Intraspecific Variation in Learning Tibbetts, Elizabeth A.; Injaian, Allison; Sheehan, Michael J. ...
The American naturalist,
05/2018, Letnik:
191, Številka:
5
Journal Article
Recenzirano
Research on individual recognition often focuses on species-typical recognition abilities rather than assessing intraspecific variation in recognition. As individual recognition is cognitively ...costly, the capacity for recognition may vary within species. We test how individual face recognition differs between nest-founding queens (foundresses) and workers in Polistes fuscatus paper wasps. Individual recognition mediates dominance interactions among foundresses. Three previously published experiments have shown that foundresses (1) benefit by advertising their identity with distinctive facial patterns that facilitate recognition, (2) have robust memories of individuals, and (3) rapidly learn to distinguish between face images. Like foundresses, workers have variable facial patterns and are capable of individual recognition. However, worker dominance interactions are muted. Therefore, individual recognition may be less important for workers than for foundresses. We find that (1) workers with unique faces receive amounts of aggression similar to those of workers with common faces, indicating that wasps do not benefit from advertising their individual identity with a unique appearance; (2) workers lack robust memories for individuals, as they cannot remember unique conspecifics after a 6-day separation; and (3) workers learn to distinguish between facial images more slowly than foundresses during training. The recognition differences between foundresses and workers are notable because Polistes lack discrete castes; foundresses and workers are morphologically similar, and workers can take over as queens. Overall, social benefits and receiver capacity for individual recognition are surprisingly plastic.
Termites live in colonies, and their members belong to different castes that each have their specific role within the termite society. In well-established colonies of higher termites, the only food ...the founding female, the queen, receives is saliva from workers; such queens can live for many years and produce up to 10,000 eggs per day. In higher termites, worker saliva must thus constitute a complete diet and therein resembles royal jelly produced by the hypopharyngeal glands of honeybee workers that serves as food for their queens; indeed, it might as well be called termite royal jelly. However, whereas the composition of honeybee royal jelly is well established, that of worker termite saliva in higher termites remains largely unknown. In lower termites, cellulose-digesting enzymes constitute the major proteins in worker saliva, but these enzymes are absent in higher termites. Others identified a partial protein sequence of the major saliva protein of a higher termite and identified it as a homolog of a cockroach allergen. Publicly available genome and transcriptome sequences from termites make it possible to study this protein in more detail. The gene coding the termite ortholog was duplicated, and the new paralog was preferentially expressed in the salivary gland. The amino acid sequence of the original allergen lacks the essential amino acids methionine, cysteine and tryptophan, but the salivary paralog incorporated these amino acids, thus allowing it to become more nutritionally balanced. The gene is found in both lower and higher termites, but it is in the latter that the salivary paralog gene got reamplified, facilitating an even higher expression of the allergen. This protein is not expressed in soldiers, and, like the major royal jelly proteins in honeybees, it is expressed in young but not old workers.
Abstract
Termite castes express specialized phenotypes for their own tasks and are a good example of insect polyphenism. To understand the comprehensive gene expression profiles during caste ...differentiation, RNA-seq analysis based on the genome data was performed during the worker, presoldier, and nymphoid molts in
Reticulitermes speratus
. In this species, artificial induction methods for each molt have already been established, and the time scale has been clarified. Three different periods (before the gut purge (GP), during the GP, and after the molt) were discriminated in each molt, and two body parts (head and other body regions) were separately sampled. The results revealed that many differentially expressed genes (head: 2884, body: 2579) were identified in each molt. Based on the independent real-time quantitative PCR analysis, we confirmed the different expression patterns of seven out of eight genes in the presoldier molt. Based on the GO and KEGG enrichment analyses, the expressions of genes related to juvenile hormone titer changes (e.g.,
JH acid methyltransferase
), nutrition status (e.g.,
Acyl-CoA Delta desaturase
), and cell proliferation (e.g.,
insulin receptor
), were shown to specifically fluctuate in each molt. These differences may have a crucial impact on caste differentiation. These data are important resources for future termite sociogenomics.
Sustaining beneficial gut symbioses presents a major challenge for animals, including holometabolous insects. Social insects may meet such challenges through partner fidelity, aided by behavioral ...symbiont transfer and transgenerational inheritance through colony founders. We address such potential through colony‐wide explorations across 13 eusocial, holometabolous insect species in the ant genus Cephalotes. Through amplicon sequencing, we show that previously characterized worker microbiomes are conserved in soldier castes, that adult microbiomes exhibit trends of phylosymbiosis, and that Cephalotes cospeciate with their most abundant adult‐enriched symbiont. We find, also, that winged queens harbor worker‐like microbiomes prior to colony founding, suggesting vertical inheritance as a means of partner fidelity. Whereas some adult‐abundant symbionts colonize larvae, larval gut microbiomes are uniquely characterized by environmental bacteria from the Enterobacteriales, Lactobacillales, and Actinobacteria. Distributions across Cephalotes larvae suggest more than 40 million years of conserved environmental filtering and, thus, a second sustaining mechanism behind an ancient, developmentally partitioned symbiosis.
Eusocial insects are characterized by a well‐developed division of labour among castes. Although the successful division of labour should stem from behavioural differentiation depending on caste ...identity, caste‐specific intrinsic behavioural characteristics might be masked by social interactions within colonies. The present study explores caste‐specific intrinsic locomotive activities of termites by quantifying them in isolation. We track individual movement trajectories of the damp‐wood termite Hodotermopsis sjostedti over 30 min and extract individual locomotion parameters. Multivariate statistical analyses reveal significant differences among castes: soldiers move more actively than workers and neotenic reproductives. The morphometric data of test individuals indicate that locomotor activities reflected caste identity more strongly compared with quantitative morphological variations among individuals. We find that the different locomotor activities of soldiers compared with those of neotenics and workers probably reflect their physiological differentiation. The present study provides a basis for a deeper understanding of the roles of individual locomotor activities in social behaviours.
Termites are characterized by a well‐developed division of labour among physical castes.
We find that different locomotor patterns among castes of the damp‐wood termite, Hodotermopsis sjostedti.
The present study provides a basis for a deeper understanding of the roles of individual locomotor activities in social behaviours.
A key mechanistic hypothesis for the evolution of division of labour in social insects is that a shared set of genes co-opted from a common solitary ancestral ground plan (a genetic toolkit for ...sociality) regulates caste differentiation across levels of social complexity. Using brain transcriptome data from nine species of vespid wasps, we test for overlap in differentially expressed caste genes and use machine learning models to predict castes using different gene sets. We find evidence of a shared genetic toolkit across species representing different levels of social complexity. We also find evidence of additional fine-scale differences in predictive gene sets, functional enrichment and rates of gene evolution that are related to level of social complexity, lineage and of colony founding. These results suggest that the concept of a shared genetic toolkit for sociality may be too simplistic to fully describe the process of the major transition to sociality.
Neuroecology theory predicts relative investment in brain regions will vary to match differences in behavior. Social insect castes provide exceptional opportunities to test for adaptive brain ...investment because castes differ in behavior and in cognitive demands. Caste development in dampwood termites (genus
Zootermopsis
) is complex, providing multiple caste comparisons for testing neuroecological predictions:
Zootermopsis
termites can remain in a worker-like sterile nymphal caste, develop into sterile defensive soldiers, or follow three distinct pathways to reproductive status (wingless neotenic reproductives, reproductive soldiers, and winged primary reproductives Queens/Kings). We measured differences in the relative sizes of key brain neuropils among
Zootermopsis
termite castes to test which caste-specific behavioral and cognitive demands (reproduction versus worker behavior) best predicted patterns of brain investment. We focused on the Antennal Lobes (centers of chemosensory processing) and the Mushroom Bodies (centers of learning, memory, and sensory integration). There was no evidence that reproductive status was associated with increased investment in either the Antennal Lobes or the Mushroom Bodies. Instead, several caste comparisons supported the hypothesis that labor/task performance was a positive predictor of brain region investment: nymphs (workers) had the greatest relative investment in both Antennal Lobes and Mushroom Bodies, compared to developmentally preceding stages (immature instars I–III) and later castes (soldiers and reproductives). These findings suggest that task performance demands were the main drivers of caste-specific adaptive brain investment in
Zootermopsis
, and that reproductive status entailed relatively few cognitive challenges.
Much of the complex anatomy of a holometabolous insect is built from disc-shaped epithelial structures found inside the larva, i.e., the imaginal discs, which undergo a rapid differentiation during ...metamorphosis. Imaginal discs-derived structures, like wings, are built through the action of genes under precise regulation.
We analyzed 30 honeybee transcriptomes in the search for the gene expression needed for wings and thoracic dorsum construction from the larval wing discs primordia. Analyses were carried out before, during, and after the metamorphic molt and using worker and queen castes. Our RNA-seq libraries revealed 13,202 genes, representing 86.2% of the honeybee annotated genes. Gene Ontology analysis revealed functional terms that were caste-specific or shared by workers and queens. Genes expressed in wing discs and descendant structures showed differential expression profiles dynamics in premetamorphic, metamorphic and postmetamorphic developmental phases, and also between castes. At the metamorphic molt, when ecdysteroids peak, the wing buds of workers showed maximal gene upregulation comparatively to queens, thus underscoring differences in gene expression between castes at the height of the larval-pupal transition. Analysis of small RNA libraries of wing buds allowed us to build miRNA-mRNA interaction networks to predict the regulation of genes expressed during wing discs development.
Together, these data reveal gene expression dynamics leading to wings and thoracic dorsum formation from the wing discs, besides highlighting caste-specific differences during wing discs metamorphosis.
The social parasitic beetle Paussus favieri (Coleoptera, Carabidae, Paussini) performs different types of stridulations, which selectively mimic those emitted by different ant castes of its host ...Pheidole pallidula (Hymenoptera, Formicidae, Myrmicinae). However, the significance of this acoustical mimicry for the success of the parasitic strategy and the behaviors elicited in the host ants by stridulations was unknown. We reared Paussus favieri in Pheidole pallidula colonies and filmed their interacting behaviors. We analyzed in slow motion the behavior of ants near a stridulating beetle. We analyzed separately trains of pulse (Pa + Pb, produced by repeated rubbings) and single pulse (Pc, produced by a single rubbing) of stridulations, clearly recognizable from the shaking up and down of the beetle hind legs, and associated them with different ant responses. The full repertoire of sounds produced by P. favieri elicited benevolent responses both in workers and soldiers. We found that different signals elicit different (sometimes multiple) behaviors in ants, with different frequency in the two ant castes. However, Pc (alone or in conjunction with other types of pulses) appears to be the type of acoustic signal mostly responsible for all recorded behaviors. These results indicate that the acoustic channel plays a pivotal role in the host–parasite interaction. Finding that a parasite uses the acoustical channel so intensively, and in such a complicated way to trigger ant behaviors, indicates that acoustic signals may be more important in ant societies than commonly recognized.
In social insects, behavioral changes are shaped by social context which includes the presence of other castes. Soldiers play a critical role in the defense of a termite colony, although their role ...beyond defense is less understood. Termites tunnel to safely acquire resources, producing an extended phenotype of the colony shaped by various environmental and genetic factors. In this study, we investigated the indirect influence of the soldier on worker tunneling behavior for three species of
Reticulitermes
subterranean termites. Groups of 50 worker termites containing either three, one, none, or the cuticular extract of soldiers were placed into planar arenas and allowed to tunnel. The speed and morphology of tunnel construction were determined for the first 36 h of tunneling. We found tunneling differences among species:
R. flavipes
(Kollar) produced more branches and tunneled faster than both
R. hageni
Banks and
R. virginicus
(Banks). Trials with live soldiers produced more branches in
R. flavipes
, while trials with live soldiers or even the chemical extract of a soldier increased tunnel speed in
R. flavipes
and accelerated tunnel initiation in
R. hageni
. In
R. virginicus
, there was little impact of soldiers. These behavioral changes in
R. flavipes
and
R. hageni
may reduce the chance of tunneling workers encountering enemies without soldiers present. All three species used dead reckoning to maintain a straight direction after being forced through two sharp turns, but the presence of soldiers had no influence on this ability. This study, showing that soldiers can influence tunneling behavior in workers in some species, provides additional evidence of the keystone role of soldiers in termite colonies, and demonstrates that this influence can be exerted through chemical cues alone in some species.
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