BIOLOGICAL ALTRUISM, EUSOCIALITY AND THE SUPERORGANISM A critical analysis of the role of biological altruism within eusociality research Mark Caine (cc)2020 MARK CAINE (cc by-nc-sa 4.0) INTRODUCTION ............................................................................................................................................. 3 Thesis objectives and methods ..................................................................................................................... 7 Overview of chapters .................................................................................................................................. 10 CHAPTER 1 — ALTRUISM AND EUSOCIAL INSECTS: A BRIEF HISTORY ............................................................ 18 INTRODUCTION .................................................................................................................................................... 18 1.1. ALTRUISM, PSYCHOLOGICAL AND BIOLOGICAL ...................................................................................................... 20 1.1.1. Altruism ............................................................................................................................................ 20 1.1.2. Biological altruism ............................................................................................................................ 21 1.1.3. The BA paradox and the levels of selection debate .......................................................................... 24 1.2. HAMILTON, EUSOCIALITY AND THE CONCEPT OF BA .............................................................................................. 30 1.2.1. Why did Hamilton apply kin selection to eusociality? ...................................................................... 31 1.2.2. Why did Hamilton apply BA to eusociality? ...................................................................................... 38 1.2.3. BA in pre-Hamiltonian eusociality research ...................................................................................... 43 1.2.4. BA in post-Hamiltonian eusociality research .................................................................................... 47 CONCLUSION ....................................................................................................................................................... 55 CHAPTER 2 — BIOLOGICAL ALTRUISM: HISTORY JUSTIFIED BY THEORY JUSTIFIED BY HISTORY ..................... 58 INTRODUCTION .................................................................................................................................................... 58 2.1. DID DARWIN DISCUSS AND/OR DEVELOP THE CONCEPT OF BA? .............................................................................. 60 2.1.1. Did Darwin discuss BA in the Descent of Man? ................................................................................ 63 2.1.2. Darwin’s “special difficulty” with eusociality .................................................................................... 68 2.1.3. Why did claims (2) and (3) emerge? ................................................................................................. 72 2.2. DARWIN AND EUSOCIALITY: GROUP SELECTION, KIN SELECTION, OR SOMETHING ELSE? ................................................ 77 CONCLUSION ....................................................................................................................................................... 86 CHAPTER 3 — EVOLUTIONARY THEORIES OF EUSOCIALITY: IS BA FUNDAMENTAL? ...................................... 91 INTRODUCTION .................................................................................................................................................... 91 3.1. BIOLOGICAL ALTRUISM: DEFINITIONAL ISSUES ...................................................................................................... 93 3.1.1. Absolute and relative (or weak and strong) definitions .................................................................... 96 3.1.2. A case for an additional clause ....................................................................................................... 100 3.1.3. Biological altruism: a proposed definition ...................................................................................... 103 3.2. THE EVOLUTION OF EUSOCIALITY .................................................................................................................... 104 3.2.1. Kin selection: BA and parental manipulation (coercion) ................................................................ 105 3.2.2. Group selection: MLS1 and MLS2 ................................................................................................... 117 3.2.3. Evolution of eusociality: a summary ............................................................................................... 121 CONCLUSION ..................................................................................................................................................... 124 CHAPTER 4 — THE SUPERORGANISM: FROM THE PAST TO THE PRESENT ................................................... 129 INTRODUCTION .................................................................................................................................................. 129 4.1. THE SUPERORGANISM: FROM A PHYSIOLOGICAL TO AN EVOLUTIONARY PERSPECTIVE ................................................. 131 4.1.1. The superorganism of old ............................................................................................................... 131 4.1.2. The decline of the superorganism .................................................................................................. 136 4.1.3. Complex eusociality ........................................................................................................................ 138 4.1.4. The revival of the superorganism ................................................................................................... 141 4.2. THE SELF-ORGANIZATION APPROACH TO COMPLEX EUSOCIALITY ............................................................................ 147 4.2.1. The problem of hierarchy ............................................................................................................... 147 4.2.2. The self-organization approach ...................................................................................................... 150 CONCLUSION ..................................................................................................................................................... 154 CHAPTER 5 — REVISING THE SUPERORGANISM: THE HIERARCHICAL-ORGANIZATIONAL APPROACH TO COMPLEX EUSOCIALITY .............................................................................................................................. 158 INTRODUCTION .................................................................................................................................................. 158 5.1. THE HIERARCHICAL-ORGANIZATIONAL APPROACH ............................................................................................... 160 5.1.1. The social physiology approach ...................................................................................................... 161 5.1.2. The hierarchical-organizational approach ...................................................................................... 163 1 5.2. THE APPLICATION OF THE HO APPROACH TO THREE REPRESENTATIVE CASE STUDIES OF SPECIES FROM ACROSS THE EUSOCIAL COMPLEXITY SPECTRUM ....................................................................................................................................... 168 5.2.1. Facultative eusocial bees, Megalopta genalis ................................................................................ 168 5.2.2. The common wasp, Vespula vulgaris ............................................................................................. 172 5.2.3. Honey bees, Apis mellifera ............................................................................................................. 177 5.3. COMPARISON OF COLONY LEVEL INDIVIDUALITY IN THREE EUSOCIAL INSECT SPECIES .................................................. 194 5.4. THE CONCEPT OF BA AND THE SUPERORGANISM ................................................................................................ 197 CONCLUSION ..................................................................................................................................................... 199 CONCLUSION .............................................................................................................................................. 204 Has the widespread use of the concept of BA been problematic for eusociality research? ..................... 206 Is the concept of BA a correct description of the behaviour of the non-reproductive castes in eusocial insect colonies? ......................................................................................................................................... 208 Eusociality without BA? Implications of the thesis ................................................................................... 210 BIBLIOGRAPHY ........................................................................................................................................... 212 2 Introduction Today the concept of biological altruism (BA) is widely used within biological