昆虫社会行为的进化与生态适应

一、引言昆虫社会行为的进化涉及两大问题:(1)社会行为的起源和进化过程;(2)社会行为的适应意义。这两个问题都曾使达尔文感到困惑。达尔文曾详尽地描述过蜜蜂复杂的造巢行     

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.     

Evidence for multiple mating in the primitively eusocial waspRopalidia marginata (Lep.) (Hymenoptera: Vespidae)

Asymmetries in genetic relatedness created by haplodiploidy have been considered to be crucially important for the evolution of worker behaviour in Hymenoptera. Multiple mating by the queens destroys this asymmetry and should make kin selection less powerful. The number of males that social insect queens mate with is thus of considerable theoretical interest especially in primitively eusocial species. The results presented here provide evidence for multiple mating by foundresses of the primitively eusocial waspRopalidia marginata (Lep.)     

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.     

Differential gene expression and phenotypic plasticity in behavioural castes of the primitively eusocial wasp, Polistes canadensis

Understanding how a single genome can produce a variety of different phenotypes is of fundamental importance in evolutionary and developmental biology. One of the most striking examples of phenotypic plasticity is the female caste system found in eusocial insects, where variation in reproductive (queens) and non-reproductive (workers) phenotypes results in a broad spectrum of caste types, ranging from behavioural through to morphological castes. Recent advances in genomic techniques allow novel comparisons on the nature of caste phenotypes to be made at the level of the genes in organisms for which there is little genome information, facilitating new approaches in studying social evolution and behaviour. Using the paper wasp Polistes canadensis as a model system, we investigated for the first time how behavioural castes in primitively eusocial insect societies are associated with differential expression of shared genes. We found that queens and newly emerged females express gene expression patterns that are distinct from each other whilst workers generally expressed intermediate patterns, as predicted by Polistes biology. We compared caste-associated genes in P. canadensis with those expressed in adult queens and workers of more advanced eusocial societies, which represent four independent origins of eusociality. Nine genes were conserved across the four taxa, although their patterns of expression and putative functions varied. Thus, we identify several genes that are putatively of evolutionary importance in the molecular biology that underlies a number of caste systems of independent evolutionary origin.     

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.     

Evolution of maternal care in diploid and haplodiploid populations

Maternal care has been suggested to evolve more readily in haplodiploid populations. Because maternal care appears to have been a prerequisite for the evolution of eusociality, this effect potentially explains the apparent preponderance of haplodiploidy among eusocial taxa. Here, I use a kin selection approach to model the evolution of maternal care in diploid and haplodiploid populations. In contrast to previous suggestions, I find that haplodiploidy may inhibit as well as promote the evolution of maternal care. Moreover, I find that the haplodiploidy effect vanishes in outbred populations if gene effects average rather than add together. I confirm these analytical results using numerical simulation of an explicit population genetics model. This analysis casts doubt upon the idea that haplodiploidy has promoted the evolution of maternal care and, consequently, the evolution of eusociality.     

Forum: The eusociality continuum

Eusocial societies are traditionally characterized by a reproductivedivision of labor, an overlap of generations, and cooperativecare of the breeders' young. Eusociality was once thought tooccur only in termites, ants, and some bee and wasp species,but striking evolutionary convergences have recently becomeapparent between the societies of these insects and those ofcooperatively breeding birds and mammals. These parallels haveblurred distinctions between cooperative breeding and eusociality,leading to calls for either drastically restricting or expandingusage of these terms. We favor the latter approach. Cooperativebreeding and eusociality are not discrete phenomena, but ratherform a continuum of fundamentally similar social systems whosemain differences lie in the distribution of lifetime reproductivesuccess among group members. Therefore we propose to array vertebrateand invertebrate cooperative breeders along a common axis, representinga standardized measure of reproductive variance, and to dropsuch (loaded) terms as "primitive" and "advanced" eusociality.The terminology we propose unites all occurrences of alloparentalhelping of kin under a single theoretical umbrella (e.g., Hamilton'srule). Thus, cooperatively breeding vertebrates can be regardedas eusocial, just as eusocial invertebrates are cooperativebreeders. We believe this integrated approach will foster potentiallyrevealing cross-taxon comparisons, which are essential to understandingsocial evolution in birds, mammals, and insects.     

Social wasps without workers: geographic variation of caste expression in the paper wasp Polistes biglumis

In primitively eusocial insects, caste expression is flexible. Even though Polistes species are well known to show social trait variation (e.g., worker vs. gyne) depending on ecological context, loss of worker caste in some populations of a eusocial, worker-containing species has never been documented. We report first data on geographic variation in caste expression in Polistes biglumis. We compared physiological and behavioural traits of the first female offspring from four populations that experience different climatic conditions and social parasite prevalence. We demonstrated that the first female offspring to emerge in cold areas with high parasite prevalence had more abundant, gyne-like fat bodies and exhibited lower foraging effort, in comparison to the first female offspring produced in warm areas with low parasite prevalence. Thus, the populations under severe environmental conditions produced a totipotent female offspring and suppressed worker production, whereas the population living in less extreme environmental conditions produced worker-like females as first female offspring and gyne-like females as offspring that emerged later. The existence of mixed social strategies among populations of primitively eusocial species could have important consequences for the study of social evolution, shedding light on the sequence of steps by which populations evolve between the extremes of solitary state and eusocial state.     

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.     

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.     

Phylogeny of eusocial Lasioglossum reveals multiple losses of eusociality within a primitively eusocial clade of bees (Hymenoptera: Halictidae)

We performed a phylogenetic analysis of the species, species groups, and subgenera within the predominantly eusocial lineage of Lasioglossum (the Hemihalictus series) based on three protein coding genes: mitochondrial cytochrome oxidase I, nuclear elongation factor 1alpha and long-wavelength rhodopsin. The entire data set consisted of 3421 aligned nucleotide sites, 854 of which were parsimony informative. Analyses by equal weights parsimony, maximum likelihood, and Bayesian methods yielded good resolution among the 53 taxa/populations, with strong bootstrap support and high posterior probabilities for most nodes. There was no significant incongruence among genes, and parsimony, maximum likelihood, and Bayesian methods yielded congruent results. We mapped social behavior onto the resulting tree for 42 of the taxa/populations to infer the likely history of social evolution within Lasioglossum. Our results indicate that eusociality had a single origin within Lasioglossum. Within the predominantly eusocial clade, however, there have been multiple (six) reversals from eusociality to solitary nesting, social polymorphism, or social parasitism, suggesting that these reversals may be more common in primitively eusocial Hymenoptera than previously anticipated. Our results support the view that eusociality is hard to evolve but easily lost. This conclusion is potentially important for understanding the early evolution of the advanced eusocial insects, such as ants, termites, and corbiculate bees.     

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.     

Building a new research framework for social evolution: intralocus caste antagonism

The breeding and non‐breeding ‘castes’ of eusocial insects provide a striking example of role‐specific selection, where each caste maximises fitness through different morphological, behavioural and physiological trait values. Typically, queens are long‐lived egg‐layers, while workers are short‐lived, largely sterile foragers. Remarkably, the two castes are nevertheless produced by the same genome. The existence of inter‐caste genetic correlations is a neglected consequence of this shared genome, potentially hindering the evolution of caste dimorphism: alleles that increase the productivity of queens may decrease the productivity of workers and vice versa, such that each caste is prevented from reaching optimal trait values. A likely consequence of this ‘intralocus caste antagonism’ should be the maintenance of genetic variation for fitness and maladaptation within castes (termed ‘caste load’), analogous to the result of intralocus sexual antagonism. The aim of this review is to create a research framework for understanding caste antagonism, drawing in part upon conceptual similarities with sexual antagonism. By reviewing both the social insect and sexual antagonism literature, we highlight the current empirical evidence for caste antagonism, discuss social systems of interest, how antagonism might be resolved, and challenges for future research. We also introduce the idea that sexual and caste antagonism could interact, creating a three‐way antagonism over gene expression. This includes unpacking the implications of haplodiploidy for the outcome of this complex interaction.     

Cooperative nest building and brood care by nestmates and non nestmates in Ropalidia marginata : implications for the evolution of eusociality

In the primitively eusocial wasp, Ropalidia marginata, low levels of intra-colony genetic relatedness, lack of intra-colony kin discrimination and acceptance of young wasps into alien colonies, prompted us to investigate whether or not there exists a cost of such high genetic variability. Freshly eclosed wasps were paired either with their nestmates or with their non nestmates and their performance in nest building and brood care were compared. There was no demonstrable difference between nestmate and non nestmate pairs in terms of success in raising adult offspring, time required for nest initiation, brood developmental period and productivity. There was also no difference in the efficiency of cooperation and division of labour between the nestmate pairs and non nestmate pairs. These results reinforce the idea that the haplodiploidy hypothesis is insufficient to explain the prevalence of worker behaviour in R. marginata and emphasize the importance of factors other than genetic relatedness in the evolution of eusociality. Received: 27 April 1998 / Accepted: 10 July 1998     

Advanced eusociality, kin selection and male haploidy

Abstract  The generation-long primacy of kin selection in explaining the evolution of advanced eusociality in social insects has been challenged in recent papers. Does this challenge succeed? I consider three questions: is kin selection still the unchallengeable explanation for the evolution of eusociality; is the male haploidy of Hymenoptera important in this explanation; and, a subsidiary question of why are there no male workers in Hymenoptera? I briefly trace the origins of kin selection back to Darwin and then consider the explanations of mutualism, group selection, parental manipulation, and kin selection and its variant 'green beard' alleles. I stress that in the kin selection equation, however written, relatedness is deeply intertwined with ecology so that both are essential. Kin selection does remain unchallengeable but, for some, the role of male haploidy has lost favour recently despite several modelling efforts all finding that it favours the evolution of eusociality. Sex allocation is deep at the heart of the evolution of hymenopteran advanced eusociality, indicating the interacting roles of population genetics and general biology. Modellers have also found no reason for a lack of male workers, so that a biological superiority of females for this role is indicated for social Hymenoptera.     

The Soldiers in Societies: Defense,Regulation, and Evolution

The presence of reproductively altruistic castes is one of the primary traits of the eusocial societies. Adaptation and regulation of the sterile caste, to a certain extent, drives the evolution of eusociality. Depending on adaptive functions of the first evolved sterile caste, eusocial societies can be categorized into the worker-first and soldier-first lineages, respectively. The former is marked by a worker caste as the first evolved altruistic caste, whose primary function is housekeeping, and the latter is highlighted by a sterile soldier caste as the first evolved altruistic caste, whose task is predominantly colony defense. The apparent functional differences between these two fundamentally important castes suggest worker-first and soldier-first eusociality are potentially driven by a suite of distinctively different factors. Current studies of eusocial evolution have been focused largely on the worker-first Hymenoptera, whereas understanding of soldier-first lineages including termites, eusocial aphids, gall-dwelling thrips, and snapping shrimp, is greatly lacking. In this review, we summarize the current state of knowledge on biology, morphology, adaptive functions, and caste regulation of the soldier caste. In addition, we discuss the biological, ecological and genetic factors that might contribute to the evolution of distinct caste systems within eusocial lineages.     

Genomic imprinting and evolution of insect societies

Reproductive division of labor is a hallmark of social insect societies where individuals follow different developmental pathways resulting in distinct morphological castes. There has been a long controversy over the factors determining caste fate of individuals in social insects. Increasing evidence in the last two decades for heritable influences on division of labor put an end to the assumption that social insect broods are fully totipotent and environmental factors alone determine castes. Nevertheless, the genes that underlie hereditary effects on division of labor have not been identified in any social insects. Studies investigating the hereditary effects on caste determination might have overlooked non-genetic inheritance, while transmission to offspring of factors other than DNA sequences including epigenetic states can also affect offspring phenotype. Genomic imprinting is one of the most informative paradigms for understanding the consequences of interactions between the genome and the epigenome. Recent studies of genomic imprinting show that genes can be differentially marked in egg and sperm and inheritance of these epigenetic marks cause genes to be expressed in a parental-origin-specific manner in the offspring. By reviewing both the eusocial Hymenoptera and termites, I highlight the current theoretical and empirical evidence for genomic imprinting in eusocial insects and discuss how genomic imprinting acts in caste determination and social behavior and challenges for future studies. I also introduce the new idea that genomic imprinting plays an essential role in the origin of eusociality.     

An alternative strategy for maintenance of eusociality after nest destruction: new nest construction in a primitively eusocial wasp

Although nests are central to colonial life in social insects, nests are sometimes damaged by predators or natural disasters. After nest destruction, individuals usually construct new nests. In this case, a sophisticated mechanism like the scent trail pheromone used in large insect colonies that recruit individuals to new nest sites would be important for the maintenance of eusociality. In independent-founding Polistes wasps, it is well known that queens enforce workers physiologically on the natal nests even if evidence of trail pheromone use has not been exhibited. We investigated the effect of the queen on an alternative strategy for the maintenance of eusociality by first females after nest destruction in the primitively eusocial wasp Polistes chinensis. We predicted that the first females in queen-absent colonies have various behavioral options after nest destruction. Even if the females construct new nests cooperatively with other individuals, the new nest construction should be conducted more smoothly in queen-present colonies because the queens regulate the behavior of wasps. We made wasps construct new nests by removing the entire brood from existing nests. The presence of the queen did not cause variation in the alternative strategy of the first females, as the first females (workers) usually constructed new nests cooperatively irrespective of the queen-presence. Thus, the workers in the queenpresent colonies affiliated to the new nest construction more smoothly and constructed new nests more efficiently than workers in the queen-absent colonies. Our results suggest that the presence of the queen is important for maintaining eusociality in primitively eusocial wasps after nest destruction. Received 8 February 2005; revised 5 October 2005; accepted 17 October 2005.