New paper in Nature Communications on the genetic basis of convergent eusocial evolution

Michael’s thesis chapter on the transcriptomic basis of the convergent evolution of caste-based division of labor in pharaoh ants and honey bees is now out at Nature Communications!

We designed this large study (based on 177 RNA seq libraries) to attempt to determine the degree to which genes underlying the expression of the eusocial caste system are shared between two species (the pharaoh ant Monomorium pharaonis and the honey bee Apis mellifera), which represent two independent origins of eusociality. We collected parallel developmental time series (egg, larval, pupal samples) for reproductive-destined and worker-destined brood, as well as adult queen, worker, and male samples for both species, and we sequenced and analyzed all samples in parallel to provide an unbiased estimate of the degree of transcriptomic overlap for caste-based division of labor in pharaoh ants and honey bees.

We identified a large set of genes (~1,500 genes) with caste-biased expression that was shared between pharaoh ants and honey bees, and this shared transcriptomic architecture represented ~30% of all caste-biased genes. Most of these genes were differentially expressed in adult abdominal tissues, providing a strong transcriptomic signature of the reproductive caste system (this is not surprising given that the main physiological difference between queens and workers in both ants and honey bees is that queens reproduce and workers do not, and female reproductive organs are in the abdomen). Interestingly, we found that this ~30-35% overlap for caste-associated genes is approaching the degree of overlap (~40%) that we observed of genes differentially expressed across development for honey bees and pharaoh ants. This is striking given that development is considered to be strongly conserved, suggesting that the molecular mechanisms underlying the reproductive caste system are also strongly conserved. All of this suggests that the convergent evolution of the reproductive caste system in ants and honey bees involved the recruitment of a pre-exisiting “reproductive groundplan” of genes associated with female reproductive physiology. At the same time, we also found that the majority (~65-70%) of genes with caste-associated expression were not shared between pharaoh ants and honey bees, also highlighting that the independent evolution of the caste system in the ancestors of ants and honey bees also involved the recruitment of many lineage-specific genes and genes with lineage-specific expression patterns. Overall, our results highlight the importance of both conserved and lineage-specific genes for the evolution of phenotypic innovations such as caste-based division of labor.

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