A comparative study of egg recognition signature mixtures in Formica ants

Processing of information from the environment, such as assessing group membership in social contexts, is a major determinant of inclusive fitness. For social insects, recognizing brood origin is crucial for inclusive fitness in many contexts, such as social parasitism and kin conflicts within colonies. Whether a recognition signature is informative in kin conflicts depends on the extent of a genetic contribution into the cues. We investigated colony‐ and matriline‐specific variation in egg surface hydrocarbons in seven species of Formica ants. We show that chemical variance is distributed similarly to genetic variation, suggesting a significant genetic contribution to eggs odors in the genus. Significant among matriline components, and significant correlations between chemical and genetic similarity among individuals also indicate kin informative egg odors in several species. We suggest that egg odor surface variation could play a large role in within colony conflicts, and that a comparative method can reveal novel insight into communication of identity.     

Blending of heritable recognition cues among ant nestmates creates distinct colony gestalt odours but prevents within‐colony nepotism

The evolution of sociality is facilitated by the recognition of close kin, but if kin recognition is too accurate, nepotistic behaviour within societies can dissolve social cohesion. In social insects, cuticular hydrocarbons act as nestmate recognition cues and are usually mixed among colony members to create a Gestalt odour. Although earlier studies have established that hydrocarbon profiles are influenced by heritable factors, transfer among nestmates and additional environmental factors, no studies have quantified these relative contributions for separate compounds. Here, we use the ant Formica rufibarbis in a cross‐fostering design to test the degree to which hydrocarbons are heritably synthesized by young workers and transferred by their foster workers. Bioassays show that nestmate recognition has a significant heritable component. Multivariate quantitative analyses based on 38 hydrocarbons reveal that a subset of branched alkanes are heritably synthesized, but that these are also extensively transferred among nestmates. In contrast, especially linear alkanes are less heritable and little transferred; these are therefore unlikely to act as cues that allow within‐colony nepotistic discrimination or as nestmate recognition cues. These results indicate that heritable compounds are suitable for establishing a genetic Gestalt for efficient nestmate recognition, but that recognition cues within colonies are insufficiently distinct to allow nepotistic kin discrimination.     

Paternal signature in kin recognition cues of a social insect: concealed in juveniles,revealed in adults

Kin recognition is a key mechanism to direct social behaviours towards related individuals or avoid inbreeding depression. In insects, recognition is generally mediated by cuticular hydrocarbon (CHC) compounds, which are partly inherited from parents. However, in social insects, potential nepotistic conflicts between group members from different patrilines are predicted to select against the expression of patriline-specific signatures in CHC profiles. Whereas this key prediction in the evolution of insect signalling received empirical support in eusocial insects, it remains unclear whether it can be generalized beyond eusociality to less-derived forms of social life. Here, we addressed this issue by manipulating the number of fathers siring clutches tended by females of the European earwig, Forficula auricularia, analysing the CHC profiles of the resulting juvenile and adult offspring, and using discriminant analysis to estimate the information content of CHC with respect to the maternal and paternal origin of individuals. As predicted, if paternally inherited cues are concealed during family life, increases in mating number had no effect on information content of CHC profiles among earwig juveniles, but significantly decreased the one among adult offspring. We suggest that age-dependent expression of patriline-specific cues evolved to limit the risks of nepotism as family-living juveniles and favour sibling-mating avoidance as group-living adults. These results highlight the role of parental care and social life in the evolution of chemical communication and recognition cues.     

Cuticular hydrocarbons are heritable in the cricket Teleogryllus oceanicus

The ability of individuals to respond differentially to conspecifics depending on their genetic relatedness is a widespread phenomenon across the animal kingdom. Despite this, little is known about the selection processes that act on the phenotypic variation of traits used during recognition. Here we use a quantitative genetic approach to examine the patterns of genetic variation in cuticular hydrocarbon (CHC) profiles, a pheromonal system used extensively in insect communication. Using gas chromatography, we found family specificity in the CHC profiles of male crickets, Teleogryllus oceanicus. Across CHC peaks, our mean coefficient of additive genetic variation was 10.8%. Multivariate principal component analysis showed that most axes of variation were weighted by CHC peaks with significant additive genetic variation. Our results provide evidence that variation in CHC profiles can reflect genetic relatedness, supporting the widely held belief that this phenotypic trait is used as a mechanism for chemosensory kin recognition.     

Strong differences in chemical recognition cues between two closely related species of ants from the genus Lasius (Hymenoptera: Formicidae)

Cuticular hydrocarbons (CHCs) are increasingly recognized as important to insects and are used for constructing taxonomies. However, multiple parameters affect the expression of CHCs besides a genetic component. We propose that selection may act differently on the expression of CHCs, depending on the evolutionary context. To explore the influence of selection, the CHCs of two closely related ant species, Lasius niger and Lasius platythorax, were studied in a multidisciplinary approach. We characterized (i) CHCs and (ii) niches (through baiting, activity observations and foraging analysis). The species were distinct in both measures, although to a varying degree. Although they showed moderate niche partitioning along diet and environmental preferences, chemical differences were unexpectedly pronounced. This may be explained by divergent selection on mate recognition cues or by other influences on CHCs. Such striking chemical differences among closely related species may not be the rule and suggest that taxonomies based on CHCs should be interpreted cautiously; though, they remain useful tools for differentiating among cryptic species.     

Evolution of the neuronal substrate for kin recognition in social Hymenoptera

In evolutionary terms, life is about reproduction. Yet, in some species, individuals forgo their own reproduction to support the reproductive efforts of others. Social insect colonies for example, can contain up to a million workers that actively cooperate in tasks such as foraging, brood care and nest defence, but do not produce offspring. In such societies the division of labour is pronounced, and reproduction is restricted to just one or a few individuals, most notably the queen(s). This extreme eusocial organisation exists in only a few mammals, crustaceans and insects, but strikingly, it evolved independently up to nine times in the order Hymenoptera (including ants, bees and wasps). Transitions from a solitary lifestyle to an organised society can occur through natural selection when helpers obtain a fitness benefit from cooperating with kin, owing to the indirect transmission of genes through siblings. However, this process, called kin selection, is vulnerable to parasitism and opportunistic behaviours from unrelated individuals. An ability to distinguish kin from non-kin, and to respond accordingly, could therefore critically facilitate the evolution of eusociality and the maintenance of non-reproductive workers. The question of how the hymenopteran brain has adapted to support this function is therefore a fundamental issue in evolutionary neuroethology. Early neuroanatomical investigations proposed that social Hymenoptera have expanded integrative brain areas due to selection for increased cognitive capabilities in the context of processing social information. Later studies challenged this assumption and instead pointed to an intimate link between higher social organisation and the existence of developed sensory structures involved in recognition and communication. In particular, chemical signalling of social identity, known to be mediated through cuticular hydrocarbons (CHCs), may have evolved hand in hand with a specialised chemosensory system in Hymenoptera. Here, we compile the current knowledge on this recognition system, from emitted identity signals, to the molecular and neuronal basis of chemical detection, with particular emphasis on its evolutionary history. Finally, we ask whether the evolution of social behaviour in Hymenoptera could have driven the expansion of their complex olfactory system, or whether the early origin and conservation of an olfactory subsystem dedicated to social recognition could explain the abundance of eusocial species in this insect order. Answering this question will require further comparative studies to provide a comprehensive view on lineage-specific adaptations in the olfactory pathway of Hymenoptera.     

Evolution of cuticular hydrocarbon diversity in ants

The cuticular hydrocarbons (CHCs) of ants provide important cues for nest-mate and caste recognition. There is enormous diversity in the composition of these CHCs, but the manner in which this diversity has evolved is poorly understood. We gathered data on CHC profiles for 56 ant species, relating this information to their phylogeny. We deduced the mode of evolution of CHC profiles by reconstructing character evolution and then relating the number of changes in CHC components along each branch of the phylogeny to the length of the branch. There was a strong correlation between branch length and number of component changes, with fewer changes occurring on short branches. Our analysis thereby indicated a gradual mode of evolution. Different ant species tend to use specific CHC structural types that are exclusive of other structural types, indicating that species differences may be generated in part by switching particular biosynthetic pathways on or off in different lineages. We found limited, and contradictory, evidence for abiotic factors (temperature and rainfall) driving change in CHC profiles.     

Recent advance of kin recognition in plant

Plants have the ability to discriminate kin members from strangers in competitive interactions and show altruistic behavior towards related individuals. Studies have showed that plants recognize their neighbors and adjust their ecological strategy mainly through leaf volatiles, root secretions and photographic carrier. The target plants can modify their morphological traits (root size, root:shoot ratio, seed numbers etc.) or metabolism characteristics (secondary metabolites, defense-related proteins etc.) when groups of plants shared common resources, so as to minimize competition with close relatives. The density of kin recognition is influenced by environmental conditions. The main reasons for controversial experimental results of kin recognition are associated with plant materials, standard of kin selection, ecological factors and measured indices. Further studies are required to understand the mechanisms of kin interactions in plants from physiological, biochemical, molecular and metabolic levels.     

Weak patriline effects are present in the cuticular hydrocarbon profiles of isolated Formica exsecta ants but they disappear in the colony environment

Chemical recognition cues are used to discriminate among species, con‐specifics, and potentially between patrilines in social insect colonies. There is an ongoing debate about the possible persistence of patriline cues despite evidence for the mixing of colony odors via a “gestalt” mechanism in social insects, because patriline recognition could lead to nepotism. We analyzed the variation in recognition cues (cuticular hydrocarbons) with different mating frequencies or queen numbers in 688 Formica exsecta ants from 76 colonies. We found no increase in the profile variance as genetic diversity increased, indicating that patriline effects were absent or possibly obscured by a gestalt mechanism. We then demonstrated that an isolated individual's profile changed considerably relative to their colony profile, before stabilizing after 5 days. We used these isolated individuals to eliminate the masking effects of the gestalt mechanism, and we detected a weak but statistically significant patriline effect in isolated adult workers and also in newly emerged callow workers. Thus, our evidence suggests that genetic variation in the cuticular hydrocarbon profile of F. exsecta ants (n‐alkanes and alkenes) resulted in differences among patrilines, but they were obscured in the colony environment, thereby avoiding costly nepotistic behaviors.     

植物亲缘识别的研究进展

植物的亲缘识别(kin recognition)指植物通过识别周边个体与自己的亲缘关系, 调整自身的生长生态策略、促进亲缘个体的生存与繁衍。研究表明, 植物主要通过特定的叶片挥发物、根系分泌物、感光载体等途径, 识别周边个体与自己的亲缘关系, 改变自身形态学策略(如根系大小、根冠比、种子数量等)或者生理代谢策略(次生代谢物质、防御蛋白等), 调整与周边个体的竞争强度, 缓和与近亲缘个体之间的竞争, 加强与远亲缘或非亲缘个体的竞争。同时亲缘识别的强度也受环境因子(养分等)的影响。结合目前的研究进展, 该文分析了导致亲缘识别的研究结果存在差异或争议的主要原因, 认为主要与实验材料的选择、亲缘关系的界定标准、环境条件及测定的指标不统一有关。将来的研究应重点从生理生化、分子、代谢水平上深入研究植物亲缘识别的机理。     

Tolerance requires the right smell: first evidence for interspecific selection on chemical recognition cues

The integument of insects is generally covered with cuticular hydrocarbons (CHC). They serve multiple functions, most prominent among them waterproofing and-especially among social insects-as communication signal. CHC profiles are incredibly diverse within and across species. However, the causes for CHC variation between species, and potential selection pressures that may shape CHC profiles, are hardly understood. Here, we investigated potential selection pressures on ant CHC. We tested the hypotheses that living in association with another species (e.g., parabiosis), and the climate of the ant's habitat, affect CHC composition. We conducted a large-scale comparison of 37 Camponotus species from five continents. Our results demonstrate that closely associated ant species possess significantly longer hydrocarbons and higher proportions of methylbranched alkenes and alkadienes than non- or loosely associated species. In contrast, climatic factors had no effects. This study shows that the need to be tolerated by another species greatly affects CHC profiles.     

Larval memory affects adult nest-mate recognition in the ant Aphaenogaster senilis

Prenatal olfactory learning has been demonstrated in a wide variety of animals, where it affects development and behaviour. Young ants learn the chemical signature of their colony. This cue-learning process allows the formation of a template used for nest-mate recognition in order to distinguish alien individuals from nest-mates, thus ensuring that cooperation is directed towards group members and aliens are kept outside the colony. To date, no study has investigated the possible effect of cue learning during early developmental stages on adult nest-mate recognition. Here, we show that odour familiarization during preimaginal life affects recognition abilities of adult Aphaenogaster senilis ants, particularly when the familiarization process occurs during the first larval stages. Ants eclosed from larvae exposed to the odour of an adoptive colony showed reduced aggression towards familiar, adoptive individuals belonging to this colony compared with alien individuals (true unfamiliar), but they remained non-aggressive towards adult individuals of their natal colony. Moreover, we found that the chemical similarity between the colony of origin and the adoptive colony does not influence the degree of aggression, meaning that the observed effect is likely to be due only to preimaginal learning experience. These results help understanding the developmental processes underlying efficient recognition systems.     

The subepithelial gland in ants: a novel exocrine gland closely associated with the cuticle surface

Two glandular systems were discovered that secrete their products onto the cuticular surface in ants. The first, the subepithelial gland, was previously undescribed in ants, and is found throughout the body just beneath the epithelium. This gland consists of independent secretory units, each made up of a single gland cell and an associated duct cell that penetrates the cuticle. Its ultrastructural appearance is consistent with possible hydrocarbon production. Examining 84 ant species, the subepithelial gland was found in eight subfamilies (out of 13), although not necessarily in all species. In a single ant species, Harpegnathos saltator, it was the epithelium itself that was enlarged and functioned as a gland. The enlarged epithelial cells secrete their products directly onto the cuticle through distinct cuticular crevasses.     

Sex allocation conflict between queens and workers in Formica pratensis wood ants predicts seasonal sex ratio variation

Sex allocation theory predicts parents should adjust their investment in male and female offspring in a way that increases parental fitness. This has been shown in several species and selective contexts. Yet, seasonal sex ratio variation within species and its underlying causes are poorly understood. Here, we study sex allocation variation in the wood ant Formica pratensis. This species displays conflict over colony sex ratio as workers and queens prefer different investment in male and female offspring, owing to haplodiploidy and relatedness asymmetries. It is unique among Formica ants because it produces two separate sexual offspring cohorts per season. We predict sex ratios to be closer to queen optimum in the early cohort but more female‐biased and closer to worker optimum in the later one. This is because the power of workers to manipulate colony sex ratio varies seasonally with the availability of diploid eggs. Consistently, more female‐biased sex ratios in the later offspring cohort over a three‐year sampling period from 93 colonies clearly support our prediction. The resulting seasonal alternation of sex ratios between queen and worker optima is a novel demonstration how understanding constraints of sex ratio adjustment increases our ability to predict sex ratio variation.     

Kin recognition by paternal half-siblings in captive Papio cynocephalus

Our objective in this study was to evaluate whether a group of paternally related, subadult baboons (Papio cynocephalus) would preferentially interact with kin or nonkin when they had been raised apart from kin other than their mothers. Subjects and their mothers were removed from the breeding group and placed in alternate housing within 24 h after birth to ensure that the subjects would not have a social history with either their sire or their half-siblings. At 90 days of age, the 23 subjects were separated from their mothers and assigned to a peer–peer social group. Behavioral performance was measured using focal animal sampling techniques and 12 molecular behavioral criteria. Analyses of the data indicate that in dyadic interactions kin did not interact more frequently than nonkin in performance of affiliative, sociosexual, and agonistic behaviors. The hypothesis that baboons recognize kin in the absence of maternal associations was not supported by the data; moreover, we suggest that social learning and social history are the most likely mechanisms for kin recognition. Am. J. Primatol. 43:147–157, 1997. © 1997 Wiley-Liss, Inc.