All organisms are designed by natural selection to maximize inclusive fitness, but we need to deconstruct Hamilton’s rule to explain the evolutionary origin of eusocial colonies with permanently unmated and morphologically differentiated castes. Life-time monogamy appears to have been a necessary, but not sufficient, condition for achieving such major eusociality transitions in the ants, corbiculate bees, vespine wasps and higher termites. Independent of ploidy, strict monogamy makes relatedness to female and male siblings constant, maximal (0.5 on average), and equal to parent-offspring relatedness, which implies that the relatedness term (r) cancels and Hamilton’s rule reduces to b/c > 1. Full-sibling relatedness did not make the evolution of permanent worker castes easy because a favorable benefit-to-cost ratio (b/c) needed to apply continuously over sufficient evolutionary time to genetically rewire and irreversibly fix caste-specific developmental pathways. The same logic applies to obligate eukaryote multicellularity (life-time committed gametes in a zygote allowing differentiation of soma) and to fungus-farming ants and termites (life-time committed eusocial colonies and clonal crop symbionts, allowing obligate mutualistic division of labor). As long as r, b and c all continued to vary simultaneously, only conditionally committed (i.e. facultative) forms of caste, soma, and interspecific cooperation could apparently evolve.

 

Jacobus (Koos) Boomsma received his PhD degree from the Free University of Amsterdam. A 5-year C. & C. Huygens Fellowship by the Netherlands Organization for Scientific Research NWO made him move to Utrecht, Oxford, and Cornell, until he took up permanent residency in Denmark as Associate Professor at the University of Aarhus (1990-1999) and Full Professor at the Department of Biology of the University of Copenhagen afterwards. He coordinated two EU-funded Research-Training Networks (1996-2004), initiated a long-term research program on fungus-growing ants in Panama where he is a senior STRI Research Associate, and founded the Copenhagen Centre for Social Evolution (2005-present). Apart from his research on fungus-growing ants, he developed split sex ratio theory and the monogamy hypothesis for the evolution of eusociality.