Division of labour characterizes all major evolutionary transitions, such as the evolution of eukaryotic cells or multicellular organisms. Social insects are characterized by reproductive division of ...labour, with one or a few reproducing individuals (queens) and many non-reproducing nestmates (workers) forming a colony. Among the workers, further division of labour can occur with different individuals performing different tasks such as foraging, brood care or building. While mechanisms underlying task division are intensively studied in social Hymenoptera, less is known for termites, which independently evolved eusociality. We investigated molecular mechanisms underlying task division in termite workers to test for communality with social Hymenoptera. We compared similar-aged foraging workers with builders of the fungus-growing termite Macrotermes bellicosus using transcriptomes, endocrine measures and estimators of physiological condition. Based on results for social Hymenoptera and theory, we tested the hypotheses that (i) foragers are in worse physiological conditions than builders, (ii) builders are more similar in their gene expression profile to queens than foragers are, and (iii) builders invest more in anti-ageing mechanism than foragers. Our results support all three hypotheses. We found storage proteins to underlie task division of these similar-aged termite workers and these genes also characterize reproductive division of labour between queens and workers. This implies a co-option of nutrient-based pathways to regulate division of labour across lineages of termites and social Hymenoptera, which are separated by more than 133 million years.
Termites (Isoptera) are the phylogenetically oldest social insects, but in scientific research they have always stood in the shadow of the social Hymenoptera. Both groups of social insects evolved ...complex societies independently and hence, their different ancestry provided them with different life‐history preadaptations for social evolution. Termites, the ‘social cockroaches’, have a hemimetabolous mode of development and both sexes are diploid, while the social Hymenoptera belong to the holometabolous insects and have a haplodiploid mode of sex determination. Despite this apparent disparity it is interesting to ask whether termites and social Hymenoptera share common principles in their individual and social ontogenies and how these are related to the evolution of their respective social life histories. Such a comparison has, however, been much hampered by the developmental complexity of the termite caste system, as well as by an idiosyncratic terminology, which makes it difficult for non‐termitologists to access the literature.
Here, we provide a conceptual guide to termite terminology based on the highly flexible caste system of the “lower termites”. We summarise what is known about ultimate causes and underlying proximate mechanisms in the evolution and maintenance of termite sociality, and we try to embed the results and their discussion into general evolutionary theory and developmental biology. Finally, we speculate about fundamental factors that might have facilitated the unique evolution of complex societies in a diploid hemimetabolous insect taxon. This review also aims at a better integration of termites into general discussions on evolutionary and developmental biology, and it shows that the ecology of termites and their astounding phenotypic plasticity have a large yet still little explored potential to provide insights into elementary evo‐devo questions.
Little is known about the molecular mechanisms that underlie the division of labor in stingless bees. We investigated the expression of a set of candidate genes associated with the nurse-to-forager ...transition in the honey bee in two stingless bee species,
Melipona quadrifasciata
and
Frieseomelitta varia
. These species differ with respect to worker reproduction. The workers of
M. quadrifasciata
lay trophic and reproductive eggs, but those of
F. varia
are completely sterile. For
M. quadrifasciata
nurses, we found elevated
vitellogenin
(
Vg
) and low
juvenile hormone esterase
(
jhe
) transcript levels in the abdomen, in agreement with their reproductive potential. In
F. varia
,
Vg
and
methyl farnesoate epoxidase
(
mfe
) transcript levels were high in the heads of foragers, indicating an association with foraging behavior. For
malvolio
(
mvl
) and
foraging (for
), both involved with food search behavior,
mvl
showed persistent low expression in the head, but increasing levels in the abdomen of both species, speaking against a role in behavioral development. The
for
transcript levels in
F. varia
were higher in foragers, both in the head and the abdomen,
i.e.
, consistent with foraging. In
M. quadrifasciata
, however,
for
expression was higher in the heads of nurse bees, and, thus, is unlikely to play a role in foraging. The results for the two stingless bee species, in comparison with honey bees and bumble bees, indicate that the degree of worker sterility appears to be the primary factor that shapes the expression pattern of key genes in the life history of social bees.
The honey bee, Apis mellifera differs from all other social bees in its gonad phenotype and mating strategy. Honey bee queens and drones have tremendously enlarged gonads, and virgin queens mate with ...several males. In contrast, in all the other bees, the male and female gonads are small, and the females mate with only one or very few males, thus, suggesting an evolutionary and developmental link between gonad phenotype and mating strategy. RNA-seq comparisons of A. mellifera larval gonads revealed 870 genes as differentially expressed in queens versus workers and drones. Based on Gene Ontology enrichment we selected 45 genes for comparing the expression levels of their orthologs in the larval gonads of the bumble bee Bombus terrestris and the stingless bee, Melipona quadrifasciata, which revealed 24 genes as differentially represented. An evolutionary analysis of their orthologs in 13 solitary and social bee genomes revealed four genes with evidence of positive selection. Two of these encode cytochrome P450 proteins, and their gene trees indicated a lineage-specific evolution in the genus Apis, indicating that cytochrome P450 genes may be involved in the evolutionary association of polyandry and the exaggerated gonad phenotype in social bees.
Cooperation requires communication; this applies to animals and humans alike. The main communication means differ between taxa and social insects (ants, termites, and some bees and wasps) lack the ...cognitive abilities of most social vertebrates. Central to the regulation of the reproductive harmony in insect societies is the production of a royalty scent which signals the fertility status of the reproducing queen to the nonreproducing workers. Here, we revealed a central genetic component underlying this hallmark of insect societies in the termite Cryptotermes secundus. Communication between queens and workers relied upon the expression of a gene, Neofem4, which belongs to the cytochrome P450 genes. We inhibited Neofem4 in queens by RNA interference. This resulted in the loss of the royalty scent in queens and the workers behaved as though the queen were absent. The queen's behavior was not generally affected by silencing Neofem4. This suggests that the lack of the royalty scent lead to workers not recognizing her anymore as queen. P450 genes are known to be involved in the production of chemical signals in cockroaches and their expression has been linked to a major fertility regulator, juvenile hormone. This makes P450 genes, both a suitable and available evolutionary substrate in the face of natural selection for production of a queen substance. Our data suggest that in an organism without elaborate cognitive abilities communication has been achieved by the exploitation of a central gene that links the fertility network with the chemical communication pathway. As termites and social Hymenoptera seem to share the same class of compounds in signaling fertility, this role of P450 genes might be more widespread across social insects.
Apidologie 50 years Courant, Christiane; Koeniger, Gudrun; Hartfelder, Klaus
Apidologie,
2021/2, Volume:
52, Issue:
1
Journal Article
Peer reviewed
Open access
Since its foundation,
Apidologie
has steadily gained recognition as a journal that reports results from high-quality scientific research on the biology of bees, and this means Apidae in general, not ...only on its most prominent species, the Western honey bee,
Apis mellifera
. All started 50 years ago in a conversation between two eminent scientists, Jean Louveaux, director of one of INRA’s bee research unit in Bures-sur-Yvette and editor of the French
Annales de l’Abeille
, and Friedrich Ruttner, director of the Bee Research Institute in Oberursel and editor of the German
Zeitschrift für Bienenforschung
, where they discussed the possibility of merging these two journals to create an international bee research journal. Here, we take
Apidologie
’s 50th anniversary as an opportunity to provide our readers with background information on the journal’s history, especially on the persons and their contributions along this journey.
Division of labor in social insect colonies relies on a strong reproductive bias that favors queens. Although the ecological and evolutionary success attained through caste systems is well sketched ...out in terms of ultimate causes, the molecular and cellular underpinnings driving the development of caste phenotypes are still far from understood. Recent genomics approaches on honey bee developmental biology revealed a set of genes that are differentially expressed genes in larval ovaries and associated with transgressive ovary size in queens and massive cell death in workers. Amongst these, two contigs called special attention, both being over 200 bp in size and lacking apparent coding potential. Herein, we obtained their full cDNA sequences. These and their secondary structure characteristics placed in evidence that they are bona fide long noncoding RNAs (lncRNA) differentially expressed in larval ovaries, thus named lncov1 and lncov2. Genomically, both map within a previously identified QTL on chromosome 11, associated with transgressive ovary size in honey bee workers. As lncov1 was over-expressed in worker ovaries we focused on this gene. Real-time qPCR analysis on larval worker ovaries evidenced an expression peak coinciding with the onset of autophagic cell death. Cellular localization analysis through fluorescence in situ hybridization revealed perinuclear spots resembling omega speckles known to regulate trafficking of RNA-binding proteins. With only four lncRNAs known so far in honey bees, two expressed in the ovaries, these findings open a novel perspective on regulatory factors acting in the fine tuning of developmental processes underlying phenotypic plasticity related to social life histories.
Like
Apis mellifera
queens and different from all other bees, drones also have an exaggerated gonad phenotype, with over 150 serial units in each gonad. Yet, compared with the ovaries of the female ...castes, little is known about the development of the honey bee testis. Here we present a histological atlas on postembryonic testis development and spermatogenesis. Already in the first instar larvae, the testioles composing each testis can be distinguished. The testioles then grow along their apical-basal axis by mitotic divisions of the spermatogonia, which eventually form germ cell clusters. Meiosis starts when brood cells are capped, and it ends with the appearance of spermatids in red-eyed pupae. Subsequently, spermiogenesis takes place, and all spermatozoa are formed before adult emergence. We also present the first data on juvenile hormone levels in drone larvae. With this, we provide a database for future research on gonad development in honey bee drones.
The honey bee queen plays a central role in the Apis mellifera L. (Hymenoptera: Apidae) colony, and her high reproductive capacity is fundamental for building up the workforce of a colony. Caste ...development in honey bee females involves elaborate physiological pathways unleashed at the beginning of the first larval instars, with juvenile hormone (JH) playing a crucial role. Here we took advantage of established in vitro rearing techniques to conduct a 2 × 2 experimental design and test initial rearing age (young vs old) and JH treatment (JH III vs solvent control) to enlighten the role of nutrient quality and JH in shaping honey bee female fertility, morphological features related to queenliness, and key physiological parameters (hemolymph vitellogenin/Vg, sugar levels, and Vg transcript levels). Our results show that while the age at initial larval rearing had major impacts on external morphology development, where younger larvae exhibited a higher probability to develop into queen-like adults morphotypes, the JH application during the larval stage improved physiological pathways related to ovary development and metabolism during the ontogenic development. We detected that the supplementation of queen larvae with JH promoted important benefits regarding queen fertility as the increase of ovariole number and vg levels at hemolymph, both crucial factors at eggs production. The data presented here provide guidance in efforts to improve honey bee queen quality, especially in light of frequent episodes of queen failures in the beekeeping industry.
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