The genome of the water strider Gerris buenoi reveals expansions of gene repertoires associated with adaptations to life on the water.

BACKGROUND: Having conquered water surfaces worldwide, the semi-aquatic bugs occupy ponds, streams, lakes, mangroves, and even open oceans. The diversity of this group has inspired a range of scientific studies from ecology and evolution to developmental genetics and hydrodynamics of fluid locomotion. However, the lack of a representative water strider genome hinders our ability to more thoroughly investigate the molecular mechanisms underlying the processes of adaptation and diversification within this group. RESULTS: Here we report the sequencing and manual annotation of the Gerris buenoi (G. buenoi) genome; the first water strider genome to be sequenced thus far. The size of the G. buenoi genome is approximately 1,000 Mb, and this sequencing effort has recovered 20,949 predicted protein-coding genes. Manual annotation uncovered a number of local (tandem and proximal) gene duplications and expansions of gene families known for their importance in a variety of processes associated with morphological and physiological adaptations to a water surface lifestyle. These expansions may affect key processes associated with growth, vision, desiccation resistance, detoxification, olfaction and epigenetic regulation. Strikingly, the G. buenoi genome contains three insulin receptors, suggesting key changes in the rewiring and function of the insulin pathway. Other genomic changes affecting with opsin genes may be associated with wavelength sensitivity shifts in opsins, which is likely to be key in facilitating specific adaptations in vision for diverse water habitats. CONCLUSIONS: Our findings suggest that local gene duplications might have played an important role during the evolution of water striders. Along with these findings, the sequencing of the G. buenoi genome now provides us the opportunity to pursue exciting research opportunities to further understand the genomic underpinnings of traits associated with the extreme body plan and life history of water striders.

Honeybee queen mandibular pheromone induces a starvation response in Drosophila melanogaster.

Eusocial insect societies are defined by the reproductive division of labour, a social structure that is generally enforced by the reproductive dominant(s) or 'queen(s)'. Reproductive dominance is maintained through behavioural dominance or production of queen pheromones, or a mixture of both. Queen mandibular pheromone (QMP) is a queen pheromone produced by queen honeybees (Apis mellifera) which represses reproduction in worker honeybees. How QMP acts to repress worker reproduction, the mechanisms by which this repression is induced, and how it has evolved this activity, remain poorly understood. Surprisingly, QMP is capable of repressing reproduction in non-target arthropods. Here we show that in Drosophila melanogaster QMP treatment mimics the starvation response, disrupting reproduction. QMP exposure induces an increase in food consumption and activation of checkpoints in the ovary that reduce fecundity and depresses insulin signalling. The magnitude of these effects is indistinguishable between QMP-treated and starved individuals. As QMP triggers a starvation response in an insect diverged from honeybees, we propose that QMP originally evolved by co-opting nutrition signalling pathways to regulate reproduction.

Noggin proteins are multifunctional extracellular regulators of cell signaling.

Noggin is an extracellular cysteine knot protein that plays a crucial role in vertebrate dorsoventral patterning. Noggin binds and inhibits the activity of bone morphogenetic proteins via a conserved N-terminal clip domain. Noncanonical orthologs of Noggin that lack a clip domain ("Noggin-like" proteins) are encoded in many arthropod genomes and are thought to have evolved into receptor tyrosine kinase ligands that promote Torso/receptor tyrosine kinase signaling rather than inhibiting bone morphogenic protein signaling. Here, we examined the molecular function of noggin/noggin-like genes (ApNL1 and ApNL2) from the arthropod pea aphid using the dorso-ventral patterning of Xenopus and the terminal patterning system of Drosophila to identify whether these proteins function as bone morphogenic protein or receptor tyrosine kinase signaling regulators. Our findings reveal that ApNL1 from the pea aphid can regulate both bone morphogenic protein and receptor tyrosine kinase signaling pathways, and unexpectedly, that the clip domain is not essential for its antagonism of bone morphogenic protein signaling. Our findings indicate that ancestral noggin/noggin-like genes were multifunctional regulators of signaling that have specialized to regulate multiple cell signaling pathways during the evolution of animals.

Ancestral hymenopteran queen pheromones do not share the broad phylogenetic repressive effects of honeybee queen mandibular pheromone.

Queen pheromones effect the reproductive division of labour, a defining feature of eusociality. Reproductive division of labour ensures that one, or a small number of, females are responsible for the majority of reproduction within a colony. Much work on the evolution and function of these pheromones has focussed on Queen Mandibular Pheromone (QMP) which is produced by the Western or European honeybee (Apis mellifera). QMP has phylogenetically broad effects, repressing reproduction in a variety of arthropods, including those distantly related to the honeybee such as the fruit fly Drosophila melanogaster. QMP is highly derived and has little chemical similarity to the majority of hymenopteran queen pheromones which are derived from cuticular hydrocarbons. This raises the question of whether the phylogenetically widespread repression of reproduction by QMP also occurs with more basal saturated hydrocarbon-based queen-pheromones. Using D. melanogaster we show that saturated hydrocarbons are incapable of repressing reproduction, unlike QMP. We also show no interaction between the four saturated hydrocarbons tested or between the saturated hydrocarbons and QMP, implying that there is no conservation in the mechanism of detection or action between these compounds. We propose that the phylogenetically broad reproductive repression seen in response to QMP is not a feature of all queen pheromones, but unique to QMP itself, which has implications for our understanding of how queen pheromones act and evolve.