Caste ratios affect the reproductive output of social trematode colonies

Intraspecific phenotypic diversification in social organisms often leads to formation of physical castes which are morphologically specialized for particular tasks within the colony. The optimal caste allocation theory argues that specialized morphological castes are efficient at specific tasks, and hence different caste ratios should affect the ergonomic efficiency, hence reproductive output of the colony. However, the reproductive output of different caste ratios has been documented in few species of insects with equivocal support for the theory. This study investigated whether the ratios of nonreproductive and reproductive morphs affect the reproductive output of a recently discovered social trematode, Philophthalmus sp., in which the nonreproductive members are hypothesized to be defensive specialists. A census of natural infections and a manipulative in vitro experiment demonstrated a positive association between the reproductive output of trematode colonies and the ratio of nonreproductive to reproductive morphs in the presence of an intra‐host trematode competitor, Maritrema novaezealandensis. On the contrary, without the competitor, reproductive output was negatively associated with the proportion of nonreproductive castes in colonies. Our findings demonstrate for the first time a clear fitness benefit associated with the nonreproductive castes in the presence of a competitor while illustrating the cost of maintaining such morphs in noncompetitive situations. Although the proximate mechanisms controlling caste ratio remain unclear in this trematode system, this study supports the prediction that the fitness of colonies is influenced by the composition of specialized functional morphs in social organisms, suggesting a potential for adaptive shifts of caste ratios over evolutionary time.     

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.     

Physiology as a caste-defining feature

Division of labour is a key factor in the ecological success of social insects. Groups of individuals specializing on a particular behaviour are known as castes and are usually distinguished by morphology or age. Physiology plays a key role in both these types of caste, in either the developmental physiology which determines morphology, or the temporal changes in physiology over an insect’s life. Physiological correlates of morphological or temporal caste include differences in gland structure, secretory products, leanness, neuroanatomy and neurochemistry. However, purely physiological castes could also occur. Physiological castes are discrete groups of same-age same-size individuals with particular physiological competencies, or groups of individuals with similar physiology crossing age or size groups. A stable physiological caste occurs in the monomorphic Pharaoh’s ant, where some ants can detect old pheromone trails and retain this specialization over time. These ants differ physiologically from other workers, and the differences arise before eclosion. More temporary physiological castes occur in the ant Ectatomma where brood care specialists have more developed ovarioles than other same-aged workers, and in the honeybee where nurses, wax-workers and soldiers all differ physiologically from same-aged nestmates. Physiology is an important aspect of caste, not only in its contribution to age-related and morphological castes, but also in its own right as a caste grouping factor. While age and morphological differences make caste structures accessible for study, more cryptic physiological castes may play just as important a role in division of labour. Received 19 December 2007; revised 24 July and 18 September 2008; accepted 19 September 2008.     

Mate‐searching behavior in the invasive German wasp,Vespula germanica,in Patagonia

In order to increase the probability of reproduction, social insects can adopt various mate‐finding strategies, such as increasing densities of males at specific locations, and/or visual and chemical cues that attract the opposite sex. In field and laboratory studies we investigated strategies used by the invasive eusocial wasp Vespula germanica (Fabricius) (Hymenoptera: Vespidae). In tethered flight assays, we established contrasting flight patterns in females and males that may partly explain how related individuals distribute spatially during the mating period. We also determined experimentally, in the field and in the laboratory via olfactometer assays, that gynes produce airborne pheromonal cues that attract drones and are important during mate location. Our field trials also suggest that visual cues play a role in mate location. We conclude that in addition to aspects of the social biology of the species, an efficient mate‐location strategy can partly explain the invasion success of the species. Tools to mitigate the damage caused by yellowjackets may be developed by focusing on reproductive castes, in addition to workers.     

Polymorphism: a weak influence on worker aggregation level in ants

Abstract.  1. Aggregation of individuals, a basic behaviour in social species, plays an essential role in many aspects of animal life (reproduction, defence, and alimentation). Understanding how this phenomenon is modulated is important to comprehend the social organisation of the group.
2. In social insects, aggregation is influenced by environmental (e.g. the light level) and social (e.g. polyethism in monomorphic ants) factors. Ants display a great variation of biological characteristics (e.g. queen number, polymorphism, division of labour, etc.) that are likely to influence the level of inter-attraction and so the aggregation.
3. The present research focused on one biological characteristic: the morphological castes (minors, majors), testing the hypothesis that minors will aggregate more than majors due to their greater need to fight against the loss of heat and to increase their self-protection.
4. Aggregation experiments were conducted on two highly polymorphic species, Atta sexdens rubropilosa and Solenopsis interrupta , using the two extreme morphological castes (majors and minors).
5. All castes exhibited a low level of aggregation: 40–50% of workers assembled for both species, the biggest cluster involving 20% of the total population. The lack of difference between morphological castes in the aggregation shows the weak influence of polymorphism on the interactions between ants.
6. It is concluded that the main factor modulating the aggregation behaviour is polyethism, i.e. the division of labour associated with the presence of an outside-the-nest experience: workers that only take care of the brood, without outside world experience (brood-tenders) assembling more than foraging workers (foragers).     

Evidence for adaptive brain tissue reduction in obligate social parasites (Polyergus mexicanus) relative to their hosts (Formica fusca)

Brain investment is evolutionarily constrained by high costs of neural tissue. Several ecological factors favour the evolution of increased brain investment; we predict reduced brain region investment will accompany the evolution of organismal or social parasitism when parasites rely on host behaviour and cognition to solve ecological problems. To test this idea we investigated whether brain region investments differed between obligate slave‐making Polyergus mexicanus ant workers and their Formica fusca slave workers. Polyergus workers perform little labour for their colonies; enslaved workers of Formica host species forage, excavate nests and tend the brood. We focused on the calyces of the mushroom bodies, central processing brain regions that are larger in social insect workers that perform complex tasks. As predicted we found lower relative investment in mushroom body calyx in P. mexicanus workers than in F. fusca workers; by contrast, enslaved and free F. fusca workers did not differ in mushroom body calyx volume. We then tested whether slave‐makers and hosts differed in brain investment among sensory modalities. Polyergus slave‐makers employ several unique classes of pheromones during raids, and eye size relative to head size was smaller in P. mexicanus workers than in F. fusca workers. The size of antennal brain tissues relative to visual tissues was greater in Polyergus, both in the peripheral sensory lobes and in the mushroom body calyx, suggesting greater relative investment in antennal processing by slave‐makers. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 415–422.     

Contact between supercolonies elevates aggression in Argentine ants

Complex recognition systems underlie the social organization of many organisms. In social insects the acceptance of other individuals as nestmates can involve a variety of different cues, but the relative importance of these cues can change in relation to the fitness costs of accepting or rejecting other individuals. In this study we investigate the mechanisms that underlie recognition behaviour in Argentine ants (Linepithema humile). Introduced populations of Argentine ants are characterized by a social structure known as unicoloniality where intraspecific aggression is absent over large distances resulting in the formation of expansive supercolonies. Recent research has identified sites where multiple, mutually aggressive supercolonies co-occur allowing an examination of Argentine ant behaviour at territorial boundaries. We found that workers from different supercolonies always interact aggressively with one another, but that neighbours from different colonies (i.e., workers from nests located in the immediate vicinity of territory borders) consistently exhibited higher levels of aggression compared to those displayed by non-neighbours from different colonies (i.e., workers from nests located far enough away from a territory border so that interactions are unlikely). This difference in the level of aggression displayed between neighbours and between non-neighbours from different supercolonies cannot be explained by differences in relatedness or genetic similarity. Instead our findings suggest that direct contact between mutually antagonistic colonies is sufficient to elevate aggression. A laboratory experiment in which we manipulated the extent to which colonies with no prior history of contact could interact with one another, revealed that aggression increased after colonies were permitted to interact, but dropped after connections between colonies were severed. Moreover, the mere presence of an aggressive supercolony was sufficient to elicit elevated aggression. Overall these patterns are opposite to the “dear enemy” phenomenon and could be the result of the intense territorial aggression exhibited by established supercolonies of this species. Received 8 January 2007; revised 27 March 2007; accepted 28 March 2007.     

Morphological and developmental analysis of peripheral antennal chemosensory sensilla and central olfactory glomeruli in worker castes of Camponotus compressus (Fabricius, 1787)

The antennal lobes of different castes of the ant species Camponotus compressus show a marked diversity in the organization of their olfactory glomeruli. Notably, there is a significant difference in the number and size of glomeruli between the reproductives and the workers and among the different worker castes. In this report, we investigate the notion that these caste-specific differences in glomerular number might be accounted for, at least in part, by the differences in numbers of olfactory sensilla that target the antennal lobe. For this, we examine the number of sensilla on the antennal flagella of all the individual castes of C. compressus. This analysis reveals a striking correlation between sensillar number and the number of antennal glomeruli in a given caste. As a first step in investigating the causal mechanisms that might give raise to this correlation, we carry out an initial characterization of olfactory system development in the minor workers of C. compressus. We analyze the temporal pattern of innervations of the developing antennal lobe by olfactory sensory neuron axons. We document the development of the olfactory glomeruli in the antennal lobe during this process, which occurs during early pupal stages. Our findings provide the basis for future manipulative developmental studies on the role of sensory afferent number in glomerular development of different castes within the same species.     

Polyethism in social interactions in ants

Worker ants, which perform various tasks in their society (division of labour or polyethism), also demonstrate different types of antennal activity in trophallactic interactions. These differences concern the variability in successions of behavioural units performed by the worker in the course of substance transmission as well as in the sequential organization of these units. The antennal activity of an aged worker varies according to whether the ant gives food to another aged worker or to a callow worker. In the latter case, the donor's behaviour does not differ according to its social function (brood-tending worker or forager). A parallel can be established between these results and those obtained in a previous study of aggressive behaviour. This behaviour is liable to appear when a callow worker extracted from its society before hatching and therefore deprived of relations with aged workers of the society, is therefore placed with an aged worker. Polyethism is then manifested in social interactions, and not only in the division of labour between members of the society.     

Competition for resources mediated by intrinsic social dominance in sympatric finches

Gouldian Erythrura gouldiae and Long‐tailed Finches Poephila acuticauda are morphologically and ecologically similar sympatric species, for which social dominance relationships are likely to determine access to critical limiting resources. Building on previous research showing that Long‐tailed Finches dominate competition for nest‐sites, I staged dyadic contests for food between the two species in captivity in order to test social dominance dynamics under controlled conditions. Long‐tailed Finches were likely to dominate interactions with Gouldian Finches and expressed higher levels of aggression while competing for access to food. These results suggest a stable dominance relationship between the two species which could be affecting Gouldian Finches' access to food resources in the wild, potentially constraining their ability to recover from recent population declines.     

Heritabilities,social environment effects and genetic correlations of social behaviours in a cooperatively breeding vertebrate

Social animals interact frequently with conspecifics, and their behaviour is influenced by social context, environmental cues and the behaviours of interaction partners, allowing for adaptive, flexible adjustments to social encounters. This flexibility can be limited by part of the behavioural variation being genetically determined. Furthermore, behaviours can be genetically correlated, potentially constraining independent evolution. Understanding social behaviour thus requires carefully disentangling genetic, environmental, maternal and social sources of variations as well as the correlation structure between behaviours. Here, we assessed heritability, maternal, common environment and social effects of eight social behaviours in Neolamprologus pulcher, a cooperatively breeding cichlid. We bred wild‐caught fish in a paternal half‐sibling design and scored ability to defend a resource against conspecifics, to integrate into a group and the propensity to help defending the group territory (“helping behaviour”). We assessed genetic, social and phenotypic correlations within clusters of behaviours predicted to be functionally related, namely “competition,” “aggression,” “aggression‐sociability,” “integration” and “integration‐help.” Helping behaviour and two affiliative behaviours were heritable, whereas there was little evidence for a genetic basis in all other traits. Phenotypic social effects explained part of the variation in a sociable and a submissive behaviour, but there were no maternal or common environment effects. Genetic and phenotypic correlation within clusters was mostly positive. A group's social environment influenced covariances of social behaviours. Genetic correlations were similar in magnitude but usually exceeding the phenotypic ones, indicating that conclusions about the evolution of social behaviours in this species could be provisionally drawn from phenotypic data in cases where data for genetic analyses are unobtainable.     

Male aggressiveness in a polygynous ungulate varies with social and ecological context

Aggression is a social behaviour which can be affected by numerous factors. The quality and quantity of food resources may play an important role in the aggressiveness of territorial ungulates as the defence of these resources influences female choice and mating opportunities. However, the relationship between food resources and aggression remains poorly understood. We assessed the ecological and social factors that influence aggression in Lama guanicoe, a territorial ungulate exhibiting resource‐defence polygyny, during three periods (group‐formation, mating and post‐mating) in the reproductive seasons of 2014 and 2016. We recorded 460 focal observations of territorial (family groups, solitary) and non‐territorial (mixed and bachelor groups) males. We performed analyses at the population level (including all focal observations) and at the group level (each social unit separately), to test whether the factors that influence aggression differ at these different scales. We also identified proxies of vegetation quality as potential predictors of aggression. At the population level, we found that the presence of aggressive behaviour peaked during the mating season and that post‐mating aggression may have been driven by inter‐annual environmental variations. For family groups and solitary males, variables reflecting high vegetation quality/quantity were predictors of aggressive behaviour, reflecting the resource‐defence strategy of this species. Conversely, for mixed‐group males, aggression may be more associated with social instability and group size, although this hypothesis has yet to be tested. Our research reinforces the idea that aggression can occur in multiple contexts depending on male status (e.g. territorial or non‐territorial) and contributes to our understanding of how ecological (i.e. availability of food resources) and social factors influence aggression in a territorial ungulate.     

Caste and sex specific olfactory glomerular organization and brain architecture in two sympatric ant species Camponotus sericeus and Camponotus compressus (Fabricius, 1798)

We use monoclonal antibodies against synaptic proteins and anterograde tracing with neurobiotin to describe the architecture of the antennal lobes in different castes of two ant species – Camponotus sericeus and Camponotus compressus. The reproductives and worker classes are readily categorized based on size and external morphology. The overall organization of brain neuropile is comparable between castes with differences only in the visual ganglia. Males have a larger fraction of neuropile occupied by the medulla and lobula than females. In the diurnal species, C. sericeus these regions are more highly represented, than in the nocturnal species C. compressus. The most striking differences are in the antennal lobe where males possess a macroglomerulus, which is about ten times larger in volume than the other glomeruli; such a specialization is absent in females. Minor workers possess a significantly larger number of glomeruli than the majors despite the smaller overall volume of the lobe. These caste-specific differences occur mainly within glomerular clusters that receive input from sensory neurons that project in tracts – T4 and T5 – within the antennal nerve. The comparative anatomy of different castes of ants provides an entry point into a future systematic analysis of how divergent brain architectures can arise within a single species.     

Macroevolutionary integration of phenotypes within and across ant worker castes

Phenotypic traits are often integrated into evolutionary modules: sets of organismal parts that evolve together. In social insect colonies, the concepts of integration and modularity apply to sets of traits both within and among functionally and phenotypically differentiated castes. On macroevolutionary timescales, patterns of integration and modularity within and across castes can be clues to the selective and ecological factors shaping their evolution and diversification. We develop a set of hypotheses describing contrasting patterns of worker integration and apply this framework in a broad (246 species) comparative analysis of major and minor worker evolution in the hyperdiverse ant genus Pheidole. Using geometric morphometrics in a phylogenetic framework, we inferred fast and tightly integrated evolution of mesosoma shape between major and minor workers, but slower and more independent evolution of head shape between the two worker castes. Thus, Pheidole workers are evolving as a mixture of intracaste and intercaste integration and rate heterogeneity. The decoupling of homologous traits across worker castes may represent an important process facilitating the rise of social complexity.     

An ambiguous function of an alarm pheromone in the collective displays of the Australian meat ant,Iridomyrmex purpureus

Alarm pheromones, which have been documented in many species of ants, are thought to elicit responses related to aggressive or defensive behaviour. The volatile odour 6-methyl-5-hepten-2-one is described as an alarm pheromone in several species of ants, including the Australian meat ant, Iridomyrmex purpureus. The alarm pheromone is released by displaying workers that aggregate in the characteristic collective display grounds, located mid-way between colonies or near contested food trees. Workers are typically more aggressive at the latter location, and the alarm pheromone may regulate the collective level of aggression. We investigated this possibility by exposing displaying workers to synthesised alarm pheromone 6-methyl-5-hepten-2-one in a field experiment, and measuring their aggressive behaviour. We found no evidence that exposure to synthesised alarm pheromone caused changes in the aggressive level of workers. Subsequent field experiments revealed that the pheromone functions as an attractant, thereby increasing the density of displaying workers. More densely populated workers also display more aggressively, indicating that the interaction rate of displaying workers may determine the level of aggression in collective displays. This underlying mechanism can explain why displaying ants are more aggressive at the more densely populated food-tree locations than those displaying at locations midway between two neighbouring colony nest sites.     

Antennal olfactory sensitivity in response to task-related odours of three castes of the ant Atta mexicana (hymenoptera: formicidae)

Abstract.  The relationship between scent composition and antennal sensitivity in different castes of Atta mexicana is investigated under laboratory conditions. Extracts of dead ants are analysed by gas chromatography-mass spectrometry to identify the compounds presumably responsible for the specific undertaking behaviour. Oleic acid is identified as one compound that triggers undertaking behaviour. To determine differences in odour reception between workers of different castes (i.e. foragers, undertakers and soldiers), further antennal sensitivity to task-related odours is tested using electroantennographic techniques. Soldiers are the most specialized caste because of their low response to all odours, except odourants related to alarm pheromones. The behavioural specialization of soldiers and their reduced behavioural repertoire are discussed.     

Morphology and number of Ommatidia in the compound eyes of Solenopsis invicta, Solenopsis richteri, and their hybrid (Hymenoptera: Formicidae)

The morphology and number of ommatidia of the compound eyes of Solenopsis invicta, Solenopsis richteri and their hybrid are investigated. Comparisons are made of the morphology and number of ommatidia in S. invicta, S. richteri and their hybrid. Major workers have significantly more facets than minor workers, male reproductive more than female reproductive, and the reproductives more than workers. Workers and reproductives have significantly more ommatidia in S. invicta than in S. richteri and significantly fewer in the hybrid than in either species. The major workers of each species have significantly wider facets than the minor workers, and workers have significantly wider facets than reproductives, which showed no difference in their facet diameter. There are no significant differences when the facet diameter is compared between the members of the castes of different species. These morphological and numerical dissimilarities are discussed in connection with known behavioral differences in the castes.     

Social organization in a flatworm: trematode parasites form soldier and reproductive castes

In some of the most complex animal societies, individuals exhibit a cooperative division of labour to form castes. The most pronounced types of caste formation involve reproductive and non-reproductive forms that are morphologically distinct. In colonies comprising separate or mobile individuals, this type of caste formation has been recognized only among the arthropods, sea anemones and mole-rats. Here, we document physical and behavioural caste formation in a flatworm. Trematode flatworm parasites undergo repeated clonal reproduction of ‘parthenitae’ within their molluscan hosts forming colonies. We present experimental and observational data demonstrating specialization among trematode parthenitae to form distinct soldier and reproductive castes. Soldiers do not reproduce, have relatively large mouthparts, and are much smaller and thinner than reproductives. Soldiers are also more active, and are disproportionally common in areas of the host where invasions occur. Further, only soldiers readily and consistently attack heterospecifics and conspecifics from other colonies. The division of labour described here for trematodes is strongly analogous to that characterizing other social systems with a soldier caste. The parallel caste formation in these systems, despite varying reproductive mode and taxonomic affiliation, indicates the general importance of ecological factors in influencing the evolution of social behaviour. Further, the ‘recognition of self’ and the defence of the infected host body from invading parasites are comparable to aspects of immune defence. A division of labour is probably widespread among trematodes and trematode species encompass considerable taxonomic, life history and environmental diversity. Trematodes should therefore provide new, fruitful systems to investigate the ecology and evolution of sociality.     

How brood influences caste aggregation patterns in the dimorphic ant species Pheidole pallidula

Spatial distribution of ant workers and, notably their aggregation/segregation behaviour, is a key-element of the colony social organization contributing to the efficiency of task performance and division of labour. In polymorphic species, specialized worker castes notably differ in their intrinsic aggregation behaviour. In this context, knowing the preponderant role of minors in brood care, we investigate how a stimulus such as brood can influence the spatial patterns of Pheidole pallidula worker castes. In a homogeneous area without brood, it was shown that minors display only a low level of aggregation while majors form large clusters in the central area. Here we find out that these aggregation patterns of both minors and majors can be deeply influenced by the presence of brood. For minors, it nucleates or enhances the formation of a large stable cluster. Such high sensitivity of minors to brood stimuli fits well with their role as main brood tenders in the colony. For majors, interattraction between individuals still remains the prevailing aggregation factor while brood strongly influences the localisation of their cluster. We discuss how the balance between interattraction and sensitivity to environmental stimuli determines the mobility of each worker castes and, consequently, the availability of minors and majors to participate in everyday colony tasks. Moreover, we will evoke the functional value of majors’ cluster location close to the brood, namely with respect to social regulation of the colony caste ratio. Received 30 May 2005; revised 11 January 2006; accepted 13 January 2006.