The evolution of queen control over worker reproduction in the social Hymenoptera

Jason Olejarz,Carl Veller,Martin A Nowak

doi:10.1002/ece3.3324

Abstract

A trademark of eusocial insect species is reproductive division of labor, in which workers forego their own reproduction while the queen produces almost all offspring. The presence of the queen is key for maintaining social harmony, but the specific role of the queen in the evolution of eusociality remains unclear. A long‐discussed scenario is that a queen either behaviorally or chemically sterilizes her workers. However, the demographic and ecological conditions that enable such manipulation are still debated. We study a simple model of evolutionary dynamics based on haplodiploid genetics. Our model is set in the commonly observed case where workers have lost the ability to lay female (diploid) eggs by mating, but retain the ability to lay male (haploid) eggs. We consider a mutation that acts in a queen, causing her to control the reproductive behavior of her workers. Our mathematical analysis yields precise conditions for the evolutionary emergence and stability of queen‐induced worker sterility. These conditions do not depend on the queen's mating frequency. We find that queen control is always established if it increases colony reproductive efficiency, but can evolve even if it decreases colony efficiency. We further derive the conditions under which queen control is evolutionarily stable against invasion by mutant workers who have recovered the ability to lay male eggs.

Highlights

Bees, and wasps form highly complex eusocial societies characterized by dominance hierarchies and reproductive division of labor (Gadagkar, 2001; Hӧlldobler & Wilson, 1990; Hunt, 2007; Michener, 1974; Wilson, 1971)
Both the queen and the workers are capable of laying male eggs parthenogenetically, but the workers often forego their own reproduction, allowing the queen to produce the majority of drones (Bourke, 1988; Fletcher & Ross, 1985; Heinze, 2004; Ratnieks, Foster, & Wenseleers, 2006; Wilson, 1971)
Our model takes as context a species in which workers can lay unfertilized eggs, but do not mate, and cannot lay fertilized eggs. (This situation is especially common in the higher eusocial Hymenoptera (Bourke, 1988; Fletcher & Ross, 1985), where workers in many species have retained functional ovaries, but have lost the ability to mate because of physiological factors like degradation of the spermatheca or diminution of the bursa copulatrix. It is a common situation in primitively eusocial bees and wasps (Fletcher & Ross, 1985), where workers often retain the physiological capability of mating, but do not mate because of an absence of males at the relevant stage of the colony life cycle, or for behavioral reasons.) In this model, we study the population genetics of alleles, dominant or recessive, that act in queens to reduce worker reproduction

Summary

| INTRODUCTION

Bees, and wasps form highly complex eusocial societies characterized by dominance hierarchies and reproductive division of labor (Gadagkar, 2001; Hӧlldobler & Wilson, 1990; Hunt, 2007; Michener, 1974; Wilson, 1971). To further determine whether the recessive b allele cannot fix, we must consider condition (20) in Olejarz et al (2015), which is the condition, for any number of matings, n, for invasion of a dominant mutation in workers that results in worker sterility. XBB, 0, XBB, 1, XBb, 0, XBb, 1, Xbb, 0, and Xbb, 1 are the frequencies of the six types of colonies in the population when considering the dynamics of the dominant reproduction allele, b (e.g., colonies headed by a type BB queen who has mated with a wild-type B male are denoted BB, 0, while colonies headed by a type BB queen who has mated with a mutant b male are denoted BB, 1). A single mutation in a worker may not be sufficient to reverse the primer or releaser effects of a queen’s (a) 1.6 1.4

Queen seizes control and workers regain control

| DISCUSSION