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.     

Wingless virgin queens assume helper roles in Acromyrmex leaf-cutting ants

Division of labour is the hallmark of advanced societies, because specialization carries major efficiency benefits in spite of costs owing to reduced individual flexibility [1]. The trade-off between efficiency and flexibility is expressed throughout the social insects, where facultative social species have small colonies and reversible caste roles and advanced eusocial species have permanently fixed queen and worker castes. This usually implies that queens irreversibly specialize on reproductive tasks [2]. Here, we report an exception to this rule by showing that virgin queens (gynes) of the advanced eusocial leaf-cutting ant Acromyrmex echinatior switch to carrying out worker tasks such as brood care and colony defence when they fail to mate and disperse. These behaviours allow them to obtain indirect fitness benefits (through assisting the reproduction of their mother) after their direct fitness options (their own reproduction) have become moot. We hypothesize that this flexibility could (re-)evolve secondarily because these ants only feed on fungal mycelium and thus could not benefit from cannibalising redundant gynes, and because queens have retained behavioural repertoires for foraging, nursing, and defense, which they naturally express during colony founding.     

An Inclusive Fitness-Based Exploration of the Origin of Soldiers: The Roles of Sex Ratio, Inbreeding, and Soldier Reproduction

I present an inclusive fitness model for the origin of soldiers that incorporates soldier production of males and females, in haplodiploids and diploids. In this paper, the term soldier refers to an individual that is morphologically and/or behaviorally specialized for defense. However, the model presented here can usefully be extended to other helping behaviors that are episodic in nature and that impact the colony as a whole rather than helping behavior that is directed to specific individuals. In general, the results of the model show that proto-soldier reproduction via sib-mating increases the ease with which soldiering evolves. Male haplodiploids appear the most apt to evolve soldier behavior compared to female haplodiploids and diploids. Haplodiploid females are expected to produce a greater proportion of male dispersers relative to their production of female dispersers and thereby increase the predilection in females to evolve soldiering compared to diploid populations. Application of the model to gall-forming thrips in Australia reveals that species basal to the phylogenetic branch where soldiers are inferred to have evolved show a lower threshold for soldier evolution than more derived species. This phylogenetic pattern is consistent with soldier production of male and female offspring facilitating the origin of soldiering in the social gall-forming thrips.     

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.     

Colony size explains the lifespan differences between queens and workers in eusocial Hymenoptera

Eusocial Hymenoptera show a unique divergence in lifespan of queens and workers; queens belong to the longest lived insects while workers in most eusocial species have significantly shorter lives. The different phenotypes within a colony emerge through reproductive division of labour, which is a characteristic trait of eusocial animals. Division of labour as a measure of organismal complexity increases with colony size in eusocial species similar to the increase of complexity with size that has been shown for the whole range of living organisms. We show that queen and worker lifespan diverge in closely related species representing the transition from solitary to social life and show that queen and worker lifespan are correlated if colony size is taken into account: with increasing colony size the lifespan differential between queen and worker increases, whereas neither queen nor worker lifespan is associated with colony size. Additionally, the lifespan differential is better explained by colony size than by the weight differences between the castes. The divergence of phenotypes found is in line with the increasing specialization of subunits in larger organisms, which leads to increasing complexity. We argue that division of labour is acting to increase colony efficiency, which in turn shapes the investments made into individuals leading to short‐lived workers and long‐lived queens. Additionally, maintenance investments may be shaped due to the variable extrinsic risk faced by different castes. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 710–724.     

Inbreeding depression and haplodiploidy: experimental measures in a parasitoid and comparisons across diploid and haplodiploid insect taxa

Abstract. It has long been assumed that inbreeding depression in haplodiploid organisms is low due to their ability to purge genetic load in haploid males. It has been suggested that this low genetic load could facilitate the evolution of inbreeding behaviors driven by local mate competition in hymenopteran parasitoids. I have examined inbreeding depression in haplodiploids in two ways. First I show that an outbreeding haplodiploid wasp Uscana semifumipennis (Hymenoptera: Trichogrammatidae) suffers substantial inbreeding depression. Longevity was 38% shorter, fecundity was 32% lower, and sex ratio was 5% more male for experimentally inbred wasps when compared to outbred controls. There were interactions between size and both fecundity and sex ratio for inbred wasps that were not seen for outbred individuals. Second, an analysis of data from the literature suggests that when inbreeding is experimentally imposed on populations, haplodiploid insects and mites as a group do suffer less from inbreeding depression than diploid insects, although substantial inbreeding depression in haplodiploid taxa does exist. The meta-analysis revealed no difference in inbreeding depression between gregarious haplodiploid wasps, which are likely to have a history of inbreeding, and solitary haplodiploid species, which are assumed to be primarily outbred.     

Colony size predicts division of labour in attine ants

Division of labour is central to the ecological success of eusocial insects, yet the evolutionary factors driving increases in complexity in division of labour are little known. The size–complexity hypothesis proposes that, as larger colonies evolve, both non-reproductive and reproductive division of labour become more complex as workers and queens act to maximize inclusive fitness. Using a statistically robust phylogenetic comparative analysis of social and environmental traits of species within the ant tribe Attini, we show that colony size is positively related to both non-reproductive (worker size variation) and reproductive (queen–worker dimorphism) division of labour. The results also suggested that colony size acts on non-reproductive and reproductive division of labour in different ways. Environmental factors, including measures of variation in temperature and precipitation, had no significant effects on any division of labour measure or colony size. Overall, these results support the size–complexity hypothesis for the evolution of social complexity and division of labour in eusocial insects. Determining the evolutionary drivers of colony size may help contribute to our understanding of the evolution of social complexity.     

Population genomics of eusocial insects: the costs of a vertebrate‐like effective population size

The evolution of reproductive division of labour and social life in social insects has lead to the emergence of several life‐history traits and adaptations typical of larger organisms: social insect colonies can reach masses of several kilograms, they start reproducing only when they are several years old, and can live for decades. These features and the monopolization of reproduction by only one or few individuals in a colony should affect molecular evolution by reducing the effective population size. We tested this prediction by analysing genome‐wide patterns of coding sequence polymorphism and divergence in eusocial vs. noneusocial insects based on newly generated RNA‐seq data. We report very low amounts of genetic polymorphism and an elevated ratio of nonsynonymous to synonymous changes – a marker of the effective population size – in four distinct species of eusocial insects, which were more similar to vertebrates than to solitary insects regarding molecular evolutionary processes. Moreover, the ratio of nonsynonymous to synonymous substitutions was positively correlated with the level of social complexity across ant species. These results are fully consistent with the hypothesis of a reduced effective population size and an increased genetic load in eusocial insects, indicating that the evolution of social life has important consequences at both the genomic and population levels.     

The evolution of caste polymorphism in social insects:0 Genetic release followed by diversifying evolution

Caste polymorphism, defined as the presence within a colony of two or more morphologically differentiated individuals of the same sex, is an important character of highly eusocial insects both in the Hymenoptera (ants, bees and wasps) and in the Isoptera (termites), the only two groups in the animal kingdom where highly eusocial species occur. Frequently, caste polymorphism extends beyond mere variations in size (although the extent of variations in size can be in the extreme) and is accompanied by allometric variations in certain body parts. How such polymorphism has evolved and why, in its extreme form, it is essentially restricted to the social insects are questions of obvious interest but without satisfactory answers at the present time. I present a hypothesis entitled ‘genetic release followed by diversifying evolution’, that provides potential answers to these questions. I argue that genetic release followed by diversifying evolution is made possible under a number of circumstances. One of them I propose is when some individuals in a species begin to rely on the indirect component of inclusive fitness while others continue to rely largely on the direct component, as workers and queens in social insects are expected to do. Thus when queens begin to rely on workers for most of the foraging, nest building and brood care, and workers begin to rely increasingly on queens to lay eggs—when queen traits and worker traits do not have to be expressed in the same individual—I postulate the relaxation of stabilizing selection and new spurts of directional selection on both queen-trait genes and worker-trait genes (in contrasting directions) leading to caste polymorphism.     

Haplodiploidy, sex, and the evolution of pesticide resistance

The assumption that males and females are equally tolerant to pesticides in haplodiploid arthropods led to the prediction that the evolution of resistance is faster in haplodiploid than in diploid arthropods. However, in this review, it was found that the ratio of male to female tolerance is substantially smaller in haplodiploid than in diploid arthropods, indicating that resistance alleles are not strongly up-regulated in haploid males. In addition, males were generally less tolerant than females in both haplodiploid and diploid arthropods. Factors such as sexual size dimorphism and sex-dependent selection may account for the lower tolerance in males than in females. Little among-population variation in the ratio of male to female tolerance was found in three species. Moreover, the tolerance ratio generally remained unchanged by selection for resistance to pesticides, although significant among-species variation was present within arthropod orders. This indicates that sexual dimorphism in pesticide tolerance evolves at a slower rate than resistance to pesticides. Simulations considering between-sex differences in pesticide tolerance showed that resistance evolution can be slower in haplodiploids than in diploids. Recessive resistance, low male tolerance to pesticides, fitness costs expressed in males, and the use of refuges contributed in substantially delaying the evolution of resistance in haplodiploid arthropods. These findings cast a new perspective on the evolution of pesticide resistance in haplodiploid herbivores and natural enemies.     

Specialised placement of morphs within the gall of the social aphid <Emphasis Type="Italic">Pemphigus spyrothecae</Emphasis>

Background  

The strategic placement and aggregation of certain castes within the nests of eusocial insects such as bees and ants results in complex colonies that enjoy increased fitness through improved efficiency of social tasks. To examine if this advanced social phenomenon might apply to social aphids, the location of the numerous morphs within the nests (plant galls) of the aphid species Pemphigus spyrothecae was examined.     

Iterative evolution of increased behavioral variation characterizes the transition to sociality in spiders and proves advantageous

Abstract The evolution of group living is regarded as a major evolutionary transition and is commonly met with correlated shifts in ancillary characters. We tested for associations between social tendency and a myriad of abiotic variables (e.g., temperature and precipitation) and behavioral traits (e.g., boldness, activity level, and aggression) in a clade of spiders that exhibit highly variable social structures (genus Anelosimus). We found that, relative to their subsocial relatives, social species tended to exhibit reduced aggressiveness toward prey, increased fearfulness toward predators, and reduced activity levels, and they tended to occur in warm, wet habitats with low average wind velocities. Within-species variation in aggressiveness and boldness was also positively associated with sociality. We then assessed the functional consequences of within-species trait variation on reconstituted colonies of four test species (Anelosimus eximius, Anelosimus rupununi, Anelosimus guacamayos, and Anelosimus oritoyacu). We used colonies consisting of known ratios of docile versus aggressive individuals and group foraging success as a measure of colony performance. In all four test species, we found that groups composed of a mixture of docile and aggressive individuals outperformed monotypic groups. Mixed groups were more effective at subduing medium and large prey, and mixed groups collectively gained more mass during shared feeding events. Our results suggest that the iterative evolution of depressed aggressiveness and increased within-species behavioral variation in social spiders is advantageous and could be an adaptation to group living that is analogous to the formation of morphological castes within the social insects.     

Influence of sociality on allometric growth and morphological differentiation in sponge-dwelling alpheid shrimp

Eusocial societies are defined by a reproductive division of labour between breeders and nonbreeders that is often accompanied by morphological differentiation. Some eusocial taxa are further characterized by a subdivision of tasks among nonbreeders, often resulting in morphological differentiation among different groups (subcastes) that specialize on different sets of tasks. We investigated the possibility of morphological castes in eusocial shrimp colonies ( Zuzalpheus , formerly part of Synalpheus ) by comparing growth allometry and body proportions of three eusocial shrimp species with three pair-forming species (species where reproductive females and males occur in equal sex ratios). Allometry of eusocial species differed in several respects from that of pair-forming species in both lineages. First, allometry of fighting claw size among individuals other than female breeders was steeper in eusocial than in pair-forming species. Second, breeding females in eusocial colonies had proportionally smaller weapons (fighting claws) than females in pair-forming species. Finally, claw allometry changed with increasing colony size in eusocial species; large colonies showed a diphasic allometry of fighting claw and finger size, indicating a distinctive group of large individuals possessing relatively larger weapons than other colony members. Shrimp are thus similar to other eusocial animals in the morphological differentiation between breeders and nonbreeders, and in the indication that some larger nonbreeders might contribute more to defence than others.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 527–540.     

Alate susceptibility in ants

Pathogens are predicted to pose a particular threat to eusocial insects because infections can spread rapidly in colonies with high densities of closely related individuals. In ants, there are two major castes: workers and reproductives. Sterile workers receive no direct benefit from investing in immunity, but can gain indirect fitness benefits if their immunity aids the survival of their fertile siblings. Virgin reproductives (alates), on the other hand, may be able to increase their investment in reproduction, rather than in immunity, because of the protection they receive from workers. Thus, we expect colonies to have highly immune workers, but relatively more susceptible alates. We examined the survival of workers, gynes, and males of nine ant species collected in Peru and Canada when exposed to the entomopathogenic fungus Beauveria bassiana. For the seven species in which treatment with B. bassiana increased ant mortality relative to controls, we found workers were significantly less susceptible compared with both alate sexes. Female and male alates did not differ significantly in their immunocompetence. Our results suggest that, as with other nonreproductive tasks in ant colonies like foraging and nest maintenance, workers have primary responsibility for colony immunity, allowing alates to specialize on reproduction. We highlight the importance of colony‐level selection on individual immunity in ants and other eusocial organisms.     

Geographic variation of caste structure among ant populations

Morphologically distinct worker castes of eusocial insects specialize in different tasks. The relative proportions of these castes and their body sizes represent the demography of a colony that is predicted to vary adaptively with environments. Despite strong theoretical foundations, there has been little empirical evidence for the evolution of colony demography in nature. We show that geographically distinct populations of the ant Pheidole morrisi differ in worker caste ratios and worker body sizes in a manner consistent with microevolutionary divergence. We further show that the developmental mechanism for caste determination accounts for the unique pattern of covariation observed in these two traits. Behavioral data reveal that the frequency of different tasks performed by workers changes in a caste-specific manner when caste ratios are altered and demonstrate the importance of the major caste in colony defense. The population-level variation documented here for P. morrisi colonies supports the predictions of adaptive demography theory and illustrates that developmental mechanisms can play a significant role in shaping the evolution of phenotype at the colony level.     

Phylogenetic analysis and the evolution of queen number in eusocial Hymenoptera

Analyses of the evolution of colony queen number in eusocial insects have generally been conducted without specific reference to phylogenetic relationships, leading to incomplete evolutionary explanations for this key attribute of social organization. Consideration of queen number in a phylogenetic context in the highly eusocial Hymenoptera reveals that its evolution has been very conservative in the bees but that it is a highly labile character in most ants. The wasps appear intermediate in this respect, with some large and widespread clades characterized by little or no phylogenetic variability in queen number. This hierarchy of phylogenetic lability suggests that while ant populations may often be responsive to selection on colony queen number linked with local ecology, bees and wasps appear less responsive in this regard, with a significant element of phylogenetic conservatism involved in the expression of this social trait in the latter two groups.     

Brain organization mirrors caste differences,colony founding and nest architecture in paper wasps (Hymenoptera: Vespidae)

The cognitive challenges that social animals face depend on species differences in social organization and may affect mosaic brain evolution. We asked whether the relative size of functionally distinct brain regions corresponds to species differences in social behaviour among paper wasps (Hymenoptera: Vespidae). We measured the volumes of targeted brain regions in eight species of paper wasps. We found species variation in functionally distinct brain regions, which was especially strong in queens. Queens from species with open-comb nests had larger central processing regions dedicated to vision (mushroom body (MB) calyx collars) than those with enclosed nests. Queens from advanced eusocial species (swarm founders), who rely on pheromones in several contexts, had larger antennal lobes than primitively eusocial independent founders. Queens from species with morphologically distinct castes had augmented central processing regions dedicated to antennal input (MB lips) relative to caste monomorphic species. Intraspecific caste differences also varied with mode of colony founding. Independent-founding queens had larger MB collars than their workers. Conversely, workers in swarm-founding species with decentralized colony regulation had larger MB calyx collars and optic lobes than their queens. Our results suggest that brain organization is affected by evolutionary transitions in social interactions and is related to the environmental stimuli group members face.     

The evolutionary dynamics of adaptive virginity,sex‐allocation,and altruistic helping in haplodiploid animals

In haplodiploids, females can produce sons from unfertilized eggs without mating. However, virgin reproduction is usually considered to be a result of a failure to mate, rather than an adaptation. Here, we build an analytical model for evolution of virgin reproduction, sex‐allocation, and altruistic female helping in haplodiploid taxa. We show that when mating is costly (e.g., when mating increases predation risk), virginity can evolve as an adaptive female reproductive strategy. Furthermore, adaptive virginity results in strongly divergent sex‐ratios in mated and virgin queen nests (“split sex ratios”), which promotes the evolution of altruistic helping by daughters in mated queen nests. However, when helpers evolve to be efficient and increase nest production significantly, virgin reproduction is selected against. Our results suggest that adaptive virginity could have been an important stepping stone on the pathway to eusociality in haplodiploids. We further show that virginity can be an adaptive reproductive strategy also in primitively social haplodiploids if workers bias the sex ratio toward females. By remaining virgin, queens are free to produce sons, the more valuable sex in a female‐biased population. Our work brings a new dimension to the studies linking reproductive strategies with social evolution.     

The role of male disease susceptibility in the evolution of haplodiploid insect societies

Heterozygosity at loci affecting resistance against parasites can benefit host fitness. We predict that, in haplodiploid species, haploid males will suffer decreased parasite resistance relative to diploid females. We suggest that elevated susceptibility in haploid males has shaped the evolution of social behaviour in haplodiploid species. Male susceptibility will select for behavioural adaptations that limit males' exposure to pathogens and that limit male transmission of pathogens within and between colonies. The relatedness-asymmetry hypothesis that has been advanced to explain female-only workers does not make these predictions. We review the relevant evidence for genetic effects on parasite resistance in insects and summarize empirical evidence that relates to the haploid-susceptibility hypothesis.