Transgenerational Effects of Early Life Starvation on Growth,Reproduction, and Stress Resistance in Caenorhabditis elegans

Starvation during early development can have lasting effects that influence organismal fitness and disease risk. We characterized the long-term phenotypic consequences of starvation during early larval development in Caenorhabditis elegans to determine potential fitness effects and develop it as a model for mechanistic studies. We varied the amount of time that larvae were developmentally arrested by starvation after hatching (“L1 arrest”). Worms recovering from extended starvation grew slowly, taking longer to become reproductive, and were smaller as adults. Fecundity was also reduced, with the smallest individuals most severely affected. Feeding behavior was impaired, possibly contributing to deficits in growth and reproduction. Previously starved larvae were more sensitive to subsequent starvation, suggesting decreased fitness even in poor conditions. We discovered that smaller larvae are more resistant to heat, but this correlation does not require passage through L1 arrest. The progeny of starved animals were also adversely affected: Embryo quality was diminished, incidence of males was increased, progeny were smaller, and their brood size was reduced. However, the progeny and grandprogeny of starved larvae were more resistant to starvation. In addition, the progeny, grandprogeny, and great-grandprogeny were more resistant to heat, suggesting epigenetic inheritance of acquired resistance to starvation and heat. Notably, such resistance was inherited exclusively from individuals most severely affected by starvation in the first generation, suggesting an evolutionary bet-hedging strategy. In summary, our results demonstrate that starvation affects a variety of life-history traits in the exposed animals and their descendants, some presumably reflecting fitness costs but others potentially adaptive.     

Effects of larval food shortage on diapause induction and adult traits in Taiwanese Monochamus alternatus alternatus

To confirm the facultative diapause of Monochamus alternatus alternatus Hope (Coleoptera: Cerambycidae) and to determine the relationships between available larval food resources, diapause, and adult traits, newly hatched larvae were inoculated singly on 98 Pinus densiflora Siebold & Zuccarini (Pinaceae) bolts and reared at 25 °C, 100% r.h., and L16:D8. Fifty adults emerged from them, between 70 and 126 days after larval inoculation. The remaining 48 bolts that did not produce adults were divided into two groups. One group was transferred to 10 °C, 100% r.h., and L8:D16, and returned 140–154 days later to the original conditions, resulting in adult emergence. The other group was maintained under the original conditions for a mean of 358 days. These bolts did not produce adults. Dissection revealed that development was arrested at final instar in pine bolts. The larvae developed into adults after being exposed to 10 °C, 100% r.h., and L8:D16 for 146 days. Consequently, this species has facultative diapause. Diapause incidence was estimated to be 0.42. Non‐linear model and one‐way ANOVA showed a positive correlation between adult body size and available food resources under conditions of food shortage, and no effects of diapause or available food resources on the ovariole number, respectively. When larvae were inoculated on 28 pine branch sections, the results were similar to those obtained from pine bolts and led to estimation of a low diapause incidence of 0.045. The combined data showed the inhibitory effect of food shortage on diapause induction. Diapause of M. a. alternatus, especially reduced diapause induction in response to environmental deterioration (food shortage), is discussed in relation to risk‐spreading.     

Bet hedging in desert winter annual plants: optimal germination strategies in a variable environment

In bet hedging, organisms sacrifice short‐term success to reduce the long‐term variance in success. Delayed germination is the classic example of bet hedging, in which a fraction of seeds remain dormant as a hedge against the risk of complete reproductive failure. Here, we investigate the adaptive nature of delayed germination as a bet hedging strategy using long‐term demographic data on Sonoran Desert winter annual plants. Using stochastic population models, we estimate fitness as a function of delayed germination and identify evolutionarily stable strategies for 12 abundant species in the community. Results indicate that delayed germination meets the criteria as a bet hedging strategy for all species. Density‐dependent models, but not density‐independent ones, predicted optimal germination strategies that correspond remarkably well with observed patterns. By incorporating naturally occurring variation in seed and seedling dynamics, our results present a rigorous test of bet hedging theory within the relevant environmental context.     

Temperature thresholds of physically dormant seeds and plant functional response to fire: variation among species and relative impact of climate change

Variation in dormancy thresholds among species is rarely studied but may provide a basis to better understand the mechanisms controlling population persistence. Incorporating dormancy‐breaking temperature thresholds into existing trait frameworks could improve predictions regarding seed bank persistence, and subsequently species resilience in response to fire, climate change and anthropogenic management. A key ecological strategy for many species from fire‐prone ecosystems is the possession of a long‐lived seed bank, ensuring recovery after fire. Physical dormancy is dominant in these ecosystems and maintaining this dormancy is directly linked to seed bank persistence. We identified a suite of seed‐related factors relevant to maintaining populations in fire‐prone regions for 14 co‐occurring physically dormant species. We measured variation in initial levels of dormancy and then applied experimental heating treatments, based on current seasonal temperatures and those occurring during fires, to seeds of all study species. Additionally, higher seasonal temperature treatments were applied to assess response of seeds to temperatures projected under future climate scenarios. Levels of germination response and mortality were determined to assess how tightly germination response was bound to either fire or seasonal cues. Six species were found to have dormancy cues bound to temperatures that only occur during fires (80°C and above) and were grouped as having obligate pyrogenic dormancy release. The remaining species, classified as having facultative pyrogenic dormancy, had lower temperature dormancy thresholds and committed at least 30% of seeds to germinate after summer‐temperature treatments. Evidence from this study supports including dormancy‐breaking temperature thresholds as an attribute for identifying functional types. High temperature thresholds for breaking dormancy, found in our obligate pyrogenic group, appear to be a fire‐adapted trait, while we predict that species in the facultative group are most at risk to increased seed bank decay resulting from elevated soil temperatures under projected climate change.     

Epigenetic gambling and epigenetic drift as an antagonistic pleiotropic mechanism of aging

Generations of biogerontologists have been puzzled by the marked intraspecific variations in lifespan of their experimental model organisms despite all efforts to control both genotype and environment. The most cogent example comes from life table studies of wild‐type Caenorhabditis elegans when grown in suspension cultures using axenic media. While nuclear and mitochondrial somatic mutations and ‘thermodynamic noise’ likely contribute to such lifespan variegations, I raise an additional hypothetical mechanism, one that may have evolved as a mechanism of phenotypic variation which could have preceded the evolution of meiotic recombination. I suggest that random changes in cellular gene expression (cellular epigenetic gambling or bet hedging) evolved as an adaptive mechanism to ensure survival of members of a group in the face of unpredictable environmental challenges. Once activated, it could lead to progressive epigenetic variegation (epigenetic drift) amongst all members of the group. Thus, while particular patterns of gene expression would be adaptive for a subset of reproductive individuals within a population early in life, once initiated, I predict that continued epigenetic drift will result in variable onsets and patterns of pathophysiology – perhaps yet another example of antagonistic pleiotropic gene action in the genesis of senescent phenotypes. The weakness of this hypothesis is that we do not currently have a plausible molecular mechanism for the putative genetic ‘randomizer’ of epigenetic expression, particularly one whose ‘setting’ may be responsive to the ecology in which a given species evolves. I offer experimental approaches, however, to search for the elusive epigenetic gambler(s).     

短命植物异喙菊异形果实的两头下注策略

异喙菊(Heteracia szovitsii)是准噶尔荒漠中常见的一种具异形果实的菊科一年生早春短命植物。该文对其同一果序中3种果实的形态结构与扩散特征进行了比较研究, 并对其生态学意义进行了探讨。结果表明: 1)异喙菊3种果实的形态特征存在明显差异, 导致其扩散特性明显不同, 避免了同胞子代在生态位上的竞争。其中, 中央果具冠毛, 成熟后以果实为散布单元借风力扩散到较大范围; 外围果与过渡果均无冠毛, 分别以果序和果实为单元扩散至母株附近。2) 3种果实胚大小的差异导致其幼苗大小和竞争能力不同。外围果与过渡果的胚比中央果的大, 萌发后可产生较大和竞争力较强的幼苗。3)与中央果相比, 外围果和过渡果果皮颜色较深, 所含酚类物质较多, 厚度较大且厚壁组织较多, 对胚的保护能力强, 且种子休眠程度深。4)异形痩果在数量上的差异, 分摊了扩散和定居中的风险。数量较多的中央果增加了随机散布的机会, 可为其扩大种群开拓更大的范围, 而数量较少的外围果和过渡果可有效地减少近距离扩散所造成的同胞子代间竞争。异喙菊异形果实的产生及其生态学行为属于典型的两头下注策略: 外围果和过渡果代表了“谨慎”或“低风险”策略, 中央果则代表了“冒险”或“高风险”策略。通过这些策略, 异喙菊可将其在准噶尔荒漠极端环境中的生存风险进行有效地分摊, 以保障其繁衍成功。     

Recovery and immune priming modulate the evolutionary trajectory of infection‐induced reproductive strategies

In response to parasite exposure, organisms from a variety of taxa undergo a shift in reproductive investment that may trade off with other life‐history traits including survival and immunity. By suppressing reproduction in favour of somatic and immunological maintenance, hosts can enhance the probability of survival and recovery from infection. By plastically enhancing reproduction through terminal investment, on the other hand, hosts under the threat of disease‐induced mortality could enhance their lifetime reproductive fitness through reproduction rather than survival. However, we know little about the evolution of these strategies, particularly when hosts can recover and even bequeath protection to their offspring. In this study, we develop a stochastic agent‐based model that competes somatic maintenance and terminal investment strategies as they trade off differentially with lifespan, parasite resistance, recovery and transgenerational immune priming. Our results suggest that a trade‐off between reproduction and recovery can drive directional selection for either terminal investment or somatic maintenance, depending on the cost of reproduction to lifespan. However, some conditions, such as low virulence with a high cost of reproduction to lifespan, can favour diversifying selection for the coexistence of both strategies. The introduction of transgenerational priming into the model favours terminal investment when all strategies are equally likely to produce primed offspring, but favours somatic maintenance if it confers even a slight priming advantage over terminal investment. Our results suggest that both immune priming and recovery may modulate the evolution of reproductive shift diversity and magnitude upon exposure to parasites.     

Multitasking and the evolution of optimal clutch size in fluctuating environments

Adaptive studies of avian clutch size variation across environmental gradients have resulted in what has become known as the fecundity gradient paradox, the observation that clutch size typically decreases with increasing breeding season length along latitudinal gradients, but increases with increasing breeding season length along elevational gradients. These puzzling findings challenge the common belief that organisms should reduce their clutch size in favor of additional nesting attempts as the length of the breeding season increases, an approach typically described as a bet‐hedging strategy. Here, we propose an alternative hypothesis—the multitasking hypothesis—and show that laying smaller clutches represents a multitasking strategy of switching between breeding and recovery from breeding. Both our individual‐based and analytical models demonstrate that a small clutch size strategy is favored during shorter breeding seasons because less time and energy are wasted under the severe time constraints associated with breeding multiply within a season. Our model also shows that a within‐generation bet‐hedging strategy is not favored by natural selection, even under a high risk of predation and in long breeding seasons. Thus, saving time—wasting less time as a result of an inability to complete a breeding cycle at the end of breeding season—is likely to be the primary benefit favoring the evolution of small avian clutch sizes during short breeding seasons. We also synthesize the seasonality hypothesis (pronounced seasonality leads to larger clutch size) and clutch size‐dependent predation hypothesis (larger clutch size causes higher predation risks) within our multitasking hypothesis to develop an integrative model to help resolve the paradox of contrasting patterns of clutch size along elevational and latitudinal gradients. Ultimately, our models provide a new perspective for understanding life‐history evolution under fluctuating environments.