Genomic imprinting drives eusociality

The origin of eusociality, altruistically foregoing personal reproduction to help others, has been a long-standing paradox ever since Darwin. Most eusocial insects and rodents likely evolved from subsocial precursors, in which older offspring “helpers” contribute to the development of younger siblings without a permanent sterile caste. The driving mechanism for the transition from subsociality (with helpers) to eusociality (with lifelong sterile workers) remains an enigma because individuals in subsocial groups are subject to direct natural selection rather than kin selection. Our genomic imprinting theory demonstrates that natural selection generates eusociality in subsocial groups when parental reproductive capacity is linked to a delay in the sexual development of offspring due to sex-antagonistic action of transgenerational epigenetic marks. Focusing on termites, our theory provides the missing evolutionary link to explain the evolution of eusociality from their subsocial wood-feeding cockroach ancestors, and provides a novel framework for understanding the origin of eusociality.

Convergent selection on juvenile hormone signaling is associated with the evolution of eusociality in bees

Life's most dramatic innovations, from the emergence of self-replicating molecules to highly-integrated societies, often involve increases in biological complexity. Some groups traverse different levels of complexity, providing a framework to identify key factors shaping these evolutionary transitions. Halictid bees span the transition from individual to group reproduction, with repeated gains and losses of eusociality. We generated chromosome-length genome assemblies for 17 species and searched for genes that both experienced positive selection when eusociality arose and relaxed selection when eusociality was secondarily lost. Loci exhibiting these complementary evolutionary signatures are predicted to carry costs outweighed by their importance for traits in eusocial lineages. Strikingly, these loci included two proteins that bind and transport juvenile hormone (JH) - a key regulator of insect development and reproduction. Though changes in JH abundance are frequently associated with polymorphisms, the mechanisms coupling JH to novel phenotypes are not well understood. Our results suggest novel links between JH and eusociality arose in halictids by altering transport and availability of JH in a tissue-specific manner, including in the brain. Through genomic comparisons of species encompassing both the emergence and breakdown of eusociality, we provide insights into the mechanisms targeted by selection to shape a key evolutionary transition.

Honeybee Queen mandibular pheromone induces starvation in Drosophila melanogaster, implying a role for nutrition signalling in the evolution of eusociality.

Eusocial insect societies are defined by the reproductive division of labour, a social structure that is generally enforced by the reproductive dominant or queen. Reproductive dominance is maintained through behavioural dominance in some species as well as production of queen pheromones in others, or a mixture of both. Queen mandibular pheromone (QMP) is produced by honeybee (Apis mellifera) queens and has been characterised chemically. How QMP acts to repress worker reproduction, and how it has evolved this activity, remains less well understood. Surprisingly, QMP is capable of repressing reproduction in non-target arthropods which have not co-evolved with QMP, are never exposed to QMP in nature, and are up to 530 million years diverged from the honeybee. Here we show that, in Drosophila melanogaster, QMP treatment mimics nutrient limiting conditions, leading to disrupted reproduction. Exposure to QMP induces an increase in food consumption, consistent with that observed in D. melanogaster in response to starvation conditions. This response induces the activation of two checkpoints within the ovary that inhibit oogenesis. The first is the 2a/b ovarian checkpoint in the germarium, which reduces the flow of presumptive oocytes. A stage 9 ovarian checkpoint is also activated, causing degradation of oocytes. The magnitude of activation of both checkpoints is indistinguishable between QMP treated and starved individuals. As QMP seems to trigger a starvation response in an insect highly diverged from honeybees, we propose that QMP originally evolved by co-opting nutrition signalling pathways to regulate reproduction, a key step in the evolution of eusociality.

Morphological evolution in the ant reproductive caste

The evolution of eusociality has led to considerable changes in the general hymenopteran body plan. In particular, the evolution of reproductive division of labour caused the worker caste to be largely freed from the demands involved in reproduction. As a consequence, workers were able to evolve highly specialized morphologies for foraging and colony maintenance, whereas the reproductive caste became specialized for reproduction. Despite these important changes, little is known about the general patterns of morphological evolution within the ant reproductive caste. Our goals here were to characterize morphological variation in the ant reproductive caste and to test whether different sexes display variation in their evolutionary rates. We obtained measurements of 897 specimens from a total of 678 ant species. The shapes of the size distributions were similar between sexes, with queens being larger than males in all traits except for eye length. Contrary to the expectation based on Rensch’s rule, although queens were larger, the degree of dimorphism increased with body size. Finally, there was strong evidence for an accelerated tempo of morphological evolution in queens in relation to males. These results represent the first comprehensive treatment of morphological variation in the ant reproductive caste and provide important new insights into their evolution.

Morphological evolution in the ant reproductive caste

The evolution of eusociality led to severe changes in the general hymenopteran body plan. In particular, the evolution of reproductive division of labour caused the worker caste to be largely freed from the demands involved in reproduction. As a consequence, workers were able to evolve highly specialized morphologies for foraging and colony maintenance, whereas the reproductive caste became specialized for reproduction. Despite these important changes, little is known about general patterns of morphological evolution within the ant reproductive caste. Our goals were to characterize morphological variation in the ant reproductive caste and to test whether different sexes display variation in their evolutionary rates. We obtained measurements of 897 specimens from a total of 678 ant species. The shapes of the size distributions were similar between sexes, with queens being larger than males in all traits except for eye length. Contrary to the expectation based on Rensch’s rule, although queens were larger, the degree of dimorphism increased with body size. Finally, there is strong evidence for an accelerated tempo of morphological evolution in queens in relation to males. These results represent the first comprehensive treatment of morphological variation in the ant reproductive caste and provide important new insights into their evolution.

Polyandry and paternity affect disease resistance in eusocial wasps

Polyandry (multiple mating by females) is a central challenge for understanding the evolution of eusociality. Several hypotheses have been proposed to explain its observed benefits in eusocial Hymenoptera, one of which, the parasite–pathogen hypothesis (PPH), posits that high genotypic variance among workers for disease resistance prevents catastrophic colony collapse. We tested the PPH in the polyandrous wasp Vespula shidai. We infected isolated workers with the entomopathogenic fungus Beauveria bassiana and quantified their survival in the laboratory. Additionally, we conducted a paternity analysis of the workers using nine microsatellite loci to investigate the relationship between survival and the matriline and patriline membership of the workers. As predicted by the PPH, nestmate workers of different patrilines showed differential resistance to B. bassiana. We also demonstrated variation in virulence among strains of B. bassiana. Our results are the first to directly support the PPH in eusocial wasps and suggest that similar evolutionary pressures drove the convergent origin and maintenance of polyandry in ants, bees, and wasps.

Lateralization of short- and long-term visual memories in an insect

The formation of memories within the vertebrate brain is lateralized between hemispheres across multiple modalities. However, in invertebrates evidence for lateralization is restricted to olfactory memories, primarily from social bees. Here, we use a classical conditioning paradigm with a visual conditioned stimulus to show that visual memories are lateralized in the wood ant, Formica rufa . We show that a brief contact between a sugar reward and either the right or left antenna (reinforcement) is sufficient to produce a lateralized memory, even though the visual cue is visible to both eyes throughout training and testing. Reinforcement given to the right antenna induced short-term memories, whereas reinforcement given to the left antenna induced long-term memories. Thus, short- and long-term visual memories are lateralized in wood ants. This extends the modalities across which memories are lateralized in insects and suggests that such memory lateralization may have evolved multiple times, possibly linked to the evolution of eusociality in the Hymenoptera.

Sibling quality and the haplodiploidy hypothesis

The ‘haplodiploidy hypothesis’ argues that haplodiploid inheritance in bees, wasps, and ants generates relatedness asymmetries that promote the evolution of altruism by females, who are less related to their offspring than to their sisters (‘supersister’ relatedness). However, a consensus holds that relatedness asymmetry can only drive the evolution of eusociality if workers can direct their help preferentially to sisters over brothers, either through sex-ratio biases or a pre-existing ability to discriminate sexes among the brood. We show via a kin selection model that a simple feature of insect biology can promote the origin of workers in haplodiploids without requiring either condition. In insects in which females must found and provision new nests, body quality may have a stronger influence on female fitness than on male fitness. If altruism boosts the quality of all larval siblings, sisters may, therefore, benefit more than brothers from receiving the same amount of help. Accordingly, the benefits of altruism would fall disproportionately on supersisters in haplodiploids. Haplodiploid females should be more prone to altruism than diplodiploid females or males of either ploidy when altruism elevates female fitness especially, and even when altruists are blind to sibling sex.