Project description:Cooperation is a classic solution to hostile environments that limit individual survival. In extreme cases this may lead to the evolution of new types of biological individuals (e.g., eusocial super-organisms). We examined the potential for interindividual cooperation to evolve via experimental evolution, challenging nascent multicellular "snowflake yeast" with an environment in which solitary multicellular clusters experienced low survival. In response, snowflake yeast evolved to form cooperative groups composed of thousands of multicellular clusters that typically survive selection. Group formation occurred through the creation of protein aggregates, only arising in strains with high (>2%) rates of cell death. Nonetheless, it was adaptive and repeatable, although ultimately evolutionarily unstable. Extracellular protein aggregates act as a common good, as they can be exploited by cheats that do not contribute to aggregate production. These results highlight the importance of group formation as a mechanism for surviving environmental stress, and underscore the remarkable ease with which even simple multicellular entities may evolve-and lose-novel social traits.
Project description:Natural environments are characterized by unpredictability over all time scales. This stochasticity is expected on theoretical grounds to result in the evolution of 'bet-hedging' traits that maximize the long term, or geometric mean fitness even though such traits do not maximize fitness over shorter time scales. The geometric mean principle is thus central to our interpretation of optimality and adaptation; however, quantitative empirical support for bet hedging is lacking. Here, I report a quantitative test using the timing of seed germination-a model diversification bet-hedging trait-in Lobelia inflata under field conditions. In a phenotypic manipulation study, I find the magnitude of fluctuating selection acting on seed germination timing-across 70 intervals throughout five seasons-to be extreme: fitness functions for survival are complex and multimodal within seasons and significantly dissimilar among seasons. I confirm that the observed magnitude of fluctuating selection is sufficient to account for the degree of diversification behaviour characteristic of individuals of this species. The geometric mean principle has been known to economic theory for over two centuries; this study now provides a quantitative test of optimality of a bet-hedging trait in nature.
Project description:Genomic imprinting, where an allele's expression pattern depends on its parental origin, is thought to result primarily from an intragenomic evolutionary conflict. Imprinted genes are widely expressed in the brain and have been linked to various phenotypes, including behaviours related to risk tolerance. In this paper, we analyse a model of evolutionary bet-hedging in a system with imprinted gene expression. Previous analyses of bet-hedging have shown that natural selection may favour alleles and traits that reduce reproductive variance, even at the expense of reducing mean reproductive success, with the trade-off between mean and variance depending on the population size. In species where the sexes have different reproductive variances, this bet-hedging trade-off differs between maternally and paternally inherited alleles. Where males have the higher reproductive variance, alleles are more strongly selected to reduce variance when paternally inherited than when maternally inherited. We connect this result to phenotypes connected with specific imprinted genes, including delay discounting and social dominance. The empirical patterns are consistent with paternally expressed imprinted genes promoting risk-averse behaviours that reduce reproductive variance. Conversely, maternally expressed imprinted genes promote risk-tolerant, variance-increasing behaviours. We indicate how future research might further test the hypotheses suggested by our analysis. This article is part of the theme issue 'Risk taking and impulsive behaviour: fundamental discoveries, theoretical perspectives and clinical implications'.
Project description:All organisms are faced with environmental uncertainty. Bet-hedging theory expects unpredictable selection to result in the evolution of traits that maximize the geometric-mean fitness even though such traits appear to be detrimental over the shorter term. Despite the centrality of fitness measures to evolutionary analysis, no direct test of the geometric-mean fitness principle exists. Here, we directly distinguish between predictions of competing fitness maximization principles by testing Cohen's 1966 classic bet-hedging model using the fungus Neurospora crassa. The simple prediction is that propagule dormancy will evolve in proportion to the frequency of 'bad' years, whereas the prediction of the alternative arithmetic-mean principle is the evolution of zero dormancy as long as the expectation of a bad year is less than 0.5. Ascospore dormancy fraction in N. crassa was allowed to evolve under five experimental selection regimes that differed in the frequency of unpredictable 'bad years'. Results were consistent with bet-hedging theory: final dormancy fraction in 12 genetic lineages across 88 independently evolving samples was proportional to the frequency of bad years, and evolved both upwards and downwards as predicted from a range of starting dormancy fractions. These findings suggest that selection results in adaptation to variable rather than to expected environments.
Project description:As ecosystems evolve, species can become extinct due to fluctuations in the environment. This leads to the evolutionary adaption known as bet-hedging, where species hedge against these fluctuations to reduce their likelihood of extinction. Environmental variation can be either within or between generations. Previous work has shown that selection for bet-hedging against within-generational variation should not occur in large populations. However, this work has been limited by assumptions of well-mixed populations, whereas real populations usually have some degree of structure. Using the framework of evolutionary graph theory, we show that through adding competition structure to the population, within-generational variation can have a significant impact on the evolutionary process for any population size. This complements research using subdivided populations, which suggests that within-generational variation is important when local population sizes are small. Together, these conclusions provide evidence to support observations by some ecologists that are contrary to the widely held view that only between-generational environmental variation has an impact on natural selection. This provides theoretical justification for further empirical study into this largely unexplored area.
Project description:In ecology, species can mitigate their extinction risks in uncertain environments by diversifying individual phenotypes. This observation is quantified by the theory of bet-hedging, which provides a reason for the degree of phenotypic diversity observed even in clonal populations. Bet-hedging in well-mixed populations is rather well understood. However, many species underwent range expansions during their evolutionary history, and the importance of phenotypic diversity in such scenarios still needs to be understood. In this paper, we develop a theory of bet-hedging for populations colonizing new, unknown environments that fluctuate either in space or time. In this case, we find that bet-hedging is a more favorable strategy than in well-mixed populations. For slow rates of variation, temporal and spatial fluctuations lead to different outcomes. In spatially fluctuating environments, bet-hedging is favored compared to temporally fluctuating environments. In the limit of frequent environmental variation, no opportunity for bet-hedging exists, regardless of the nature of the environmental fluctuations. For the same model, bet-hedging is never an advantageous strategy in the well-mixed case, supporting the view that range expansions strongly promote diversification. These conclusions are robust against stochasticity induced by finite population sizes. Our findings shed light on the importance of phenotypic heterogeneity in range expansions, paving the way to novel approaches to understand how biodiversity emerges and is maintained.
Project description:Helping kin or nonkin can provide direct fitness benefits, but helping kin also benefits indirect fitness. Why then should organisms invest in cooperative partnerships with nonkin, if kin relationships are available and more beneficial? One explanation is that a kin-limited support network is too small and risky. Even if additional weaker partnerships reduce immediate net cooperative returns, individuals extending cooperation to nonkin can maintain a larger social network which reduces the potential costs associated with losing a primary cooperation partner. Just as financial or evolutionary bet-hedging strategies can reduce risk, investing in quantity of social relationships at the expense of relationship quality ('social bet-hedging') can reduce the risks posed by unpredictable social environments. Here, we provide evidence for social bet-hedging in food-sharing vampire bats. When we experimentally removed a key food-sharing partner, females that previously fed a greater number of unrelated females suffered a smaller reduction in food received. Females that invested in more nonkin bonds did not do better under normal conditions, but they coped better with partner loss. Hence, loss of a key partner revealed the importance of weaker nonkin bonds. Social bet-hedging can have important implications for social network structure by influencing how individuals form relationships.
Project description:Bacterial cells, like many other organisms, face a tradeoff between longevity and fecundity. Planktonic cells are fast growing and fragile, while biofilm cells are often slower growing but stress resistant. Here we ask why bacterial lineages invest simultaneously in both fast- and slow-growing types. We develop a population dynamic model of lineage expansion across a patchy environment and find that mixed investment is favored across a broad range of environmental conditions, even when transmission is entirely via biofilm cells. This mixed strategy is favored because of a division of labor where exponentially dividing planktonic cells can act as an engine for the production of future biofilm cells, which grow more slowly. We use experimental evolution to test our predictions and show that phenotypic heterogeneity is persistent even under selection for purely planktonic or purely biofilm transmission. Furthermore, simulations suggest that maintenance of a biofilm subpopulation serves as a cost-effective hedge against environmental uncertainty, which is also consistent with our experimental findings.IMPORTANCE Cell types specialized for survival have been observed and described within clonal bacterial populations for decades, but why are these specialists continually produced under benign conditions when such investment comes at a high reproductive cost? Conversely, when survival becomes an imperative, does it ever benefit the population to maintain a pool of rapidly growing but vulnerable planktonic cells? Using a combination of mathematical modeling, simulations, and experiments, we find that mixed investment strategies are favored over a broad range of environmental conditions and rely on a division of labor between cell types, where reproductive specialists amplify survival specialists, which can be transmitted through the environment with a limited mortality rate. We also show that survival specialists benefit rapidly growing populations by serving as a hedge against unpredictable changes in the environment. These results help to clarify the general evolutionary and ecological forces that can generate and maintain diverse subtypes within clonal bacterial populations.
Project description:When bacteria grow in a medium with two sugars, they first use the preferred sugar and only then start metabolizing the second one. After the first exponential growth phase, a short lag phase of nongrowth is observed, a period called the diauxie lag phase. It is commonly seen as a phase in which the bacteria prepare themselves to use the second sugar. Here we reveal that, in contrast to the established concept of metabolic adaptation in the lag phase, two stable cell types with alternative metabolic strategies emerge and coexist in a culture of the bacterium Lactococcus lactis. Only one of them continues to grow. The fraction of each metabolic phenotype depends on the level of catabolite repression and the metabolic state-dependent induction of stringent response, as well as on epigenetic cues. Furthermore, we show that the production of alternative metabolic phenotypes potentially entails a bet-hedging strategy. This study sheds new light on phenotypic heterogeneity during various lag phases occurring in microbiology and biotechnology and adjusts the generally accepted explanation of enzymatic adaptation proposed by Monod and shared by scientists for more than half a century.
Project description:In order to understand how organisms cope with ongoing changes in environmental variability, it is necessary to consider multiple adaptations to environmental uncertainty on different time scales. Conservative bet-hedging (CBH) represents a long-term genotype-level strategy maximizing lineage geometric mean fitness in stochastic environments by decreasing individual fitness variance, despite also lowering arithmetic mean fitness. Meanwhile, variance-prone (aka risk-prone) strategies produce greater variance in short-term payoffs, because this increases expected arithmetic mean fitness if the relationship between payoffs and fitness is accelerating. Using evolutionary simulation models, we investigate whether selection for such variance-prone strategies is counteracted by selection for bet-hedging that works to adaptively reduce fitness variance. In our model, variance proneness evolves in fine-grained environments (lower correlations among individuals in energetic state and/or payoffs), and with larger numbers of independent decision events over which resources accumulate prior to selection. Conversely, multiplicative fitness accumulation, caused by coarser environmental grain and fewer decision events selection, favours CBH via greater variance aversion. We discuss examples of variance-sensitive strategies in optimal foraging, migration, life histories and cooperative breeding using this bet-hedging perspective. By linking disparate fields of research studying adaptations to variable environments, we should be better able to understand effects of human-induced rapid environmental change.