Abstract

The caste fate of developing female honey bee larvae is strictly socially regulated by adult nurse workers. As a result of this social regulation, nurse-expressed genes as well as larval-expressed genes may affect caste expression and evolution. We used a novel transcriptomic approach to identify genes with putative direct and indirect effects on honey bee caste development, and we subsequently studied the relative rates of molecular evolution at these caste-associated genes. We experimentally induced the production of new queens by removing the current colony queen, and we used RNA sequencing to study the gene expression profiles of both developing larvae and their caregiving nurses before and after queen removal. By comparing the gene expression profiles of queen-destined versus worker-destined larvae as well as nurses observed feeding these two types of larvae, we identified larval and nurse genes associated with caste development. Of 950 differentially expressed genes associated with caste, 82% were expressed in larvae with putative direct effects on larval caste, and 18% were expressed in nurses with putative indirect effects on caste. Estimated selection coefficients suggest that both nurse and larval genes putatively associated with caste are rapidly evolving, especially those genes associated with worker development. Altogether, our results suggest that indirect effect genes play important roles in both the expression and evolution of socially influenced traits such as caste.

Highlights

  • The social insect sterile worker caste is the archetypal example of reproductive altruism that initially puzzledDarwin(Darwin 1859) and spurred Hamilton(Hamilton 1964) to develop kin selection theory

  • Unlike some other well-studied polyphenisms that are controlled by simple abiotic factors such as temperature or photoperiod(Nijhout 2003), honey bee queen-worker dimorphism critically depends on social control of larval development by adult nestmates(Linksvayer et al 2011)

  • We simultaneously studied the gene expression profiles of two classes of socially-interacting individuals -developing larvae and their care-giving nurses -- in order to identify genes expressed in larvae and their nurses that are associated with larval caste development

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Summary

Introduction

The social insect sterile worker caste is the archetypal example of reproductive altruism that initially puzzledDarwin(Darwin 1859) and spurred Hamilton(Hamilton 1964) to develop kin selection theory. Kin selection theory presupposes the existence of genes that are expressed in one individual but have fitness effects on relatives(Hamilton 1964). Despite this clear focus of social evolution theory on socially-acting genes, empirical studies of the genetic basis of social insect traits, including caste, have widely overlooked the potential effects of genes that are expressed in one individual but affect the traits of social partners. Unlike some other well-studied polyphenisms that are controlled by simple abiotic factors such as temperature or photoperiod(Nijhout 2003), honey bee queen-worker dimorphism critically depends on social control of larval development by adult nestmates(Linksvayer et al 2011). In vitro rearing studies demonstrate that in the absence of social control, queen-worker dimorphism disappears and a continuous range of phenotypes are produced(Linksvayer et al 2011)

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