Self-organisation of plasticity and specialisation in a primitively social insect

Biological systems have the capacity to not only build and robustly maintain complex structures but also to rapidly break up and rebuild such structures. Here, using primitive societies of Polistes wasps, we show that both robust specialization and rapid plasticity are emergent properties of multi-scale dynamics. We combine theory with experiments that, after perturbing the social structure by removing the queen, correlate time-resolved multi-omics with video recordings. We show that the queen-worker dimorphism relies on the balance between the development of a molecular queen phenotype in all insects and colony-scale inhibition of this phenotype via asymmetric interactions. This allows Polistes to be stable against intrinsic perturbations of molecular states while reacting plastically to extrinsic cues affecting the whole society. Long-term stability of the social structure is reinforced by dynamic DNA methylation. Our study provides a general principle of how both specialization and plasticity can be achieved in biological systems. A record of this paper’s transparent peer review process is included in the supplemental information

Social parasitism and the molecular basis of phenotypic evolution

Contrasting phenotypes arise from similar genomes through a combination of losses, gains, co-option and modifications of inherited genomic material. Understanding the molecular basis of this phenotypic diversity is a fundamental challenge in modern evolutionary biology. Comparisons of the genes and their expression patterns underlying traits in pairs of closely related species offer an unrivalled opportunity to evaluate the extent to which genomic material is reorganised to produce novel traits. Advances in molecular methods now allow us to dissect the molecular machinery underlying phenotypic diversity in almost any organism, from single-celled organisms to the most complex vertebrates. Here we discuss how comparisons of social parasites and their free-living hosts may provide unique insights into the molecular basis of phenotypic evolution. Social parasites evolve from a social ancestor and are specialised to exploit the socially acquired resources of their closely-related, free-living social host. Molecular comparisons of such species pairs can reveal how genomic material is re-organised in the loss of ancestral traits (i.e. of free-living traits in the parasites) and the gain of new ones (i.e. specialist traits required for a parasitic lifestyle). We define hypotheses on the molecular basis of phenotypes in the evolution of social parasitism and discuss their wider application in understanding the molecular basis of phenotypic diversity within the theoretical framework of phenotypic plasticity and shifting reaction norms. Currently there are no data available to test these hypotheses, and so we also provide some proof of concept data for our conceptual model using the paper wasp social parasite-host system (Polistes sulcifer - Polistes dominula). This conceptual framework and first empirical data provide a spring-board for directing future genomic analyses on exploiting social parasites as a route to understanding the evolution of phenotypic specialisation

Convergent phenotypes but non-convergent genomes in simple social insect societies

Dissertação de Mestrado na área de especialização em Ciências Jurídico-Forenses apresentada à Faculdade de Direito da Universidade de Coimbr

Transcriptome analyses of primitively eusocial wasps reveal novel insights into the evolution of sociality and the origin of alternative phenotypes

This is the final version of the article. Available from the publisher via the DOI in this record.BACKGROUND: Understanding how alternative phenotypes arise from the same genome is a major challenge in modern biology. Eusociality in insects requires the evolution of two alternative phenotypes - workers, who sacrifice personal reproduction, and queens, who realize that reproduction. Extensive work on honeybees and ants has revealed the molecular basis of derived queen and worker phenotypes in highly eusocial lineages, but we lack equivalent deep-level analyses of wasps and of primitively eusocial species, the latter of which can reveal how phenotypic decoupling first occurs in the early stages of eusocial evolution. RESULTS: We sequenced 20 Gbp of transcriptomes derived from brains of different behavioral castes of the primitively eusocial tropical paper wasp Polistes canadensis. Surprisingly, 75% of the 2,442 genes differentially expressed between phenotypes were novel, having no significant homology with described sequences. Moreover, 90% of these novel genes were significantly upregulated in workers relative to queens. Differential expression of novel genes in the early stages of sociality may be important in facilitating the evolution of worker behavioral complexity in eusocial evolution. We also found surprisingly low correlation in the identity and direction of expression of differentially expressed genes across similar phenotypes in different social lineages, supporting the idea that social evolution in different lineages requires substantial de novo rewiring of molecular pathways. CONCLUSIONS: These genomic resources for aculeate wasps and first transcriptome-wide insights into the origin of castes bring us closer to a more general understanding of eusocial evolution and how phenotypic diversity arises from the same genome.We thank Centre for Genomic Regulation (CRG) (Heinz Himmelbauer and Francisco Câmara), GenePool and the Babraham Institute (Wolf Reik and Simon Andrews) for support and access to their sequencing facilities. We thank RCUK, CONSOLIDER (CSD2007-0005), the Spanish Ministry of Science (BIO2006-03380, BFU2009-09168), GTEX (NIH Project 1RO1MH090941-01), and a Wellcome Trust Senior Investigator Award to Wolf Reik. SS was supported by a UK Research Council (RCUK) fellowship, and PGF by a FCT postdoctoral grant (SFRH/BPD/42003/2007) from the Portuguese Ministry of Science and Technology. We thank the Smithsonian Tropical Research Institute (particularly William Wcislo, Mary Jane West-Eberhard, Jorge Morales and staff at the Galeta Field Station) for hosting the fieldwork, and Stephanie Dreier and Thibault Lengronne for assistance in the field. The fieldwork was conducted under ANAM Permit No. SE/A-33-0

Deconstructing superorganisms and societies to address big questions in biology

Social insect societies are long-standing models for understanding social behaviour and evolution. Unlike other advanced biological societies (such as the multicellular body), the component parts of social insect societies can be easily deconstructed and manipulated. Recent methodological and theoretical innovations have exploited this trait to address an expanded range of biological questions. We illustrate the broadening range of biological insight coming from social insect biology with four examples. These new frontiers promote open-minded, interdisciplinary exploration of one of the richest and most complex of biological phenomena: sociality

Honey bee colony winter loss rates for 35 countries participating in the COLOSS survey for winter 2018–2019, and the effects of a new queen on the risk of colony winter loss

peer-reviewedThis article presents managed honey bee colony loss rates over winter 2018/19 resulting from using the standardised COLOSS questionnaire in 35 countries (31 in Europe). In total, 28,629 beekeepers supplying valid loss data wintered 738,233 colonies, and reported 29,912 (4.1%, 95% confidence interval (CI) 4.0–4.1%) colonies with unsolvable queen problems 79,146 (10.7%, 95% CI 10.5–10.9%) dead colonies after winter and 13,895 colonies (1.9%, 95% CI 1.8–2.0%) lost through natural disaster. This gave an overall colony winter loss rate of 16.7% (95% CI 16.4–16.9%), varying greatly between countries, from 5.8% to 32. 0%. We modelled the risk of loss as a dead/empty colony or from unresolvable queen problems and found that, overall, larger beekeeping operations with more than 150 colonies experienced significantly lower losses (p<0.001), consistent with earlier studies. Additionally, beekeepers included in this survey who did not migrate their colonies at least once in 2018 had significantly lower losses than those migrating (p<0.001). The percentage of new queens from 2018 in wintered colonies was also examined as a potential risk factor. The percentage of colonies going into winter with a new queen was estimated as 55.0% over all countries. Higher percentages of young queens corresponded to lower overall losses (excluding losses from natural disaster), but also lower losses from unresolvable queen problems, and lower losses from winter mortality (p<0.001). Detailed results for each country and overall are given in a table, and a map shows relative risks of winter loss at regional level