Environmentally induced responses co-opted for reproductive altruism

Reproductive altruism is an extreme form of altruism best typified by sterile castes in social insects and somatic cells in multicellular organisms. Although reproductive altruism is central to the evolution of multicellularity and eusociality, the mechanistic basis for the evolution of this behaviour is yet to be deciphered. Here, we report that the gene responsible for the permanent suppression of reproduction in the somatic cells of the multicellular green alga, Volvox carteri, evolved from a gene that in its unicellular relative, Chlamydomonas reinhardtii, is part of the general acclimation response to various environmental stress factors, which includes the temporary suppression of reproduction. Furthermore, we propose a model for the evolution of soma, in which by simulating the acclimation signal (i.e. a change in cellular redox status) in a developmental rather than environmental context, responses beneficial to a unicellular individual can be co-opted into an altruistic behaviour at the group level. The co-option of environmentally induced responses for reproductive altruism can contribute to the stability of this behaviour, as the loss of such responses would be costly for the individual. This hypothesis also predicts that temporally varying environments, which will select for more efficient acclimation responses, are likely to be more conducive to the evolution of reproductive altruism.     

Honey bee queen mandibular pheromone inhibits ovary development and fecundity in a fruit fly

A key feature of eusocial insects is their reproductive division of labour. The queen signals her fecundity to her potentially reproductive daughters via a pheromone, which renders them sterile. In contrast, solitary insects lack division in reproductive labour and there is no such social signalling or need for ovary‐regulating pheromones. Nonetheless, females from both non‐social and eusocial lineages are expected to regulate their ovaries to maximize inclusive lifetime reproductive success. It is not known, however, whether the underlying networks that regulate ovary activation are homologous between non‐social and eusocial taxa, especially when these taxa are phylogenetically distant. In this study, we provide evidence that solitary fruit flies may share a conserved ovary‐regulating pathway with a eusocial honey bee, Apis mellifera L. (Hymenoptera: Apidae). Specifically, we demonstrate that honey bee queen mandibular pheromone (QMP) inhibits fly ovaries in much the same way as it suppresses worker ovaries. Drosophila melanogaster Meigen (Diptera: Drosophilidae) exposed to sufficient doses of QMP showed a reduction in ovary size, produced fewer eggs, and generated fewer viable offspring, relative to unexposed controls. Drosophila melanogaster therefore responds to an interspecific social cue to which it would not normally be exposed. Although we cannot strictly rule out an incidental effect, this conspicuous response suggests that these two species may share an underlying mechanism for ovary regulation. Why a non‐social species of fly responds to a highly social bee's pheromone is not clear, but one possibility is that solitary and social insects share pathways associated with female reproduction, as predicted by the ‘groundplan’ hypothesis of social evolution.     

Population viscosity can promote the evolution of altruistic sterile helpers and eusociality

Because it increases relatedness between interacting individuals, population viscosity has been proposed to favour the evolution of altruistic helping. However, because it increases local competition between relatives, population viscosity may also act as a brake for the evolution of helping behaviours. In simple models, the kin selected fecundity benefits of helping are exactly cancelled out by the cost of increased competition between relatives when helping occurs after dispersal. This result has lead to the widespread view, especially among people working with social organisms, that special conditions are required for the evolution of altruism. Here, we re-examine this result by constructing a simple population genetic model where we analyse whether the evolution of a sterile worker caste (i.e. an extreme case of altruism) can be selected for by limited dispersal. We show that a sterile worker caste can be selected for even under the simplest life-cycle assumptions. This has relevant consequences for our understanding of the evolution of altruism in social organisms, as many social insects are characterized by limited dispersal and significant genetic population structure.     

The gene vitellogenin has multiple coordinating effects on social organization

Temporal division of labor and foraging specialization are key characteristics of honeybee social organization. Worker honeybees (Apis mellifera) initiate foraging for food around their third week of life and often specialize in collecting pollen or nectar before they die. Variation in these fundamental social traits correlates with variation in worker reproductive physiology. However, the genetic and hormonal mechanisms that mediate the control of social organization are not understood and remain a central question in social insect biology. Here we demonstrate that a yolk precursor gene, vitellogenin, affects a complex suite of social traits. Vitellogenin is a major reproductive protein in insects in general and a proposed endocrine factor in honeybees. We show by use of RNA interference (RNAi) that vitellogenin gene activity paces onset of foraging behavior, primes bees for specialized foraging tasks, and influences worker longevity. These findings support the view that the worker specializations that characterize hymenopteran sociality evolved through co-option of reproductive regulatory pathways. Further, they demonstrate for the first time how coordinated control of multiple social life-history traits can originate via the pleiotropic effects of a single gene that affects multiple physiological processes.     

The Gene vitellogenin Has Multiple Coordinating Effects on Social Organization

Temporal division of labor and foraging specialization are key characteristics of honeybee social organization. Worker honeybees (Apis mellifera) initiate foraging for food around their third week of life and often specialize in collecting pollen or nectar before they die. Variation in these fundamental social traits correlates with variation in worker reproductive physiology. However, the genetic and hormonal mechanisms that mediate the control of social organization are not understood and remain a central question in social insect biology. Here we demonstrate that a yolk precursor gene, vitellogenin, affects a complex suite of social traits. Vitellogenin is a major reproductive protein in insects in general and a proposed endocrine factor in honeybees. We show by use of RNA interference (RNAi) that vitellogenin gene activity paces onset of foraging behavior, primes bees for specialized foraging tasks, and influences worker longevity. These findings support the view that the worker specializations that characterize hymenopteran sociality evolved through co-option of reproductive regulatory pathways. Further, they demonstrate for the first time how coordinated control of multiple social life-history traits can originate via the pleiotropic effects of a single gene that affects multiple physiological processes.     

Variation in cuticular hydrocarbon signatures, hormonal correlates and establishment of reproductive dominance in a polistine wasp

In many social insects the relationship between reproductive dominance and physiological correlates is poorly understood. Recent evidence now strongly suggests that cuticular hydrocarbons are important in reproductive differentiation in these societies where they are used as signals of ovarian activity in reproductive females. In this study we investigated the relationship between reproductive dominance, size of the corpora allata (CA, producer of Juvenile Hormone, JH) and the proportions of cuticular hydrocarbons present on the cuticle in overwintering foundresses and both associative (polygynous) and solitary (monogynous) pre-emergence colonies of the social wasp Polistes dominulus. Size of the CA was positively correlated with ovarian development in polygynous colonies. In contrast, solitary foundresses possessed significantly smaller CAs than dominant foundresses from polygynous nests, yet ovarian activity was similar for both female types. CA size variation was associated with variation in cuticular hydrocarbon proportions. Overwintering, solitary, dominant and subordinate (from associative nests) females all possessed distinctive cuticular chemical profiles revealed by multivariate discriminant analyses. Our data indicate that the social environment strongly affects reproductive physiology in this wasp, and we discuss the role of cuticular hydrocarbons in reproductive signaling in P. dominulus and other social insects.     

Kin discrimination and altruism in the larvae of a solitary insect

Kin selection theory predicts altruism between related individuals, which requires the ability to recognize kin from non-kin. In insects, kin discrimination associated with altruistic behaviour is well-known in clonal and social species but in very few solitary insects. Here, we report that the solitary larvae of a non-social insect Aleochara bilineata Gyll. (Coleoptera; Staphylinidae) show kin discrimination and sibling-directed altruistic behaviour. Larvae superparasitize more frequently the hosts parasitized by non-kin individuals than those hosts parasitized by siblings. Kin discrimination probably occurs by self-referent phenotype matching, where an individual compares its own phenotype with that of a non-familiar related individual, a mechanism rarely demonstrated in animals. The label used to recognize kin from non-kin corresponds to substances contained in the plug placed on the hosts by the resident larvae during the parasitization process. Kin competition induced by a limited larval dispersion may have favoured the evolution of kin recognition in this solitary species.     

Phylogenetic reconstruction of carnivore social organizations

It is generally assumed that carnivore social organizations evolved directionally from a solitary ancestor into progressively more advanced forms of group living. Although alternative explanations exist, this evolutionary hypothesis has never been tested. Here, I used literature data and maximum likelihood reconstruction on a complete carnivore phylogeny to test this hypothesis against two others: one assuming directional evolution from a non-solitary ancestor, and one assuming parallel evolutions from a socially flexible ancestor, that is, an ancestor with abilities to live in a variety of social organizations. The phylogenetic reconstructions did not support any of the three hypotheses of social evolution at the root of Carnivora. At the family level, however, there was support for a non-solitary and socially flexible ancestor to Canidae, a socially flexible or solitary ancestor to Mustelidae, a solitary or socially flexible ancestor to Mephitidae, a solitary or group living ancestor to Phocidae, a group living ancestor to Otariidae and a solitary ancestor to Ursidae, Felidae, Herpestidae and Viverridae. There was equivocal support for the ancestral state of Procyonidae and Hyaenidae. It is unclear whether the common occurrence of a solitary ancestry at the family level was caused by a solitary ancestor at the root of Carnivora or by multiple transitions into a solitary state. The failure to support a solitary ancestor to Carnivora calls for caution when using this hypothesis in an evolutionary framework, and I suggest continued investigations of the pathways of the evolution of carnivore social organizations.     

Pleiotropic effects of juvenile hormone in ant queens and the escape from the reproduction–immunocompetence trade-off

The ubiquitous trade-off between survival and costly reproduction is one of the most fundamental constraints governing life-history evolution. In numerous animals, gonadotropic hormones antagonistically suppressing immunocompetence cause this trade-off. The queens of many social insects defy the reproduction–survival trade-off, achieving both an extraordinarily long life and high reproductive output, but how they achieve this is unknown. Here we show experimentally, by integrating quantification of gene expression, physiology and behaviour, that the long-lived queens of the ant Lasius niger have escaped the reproduction–immunocompetence trade-off by decoupling the effects of a key endocrine regulator of fertility and immunocompetence in solitary insects, juvenile hormone (JH). This modification of the regulatory architecture enables queens to sustain a high reproductive output without elevated JH titres and suppressed immunocompetence, providing an escape from the reproduction–immunocompetence trade-off that may contribute to the extraordinary lifespan of many social insect queens.     

How to make a sterile helper

The sterile worker castes found in the colonies of social insects are often cited as archetypal examples of altruism in nature. The challenge is to explain why losing the ability to mate has evolved as a superior strategy for transmitting genes into future generations. We propose that two conditions are necessary for the evolution of sterility: completely overlapping generations and monogamy. A review of the literature indicates that when these two conditions are met we consistently observe the evolution of sterile helpers. We explain the theory and evidence behind these ideas, and discuss the importance of ecology in predicting whether sterility will evolve using examples from social birds, mammals, and insects. In doing so, we offer an explanation for the extraordinary lifespans of some cooperative species which hint at ways in which we can unlock the secrets of long life.     

Variable worker behaviour in the weakly eusocial sweat bee, <Emphasis Type="Italic">Halictus sexcinctus</Emphasis> Fabricius

Summary Studies of eusocial halictines suggest that workers have many reproductive options, including sterile altruism in the maternal nest, combined helping and personal reproduction, and diapause and spring nest founding. How and when workers exercise these various options influences the strength of colony social organization. Halictus sexcinctus exhibits highly polymorphic social behaviour, with solitary colonies in central Europe and both eusocial and communal colonies in southern Greece. Indirect evidence suggests that some worker-brood females are actually gynes. A distinctly bimodal size distribution among foundresses in 1998, the lower size peak being close to the modal body size of workers from 1997, suggests that large worker-brood females overwinter and return to the aggregation as eusocial foundresses. Other first-brood females remain in the maternal nest as workers, although few can be classified as classical, sterile altruists. Only 17% of older, healthy workers are sterile (i.e. had ovarian development scores 0.1), whereas about 83% are reproductive, exhibiting at least one 1/4-developed oocyte. About 57% of older workers have at least one fully or 3/4 developed oocyte, signifying that they are ready or almost ready to lay. Sterile workers exhibit greater total wear (combined mandibular and wing wear) scores than reproductive workers, suggesting that they are older, have higher activity rates, or both.     

Effects of selection for honey bee worker reproduction on foraging traits

The “reproductive ground plan” hypothesis (RGPH) proposes that reproductive division of labour in social insects had its antecedents in the ancient gene regulatory networks that evolved to regulate the foraging and reproductive phases of their solitary ancestors. Thus, queens express traits that are characteristic of the reproductive phase of solitary insects, whereas workers express traits characteristic of the foraging phase. The RGPH has also been extended to help understand the regulation of age polyethism within the worker caste and more recently to explain differences in the foraging specialisations of individual honey bee workers. Foragers that specialise in collecting proteinaceous pollen are hypothesised to have higher reproductive potential than individuals that preferentially forage for nectar because genes that were ancestrally associated with the reproductive phase are active. We investigated the links between honey bee worker foraging behaviour and reproductive traits by comparing the foraging preferences of a line of workers that has been selected for high rates of worker reproduction with the preferences of wild-type bees. We show that while selection for reproductive behaviour in workers has not altered foraging preferences, the age at onset of foraging of our selected line has been increased. Our findings therefore support the hypothesis that age polyethism is related to the reproductive ground plan, but they cast doubt on recent suggestions that foraging preferences and reproductive traits are pleiotropically linked.     

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'.     

An invitation to die: initiators of sociality in a social amoeba become selfish spores

Greater size and strength are common attributes of contest winners. Even in social insects with high cooperation, the right to reproduce falls to the well-fed queens rather than to poorly fed workers. In Dictyostelium discoideum, formerly solitary amoebae aggregate when faced with starvation, and some cells die to form a stalk which others ride up to reach a better location to sporulate. The first cells to starve have lower energy reserves than those that starve later, and previous studies have shown that the better-fed cells in a mix tend to form disproportionately more reproductive spores. Therefore, one might expect that the first cells to starve and initiate the social stage should act altruistically and form disproportionately more of the sterile stalk, thereby enticing other better-fed cells into joining the aggregate. This would resemble caste determination in social insects, where altruistic workers are typically fed less than reproductive queens. However, we show that the opposite result holds: the first cells to starve become reproductive spores, presumably by gearing up for competition and outcompeting late starvers to become prespore first. These findings pose the interesting question of why others would join selfish organizers.     

Genome-wide analysis of alternative reproductive phenotypes in honeybee workers

A defining feature of social insects is the reproductive division of labour, in which workers usually forego all reproduction to help their mother queen to reproduce. However, little is known about the molecular basis of this spectacular form of altruism. Here, we compared gene expression patterns between nonreproductive, altruistic workers and reproductive, non-altruistic workers in queenless honeybee colonies using a whole-genome microarray analysis. Our results demonstrate massive differences in gene expression patterns between these two sets of workers, with a total of 1292 genes being differentially expressed. In nonreproductive workers, genes associated with energy metabolism and respiration, flight and foraging behaviour, detection of visible light, flight and heart muscle contraction and synaptic transmission were overexpressed relative to reproductive workers. This implies they probably had a higher whole-body energy metabolism and activity rate and were most likely actively foraging, whereas same-aged reproductive workers were not. This pattern is predicted from evolutionary theory, given that reproductive workers should be less willing to compromise their reproductive futures by carrying out high-risk tasks such as foraging or other energetically expensive tasks. By contrast, reproductive workers mainly overexpressed oogenesis-related genes compared to nonreproductive ones. With respect to key switches for ovary activation, several genes involved in steroid biosynthesis were upregulated in reproductive workers, as well as genes known to respond to queen and brood pheromones, genes involved in TOR and insulin signalling pathways and genes located within quantitative trait loci associated with reproductive capacity in honeybees. Overall, our results provide unique insight into the molecular mechanisms underlying alternative reproductive phenotypes in honeybee workers.     

Subfamily‐dependent alternative reproductive strategies in worker honeybees

Functional worker sterility is the defining feature of insect societies. Yet, workers are sometimes found reproducing in their own or foreign colonies. The proximate mechanisms underlying these alternative reproductive phenotypes are keys to understanding how reproductive altruism and selfishness are balanced in eusocial insects. In this study, we show that in honeybee (Apis mellifera) colonies, the social environment of a worker, that is, the presence and relatedness of the queens in a worker's natal colony and in surrounding colonies, significantly influences her fertility and drifting behaviour. Furthermore, subfamilies vary in the frequency of worker ovarian activation, propensity to drift and the kind of host colony that is targeted for reproductive parasitism. Our results show that there is an interplay between a worker's subfamily, reproductive state and social environment that substantially affects her reproductive phenotype. Our study further indicates that honeybee populations show substantial genetic variance for worker reproductive strategies, suggesting that no one strategy is optimal under all the circumstances that a typical worker may encounter.     

Selection on defensive traits in a sterile caste – caste evolution: a mechanism to overcome life‐history trade‐offs?

SUMMARY During development and evolution individuals generally face a trade-off between the development of weapons and gonads. In termites, characterized by reproductive division of labor, a caste evolved—the soldiers—which is completely sterile and which might be released from developmental trade-offs between weapons and testes. These soldiers are exclusively dedicated to defense. First, we investigated whether defensive traits are under selection in sterile termite soldiers using allometric analyses. In soldiers of the genus Cryptotermes phragmotic traits such as a sculptured and foreshortened head evolve rapidly but were also lost twice. Second, we compared the scaling relationships of these weapons with those in solitary insects facing a trade-off between weapons and gonads. Defensive traits consistently had lower slopes than nondefensive traits which supports the existence of stabilizing selection on soldier phragmotic traits in order to plug galleries. Moreover, soldier head widths were colony specific and correlated with the minimum gallery diameter of a colony. This can proximately be explained by soldiers developing from different instars. The scaling relationships of these termite soldiers contrast strikingly with those of weapons of solitary insects, which are generally exaggerated (i.e., overscaling) male traits. These differences may provide important insights into trait evolution. Trade-offs constraining the development of individuals may have been uncoupled in termites by evolving different castes, each specialized for one function. When individuals in social insect are "released" from developmental constraints through the evolution of castes, this certainly contributed to the ecological and evolutionary success of social insects.     

Support for the reproductive ground plan hypothesis of social evolution and major QTL for ovary traits of Africanized worker honey bees (Apis mellifera L.)

Background  

The reproductive ground plan hypothesis of social evolution suggests that reproductive controls of a solitary ancestor have been co-opted during social evolution, facilitating the division of labor among social insect workers. Despite substantial empirical support, the generality of this hypothesis is not universally accepted. Thus, we investigated the prediction of particular genes with pleiotropic effects on ovarian traits and social behavior in worker honey bees as a stringent test of the reproductive ground plan hypothesis. We complemented these tests with a comprehensive genome scan for additional quantitative trait loci (QTL) to gain a better understanding of the genetic architecture of the ovary size of honey bee workers, a morphological trait that is significant for understanding social insect caste evolution and general insect biology.     

Testing the reproductive groundplan hypothesis in ants (Hymenoptera: Formicidae)

The evolution of complex societies with obligate reproductive division of labor represents one of the major transitions in evolution. In such societies, functionally sterile individuals (workers) perform many of fitness‐relevant behaviors including allomaternal ones, without getting any direct fitness benefits. The question of how such worker division of labor has evolved remains controversial. The reproductive groundplan hypothesis (RGPH) offers a powerful proximate explanation for this evolutionary leap. The RGPH argues that the conserved genetic and endocrinological networks regulating fitness‐relevant behavior (e g. foraging and brood care) in their solitary ancestors have become decoupled from actual reproduction in the worker caste and now generate worker behavioral phenotypes. However, the empirical support for this hypothesis remains limited to a handful of species making its general validity uncertain. In this study, we combine data from the literature with targeted sampling of key species and apply phylogenetically controlled comparative analysis to investigate if the key prediction of the RGPH, namely an association between allomaternal behavior and an allomaternal physiological state holds in the largest and most species‐rich clade of social insects, the ants. Our findings clearly support the RPGH as a general framework to understand the evolution of the worker caste and shed light on one of the major transition in evolutionary history.     

Evolution of social behaviour in the primitively eusocial wasp Ropalidia marginata: do we need to look beyond kin selection?

Ropalidia marginata is a primitively eusocial wasp widely distributed in peninsular India. Although solitary females found a small proportion of nests, the vast majority of new nests are founded by small groups of females. In such multiple foundress nests, a single dominant female functions as the queen and lays eggs, while the rest function as sterile workers and care for the queen''s brood. Previous attempts to understand the evolution of social behaviour and altruism in this species have employed inclusive fitness theory (kin selection) as a guiding framework. Although inclusive fitness theory is quite successful in explaining the high propensity of the wasps to found nests in groups, several features of their social organization suggest that forces other than kin selection may also have played a significant role in the evolution of this species. These features include lowering of genetic relatedness owing to polyandry and serial polygyny, nest foundation by unrelated individuals, acceptance of young non-nest-mates, a combination of well-developed nest-mate recognition and lack of intra-colony kin recognition, a combination of meek and docile queens and a decentralized self-organized work force, long reproductive queues with cryptic heir designates and conflict-free queen succession, all resulting in extreme intra-colony cooperation and inter-colony conflict.