The molecular basis of socially mediated phenotypic plasticity in a eusocial paper wasp

Phenotypic plasticity, the ability to produce multiple phenotypes from a single genotype, represents an excellent model with which to examine the relationship between gene expression and phenotypes. Analyses of the molecular foundations of phenotypic plasticity are challenging, however, especially in the case of complex social phenotypes. Here we apply a machine learning approach to tackle this challenge by analyzing individual-level gene expression profiles of Polistes dominula paper wasps following the loss of a queen. We find that caste-associated gene expression profiles respond strongly to queen loss, and that this change is partly explained by attributes such as age but occurs even in individuals that appear phenotypically unaffected. These results demonstrate that large changes in gene expression may occur in the absence of outwardly detectable phenotypic changes, resulting here in a socially mediated de-differentiation of individuals at the transcriptomic level but not at the levels of ovarian development or behavior

Alternative Splicing Changes Promoted by NOVA2 Upregulation in Endothelial Cells and Relevance for Gastric Cancer

Angiogenesis is crucial for cancer progression. While several anti-angiogenic drugs are in use for cancer treatment, their clinical benefits are unsatisfactory. Thus, a deeper understanding of the mechanisms sustaining cancer vessel growth is fundamental to identify novel biomarkers and therapeutic targets. Alternative splicing (AS) is an essential modifier of human proteome diversity. Nevertheless, AS contribution to tumor vasculature development is poorly known. The Neuro-Oncological Ventral Antigen 2 (NOVA2) is a critical AS regulator of angiogenesis and vascular development. NOVA2 is upregulated in tumor endothelial cells (ECs) of different cancers, thus representing a potential driver of tumor blood vessel aberrancies. Here, we identified novel AS transcripts generated upon NOVA2 upregulation in ECs, suggesting a pervasive role of NOVA2 in vascular biology. In addition, we report that NOVA2 is also upregulated in ECs of gastric cancer (GC), and its expression correlates with poor overall survival of GC patients. Finally, we found that the AS of the Rap Guanine Nucleotide Exchange Factor 6 (RapGEF6), a newly identified NOVA2 target, is altered in GC patients and associated with NOVA2 expression, tumor angiogenesis, and poor patient outcome. Our findings provide a better understanding of GC biology and suggest that AS might be exploited to identify novel biomarkers and therapeutics for anti-angiogenic GC treatments

Genomic adaptations to aquatic and aerial life in mayflies and the origin of insect wings

The evolution of winged insects revolutionized terrestrial ecosystems and led to the largest animal radiation on Earth. However, we still have an incomplete picture of the genomic changes that underlay this diversification. Mayflies, as one of the sister groups of all other winged insects, are key to understanding this radiation. Here, we describe the genome of the mayfly Cloeon dipterum and its gene expression throughout its aquatic and aerial life cycle and specific organs. We discover an expansion of odorant-binding-protein genes, some expressed specifically in breathing gills of aquatic nymphs, suggesting a novel sensory role for this organ. In contrast, flying adults use an enlarged opsin set in a sexually dimorphic manner, with some expressed only in males. Finally, we identify a set of wing-associated genes deeply conserved in the pterygote insects and find transcriptomic similarities between gills and wings, suggesting a common genetic program. Globally, this comprehensive genomic and transcriptomic study uncovers the genetic basis of key evolutionary adaptations in mayflies and winged insects

High indirect fitness benefits for helpers across the nesting cycle in the tropical paper wasp polistes canadensis

Explaining the evolution of helping behaviour in the eusocial insects where non-reproductive ('worker') individuals help raise the offspring of other individuals ('queens'), remains one of the most perplexing phenomena in the natural world. Polistes paper wasps are popular study models, as workers retain the ability to reproduce: such totipotency is likely representative of the early stages of social evolution. Polistes is thought to have originated in the tropics, where seasonal constraints on reproductive options are weak and social groups are effectively perennial. Yet, most Polistes research has focused on non-tropical species, where seasonality causes family groups to disperse; cofoundresses forming new colonies the following spring are often unrelated, leading to the suggestion that direct fitness through nest inheritance is key in the evolution of helping behaviour. Here we present the first comprehensive genetic study of social structure across the perennial nesting cycle of a tropical Polistes - Polistes canadensis. Using both microsatellites and newly-developed single-nucleotide polymorphism (SNP) markers we show that adult cofoundresses are highly related, and that brood production is monopolised by a single female across the nesting cycle. Non-reproductive cofoundresses in tropical Polistes therefore have the potential to gain high indirect fitness benefits as helpers from the outset of group formation, and these benefits persist through the nesting cycle. Direct fitness may have been less important in the origin of Polistes sociality than previously suggested. These findings stress the importance of studying a range of species with diverse life-history and ecologies when considering the evolution of reproductive strategies

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

Amphioxus functional genomics and the origins of vertebrate gene regulation

Vertebrates have greatly elaborated the basic chordate bodyplan and evolved highly distinctive genomes, sculpted by two whole genome duplications (WGD). To investigate the evolution of genome regulation in chordates, we characterized promoters, DNA methylation, chromatin accessibility, histone modifications and transcriptomes in multiple tissues and throughout development of amphioxus. This revealed an intermediate stage in the evolution of differentially methylated regulatory elements, and high conservation of gene expression and its cis-regulatory logic between amphioxus and vertebrates, maximally at an earlier mid-embryonic phylotypic period. We also unraveled the principal route of regulatory evolution following vertebrate WGDs: over 80% of broadly expressed gene families with multiple WGD-paralogs in vertebrates have members that restricted their ancestral expression, undergoing specialization rather than subfunctionalization. Counter-intuitively, vertebrate genes that underwent expression restriction increased the complexity of their regulatory landscapes. Altogether, these data pave the way for a better understanding of the regulatory principles underlying key vertebrate innovations