Evidence for a conserved queen-worker genetic toolkit across slave-making ants and their ant hosts

The ecological success of social Hymenoptera (ants, bees, wasps) depends on the division of labour between the queen and workers. Each caste is highly specialized in their respective function in morphology, behaviour and life history traits, such as lifespan and fecundity. Despite strong defences against alien intruders, insect societies are vulnerable to social parasites, such as workerless inquilines or slave-making (dulotic) ants. Here, we investigate whether gene expression varies in parallel ways between slave-making ants and their host ants across five independent origins of ant slavery in the Formicoxenus-group of the ant tribe Crematogastrini. As caste differences are often less pronounced in slave-making ants than non-parasitic ants, we also compare the transcriptomes of queens and workers in these species. We demonstrate a substantial overlap in expression differences between queens and workers across taxa, irrespective of lifestyle. Caste affects the transcriptomes much more profoundly than lifestyle, as indicated by 37 times more genes being linked to caste than to lifestyle and by multiple caste-associated gene modules with strong connectivity. However, several genes and one gene module are linked to the slave-making lifestyle across the independent origins, pointing to some evolutionary convergence. Finally, we do not find evidence for an interaction between caste and lifestyle, indicating that caste differences remain consistent even when species switch to a parasitic lifestyle. Our findings are a strong indication for the existence of a core set of genes whose expression is linked to the queen and worker caste in this ant taxon, supporting the genetic-toolkit hypothesis.

Recombination mapping of the Brazilian stingless bee Frieseomelitta varia confirms high recombination rates in social hymenoptera

Background Meiotic recombination is a fundamental genetic process that shuffles allele combinations and promotes accurate segregation of chromosomes. Analyses of the ubiquitous variation of recombination rates within and across species suggest that recombination is evolving adaptively. All studied insects with advanced eusociality have shown exceptionally high recombination rates, which may represent a prominent case of adaptive evolution of recombination. However, our understanding of the relationship between social evolution and recombination rates is incomplete, partly due to lacking empirical data. Here, we present a linkage map of the monandrous, advanced eusocial Brazilian stingless bee, Frieseomelitta varia, providing the first recombination analysis in the diverse Meliponini (Hymenoptera, Apidae). Results Our linkage map includes 1417 markers in 19 linkage groups. This map spans approximately 2580 centimorgans, and comparisons to the physical genome assembly indicate that it covers more than 75 % of the 275 Megabasepairs (Mbp) F. varia genome. Thus, our study results in a genome-wide recombination rate estimate of 9.3–12.5 centimorgan per Mbp. This value is higher than estimates from nonsocial insects and comparable to other highly social species, although it does not support our prediction that monandry and strong queen-worker caste divergence of F. varia lead to even higher recombination rates than other advanced eusocial species. Conclusions Our study expands the association between elevated recombination and sociality in the order Hymenoptera and strengthens the support for the hypothesis that advanced social evolution in hymenopteran insects invariably selects for high genomic recombination rates.

Molecular underpinnings of division of labour among workers in a socially complex termite

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.

Colony fitness increases in the honey bee at queen mating frequencies higher than genetic diversity asymptote

Across the eusocial Hymenoptera, a queen’s mating frequency is positively associated with her workers’ genetic diversity and colony’s fitness. Over 90% of a colony’s diversity potential is achieved by its mother’s tenth effective mating (me); however, many females mate at levels of me > 10, a zone we here call hyperpolyandry. We compared honey bee colony fitness at mating levels near and above this genetic diversity asymptote. We were interested in how hyperpolyandry affects colony phenotypes arising from both common tasks (brood care) and rare specialized tasks (parasite resistance). We used an unselected wild line of bees and a Varroa Sensitive Hygiene (VSH) line selected to resist the parasite Varroa destructor. Virgin queens were instrumentally inseminated to replicate the following queen/colony conditions: (1) VSH semen/low polyandry (observed mating number = mo = 9), (2) VSH semen/high polyandry (mo = 54), (3) wild type semen/low polyandry, or (4) wild semen/high polyandry. There was a positive effect of polyandry on brood survival, an outcome of common tasks, with highest values at mo = 54. There was an interaction between polyandry and genetics such that differences between genetic lines expressed only at mo = 54, with fewer mites in VSH colonies. These results are consistent with two hypotheses for the evolution of mating levels in excess of the genetic diversity asymptote: hyperpolyandry improves colony fitness by (1) optimizing genotype compositions for common tasks and (2) by capturing rare specialist allele combinations, resisting cliff-edge ecological catastrophes. Significance statement Polyandry is a female’s practice of mating with several males, storing their sperm, and using it to produce one or more clutches of genetically diverse offspring. In the social Hymenoptera, polyandry increases the genetic diversity and task efficiency of workers, leading to improved colony fitness. Over 90% of the increase in a colony’s diversity potential is achieved by its mother’s tenth mating; however, many females practice hyperpolyandry, a term we reserve here for mating levels above this genetic diversity asymptote. We show that a token of colony fitness arising from common tasks, brood survival, improves universally as one moves from sub- to hyperpolyandrous mating levels. However, a colony phenotype arising from a rare parasite resistance task is only expressed in the presence of the controlling alleles and under conditions of hyperpolyandry. These results suggest adaptive mechanisms by which hyperpolyandry could evolve.

Juvenile hormone affects age polyethism, ovarian status, and cuticular hydrocarbon profile in workers of a Polybia occidentalis wasp

Division of labor is one of the most striking features in the evolution of eusociality. Juvenile hormone (JH) mediates reproductive status and aggression among nestmates in primitively eusocial Hymenoptera (species without morphologically distinct castes). In highly social species it has apparently lost its gonadotropic role and primarily regulates the division of labor in the worker caste. Polybia occidentalis, a Neotropical swarm-founding wasp, is an ideal model to understand how JH levels mirror social context and reproductive opportunities because of the absence of a clear morphological caste dimorphism. In this study, we tested the hypothesis that JH influences division of labor, ovary activation and cuticular hydrocarbon profiles of workers. Our observations confirmed that JH analog (methoprene) and precocene affected the cuticular chemical profile associated with the age polyethism. Also, methoprene and precocene-I influenced differently ovarian activation of treated females (individuals treated with methoprene expressed more activated ovaries while precocene treatment did not have significant effect). These results suggest that different hormonal levels induce a differential expression in the cuticular chemical profiles associated with the workers’ age polyethism, which may be essential for keeping the social cohesion among workers throughout their lives in the colony. Furthermore, JH is likely to play a gonadotropic role in P. occidentalis. JH has apparently undergone certain modifications in social Hymenoptera, presenting multifaceted functions in different species.

Queens remate despite traumatic mating in stingless bees

Males can control female reproduction using genital plugs to impede access by rivals. In social bees, ants, and wasps, plugging may involve traumatic mating, with females being harmed. In stingless bees, chances are that plugs may promote ovarian activan, and are thought to ensure single mating—a general tendency among the social Hymenoptera. However, understanding on relationships between mating plugs, traumatic mating, and mating systems in stingless bees remains limited. To address this, we (1) compared mated queens of 7 Neotropical species to understand the patterns of copulatory marks in females and (2) compared pre- and post-mating genitalia of males and females in Melipona fasciculata to depict plug functional morphology. Data revealed an unprecedented consequence of mating in stingless bees: the characteristic marks left by mating plugs on female abdomens and the inferences that can be made from them. To our surprise, in 1 species M. fasciculata we found that queens retain the plug long after mating, and may carry it for the rest of their lives. All the other 6 species retained the plug for only a short period. Remated queens were only found in M. seminigra, whose multiple copulatory marks match previous findings of polyandry in this species. Our study shows that queens can remate, and suggests that male genital morphology may determine in part the time persistence of plugs. We conclude that traumatic mating plugs do not fully prevent remating in stingless bees and that mating systems are not uniform in this group. Nonetheless, exceptional cases of facultative polyandry in social insects—for example, when mating plugs fail—may confirm a general tendency for single mating in close link with efficient mating plugs.

Trade-offs between sperm viability and immune protein expression in honey bee queens (Apis mellifera)

Queens of many social hymenoptera keep sperm alive within their specialized storage organ, the spermatheca, for years, defying the typical trade-off between lifespan and reproduction. However, whether honey bee (Apis mellifera) queens experience a trade-off between reproduction and immunity is unknown, and the biochemical processes underlying sperm viability are poorly understood. Here, we survey quality metrics and viral loads of honey bee queens from nine genetic sources. Queens rated as ‘failed’ by beekeepers had lower sperm viability, fewer sperm, and higher levels of sacbrood virus and black queen cell virus. Quantitative proteomics on N = 123 spermathecal fluid samples shows, after accounting for sperm count, health status, and apiary effects, five spermathecal fluid proteins significantly correlating with sperm viability: odorant binding protein (OBP)14, lysozyme, serpin 88Ea, artichoke, and heat-shock protein (HSP)10. The significant negative correlation of lysozyme—a conserved immune effector—with sperm viability is consistent with a reproduction vs. immunity trade-off in honey bee queens.

Plasticity and modulation of olfactory circuits in insects

Olfactory circuits change structurally and physiologically during development and adult life. This allows insects to respond to olfactory cues in an appropriate and adaptive way according to their physiological and behavioral state, and to adapt to their specific abiotic and biotic natural environment. We highlight here findings on olfactory plasticity and modulation in various model and non-model insects with an emphasis on moths and social Hymenoptera. Different categories of plasticity occur in the olfactory systems of insects. One type relates to the reproductive or feeding state, as well as to adult age. Another type of plasticity is context-dependent and includes influences of the immediate sensory and abiotic environment, but also environmental conditions during postembryonic development, periods of adult behavioral maturation, and short- and long-term sensory experience. Finally, plasticity in olfactory circuits is linked to associative learning and memory formation. The vast majority of the available literature summarized here deals with plasticity in primary and secondary olfactory brain centers, but also peripheral modulation is treated. The described molecular, physiological, and structural neuronal changes occur under the influence of neuromodulators such as biogenic amines, neuropeptides, and hormones, but the mechanisms through which they act are only beginning to be analyzed.