Five decades of misunderstanding in the socialHymenoptera: a review and meta‐analysis ofMichener's paradox

Abstract

In a much-cited 1964 paper entitled "Reproductive efficiency in relation to colony size in hymenopterous societies," Charles Michener investigated the correlation between a colony's size and its reproductive efficiencythe ability of its adult females to produce reproductives, measured as per-capita output. Based on his analysis of published data from destructively sampled colonies in 18 species, he reported that in most of these species efficiency decreased with increasing colony size. His conclusion that efficiency is higher in smaller groups has since gained widespread acceptance. But it created a seeming paradox: how can natural selection maintain social behaviour when a female apparently enjoys her highest per-capita output by working alone? Here we treat Michener's pattern as a hypothesis and perform the first large-scale test of its prediction across the eusocial Hymenoptera. Because data on actual output of reproductives were not available for most species, Michener used various proxies, such as nest size, numbers of brood, or amounts of stored food. We show that for each of Michener's data sets the reported decline in per-capita productivity can be explained by factors other than decreasing efficiency, calling into question his conclusion that declining efficiency is the cause of the pattern. The most prominent cause of bias is the failure of the proxy to capture all forms of output in which the colony invests during the course of its ontogeny. Other biasing factors include seasonal effects and a variety of methodological flaws in the data sets he used. We then summarize the results of 215 data sets drawn from post-1964 studies of 80 species in 33 genera that better control for these factors. Of these, 163 data sets are included in two meta-analyses that statistically synthesize the available data on the relationship between colony size and efficiency, accounting for variable sample sizes and non-independence among the data sets. The overall effect, and those for most taxonomic subgroups, indicates no loss of efficiency with increasing colony size. Two exceptional taxa, the halictid bees and independent-founding paper wasps, show negative trends consistent with the Michener hypothesis in some species. We conclude that in most species, particularly those with large colony sizes, the hypothesis of decreasing efficiency with increasing colony size is not supported. Finally, we explore potential mechanisms through which the level of efficiency can decrease, be maintained, or even increase, as colonies increase in size.

Self-complexification through integral feedback in eusocial paper wasps of various levels of sociality

“…Our study demonstrates how local and simple physical interactions (material exchanges) can give rise to such emerging patterns with similar key properties. Although Michener's Paradox was neglected at first and criticized thereafter [ 44 ], it is a significant biological observation of biological scalability that is highly relevant beyond biology today. Michener discovered, years ahead of Amdahl, a general law of scalability that became crucial in understanding complex systems such as economy and complex computational systems.…”

The evolution of morphological castes under decoupled control

“…Across the social Hymenoptera, worker productivity varies widely (Michener, 1964; Jeanne et al, 2022), depending on factors such as group size (Michener, 1964; Jeanne et al, 2022), time constraints (Lucas and Field, 2013) and environmental constraints (Bourke, 1999; Jeanne et al, 2022) due to seasonal variations in resource availability (Poitrineau et al, 2009). Variation in worker productivity can occur between species (Field and Toyoizumi, 2020) but also within them over time (Michener, 1964; Jeanne et al, 2022). The increase in worker productivity that a specialist worker morphological trait represents for a given worker will often depend on baseline worker productivity (worker productivity without that morphological trait).…”

Optimal fissioning strategies of social insects in dependence of colony dynamics and nest founding probability

“…It is argued that DCF evolved as a strategy to avoid -due to performance benefits of larger colonies -the particular risks, hardships and efficiency deficits solitary queens or young (small) colonies are exposed to (Keller, 1991;Debout et al, 2007;Cronin et al, 2013;Jeanne et al, 2022). Such risks include the difficulty of establishing a new nest by a single individual, time-constraints on ICF founded colonies when season length becomes short (Onoyama, 1981;Hölldobler and Wilson, 1990;Heinze et al, 1996;Cronin et al, 2020), high risks of predation, the stochastic risk of complete colony failure if the number of individuals is very small (Choe, 2010), but also the competitive weakness against larger, established colonies of the own or other species (Cronin et al, 2016b,a;Peeters and Molet, 2010;Tilman, 1994) and the limitation of suitable nest-sites if nest densities are high (Kokko and Lundberg, 2001).…”