Relatedness, Conflict, and the Evolution of Eusociality

<div><p>The evolution of sterile worker castes in eusocial insects was a major problem in evolutionary theory until Hamilton developed a method called inclusive fitness. He used it to show that sterile castes could evolve via kin selection, in which a gene for altruistic sterility is favored when the altruism sufficiently benefits relatives carrying the gene. Inclusive fitness theory is well supported empirically and has been applied to many other areas, but a recent paper argued that the general method of inclusive fitness was wrong and advocated an alternative population genetic method. The claim of these authors was bolstered by a new model of the evolution of eusociality with novel conclusions that appeared to overturn some major results from inclusive fitness. Here we report an expanded examination of this kind of model for the evolution of eusociality and show that all three of its apparently novel conclusions are essentially false. Contrary to their claims, genetic relatedness is important and causal, workers are agents that can evolve to be in conflict with the queen, and eusociality is not so difficult to evolve. The misleading conclusions all resulted not from incorrect math but from overgeneralizing from narrow assumptions or parameter values. For example, all of their models implicitly assumed high relatedness, but modifying the model to allow lower relatedness shows that relatedness is essential and causal in the evolution of eusociality. Their modeling strategy, properly applied, actually confirms major insights of inclusive fitness studies of kin selection. This broad agreement of different models shows that social evolution theory, rather than being in turmoil, is supported by multiple theoretical approaches. It also suggests that extensive prior work using inclusive fitness, from microbial interactions to human evolution, should be considered robust unless shown otherwise.</p></div

Data: Spore carriage by flies

Data for experiment on spore carriage by flies after exposure to fruiting bodies. Formatted as tab-delimited text file for use with R. Columns and values described in comments (lines beginning with #)

Relatedness (<i>r</i>) and the evolution of eusociality.

<p>The worker-assisted birthrate <i>b</i> and the probability of staying <i>q</i> are allowed to vary, while other parameters are as in Figure 4 of Nowak et al. [<a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002098#pbio.1002098.ref013" target="_blank">13</a>] (<i>m</i> = 3, <i>b</i>_<i>0</i> = 0.5, <i>d</i>_<i>0</i> = 0.1, <i>d</i> = 0.01, α = 0.1, η = 0.01). Filled circles show values of relatedness <i>r</i> and worker-assisted queen birthrate <i>b</i> that select for eusociality (for at least one value of <i>q</i>) if the decision is made by offspring (<a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002098#pbio.1002098.e003" target="_blank">Equation 2</a>). Reducing relatedness makes eusociality harder to evolve (requires higher <i>b</i>). When the decision is made by genes acting in mothers (<a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002098#pbio.1002098.e004" target="_blank">Equation 3</a>), eusociality evolves under much broader conditions (open and filled circles), and lowering relatedness make eusociality easier to evolve. The open circles represent the zone of potential conflict, in which mothers but not offspring favor eusociality. The data used to make this figure can be found in <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002098#pbio.1002098.s006" target="_blank">S1 Dataset</a>.</p

Definition and number of behavioral choices (n = 125) foundresses made during the pre-emergence period in the study population.

<p>Definition and number of behavioral choices (n = 125) foundresses made during the pre-emergence period in the study population.</p

Cumulative frequency of foundress behaviors.

<p>Foundresses that initiate nests (n = 30) are indicated as filled diamonds, joining foundresses (n = 57) as open diamonds, and moving foundresses (n = 34) as filled triangles. In addition, adoptions are marked with @ signs on the day of adoption. Below the graph, the timing of moving events is divided into switching, deserting, and visiting (mean and range), showing that switchers moved earlier than other movers. A full explanation of the behaviors is given in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0045386#pone-0045386-t001" target="_blank">Table 1</a>.</p

Eusociality evolves more readily under a step model (both open and closed circles) than under the threshold model (closed circles only).

<p>The threshold model is that assumed in Figure 4 of Nowak et al. [<a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002098#pbio.1002098.ref013" target="_blank">13</a>] (<i>m</i> = 3, <i>b</i>_<i>0</i> = 0.5, <i>d</i>_<i>0</i> = 0.1, <i>d</i> = 0.01, α = 0.1, η = 0.01), with no benefits of working below colony size 3 (two workers). The step model is identical except one worker benefits the queen half as much as two workers do. The data used to make this figure can be found in <a href="http://www.plosbiology.org/article/info:doi/10.1371/journal.pbio.1002098#pbio.1002098.s006" target="_blank">S1 Dataset</a>.</p

Cumulative number of foundresses appearing and disappearing from the population.

<p>Foundresses appearing (n = 104) are indicated as diamonds, foundresses disappearing from the population (n = 54) as triangles. Below the graph, the date when eggs, larvae and pupae started appearing in the nests is indicated.</p

Fig. 2 - Images of flies carrying spores

High resolution version of Figure 2, showing composite images of D. melanogaster after exposure to fruiting bodies of D. discoideum genetically marked to express red fluorescent protein

A map showing location of the study nests and moving of foundresses.

<p>The field site was a c. 10 ha section of pecan/oak forest in Brazos Bend State Park, TX. The yellow area on the left is an open prairie; the green area on the right is a swamp, superior and inferior foraging areas, respectively. In <i>panel A</i>, nests marked with a larger font and a bolded circle are nests that survived until the end of the field period. Nests with a smaller font and a non-bolded circle are the ones that failed before the end of the field period. A red circle shows the nests that were adopted during the field period. Movements of the wasps are indicated with arrows. Purple, red, and blue arrows show switching, deserting and visiting, respectively, with the arrowhead indicating the target nest. Nests inhabited by full sister foundresses are filled with consistent colors (green nests: 14, 26; yellow: 29, 33 34; red: 7, 44, 45, 46; blue: 32, 35, 42, 43); nests not filled with a color were inhabited by a single foundress or full sister foundresses restricted to that nest. In <i>panel B</i>, the arrows indicate the direction of the moves, black arrows show switching and deserting (combined) and blue arrows visiting. The figures above the arrows (mean ±SD) show how much movers increased/decreased their distance from/to prairie/swamp by moving between nests (in meters); the figures below the arrows are the expected increases in distance had the movers selected their target nests randomly; all increases in distance were as expected (Mann-Whitney, all P’s >0.31).</p

Proportion of movers that were alone, dominant, or subordinate foundresses at their original and target nests.

<p>Proportion of movers that were alone, dominant, or subordinate foundresses at their original and target nests.</p