Multilevel selection favors fragmentation modes that maintain cooperative interactions in multispecies communities.

Reproduction is one of the requirements for evolution and a defining feature of life. Yet, across the tree of life, organisms reproduce in many different ways. Groups of cells (e.g., multicellular organisms, colonial microbes, or multispecies biofilms) divide by releasing propagules that can be single-celled or multicellular. What conditions determine the number and size of reproductive propagules? In multicellular organisms, existing theory suggests that single-cell propagules prevent the accumulation of deleterious mutations (e.g., cheaters). However, groups of cells, such as biofilms, sometimes contain multiple metabolically interdependent species. This creates a reproductive dilemma: small daughter groups, which prevent the accumulation of cheaters, are also unlikely to contain the species diversity that is required for ecological success. Here, we developed an individual-based, multilevel selection model to investigate how such multi-species groups can resolve this dilemma. By tracking the dynamics of groups of cells that reproduce by fragmenting into smaller groups, we identified fragmentation modes that can maintain cooperative interactions. We systematically varied the fragmentation mode and calculated the maximum mutation rate that communities can withstand before being driven to extinction by the accumulation of cheaters. We find that for groups consisting of a single species, the optimal fragmentation mode consists of releasing single-cell propagules. For multi-species groups we find various optimal strategies. With migration between groups, single-cell propagules are favored. Without migration, larger propagules sizes are optimal; in this case, group-size dependent fissioning rates can prevent the accumulation of cheaters. Our work shows that multi-species groups can evolve reproductive strategies that allow them to maintain cooperative interactions.

Cooperation can promote rescue or lead to evolutionary suicide during environmental change.

The adaptation of populations to changing conditions may be affected by interactions between individuals. For example, when cooperative interactions increase fecundity, they may allow populations to maintain high densities and thus keep track of moving environmental optima. Simultaneously, changes in population density alter the marginal benefits of cooperative investments, creating a feedback loop between population dynamics and the evolution of cooperation. Here we model how the evolution of cooperation interacts with adaptation to changing environments. We hypothesize that environmental change lowers population size and thus promotes the evolution of cooperation, and that this, in turn, helps the population keep up with the moving optimum. However, we find that the evolution of cooperation can have qualitatively different effects, depending on which fitness component is reduced by the costs of cooperation. If the costs decrease fecundity, cooperation indeed speeds adaptation by increasing population density; if, in contrast, the costs decrease viability, cooperation may instead slow adaptation by lowering the effective population size, leading to evolutionary suicide. Thus, cooperation can either promote or-counterintuitively-hinder adaptation to a changing environment. Finally, we show that our model can also be generalized to other social interactions by discussing the evolution of competition during environmental change.

Queen-worker conflict can drive the evolution of social polymorphism and split sex ratios in facultatively eusocial life cycles.

Hamilton's idea that haplodiploidy favors the evolution of altruism-the haplodiploidy hypothesis-relies on the relatedness asymmetry between the sexes caused by the sex-specific ploidies. Theoretical work on the consequences of relatedness asymmetries has significantly improved our understanding of sex allocation and intracolony conflicts, but the importance of haplodiploidy for the evolution of altruism came to be seen as minor. However, recently it was shown that haplodiploidy can strongly favor the evolution of eusociality, provided additional "preadaptations" are also present, such as the production of multiple broods per season and maternal ability to bias offspring sex ratios. These results were obtained assuming no influence of workers on the sex ratio, even though worker control of the sex ratio is known to occur. Here, we model the evolution of sex-specific fratricide as a mechanism of worker control over the sex ratio. We show that fratricide can facilitate the initial evolution of helping. However, fratricide can also hamper the evolution of unconditional help. Instead, social polymorphism evolves a mixture of helping and dispersing offspring. Finally, we show that the co-evolution of sex-allocation strategies of workers (fratricide) and queens leads to a split production of the sexes, with some colonies specializing in males and others in females. Thus, the model predicts that fratricide spawns a diversity of co-existing life cycles that strongly vary in degree of sociality and sex ratios.

Acculturation drives the evolution of intergroup conflict.

Conflict between groups of individuals is a prevalent feature in human societies. A common theoretical explanation for intergroup conflict is that it provides benefits to individuals within groups in the form of reproduction-enhancing resources, such as food, territory, or mates. However, it is not always the case that conflict results from resource scarcity. Here, we show that intergroup conflict can evolve, despite not providing any benefits to individuals or their groups. The mechanism underlying this process is acculturation: the adoption, through coercion or imitation, of the victor's cultural traits. Acculturation acts as a cultural driver (in analogy to meiotic drivers) favoring the transmission of conflict, despite a potential cost to both the host group as a whole and to individuals in that group. We illustrate this process with a two-level model incorporating state-dependent event rates and evolving traits for both individuals and groups. Individuals can become "warriors" who specialize in intergroup conflicts, but are costly otherwise. Additionally, groups are characterized by cultural traits, such as their tendency to engage in conflict with other groups and their tendency for acculturation. We show that, if groups engage in conflicts, group selection will favor the production of warriors. Then, we show that group engagement can evolve if it is associated with acculturation. Finally, we study the coevolution of engagement and acculturation. Our model shows that horizontal transmission of culture between interacting groups can act as a cultural driver and lead to the maintenance of costly behaviors by both individuals and groups.

Maladaptive Sex Ratio Adjustment in the Invasive Brine Shrimp Artemia franciscana.

Sex allocation theory is often hailed as the most successful area of evolutionary theory due to its striking success as a predictor of empirical observations [1]. Most naturally occurring sex ratios can be explained by the principle of equal investment in the sexes [2-4] or by cases of "extraordinary" sex allocation [5]. Deviations from the expected sex ratio are often correlated with weak selection or low environmental predictability (e.g., [6, 7]); true cases of aberrant sex allocation are surprisingly rare [8]. Here, we present a case of long-lasting maladaptive sex allocation, which we discovered in invasive populations of the exclusively sexual brine shrimp Artemia franciscana. A. franciscana was introduced to Southern France roughly 500 generations ago [9]; since then, it has coexisted with the native asexual species Artemia parthenogenetica [10]. Although we expect A. franciscana to produce balanced offspring sex ratios, we regularly observed extremely male-biased sex ratios in invasive A. franciscana, which were significantly correlated to the proportion of asexuals in the overall population. We experimentally proved that both invasive- and native-range A. franciscana overproduced sons when exposed to excess females, without distinguishing between conspecific and asexual females. We conclude that A. franciscana adjust their offspring sex ratio in function of the adult sex ratio but are information limited in the presence of asexual females. Their facultative adjustment trait, which is presumably adaptive in their native range, has thus become maladaptive in the invasive range where asexuals occur. Despite this, it has persisted unchanged for hundreds of generations.