Social Insect Castes Research Articles

Endocrine mediated phenotypic plasticity: Condition-dependent effects of juvenile hormone on dominance and fertility of wasp queens

There has been increasing interest in the mechanisms that mediate behavioral and physiological plasticity across individuals with similar genotypes. Some of the most dramatic plasticity is found within and between social insect castes. For example, Polistes wasp queens can nest alone, dominate a group of cooperative queens, or act as worker-like subordinates who rarely reproduce. Previous work suggests that condition-dependent endocrine responses may play a role in plasticity between castes in the hymenoptera. Here, we test whether condition-dependent endocrine responses influence plasticity within castes in the wasp Polistes dominulus. We experimentally manipulate juvenile hormone (JH) titers in nest-founding queens and assess whether JH mediates variation in behavior and physiology. JH generally increased dominance and fertility of queens, but JH's effects were not uniform across individuals. JH had a stronger effect on the dominance and fertility of large individuals and individuals with facial patterns advertising high quality than on the dominance and fertility of small individuals and those advertising low quality. These results demonstrate that JH has condition-dependent effects. As such, they clarify how JH can mediate different behaviors in well nourished queens and poorly nourished workers. Many Polistes queens nest cooperatively with other queens, so condition-dependent hormonal responses provide a mechanism for queens to adaptively allocate energy based on their probability of successfully becoming the dominant queen. Research on the endocrine basis of plasticity often focuses on variation in endocrine titers alone. However, differential endocrine responses are likely to be a widespread mechanism mediating behavioral and physiological plasticity.

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.

A diapause pathway underlies the gyne phenotype inPolisteswasps, revealing an evolutionary route to caste-containing insect societies

Colonies of social wasps, ants, and bees are characterized by the production of two phenotypes of female offspring, workers that remain at their natal nest and nonworkers that are potential colony reproductives of the next generation. The phenotype difference includes morphology and is fixed during larval development in ants, honey bees, and some social wasps, all of which represent an advanced state of sociality. Paper wasps (Polistes) lack morphological castes and are thought to more closely resemble an ancestral state of sociality wherein the phenotype difference between workers and nonworkers is established only during adult life. We address an alternative hypothesis: a bias toward the potential reproductive (gyne) phenotype among Polistes female offspring occurs during larval development and is based on a facultatively expressed ancestral life history trait: diapause. We show that two signatures of diapause (extended maturation time and enhanced synthesis and sequestration of a hexameric storage protein) characterize the development of gyne offspring in Polistes metricus. Hexameric storage proteins are implicated in silencing juvenile hormone signaling, which is a prerequisite for diapause. Diverging hexamerin protein dynamics driven by changes in larval provisioning levels thereby provide one possible mechanism that can cause an adaptive shift in phenotype bias during the Polistes colony cycle. This ontogenetic basis for alternative female phenotypes in Polistes challenges the view that workers and gynes represent behavior options equally available to every female offspring, and it exemplifies how social insect castes can evolve from casteless lineages.

The Evolutionary Origin of an Altruistic Gene

Although the conditions favoring altruism are being increasingly understood, the evolutionary origins of the genetic basis for this behavior remain elusive. Here, we show that reproductive altruism (i.e., a sterile soma) in the multicellular green alga, Volvox carteri, evolved via the co-option of a life-history gene whose expression in the unicellular ancestor was conditioned on an environmental cue (as an adaptive strategy to enhance survival at an immediate cost to reproduction) through shifting its expression from a temporal (environmentally induced) into a spatial (developmental) context. The gene belongs to a diverged and structurally heterogeneous multigene family sharing a SAND-like domain (a DNA-binding module involved in gene transcription regulation). To our knowledge, this is the first example of a social gene specifically associated with reproductive altruism, whose origin can be traced back to a solitary ancestor. These findings complement recent proposals that the differentiation of sterile castes in social insects involved the co-option of regulatory networks that control sequential shifts between phases in the life cycle of solitary insects.

A genetic component in the determination of worker polymorphism in the Florida harvester ant Pogonomyrmex badius

The interplay of genetic and environmental factors in the determination of social insect castes has long intrigued biologists. Though an overwhelming majority of studies establish that factors such as nutrition, pheromones and temperature determine the developmental fate of worker larvae, genetic components have recently been shown to play a role in the determination of morphological worker castes in leaf-cutting ants. Here we demonstrate that the determination of worker castes in the strongly polyandrous Florida harvester ant, Pogonomyrmex badius, has a genetic component. The overall distribution of caste members among patrilines in our study colonies is significantly different from the intracolonial caste ratio. Though this effect was not apparent in all colonies, our results suggest that workers of different patrilines in P. badius differ significantly in their propensities to develop into a certain worker caste. This genetic basis of worker polymorphism may go unnoticed in many social hymenopterans because of their low intracolonial genetic diversity due to monogamous colony structure. The worker polymorphism of P. badius is a taxonomic isolate and presumably a young trait in the genus. Therefore, a common genetic component of the determination of morphological and behavioral worker castes in social insects might be farranging taxonomically and may even be based on a genetic machinery inherent to all hymenopterans, but dormant in most.

Caste-specific gene expression in the stingless bee Melipona quadrifasciata ? Are there common patterns in highly eusocial bees?

Caste polyphenism is a multifaceted phenomenon, most evident in the marked differences in reproductive capacity and longevity between queens and workers. The mechanisms underlying caste differentiation and division of labor are mainly addressed in the honey bee, and recently have been studied at the molecular level. Yet, generalizations drawn from studies on this model organism require validation by comparative studies. We choose Melipona quadrifasciata, a sister-group species to honey bees, to investigate differences in gene expression between newly emerged adult queens and workers. RNA extracts were subjected to a differential display protocol (DDRT-PCR). The putative differentially expressed genes, for which annotation was available, were validated by RT-PCR and hybridization. Differential expression was observed for myosin, projectin, kettin, cytochrome P450, Rab11 and Sas10. Except for kettin, all of these were overexpressed in the worker caste. Projectin and kettin could play roles in caste-specific flight muscle organization. The putative Rab11 and Sas10 homolog genes could be involved in fertility-related cell signaling and in longevity-related gene silencing, respectively. Cytochrome P450 overexpression in Melipona workers corroborates similar findings in the honey bee, thus indicating a common function in the social insect caste syndrome.

A member of the short-chain dehydrogenase/reductase (SDR) superfamily is a target of the ecdysone response in honey bee (Apis mellifera) caste development

Many aspects in caste polyphenism result from hormonally controlled differential gene expression. A DDRT-PCR screen for ecdysteroid-regulated genes in ovaries revealed a set of ESTs coding for metabolic enzymes. For a cDNA encoding a short-chain dehydrogenase/reductase (SDR) we obtained the complete coding sequence (246 amino acids), revealing the protein motifs typical of insect SDRs. Its initially high expression in early fifth-instar larvae vanished in prepupae. Expression levels in worker larvae were higher than in queen larvae, suggesting negative regulation by the caste-specific ecdysteroid titer. This finding was confirmed by in vitro exposure of competent worker ovaries to makisterone A. In contrast to whole body RNA extracts, two SDR transcripts were detected in the ovaries. Both had their expression downregulated by makisterone A. Hormonal regulation and tissue-specific expression pattern makes this SDR an interesting enzyme for comparative molecular studies on social insect caste polyphenisms. Apis mellifera / differential display PCR / ecdysteroid / alcohol dehydrogenase / caste polyphenism

Worker caste polymorphism has a genetic basis in Acromyrmex leaf-cutting ants.

Division of labor is fundamental to the success of all societies. The most striking examples are the physically polymorphic worker castes in social insects with clear morphological adaptations to different roles. These polymorphic worker castes have previously been thought to be a classic example of nongentically controlled polymorphism, being mediated entirely by environmental cues. Here we show that worker caste development in the leaf-cutting ant Acromyrmex echinatior has a significant genetic component. Individuals of different patrilines within the same colony differ in their propensities to develop into minor or major workers. The mechanism appears to be plastic, with caste destiny resulting from interplay between nurture and nature. Unlike the few other recently discovered examples of a genetic influence on caste determination, the present result does not relate to any rare or exceptional circumstances, such as interspecific hybridization. The results suggest that a significant role of genetics may have been overlooked in our understanding of other complex polymorphisms of social insects.

Phenotypic plasticity: linking molecular mechanisms with evolutionary outcomes

We argue that phenotypic plasticity should be broadly construed to encompass a diversity of phenomena spanning several hierarchical levels of organization. Despite seemingly disparate outcomes among different groups of organisms (e.g., the opening/closing of stomata in leaves, adjustments of allocation to growth/reproduction, or the production of different castes in social insects), there are underlying shared processes that initiate these responses. At the most fundamental level, all plastic responses originate at the level of individual cells, which receive and process signals from their environment. The broad variations in physiology, morphology, behavior, etc., that can be produced by a single genotype, can be accounted for by processes regulating gene expression in response to environmental variation. Although evolution of adaptive plasticity may not be possible for some types of environmental signals, in many cases selection has molded responses to environmental variation that generate precise and repeatable patterns of gene expression. We highlight the example of responses of plants to variation in light quality and quantity, mediated via the phytochrome genes. Responses to changes in light at particular stages of plants' life cycles (e.g., seed germination, competition, reproduction) are controlled by different members of this gene family. The mechanistic details of the cell and molecular biology of phytochrome gene action (e.g., their effects on expression of other genes) is outlined. Plasticity of cells and organisms to internal and external environmental signals is pervasive, and represents not just an outcome of evolutionary processes, but also a potentially important molder of them. Phenotypes originally initiated via a plastic response, can be fixed through genetic assimilation as alternate regulatory pathways are shut off. Evolution of mechanisms of plasticity and canalization can both reduce genetic variation, as well as shield it. When the organism encounters novel environmental conditions, this shielded variation may be expressed, revealing hidden reaction norms that represent the raw material for subsequent evolution.

Gene expression and the evolution of insect polyphenisms.

Polyphenic differences between individuals arise not through differences at the genome level but as a result of specific cues received during development. Polyphenisms often involve entire suites of characters, as shown dramatically by the polyphenic castes found in many social insect colonies. An understanding of the genetic architecture behind polyphenisms provides a novel means of studying the interplay between genomes, gene expression and phenotypes. Here we discuss polyphenisms and molecular genetic tools now available to unravel their developmental bases in insects. We focus on several recent studies that have tracked gene-expression patterns during social insect caste determination. BioEssays 23:62-68, 2001. Published 2001 John Wiley & Sons, Inc.

Gene flow and selection balance in haplodiploid social insects.

Understanding the joint effects of gene flow and selection is one of the more important but difficult areas of evolutionary genetics. A method is presented to describe cases of gene flow-selection balance while accounting for the life history of haplodiploid social insects (eusocial Hymenoptera). A continent-island model is used to estimate gene flow rates from allele frequency data and provide variance formulae. The occurrence of unequal yet stable allele frequencies among social insect castes is explained and the usefulness of models with discrete generations for eusocial insects is explained. Gene flow and selection balance has been demonstrated for the fire ant Solenopsis invicta at two allozyme loci. This continent-island model gives results that well describe the system. Issues fundamental to the differences between X-linked and haplodiploid genetic systems and diploid genetic systems are also discussed.

Expression profiles during honeybee caste determination.

Depending on their larval environment, female honeybees develop into either queens or workers. As in other polyphenisms, this developmental switch depends not on genomic differences between queens and workers but on the differential expression of entire suites of genes involved with larval fate. As such, this and other polyphenic systems can provide a novel tool for understanding how genomes and environmental conditions interact to produce different developmental trajectories. Here we use gene-expression profiles during honeybee caste determination to present the first genomic view of polyphenic development. Larvae raised as queens or workers differed greatly in their gene-expression patterns. Workers remained more faithful than queens to the expression profiles of younger, bipotential, larvae. Queens appeared to both downregulate many of the genes expressed by bipotential larvae and turn on a distinct set of caste-related genes. Queens overexpressed several metabolic enzymes, workers showed increased expression of a member of the cytochrome P450 family, hexameric storage proteins and dihydrodiol dehydrogenase, and young larvae overexpressed two putative heat-shock proteins (70 and 90 kDa), and several proteins related to RNA processing and translation. Large differences in gene expression between queens and workers indicate that social insect castes have faced strong directional selection pressures. Overexpression of metabolic enzymes by queen-destined larvae appears to reflect the enhanced growth rate of queens during late larval development. Many of the differently expressed genes we identified have been tied to metabolic rates and cellular responses to hormones, a result consistent with known physiological differences between queen and worker larvae.

Slime molds, ascidians, and the utility of evolutionary theory

This game is about discovering generality in biology. How so? Let’s give the face values on the cards biological interpretations. An ace represents genes and molecules underlying biosynthetic pathways of great antiquity, the kings mechanisms of transcription and translation, the queens regulatory or signaling molecules. The cards comprising the stacked deck correspond to events that arose early in the history of life. The conventional deck, with its deuces and treys, represent taxon-specific biological features, say, the morphologies of antelope horns, the variety of social insect castes, or the polyp polymorphisms of siphonophores. A winning hand is a general finding, one germane to all or a large fraction of extant organisms.

2 Social Insect Polymorphism: Hormonal Regulation of Plasticity in Development and Reproduction in the Honeybee

This chapter discusses the hormonal regulation of plasticity in development and reproduction in the honeybee. The insight that hormones may be the cornerstones for understanding the developmental regulation, not only in preimaginal caste differentiation but also in adult life, has turned honeybee into a model for studies on caste in social insects, the reasons being its relatively large size and its ready availability together with a wealth of knowledge concerning honeybee biology and management. More recent views on caste differentiation seek to understand the developmental regulation in honeybee in the context of metamorphosis, particularly focusing on the role of the morphogenetic hormones, juvenile hormone, and ecdysone. These hormones exert additional and apparently novel functions in the adult life of honeybee. Reproduction and division of labor are also discussed in the chapter in the context of endocrine regulation. Long-term integration of the developmental processes and reproduction cycles with environmental conditions poses a key problem for any organism. In general, the required interaction of external stimuli with the genotype of an organism is mediated and orchestrated by hormones. During critical periods of caste differentiation, research on the regulatory pathways in the endocrine system of the honeybee larvae has shown that the corpora allata exhibit a caste-specific program of activity during the last larval instar and that this program can set the activity pattern of the prothoracic gland.

‘Male-stuffing’ in wasp societies

Intracolony aggression within and between castes of social insects is common1,3. We have observed an unusual aggressive interaction between nestmates of the paper wasp Polistes dominulus. In response to foragers returning to the colony, females (workers) initiate aggressive encounters with males culminating with the male being forced head-first into an empty nest-cell (‘male-stuffing’). ‘Stuffed’ males are unable to feed, so the behaviour seems to ensure that food is preferentially channelled to larvae, which are likely to be more closely related to the workers than are the adult males.

Different Evolutionary Conditions for Worker and Soldier Castes: Genetic Systems Explaining Caste Distribution among Eusocial Insects

Although evolution of sterile castes in social insects has been extensively studied, the differences between worker and soldier castes have not been addressed sufficiently. It is suggested here that the evolution of worker and soldier castes must be considered in terms of different trade-offs, specifically, the different relations between benefits and costs of sterility. An individual should be a sterile worker if the genetic gain of raising its sibling is higher than the genetic cost of losing its own offspring, while an individual should be a sterile soldier if the sacrifice of its own life is genetically compensated for by survival of other family members. Using these different conditions for evolution of sterility, caste distribution among existing eusocial insects can be explained by a difference in genetic systems: Aphids and a parasitic wasp with asexual reproduction have only the soldier caste; wasps, bees, and ants with male-haploidy have mainly the worker caste; and termites with diploidy have dominantly the soldier caste.

Oxford Surveys in Evolutionary Biology

Weismann and modern biology, John Maynard Smith life history variation in placental mammals - unifying the data with theory, Paul H.Harvey et al comparative methods using phylogenetically independent contrasts, Austin Burt caste and change in social insects, D.M.Gordon inclusive fitnesw in a nutshell, David C.Queller levels of selection and sorting with special reference to the species level, Elisabeth S.Vrba the emergence, maintenance, and transitions of the earliest evolutionary units, Eors Szathmary population genetics at the DNA level - a review of the conribution of restriction enzyme studies.

Altruism's Evolution

What can recent theories in evolutionary biology about the problem of altruism contribute to a Christian perspective on the nature of humanity?Altruism is considered a ‘problem’ because Darwin’s theory of natural selection leads us to expect all organisms, including humans, to be selfish. According to the theory of natural selection those traits which we expect to see in the natural world are the ones which have conferred on their bearers the greatest reproductive success. As altruism means the giving of aid, a preliminary reading of Darwinism suggests that altruism poses a challenge to the whole theory of adaptation by natural selection. Sociobiology has a great deal to say about the evolution of altruism in non-humans. How far does the study of altruism in non-humans help us to understand altruism in us?Sociobiological theories for the evolution of altruism Sociobiology, the systematic study of the biological basis of all social behaviour, dates as a named discipline from only 1975, when E.O. Wilson’s now much-discussed book, Sociobiology: The New Synthesis, was published. As altruism manifestly requires social behaviour—an organism cannot be altruistic on its own!—theories for the evolution of altruism lie at the centre of sociobiology.The first biological explanation for altruism was, however, proposed by none other than Darwin himself. Having developed the theory of natural selection, Darwin went on to consider how the sterile castes in many social insects could have evolved. He realised that it might be argued that such castes could not have evolved by natural selection because the bearers of traits associated with sterility leave, by definition, no offspring, but he proposed that sterility in such circumstances could evolve by a process he termed ‘family selection’.

Enemy deterrence in the recruitment strategy of a termite: Soldier-organized foraging in Nasutitermes costalis

The nasute soldiers of the neotropical termite Nasutitermes costalis function as scouts by exploring new terrain for food in advance of the worker caste and regulate foraging activity by laying trails composed of sternal gland pheromone. Additional soldiers are at first recruited in large numbers, and subsequently workers appear as the pheromone concentration increases. The role of the nasutes in the organization of foraging is extremely unusual for the soldier caste in social insects and appears to be a component of a foraging/defense system that controls the recruitment of foragers and effectively deters attacks by ants, the most fierce and important predators of termites.

Group Selection and Its Significance for Ecology

Selection can be said to operate at the group level and deserves to be called group selection, when it affects two or more members of a lineage group as a unit. Just above the level of the individual we can delimit various of these lineage groups: a set of sibs, parents, and their offspring, a close-knit tribe of families related by at least the degree of third cousin, and so on. If selection operates on any of the groups as a unit, the process is referred to as kin selection. At a higher level, an entire breeding population may be the unit, so that populations (i.e., demes) possessing different genotypes are diminished or extinguished differentially, in which case we speak of interdemic (or interpopulation) selection. hierarchy of ascending levels of selection is visualized in Figure 1. concept of group selection was introduced by Darwin in The Origin of Species to account for the evolution of sterile castes in social insects. term intergroup selection, in the sense of interdemic selection defined here, was used by Sewall Wright in 1945. Essentially the same expression (Gruppenauslese), was used independently and with the same meaning by Olavi Kalela (1954, 1957), while the phrase kin selection was coined by J. Maynard Smith (1964). classification adopted here is approximately that recommended by J. L. Brown (1966). Selection can also operate at the level of species or entire clusters of related species. process, well known to paleontologists and biogeographers, is responsible for the familiar patterns of dynastic succession of major groups such as ammonites, sharks, graptolites, and dinosaurs through geologic time (Simpson 1953, P. J. Darlington 1971). It is even possible to conceive of the differential extinction of entire ecosystems, involving all trophic levels (Dunbar 1960). However, selection at these highest levels is not likely to be important in the evolution of altruism, for the following simple reason. In order to counteract individual