Evolution of paternal care in diploid and haplodiploid populations

W. D. Hamilton famously suggested that the inflated relatedness of full sisters under haplodiploidy explains why all workers in the social hymenoptera are female. This suggestion has not stood up to further theoretical scrutiny and is not empirically supported. Rather, it appears that altruistic sib‐rearing in the social hymenoptera is performed exclusively by females because this behaviour has its origins in parental care, which was performed exclusively by females in the ancestors of this insect group. However, haplodiploidy might still explain the sex of workers if this mode of inheritance has itself been responsible for the rarity of paternal care in this group. Here, we perform a theoretical kin selection analysis to investigate the evolution of paternal care in diploid and haplodiploid populations. We find that haplodiploidy may either inhibit or promote paternal care depending on model assumptions, but that under the most plausible scenarios it promotes – rather than inhibits – paternal care. Our analysis casts further doubt upon there being a causal link between haplodiploidy and eusociality.     

The evolutionary origin and elaboration of sociality in the aculeate Hymenoptera: maternal effects, sib-social effects, and heterochrony

We discuss the evolutionary origin and elaboration of sociality using an indirect genetic effects perspective. Indirect genetic effects models simultaneously consider zygotic genes, genes expressed in social partners (especially mothers and siblings), and the interactions between them. Incorporation of these diverse genetic effects should lead to more realistic models of social evolution. We first review haplodiploidy as a factor that promotes the evolution of eusociality. Social insect biologists have doubted the importance of relatedness asymmetry caused by haplodiploidy and focused on other predisposing factors such as maternal care. However; indirect effects theory shows that maternal care evolves more readily in haplodiploids, especially with inbreeding and despite multiple mating. Because extended maternal care is believed to be a precondition for the evolution of eusociality, the evolutionary bias towards maternal care in haplodiploids may result in a further bias towards eusociality in these groups. Next, we compare kin selection and parental manipulation and then briefly review additional hypotheses for the evolutionary origin of eusociality. We present a verbal model for the evolutionary origin and elaboration of sib-social care from maternal care based on the modification of the timing of expression of maternal care behaviors. Specifically, heterochrony genes cause maternal care behaviors to be expressed prereproductively towards siblings instead of postreproductively towards offspring. Our review demonstrates that both maternal effect genes (expressed in a parental manipulation manner) and direct effect zygotic genes (expressed in an offspring control manner) are likely involved in the evolution of eusociality. We conclude by describing theoretical and empirical advances with indirect genetic effects and sociogenomics, and we provide specific quantitative genetic and genomic predictions from our heterochrony model for the evolutionary origin and elaboration of eusociality.     

Ploidy of the eusocial beetle Austroplatypus incompertus (Schedl) (Coleoptera, Curculionidae) and implications for the evolution of eusociality

In the hymenopterans, haplodiploidy, leading to high-genetic relatedness amongst full sisters has been regarded as critical to kin selection and inclusive fitness hypotheses that explain the evolution of eusociality and altruistic behaviours. Recent evidence for independent origins of eusociality in phylogenetically diverse taxa has led to the controversy regarding the general importance of relatedness to eusociality and its evolution. Here, we developed a highly polymorphic microsatellite marker to test whether the eusocial ambrosia beetle Austroplatypus incompertus (Schedl) is haplodiploid or diplodiploid. We found that both males and females of A. incompertus are diploid, signifying that altruistic behaviour resulting from relatedness asymmetries did not play a role in the evolution of eusocialty in this species. This provides additional evidence against the haplodiploidy hypothesis and implicates alternative hypotheses for the evolution of eusociality.     

Haplodiploidy and the evolution of eusociality: split sex ratios

It is generally accepted that from a theoretical perspective, haplodiploidy should facilitate the evolution of eusociality. However, the "haplodiploidy hypothesis" rests on theoretical arguments that were made before recent advances in our empirical understanding of sex allocation and the route by which eusociality evolved. Here we show that several possible promoters of the haplodiploidy effect would have been unimportant on the route to eusociality, because they involve traits that evolved only after eusociality had become established. We then focus on two biological mechanisms that could have played a role: split sex ratios as a result of either queen virginity or queen replacement. We find that these mechanisms can lead haplodiploidy to facilitating the evolution of helping but that their importance varies from appreciable to negligible, depending on the assumptions. Furthermore, under certain conditions, haplodiploidy can even inhibit the evolution of helping. In contrast, we find that the level of promiscuity has a strong and consistently negative influence on selection for helping. Consequently, from a relatedness perspective, monogamy is likely to have been a more important driver of eusociality than the haplodiploidy effect.     

A theory of natural selection incorporating interaction among individuate. X. Use of groups consisting of a mating pair together with haploid and diploid caste members

This paper and the previous member of the series, deal with genetical mechanisms responsible for the evolution of eusociality (a level of social organization that includes differentiated sterile castes) among the “social” insects. Eusociality has evolved in a number of different species. Two different types of genetic systems are represented among these species: diplodiploidy (both sexes diploid) and haplodiploidy (haploid males and diploid females). The previous paper examined the evolution of a sterile caste system in the context of diplodiploidy, and the present paper considers the evolution of eusociality in the context of haplodiploidy.The present study demonstrates that selection operating with regard to random groups within the haplodiploid inheritance system cannot result in the evolution of a sterile caste system. Thus haplodiploidy, in itself, is not sufficient for the evolution of eusociality. However, if the sterile caste members are related to the reproductive members of the group, the appropriate caste associate gene effects are included in the function determining gene frequency change (i.e. Δp_i), and therefore, eusociality can evolve. This is true for both haploid and diploid castes.In comparing the two modes of inheritance, it is demonstrated that haplodiploidy provides up to 37·5% increased selection efficiency relative to diplodiploidy in evolving a social caste system in the absence of inbreeding.     

Can maternally transmitted endosymbionts facilitate the evolution of haplodiploidy?

Whilst many invertebrate taxa are haplodiploid, the factors underlying the evolution of haplodiploidy remain unresolved. We investigate theoretically whether haplodiploidy might evolve as an outcome of the co-evolution between maternally inherited endosymbionts and their hosts. First, we substantially extend a recently developed model that involves maternally inherited endosymbionts that kill male offspring by eliminating the paternal genome. We also put forward a new hypothesis and develop a model that involves bacteria that induce cytoplasmic incompatibility (CI). Based on these models, we explore the co-evolutionary events that might occur between hosts and symbionts. We find that both with male-killers and CI-inducing endosymbionts, the hosts are likely to develop increased viability of haploid males, which can be considered a preadaptation to haplodiploidy. In addition, populations with haploidizing male-killers can in some cases evolve directly towards a genetic system of paternal genome elimination, a special form of haplodiploidy. These results are combined with consideration of mechanism and ecology to appraise the likelihood of male-killers and CI inducing bacteria being involved in the evolution of haplodiploidy.     

Factors governing the evolution of eusociality through kin selection

The evolution of eusociality through kin selection was analyzed by simple population genetical models. Models were solved analytically with no approximation. The main results are

1. Sex ratio in reproductives in a colony of haplodiploid species does not affect the direction of evolution, contrary to the hypothesis ofTrivers andHare (1976). Female biased sex ratio increases the rate of evolution irrespective of its direction.
2. The only factor that determines the direction of evolution is the balance of benefit and cost of altruism of workers.
3. The value of ratio of benefit to cost of altruism of workers when the change of gene frequency of altruistic allele does not take place is unity in both haplodiploid and diploid species. There is no theoretical reason that the eusociality through kin selection evolves more easily in haplodiploidy than in diploidy, contrary to the hypotheses ofHamilton (1964) andTrivers andHare (1976).
4. The larger the colony size is, the lower the rate of evolution is irrespective of its direction.

It was concluded that discussion on the evolution of altruism which depended on only the values of the degrees of relatedness is misleading. The importance of life history structure, oviposition of workers and number of relating gene(s) in the evolution of eusociality were discussed.     

Evolution of haplodiploidy: Models for inbred and outbred systems

Several new models are proposed for the evolution of haplodiploidy. Each of these models is evaluated for its ability to explain (1) special problems associated with transition to haplodiploidy from a population of diplodiploid progenitors, (2) current patterns of population structure in haplodiploid and related species, and (3) the evolution of genetic systems similar but not identical to haplodiploid systems. Of the new models, three are based on special conditions associated with inbreeding. Close inbreeding provides for the automatic effects of reduced problems in expressing recessives, lowered differences in gain from heterozygosity (to produce both heterotic effects and a greater variety of offspring) between haploid and diploid males, effective protection of haploids from direct competition with diploids, and a mechanism for the spread of haplodiploidy through gains derived from increased ability to control sex ratio. These models differ in the context where gain from sex ratio control is expressed. Pathways for the evolution of haplodiploidy in outbreeding populations are also discussed. Females who parthenogenetically produce haploid males have high genetic relatedness to their sons. If the sperm of these males is used to make both sons and daughters, i.e., through matings with diplodiploid females, there may be a net gain for haplodiploids. Another outbreeding model, modified from S. W. Brown (1964, Genetics49, 797–817), deals with selection for females producing haploid males in populations where there are driving sex chromosomes. Biases created by drive in sex ratio may allow haplodiploid females to be the only effective producers of males in the population. Several of the new models explain the whole range of haplodiploid and related adaptations and provide predictions that appear to be more consistent with the known structure of contemporary populations than those available in current models.     

On testing the role of genetic asymmetries created by haplodiploidy in the evolution of eusociality in the Hymenoptera

The haplodiploid genetic system found in all Hymenopterans creates an asymmetry in genetic relatedness so that full-sisters are more closely related to each other than a mother is to her daughters. Thus Hymenopteran workers who rear siblings can obtain higher inclusive fitness compared to individuals who rear offspring. However, polyandry and polygyny reduce relatedness between workers and their sisters and thus tend to break down the genetic asymmetry created by haplodiploidy. Since the advent of electrophoretic analysis of variability at enzyme loci, several estimates of intra-colony genetic relatedness in the Hymenoptera have been published. To test the role of the genetic asymmetry created by haplodiploidy in the evolution of eusociality, I assume that workers are capable of investing in their brothers and sisters in their ratio of relatedness to them. I then compute ahaplodiploidy threshold, which is the threshold relatedness to sisters required for workers to obtain a weighted mean relatedness of 0.5 to siblings and thus break even with solitary foundresses. When workers rear mixtures of sisters and brothers in an outbred population, the value of this threshold is 0.604. An examination of the distribution of 185 estimates of mean genetic relatedness between sisters in Hymenopteran colonies shows that the values are well below the expected 0.75 for full sisters, both in higly eusocial as well as in primitively eusocial species although relatedness values in the latter are higher than in the former. Of the 177 estimates with standard error, 49 are significantly lower than the haplodiploidy threshold and 22 are significantly higher. Of the 35 species studied only 6 have one or more estimates that are significantly higher than the haplodiploidy threshold. For more than half the estimates, the probability of the relatedness value being above the haplodiploidy threshold is less than 0.5. Reanalysis of these data using 0.5 as the threshold does not drastically alter these conclusions. I conclude that the genetic asymmetry created by haplodiploidy is, in most cases, insufficient by itself either topromote the origin of eusociality or tomaintain the highly eusocial state.     

The evolutionary dynamics of haplodiploidy: Genome architecture and haploid viability

Haplodiploid reproduction, in which males are haploid and females are diploid, is widespread among animals, yet we understand little about the forces responsible for its evolution. The current theory is that haplodiploidy has evolved through genetic conflicts, as it provides a transmission advantage to mothers. Male viability is thought to be a major limiting factor; diploid individuals tend to harbor many recessive lethal mutations. This theory predicts that the evolution of haplodiploidy is more likely in male heterogametic lineages with few chromosomes, as genes on the X chromosome are often expressed in a haploid environment, and the fewer the chromosome number, the greater the proportion of the total genome that is X‐linked. We test this prediction with comparative phylogenetic analyses of mites, among which haplodiploidy has evolved repeatedly. We recover a negative correlation between chromosome number and haplodiploidy, find evidence that low chromosome number evolved prior to haplodiploidy, and that it is unlikely that diplodiploidy has reevolved from haplodiploid lineages of mites. These results are consistent with the predicted importance of haploid male viability.     

TRAIT MAPPING AND SALIENCE IN THE EVOLUTION OF EUSOCIAL VESPID WASPS

The multiple independent origins of eusociality in the insect order Hymenoptera are clustered in only four of more than 80 families, and those four families are two pairs of closely related taxa in a single part of the order. Therefore, although ordinal-level characteristics can contribute to hymenopteran eusocial evolution, more important roles have been played by traits of infraordinal taxa that contain the eusocial forms. Many factors have been proposed and discussed, but assessments of traits' salience to eusocial evolution have heretofore not been joined to phylogenetics. In the present analysis, cladograms of superfamilies and families of Hymenoptera and of the family Vespidae are used to ordinate the appearance of traits that play roles in vespid eusociality. Proximity of traits' first appearance to the origin of eusocial Vespidae is taken as one measure of traits' salience to vespid eusocial evolution. Traits that subtend only eusocial taxa and that are uniquely associated with eusociality have foundations in more general traits that subtend more inclusive taxa. No single trait is uniquely causative of vespid eusocial evolution. High-salience traits that closely subtend vespid eusociality include nesting, oviposition into an empty nest cell, progressive provisioning of larvae, adult nourishment during larval provision malaxation, and inequitable food distribution among nestmates. The threshold characteristic of Polistes-grade eusociality is life-long alloparental brood care by first female offspring who remain, uninseminated, at their natal nest. Traits directly associated with occurrence of such workers are larva-adult trophallaxis, which can foster relatively low larval nourishment early in a colony cycle, and protogyny and direct larval development, which combine to yield restricted mating opportunities for female offspring that are the first to emerge in the colony cycle. Trait mapping suggests no role for asymmetry of relatedness due to haplodiploidy, but it suggests high salience for haplodiploidy as a mechanism enabling the production of all-female clutches of first offspring.     

Origin and evolution of eusociality: a perspective from studying primitively eusocial wasps

Eusocial insects are those that show overlap of generations, cooperative brood care and reproductive caste differentiation. Of these, primitively eusocial insects show no morphological differences between reproductive and worker castes and exhibit considerable flexibility in the social roles that adult females may adopt. This makes them attractive model systems for investigations concerning the origin of eusociality. The rapidly accumulating information on primitively eusocial wasps suggests that haplodiploidy is unlikely to have an important role in the origin of eusociality. General kin selection (without help from haplodiploidy) could however have been an important factor due to the many advantages of group living. Pre-imaginal caste bias leading to variations in fertility is also likely to have some role. Because workers often have some chance of becoming reproductives in future, mutualism and other individual selection models suggest themselves as important factors. A hypothesis for the route to eusociality which focuses on the factors selecting for group living at different stages in social evolution is presented. It is argued that group living originates owing to the benefit of mutualism (the ‘Gambling Stage’) but parental manipulation and subfertility soon become important (the ‘Manipulation Stage’) and finally the highly eusocial state is maintained because genetic asymmetries created by haplodiploidy are exploited by kin recognition (the ‘Recognition Stage’).     

Maternal effect genes and the evolution of sociality in haplo-diploid organisms

Maternal care and female-biased sex ratios are considered by many to be essential prerequisites for the evolution of eusocial behaviors among the hymenoptera. Using population genetic models, I investigate the evolution of genes that have positive maternal effects but negative, direct effects on offspring fitness. I find that, under many conditions, such genes evolve more easily in haplo-diploids than in diplo-diploids. In fact, the conditions are less restrictive than those of kin selection theory, which postulate genes with negative direct effects but positive sib-social effects. For example, the conditions permitting the evolution of maternal effect genes are not affected if females mate multiply, whereas multiple mating reduces the efficacy of kin selection by reducing genetic relatedness within colonies. Inbreeding also differentially facilitates evolution of maternal effect genes in haplo-diploids relative to diplo-diploids, although it does not differentially affect the evolution of sib-altruism genes. Furthermore, when the direct, deleterious pleiotropic effect is restricted to sons, a maternal effect gene can evolve when the beneficial maternal effect is less than half (with inbreeding, much less) of the deleterious effect on sons. For kin selection, however, the sib-social benefits must always exceed the direct costs because genetic relatedness is always less than or equal to 1.0. The results suggest that haplo-diploidy facilitates (1) the evolution of maternal care, and (2) the evolution of maternal effect genes with antagonistic pleiotropic effects on sons. The latter effect may help explain the tendency toward female-biased sex ratios in haplo-diploids, especially those with inbreeding. I conclude that haplo-diploidy not only facilitates the evolution of sister-sister altruism by kin selection but also facilitates the evolution of maternal care and female-biased sex ratios, two prerequisites for eusociality.     

The validity and value of inclusive fitness theory

Social evolution is a central topic in evolutionary biology, with the evolution of eusociality (societies with altruistic, non-reproductive helpers) representing a long-standing evolutionary conundrum. Recent critiques have questioned the validity of the leading theory for explaining social evolution and eusociality, namely inclusive fitness (kin selection) theory. I review recent and past literature to argue that these critiques do not succeed. Inclusive fitness theory has added fundamental insights to natural selection theory. These are the realization that selection on a gene for social behaviour depends on its effects on co-bearers, the explanation of social behaviours as unalike as altruism and selfishness using the same underlying parameters, and the explanation of within-group conflict in terms of non-coinciding inclusive fitness optima. A proposed alternative theory for eusocial evolution assumes mistakenly that workers' interests are subordinate to the queen's, contains no new elements and fails to make novel predictions. The haplodiploidy hypothesis has yet to be rigorously tested and positive relatedness within diploid eusocial societies supports inclusive fitness theory. The theory has made unique, falsifiable predictions that have been confirmed, and its evidence base is extensive and robust. Hence, inclusive fitness theory deserves to keep its position as the leading theory for social evolution.     

Stable eusociality via maternal manipulation when resistance is costless

In many eusocial species, queens use pheromones to influence offspring to express worker phenotypes. Although evidence suggests that queen pheromones are honest signals of the queen's reproductive health, here I show that queen's honest signalling can result from ancestral maternal manipulation. I develop a mathematical model to study the coevolution of maternal manipulation, offspring resistance to manipulation and maternal resource allocation. I assume that (i) maternal manipulation causes offspring to be workers against offspring's interests; (ii) offspring can resist at no direct cost, as is thought to be the case with pheromonal manipulation; and (iii) the mother chooses how much resource to allocate to fertility and maternal care. In the coevolution of these traits, I find that maternal care decreases, thereby increasing the benefit that offspring obtain from help, which in the long run eliminates selection for resistance. Consequently, ancestral maternal manipulation yields stable eusociality despite costless resistance. Additionally, ancestral manipulation in the long run becomes honest signalling that induces offspring to help. These results indicate that both eusociality and its commonly associated queen honest signalling can be likely to originate from ancestral manipulation.     

Origin of a haplodiploid beetle lineage

The beetle family Scolytidae includes several groups having regular sib-mating and extremely female-biased sex ratios. Two such groups are known to include haplodiploid species: (i) the tribe Xyleborini and (ii) Coccotrypes and related genera within the tribe Dryocoetini. Relationships of these groups have been controversial. We analysed elongation factor 1-α (852 bp) and cytochrome oxidase 1 (1179 bp) sequences for 40 species. The most-parsimonious trees imply a single origin of haplodiploidy uniting Xyleborini (approximately 1200 species) and sib-mating Dryocoetini (approximately 160 species). The sister-group of the haplodiploid clade is the outcrossing genus Dryocoetes. The controversial genus Premnobius is outside the haplodiploid clade. Most haplodiploid scolytids exploit novel resources, ambrosia fungi or seeds, but a few have the ancestral habit of feeding on phloem. Thus, scolytids provide the clearest example of W. D. Hamilton''s scenario for the evolution of haplodiploidy (life under bark leading to inbreeding and hence to female-biased sex ratios through haplodiploidy) and now constitute a unique opportunity to study diplodiploid and haplodiploid sister-lineages in a shared ancestral habitat. There is some evidence of sex determination by maternally inherited endosymbiotic bacteria, which may explain the consistency with which female-biased sex ratios and close inbreeding have been maintained.     

The general protected invasion theory: Sex biases in parental and alloparental care

The biases towards eusociality, female workers and maternal care in haplodiploid versus diploid insects may result from the relatively low probabilities that rare mutant, partially dominant alleles promoting these behaviours will be lost by genetic drift in haplodiploid populations (Reeve, 1993). A generalization of this 'protected invasion' theory also predicts that parental and alloparental care will tend to be associated with the homogametic sex in diploid populations if the Y chromosome of the heterogametic sex is absent or largely inert. Sex differences in (allo)parental care (i.e. either parental or alloparental care) should increase with increased asymmetry between the sexes in the fraction of behaviour-influencing loci occurring on their characteristic sex chromosomes. The theory explains the strong predisposition towards female (allo)parental care in mammals, a contrasting tendency towards male (allo)parental care in birds, the propensity for joint male and female (allo)parental care in termites, and biases towards female cooperation in social spiders. The theory also explains the apparent rarity or absence of alloparental care in marsupials, an intriguing consequence of preferential paternal X-chromosome inactivation in this taxon. Thus protected invasion theory possibly provides new insights into the relationship between social structure and the genetic system. The theory does not compete with ecological or kin-selective hypotheses for the advantages of (allo)parental care; indeed, such advantages must exist for protected-invasion biases to operate.     

An inclusive fitness model for the sex ratio in a partially sibmating population with inbreeding cost

Summary We construct an inclusive fitness model to find the evolutionarily stable sex ratios in a partially sibmating diploid or haplodiploid population. We assume a constant rate of sibmating with inbred offspring incurring a fitness penalty which, under haplodiploidy, is only suffered by females. We construct a one-locus genetic model for the same problem and observe that when selection is weak it gives the same numerical results as the inclusive fitness model.     

A theory of natural selection incorporating interaction among individuals. IX. Use of groups consisting of a mating pair and sterile diploid caste members

This paper and the next member of the series, deal with genetical mechanisms responsible for the evolution of eusociality (a level of social organization that includes differentiated sterile castes) among the “social” insects. Eusociality has evolved in a number of different species. Two different types of genetic systems are represented among these species: diplodiploidy (both sexes diploid) and haplodiploidy (haploid males and diploid females). The present paper examines the evolution of a sterile caste system in the context of diplodiploidy, and the next paper considers the evolution of eusociality in the context of haplodiploidy.The present study demonstrates that if the sterile diploid caste members are related to the reproductive members of the group, eusociality can evolve. This is true because the caste associate gene effects are included in the function determining gene frequency change (i.e. Δp_i). Also, since the caste gene effects are expressed only through the associate dimension of gene activity, they can cause morphological and behavioral adaptations to occur which are peculiar to the caste members, and need not be expressed in the reproducing members of the group. Thus caste differentiation is possible.     

Deleterious mutation and the evolution of eusociality

Abstract.— Certain arguments concerning the evolution of eusociality form a classic example of the application of the principles of kin selection. These arguments center on the different degrees of relatedness of potential beneficiaries of an individual's efforts, for example a female's higher relatedness to her sisters than to her daughters in a haplodiploid system. This type of reasoning is insufficient to account for the evolution and maintainence of sexual reproduction, because parthenogenic females produce offspring that are more closely related to them than are offspring produced sexually. Among the forces invoked to explain sexual reproduction is deleterious mutation. This factor can be shown to favor eusociality as well, because siblings produced by helping carry fewer deleterious alleles on average than would offspring. The strength of this effect depends on the genomewide deleterious mutation rate, U, and on the selection coefficient, s, associated with deleterious alleles. For small s, the effect depends approximately on the product Us. This phenomenon illustrates that an assumption implicit in some analyses–that the relatedness of an individual to an actor is all that matters to its value to that actor–can fail for the evolution of eusociality as it does for the evolution of sex.