative relatedness to females and males) of the individuals controlling sex allocation. In monogynous ants (with one queen per colony), assuming worker control, the theory therefore predicts female‐biased sex investment ratios, as found in natural populations. Recently, E.O. Wilson and M.A. Nowak criticized this explanation and presented an alternative hypothesis. The Wilson–Nowak sex ratio hypothesis proposes that, in monogynous ants, there is selection for a 1 : 1 numerical sex ratio to avoid males remaining unmated, which, given queens exceed males in size, results in a female‐biased sex investment ratio. The hypothesis also asserts that, contrary to inclusive fitness theory, queens not workers control sex allocation and queen–worker conflict over sex allocation is absent. Here, I argue that the Wilson–Nowak sex ratio hypothesis is flawed because it contradicts Fisher's sex ratio theory, which shows that selection on sex ratio does not maximize the number of mated offspring and that the sex ratio proposed by the hypothesis is not an equilibrium for the queen. In addition, the hypothesis is not supported by empirical evidence, as it fails to explain ‘split’ (bimodal) sex ratios or data showing queen and worker control and ongoing queen–worker conflict. By contrast, these phenomena match predictions of inclusive fitness theory. Hence, the Wilson–Nowak sex ratio hypothesis fails both as an alternative hypothesis for sex investment ratios in eusocial Hymenoptera and as a critique of inclusive fitness theory.     

Evolution of social parasitism in ants: size of sexuals,sex ratio and mechanisms of caste determination

Social parasitism, one of the most intriguing phenomena in ants, has evolved to various levels, the most extreme form being parasites that have lost the worker caste and rely completely on the host''s worker force to raise their brood. A remarkable feature of workerless social parasites is the small size of sexuals. It has been suggested that reduced size evolved as a means to take advantage of the host''s caste-determination system, so that parasite larvae develop into sexuals with less food than is required to produce host workers. An important consequence of size reduction is that it might restrict the host workers'' ability to discriminate between the brood of the social parasite and their own brood and might protect parasite sexuals from elimination. We found that sexuals of the workerless inquiline ant Plagiolepis xene were significantly smaller than the sexuals of their host Plagiolepis pygmaea, but remarkably similar to the host workers. The size variance of parasite sexuals was much lower than that of their host; this result possibly suggests that there is very stabilizing selection acting on size of the parasite sexuals. Comparison of the primary (egg) and secondary (adult) sex ratios of the parasite and host showed that miniaturization of P. xene sexuals has been accompanied by their ability to develop into sexuals even when the host P. pygmaea actively prevents production of its own sexuals. These results suggest that the inquiline''s size and caste threshold have been reduced such that all individuals in a parasite brood will develop into sexuals. We also found that the adult sex ratio of P. xene was heavily female-biased. This bias probably stems from local mate competition that arises from sexuals mating within the nest. There was no significant difference between the proportion of haploid eggs and adult males produced; this observation indicates that a female-biased sex ratio is achieved by queens producing a higher proportion of diploid eggs rather than by a higher mortality of haploid males.     

Properties of the Mg2+-induced low-affinity nucleotide binding site of (Na++ K+)-activated ATPase

(1) The Mg²⁺-induced low-affinity nucleotide binding by (Na⁺ + K⁺)-ATPase has been further investigated. Both heat treatment (50–65°C) and treatment with N-ethylmaleimide reduce the binding capacity irreversibly without altering the K_d value. The rate constant of inactivation is about one-third of that for the high-affinity site and for the (Na⁺ + K⁺)-ATPase activity. (2) Thermodynamic parameters (ΔH° and ΔS°) for the apparent affinity in the ATPase reaction (K_m ATP) and for the true affinity in the binding of AdoPP[NH]P (K_d and K_i) differ greatly in sign and magnitude, indicating that one or more reaction steps following binding significantly contribute to the K_m value, which thus is smaller than the K_d value. (3) Ouabain does not affect the capacity of low-affinity nucleotide binding, but only increases the K_d value to an extent depending on the nucleotide used. GTP and CTP appear to be most sensitive, ATP and ADP intermediately sensitive and AdoPP[NH]P and least sensitive to ouabain. Ouabain reduces the high-affinity nucleotide binding capacity without affecting the K_d value. (4) The nucleotide specificity of low-affinity binding site is the same for binding (competition with AdoPP[NH]P) and for the ATPase activity (competition with ATP): AdoPP[NH]P > ATP > ADP > AMP. (5) The low-affinity nucleotide binding capacity is preserved in the ouabain-stabilized phosphorylated state, and the K_d value is not increased more than by ouabain alone. (6) It is inferred that the low-affinity site is Iocated on the enzyme, more specifically its α-subunit, and not on the surrounding phospholipids. It is situated outside the phosphorylation centre. The possible functional role of the low-affinity binding is discussed.     

Sex Ratios in a Socially Parasitic Bee and Implications for Host-Parasite Interactions

Obligate social parasites of Hymenoptera, known as inquilines, have received enormous attention due to the elaborate adaptations they exhibit for exploiting their hosts, and because they have frequently been used to infer sympatric speciation. Their population biology can be difficult to infer as they are both rare and difficult to extract from host nests. Sex allocation has been studied for very few inquilines of social Hymenoptera. Here we report sex ratio patterns in the allodapine bee Inquilina schwarzi, which is an obligate social parasite of another allodapine, Exoneura robusta. We show that the sex ratio of this inquiline varies with its brood number, it is female-biased in the smallest broods, but becomes more even in larger broods, where the population-wide sex ratio is close to parity. We argue that this pattern of bias is consistent with local resource competition, where inquiline females compete to inherit their natal colony. We also argue that extremely female-biased sex ratios of the host species, combined with overall sex ratio parity in the parasite, may help ameliorate disparity in effective population sizes between these two species which are locked in an evolutionary arms race.