Seasonality and competition select for variable germination behavior in perennials

The common occurrence of within-population variation in germination behavior and associated traits such as seed size has long fascinated evolutionary ecologists. In annuals, unpredictable environments are known to select for bet-hedging strategies causing variation in dormancy duration and germination strategies. Variation in germination timing and associated traits is also commonly observed in perennials, and often tracks gradients of environmental predictability. Although bet-hedging is thought to occur less frequently in long-lived organisms, these observations suggest a role of bet-hedging strategies in perennials occupying unpredictable environments. We use complementary numerical and evolutionary simulation models of within- and among-individual variation in germination behavior in seasonal environments to show how bet-hedging interacts with density dependence, life-history traits, and priority effects due to competitive differences among germination strategies. We reveal substantial scope for bet-hedging to produce variation in germination behavior in long-lived plants, when "false starts" to the growing season results in either competitive advantages or increased mortality risk for alternative germination strategies. Additionally, we find that two distinct germination strategies can evolve and coexist through negative frequency-dependent selection. These models extend insights from bet-hedging theory to perennials and explore how competitive communities may be affected by ongoing changes in climate and seasonality patterns.

Avoiding dead ends: the experimental evolution of constraint as adaptation to environmental variation in Saccharomyces cerevisiae

Environmental unpredictability results in the evolution of bet-hedging traits, which maximize long-term fitness but are, by definition, suboptimal over short time scales. However, because suboptimal traits are expected to be purged by selection in the shorter term, the persistence of bet hedging remains perplexing. Here, we test the hypothesis that bet hedging persists through the evolution of constraint on short-term adaptation. We experimentally evolve Saccharomyces cerevisiae across two sequential treatments in which the frequency of extreme heat shocks decreases. We predict that experimental evolution under lower frequency heat shocks will result in greater adaptive constraint, or “purge-resistant” bet hedging. Constraint is assayed as evolutionary persistence of heat shock tolerance (HST) under constant benign conditions. As predicted, we find the retention of HST only in lines evolved under reduced frequency detrimental conditions. Results help explain the evolution of bet hedging, and challenge the traditional view that evolutionary constraint is inherently maladaptive.

Digital control of c-di-GMP in E. coli balances population-wide developmental transitions and phage sensitivity

Nucleotide-based signaling molecules (NSMs) are widespread in bacteria and eukaryotes, where they control important physiological and behavioral processes. In bacteria, NSM-based regulatory networks are highly complex, entailing large numbers of enzymes involved in the synthesis and degradation of active signaling molecules. How the converging input from multiple enzymes is transformed into robust and unambiguous cellular responses has remained unclear. Here we show that Escherichia coli converts dynamic changes of c-di-GMP into discrete binary signaling states, thereby generating heterogeneous populations with either high or low c-di-GMP. This is mediated by an ultrasensitive switch protein, PdeL, which senses the prevailing cellular concentration of the signaling molecule and couples this information to c-di-GMP degradation and transcription feedback boosting its own expression. We demonstrate that PdeL acts as a digital filter that facilitates precise developmental transitions, confers cellular memory, and generates functional heterogeneity in bacterial populations to evade phage predation. Based on our findings, we propose that bacteria apply ultrasensitive regulatory switches to convert dynamic changes of NSMs into binary signaling modes to allow robust decision-making and bet-hedging for improved overall population fitness.

Neither sex appears to benefit from divorce within migratory Northern Flickers consistent with accidental loss and bet-hedging

Divorce is widespread among species of birds and may either be an adaptive strategy to secure a better mate or territory or be a nonadaptive result of a failure to maintain the pairbond. I examined the causes and consequences for divorce in the Northern Flicker (Colaptes auratus), a migratory woodpecker with a high annual mortality rate. In a long-term population study of 1,793 breeding pairs over 17 years, the within-season divorce rate was 4.6% and the between-season divorce rate was 15.5%. Retained pairs within a season initiated their renest 5 days faster than divorced birds that had no greater fledgling production, suggesting that within-season divorce was making the best of a bad job with severe time constraints. Poor performance in the year prior to divorce was not strongly associated with divorce, and analysis of multiple breeding stages revealed that divorcing individuals in the subsequent year had later laying dates, smaller clutches, and fewer fledglings than retained pairs but no better performance than widowed individuals. Analyzing the data separately by sex showed that neither males nor females benefitted from divorce. Thus, there is a reproductive cost linked to finding a new partner per se, but no reproductive advantage associated with divorce. New mates after divorce were usually not older (not higher quality) than previous mates, so intrasexual competition was probably not driving partnership splits. The most plausible explanation seems to be a “bet-hedging” hypothesis in which birds re-pair rapidly in spring if their previous mate does not quickly arrive during spring migration. Divorce in Northern Flickers does not appear to be adaptive and future studies on arrival and interactions of individuals in spring will elucidate proximate constraints on relocating the previous partner.

“Indirect development” increases reproductive plasticity and contributes to the success of scyphozoan jellyfish in the oceans

Ecologists and evolutionary biologists have been looking for the key(s) to the success of scyphomedusae through their long evolutionary history in multiple habitats. Their ability to generate young medusae (ephyrae) via two distinct reproductive strategies, strobilation or direct development from planula into ephyra without a polyp stage, has been a potential explanation. In addition to these reproductive modes, here we provide evidence of a third ephyral production which has been rarely observed and often confused with direct development from planula into ephyra. Planulae of Aurelia relicta Scorrano et al. 2017 and Cotylorhiza tuberculata (Macri 1778) settled and formed fully-grown polyps which transformed into ephyrae within several days. In distinction to monodisk strobilation, the basal polyp of indirect development was merely a non-tentaculate stalk that dissolved shortly after detachment of the ephyra. We provide a fully detailed description of this variant that increases reproductive plasticity within scyphozoan life cycles and is different than either true direct development or the monodisk strobilation. Our observations of this pattern in co-occurrence with mono- and polydisk strobilation in Aurelia spp. suggest that this reproductive mode may be crucial for the survival of some scyphozoan populations within the frame of a bet-hedging strategy and contribute to their long evolutionary success throughout the varied conditions of past and future oceans.

Context, competition, and symbiont-induced bet-hedging between Dictyostelium discoideum and Paraburkholderia

Symbiotic interactions change with environmental context. We investigated context-dependence and bet-hedging in the symbiosis between social amoeba hosts and Paraburkholderia bacteria, where the context is the abundance of host food bacteria. Paraburkholderia have been shown to harm hosts dispersed to food-rich environments, but aid hosts dispersed to food-poor environments by allowing hosts to carry food bacteria. Through measuring symbiont density and host spore production, we show that this food context matters in three other ways. First, it matters for symbionts, who suffer a greater cost from competition with food bacteria in the food-rich context. Second, it matters for host-symbiont conflict, changing how symbiont density negatively impacts host spore production. Third, data-based simulations show in some cases this context-dependence can lead to a symbiont-induced bet-hedging advantage for hosts. These results show how food context can have many consequences for the Dictyostelium-Paraburkholderia symbiosis and suggest that symbionts can induce bet-hedging in hosts.