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In recent years, sociobiology has been extended to microorganisms. Viewed through this lens, the microbial world is replete with cooperative behaviors. However, little attention has been paid to alternate hypotheses, making many studies self-confirming. Somewhat apart is a recent analysis of pyoverdin production-a paradigmatic public good and social trait-by Pseudomonas, which has revealed discord between predictions arising from sociobiology and the biology of microbes. This led the authors, Zhang and Rainey (Z&R), to question the generality of the conclusion that pyoverdin is a social trait, and to question the fit between the sociobiology framework and microbiology. This has unsettled Kummerli and Ross-Gillespie (K&R), who in a recent "Technical Comment" assert that arguments presented by Z&R are flawed, their experiments technically mistaken, and their understanding of social evolution theory naive. We demonstrate these claims to be without substance and show the conclusions of K&R to be based on a lack of understanding of redox chemistry and on misinterpretation of data. We also point to evidence of cherry-picking and raise the possibility of confirmation bias. Finally, we emphasize that the sociobiology framework applied to microbes is a hypothesis that requires rigorous and careful appraisal.

The question of how altruism can evolve despite its local disadvantage to selfishness has produced a wealth of theoretical and empirical research capturing the attention of scientists across disciplines for decades. One feature that has remained consistent through this outpouring of knowledge has been that researchers have looked to the altruists themselves for mechanisms by which altruism can curtail selfishness. An alternative perspective may be that just as altruists want to limit selfishness in the population, so may the selfish individuals themselves. These alternative perspectives have been most evident in the fairly recent development of enforcement strategies. Punishment can effectively limit selfishness in the population, but it is not free. Thus, when punishment evolves among altruists, the double costs of exploitation from cheaters and punishment make the evolution of punishment problematic. Here we show that punishment can more readily invade selfish populations when associated with selfishness, whereas altruistic punishers cannot. Thereafter, the establishment of altruism because of enforcement by selfish punishers provides the ideal invasion conditions for altruistic punishment, effectively creating a transition of punishment from selfishness to altruistic. Thus, from chaotic beginnings, a little hypocrisy may go a long way in the evolution and maintenance of altruism.

Organisms from prokaryotes to plants and animals make costly investments in diffusible beneficial external products. While the costs of producing such products are born only by the producer, the benefits may be distributed more widely. How are external goods-producing populations stabilized against invasion by nonproducing variants that receive the benefits without paying the cost? This question parallels the classic question of altruism, but because external goods production need not be altruistic per se, a broader range of conditions may lead to the maintenance of these traits. We start from the physics of diffusion to develop an expression for the conditions that favor the production of diffusible external goods. Important variables in determining the evolutionary outcome include the diffusion coefficient of the good, the distance between individuals, and the uptake rate of the external good. These variables join the coefficient of relatedness and the cost/benefit ratio in an expanded form of Hamilton's rule that includes both selfish and altruistic paths to the evolution of external goods strategies. This expanded framework can be applied to any external goods trait, and is a useful heuristic even when it is difficult to quantify the fitness consequences of producing the good.

The importance of 'eco-evolutionary feedbacks' in natural systems is currently unclear. Here, we advance a general hypothesis for a particular class of eco-evolutionary feedbacks with potentially large, long-lasting impacts in complex ecosystems. These eco-evolutionary feedbacks involve traits that mediate important interactions with abiotic and biotic features of the environment and a self-driven reversal of selection as the ecological impact of the trait varies between private (small scale) and public (large scale). Toxic algal blooms may involve such eco-evolutionary feedbacks due to the emergence of public goods. We review evidence that toxin production by microalgae may yield 'privatised' benefits for individual cells or colonies under pre- and early-bloom conditions; however, the large-scale, ecosystem-level effects of toxicity associated with bloom states yield benefits that are necessarily 'public'. Theory predicts that the replacement of private with public goods may reverse selection for toxicity in the absence of higher level selection. Indeed, blooms often harbor significant genetic and functional diversity: bloom populations may undergo genetic differentiation over a scale of days, and even genetically similar lineages may vary widely in toxic potential. Intriguingly, these observations find parallels in terrestrial communities, suggesting that toxic blooms may serve as useful models for eco-evolutionary dynamics in nature. Eco-evolutionary feedbacks involving the emergence of a public good may shed new light on the potential for interactions between ecology and evolution to influence the structure and function of entire ecosystems.

Many microbes cooperatively secrete extracellular products that favorably modify their environment. Consistent with social evolution theory, structured habitats play a role in maintaining these traits in microbial model systems, by localizing the benefits and separating strains that invest in these products from ‘cheater’ strains that benefit without paying the cost. It is thus surprising that many unicellular, well-mixed microalgal populations invest in extracellular toxins that confer ecological benefits upon the entire population, for example, by eliminating nutrient competitors (allelopathy). Here we test the hypotheses that microalgal exotoxins are (1) exploitable public goods that benefit all cells, regardless of investment, or (2) non-exploitable private goods involved in cell-level functions. We test these hypotheses with high-toxicity (TOX+) and low-toxicity (TOX-) strains of the damaging, mixotrophic microalga Prymnesium parvum and two common competitors: green algae and diatoms. TOX+ actually benefits from dense populations of competing green algae, which can also be prey for P. parvum, yielding a relative fitness advantage over coexisting TOX-. However, with non-prey competitors (diatoms), TOX- increases in frequency over TOX+, despite benefiting from the exclusion of diatoms by TOX+. An evolutionary unstable, ecologically devastating public good may emerge from traits selected at lower levels expressed in novel environments.