Within-generation and transgenerational plasticity in growth and regeneration of a subordinate annual grass in a rainfall experiment

Precipitation changes may induce shifts in plant species or life form dominance in ecosystems, making some previously subordinate species abundant. The plasticity of certain plant functional traits of these expanding subordinate species may be one possible mechanism behind their success. In this study, we tested if the subordinate winter annual grass Secale sylvestre shows plasticity in growth and reproduction in response to altered environment associated with field-scale rainfall manipulations (severe drought, moderate drought, and watering) in a semiarid grassland, and whether the maternal environment influences offspring germination or growth in a subsequent pot experiment. Compared to control plots, S. sylvestre plants grew 38% taller, and produced 32% more seeds in severe drought plots, while plants in watered plots were 17% shorter, and had 22% less seeds. Seed mass was greatest in severe drought plots. Plants growing in drought plots had offspring with enhanced juvenile shoot growth compared to the progeny whose mother plants grew in watered plots. These responses are most likely explained by the decreased cover of previously dominant perennial grasses in severe drought plots, which resulted in wetter soil compared to control and watered plots during the peak growth of S. sylvestre. We conclude that the plasticity of this subordinate annual species in response to changing environment may help to gain dominance with recurring droughts that suppress perennial grasses. Our results highlight that exploring both within-generation and transgenerational plasticity of subordinate species may lead to a better prediction of changes in plant species dominance under climate change.

     

Phenotypic plasticity and bet‐hedging in a heterocarpic winter annual/spring ephemeral cold desert species of Brassicaceae

Phenotypic plasticity can play an important role in colonization and survival of plants in an environmentally fluctuating habitat. The primary aim of this study was to determine the influence of level of abiotic (soil moisture and nutrient availability) and biotic (density and herbivory) factors on phenotypic plasticity in the number and proportional mass allocation to the heteromorphic dehiscent upper (high dispersal, low dormancy) and indehiscent lower (low dispersal, high dormancy) siliques of individuals of the cold desert winter annual/spring ephemeral Diptychocarpus strictus derived from different seed morphs. Plants produced from seeds sown in an experimental garden were subjected to different levels of soil moisture, nutrient supply, density and simulated herbivory. Mass allocated to vegetative and reproductive components was measured and number of upper and lower siliques counted. Except for number ratio of upper: lower siliques under nutrient supply, levels of the four treatments resulted in significant variation in total plant mass, reproductive mass, number of siliques (upper and lower), number and mass of each silique morph, individual seed mass, upper/lower silique ratio and mass allocation to each organ in an individual. In favorable environments, the upper/lower silique ratio was relatively high, while in unfavorable environments it was relatively low. The relative allocation to upper and lower siliques was significantly negatively correlated, suggesting that allocation to upper siliques in good growth conditions occurred at the expense of allocation to lower siliques. This appears to be the first report on the effect of herbivory on diaspore morph ratio in heterocarpic plants and one of only a very few on the effect of density on morph ratio in this group. In D. strictus, stressful vs nonstressful growth conditions caused a shift in the ratio of heteromorphic diaspores, which themselves are assumed to be bet‐hedging.     

Effects of maternal and grandmaternal flea infestation on offspring quality and quantity in a desert rodent: evidence for parasite-mediated transgenerational phenotypic plasticity

Parasites can cause a broad range of sublethal fitness effects across a wide variety of host taxa. However, a host’s efforts to compensate for possible parasite-induced fitness effects are less well-known. Parental effects may beneficially alter the offspring phenotype if parental environments sufficiently predict the offspring environment. Parasitism is a common stressor across generations; therefore, parental infestation could reliably predict the likelihood of infestation for offspring. However, little is known about relationships between parasitism and transgenerational phenotypic plasticity. Thus, we investigated how maternal and grandmaternal infestation with fleas (Xenopsylla ramesis) affected offspring quality and quantity in a desert rodent (Meriones crassus). We used a fully-crossed design with control and infested treatments to examine litter size, pup body mass at birth, and pup mass gain before weaning for combinations of maternal and grandmaternal infestation status. No effect of treatment on litter size or pup body mass at birth was found. However, maternal and grandmaternal infestation status significantly affected pre-weaning body mass gain, a proxy for the rate of maturation, in male pups. Pups gained significantly more weight before weaning if maternal and grandmaternal infestation statuses matched, regardless of the treatment. Thus, pups whose mothers and grandmothers experienced similar risks of parasitism, either both non-parasitized or both infested, would reach sexual maturity more quickly than those pups whose mothers’ infestation status did not match that of their grandmothers. These results support the contention that parents can receive external cues such as the risk of parasitism, that prompt them to alter offspring provisioning. Therefore, parasites could be a mediator of environmentally-induced maternal effects and could affect host reproductive fitness across multiple generations.     

Adaptive transgenerational plasticity in the perennial Plantago lanceolata

Phenotypes of plants, and thus their ecology and evolution, can be affected by the environmental conditions experienced by their parents, a phenomenon called parental effects or transgenerational plasticity. However, whether such effects are just passive responses or represent a special type of adaptive plasticity remains controversial because of a lack of solid tests of their adaptive significance. Here, we investigated transgenerational effects of different nutrient environments on the productivity, carbon storage and flowering phenology of the perennial plant Plantago lanceolata, and whether these effects are influenced by seasonal variation in the maternal environment. We found that maternal environments significantly affected the offspring phenotype, and that plants consistently produced more biomass and had greater root carbohydrate storage if grown under the same environmental conditions as experienced by their mothers. The observed transgenerational effects were independent of the season in which seeds had matured. We therefore conclude that transgenerational effects on biomass and carbon storage in P. lanceolata are adaptive regardless of the season of seed maturation.     

Predator-induced transgenerational phenotypic plasticity in the cotton aphid

Transgenerational phenotypic changes, whereby offspring have an altered trait or a distinct alternate phenotype, frequently occur in response to increased maternal predation risk. The cotton aphid, Aphis gossypii (Glover), is unique, however, as offspring consist of four distinct phenotypes (normal light green apterae, normal dark green apterae, dwarf yellow apterae, and alatae), all with divergent life history patterns and resulting population dynamics. Here, we show that increased predation risk induces transgenerational phenotypic changes in cotton aphids. When exposed to search tracks from larval or adult convergent ladybird beetles, Hippodamia convergens Guérin-Méneville, cotton aphids produced greater numbers of winged offspring. In a subsequent experiment, apterous and alate individuals on clean plants were found to have primarily normal and dwarf offspring, respectively. We suggest that elevated predation risk may cause phenotypic changes in aphids over multiple generations, resulting in a more precipitous decline in herbivore populations than could be explained solely by increased predation rates.     

Trade-offs between seed dispersal and dormancy in an amphi-basicarpic cold desert annual

Background and Aims

Several studies have demonstrated trade-offs between depth of seed dormancy and dispersal ability for diaspore-dimorphic species. However, relatively little is known about trade-offs between these two life history traits for a species that produces more than two diaspore morphs. The aim of this study was to investigate the relationship between seed dormancy and dispersal in Ceratocarpus arenarius, an amphi-basicarpic cold desert annual that produces a continuum of dispersal unit morphs.

Methods

A comparison was made of dispersal and dormancy breaking/germination responses of dispersal units from ground level (a), the middle of the plant canopy (c) and the top of the plant canopy (f). Various features of the morphology and mass of dispersal units and fruits (utricles) were measured. The role of bracteoles in diaspore dispersal by wind, settlement onto the soil surface and dormancy/germination was determined by comparing responses of intact dispersal units and fruits. Movement of dispersal units by wind and animals, seed after-ripening, germination phenology and the presence of water-soluble germination inhibitors in bracteoles were tested using standard procedures.

Key Results

Dispersal units a, c and f differed in morphology and mass; in the majority of cases, extremes were exhibited by a and f, with c being intermediate. Overall, relative dispersal ability was f > c > a, whereas relative intensity of dormancy was a > c > f. Bracteoles increased dispersal distance by wind, enhanced settlement of diaspores onto the soil surface and mechanically inhibited germination.

Conclusions

The results provide evidence for a model in which there is a continuous inverse-linear relationship between diaspore dispersal ability and depth of dormancy. Thus, dispersal unit heteromorphism of C. arenarius results in a continuum, from no dispersal ability/high dormancy (dispersal unit a) to high dispersal ability/low dormancy (unit f), which may be a bet-hedging strategy in the cold desert environment.     

Adaptive transgenerational plasticity in an annual plant: grandparental and parental drought stress enhance performance of seedlings in dry soil

Stressful parental (usually maternal) environments can dramatically influence expression of traits in offspring, in some cases resulting in phenotypes that are adaptive to the inducing stress. The ecological and evolutionary impact of such transgenerational plasticity depends on both its persistence across generations and its adaptive value. Few studies have examined both aspects of transgenerational plasticity within a given system. Here we report the results of a growth-chamber study of adaptive transgenerational plasticity across two generations, using the widespread annual plant Polygonum persicaria as a naturally evolved model system. We grew five inbred Polygonum genetic lines in controlled dry vs. moist soil environments for two generations in a fully factorial design, producing replicate individuals of each genetic line with all permutations of grandparental and parental environment. We then measured the effects of these two-generational stress histories on traits critical for functioning in dry soil, in a third (grandchild) generation of seedling offspring raised in the dry treatment. Both grandparental and parental moisture environment significantly influenced seedling development: seedlings of drought-stressed grandparents or parents produced longer root systems that extended deeper and faster into dry soil compared with seedlings of the same genetic lines whose grandparents and/or parents had been amply watered. Offspring of stressed individuals also grew to a greater biomass than offspring of nonstressed parents and grandparents. Importantly, the effects of drought were cumulative over the course of two generations: when both grandparents and parents were drought-stressed, offspring had the greatest provisioning, germinated earliest, and developed into the largest seedlings with the most extensive root systems. Along with these functionally appropriate developmental effects, seedlings produced after two previous drought-stressed generations had significantly greater survivorship in very dry soil than did seedlings with no history of drought. These findings show that plastic responses to naturalistic resource stresses experienced by grandparents and parents can "preadapt" offspring for functioning under the same stresses in ways that measurably influence realized fitness. Possible implications of these environmentally-induced, inherited adaptations are discussed with respect to ecological distribution, persistence under novel stresses, and evolution in natural populations.     

Architectural plasticity in a Mediterranean winter annual

Size variability in plants may be underlain by overlooked components of architectural plasticity. In annual plants, organ sizes are expected to depend on the availability and reliability of resources and developmental time. Given sufficient resources and developmental time, plants are expected to develop a greater number of large branches, which would maximize fitness in the long run. However, under restrictive growth conditions and environmental reliability, developing large branches might be risky and smaller branches are expected to foster higher final fitness. Growth and architecture of Trifolium purpureum (Papilionaceae) plants from both Mediterranean (MED) and semi-arid (SAR) origins were studied, when plants were subjected to variable water availability, photoperiod cues and germination timing. Although no clear architectural plasticity could be found in response to water availability, plants subjected to photoperiod cuing typical to late spring developed fewer basal branches. Furthermore, plants that germinated late were significantly smaller, with fewer basal branches, compared with plants which grew for the same time, starting at the beginning of the growing season. The results demonstrate an intricate interplay between size and architectural plasticities, whereby size modifications are readily induced by environmental factors related to prevalent resource availability but architectural plasticity is only elicited following the perception of reliable anticipatory cues.     

Solar tracking response to drought in a desert annual

Summary The responses to drought of the solar tracking winter annualLupinus arizonicus (Wats.) were examined under field and laboratory growth regimes. Under drought conditions tracking movements were maintained until the plant reached the wilting point. The leaves and leaflets were observed to cup in response to decreases in the xylem water potential. This resulted in a negative, but linear relationship between the cosine of the angle of incidence of the direct solar beam upon the leaf and water potential. Leaf conductance was also significantly related to xylem water potential in natural populations. Leaf and leaflet cupping seem to be responding directly to changing plant water status, resulting in reduced solar radiation load to drought stressed plants. It is hypothesized that this property may have adaptive consequences in relation to the water relations, energy budget, and carbon balance of the plant.     

Effects of grazing on the abundance and diversity of annual plants in Chihuahuan desert scrub habitat

We assess the impact of release from cattle grazing on the abundance and diversity of both winter and summer annual plant communities at an upper Chihuahuan Desert scrub site in south-eastern Arizona. In contrast to previous studies, we found that removal of herbivores (cattle) had little impact on ephemeral plant assemblages at our site. The total number of summer annual individuals per quadrat did not differ significantly, but there were significantly more winter annual plants on ungrazed quadrats. The number of species per quadrat, however, did not differ significantly between sites exposed to, or protected from, grazing in either season. Of 79 annual species recorded (34 in winter, 45 in summer), only 2 species, 1 in each season, responded significantly to the removal of cattle: Stephanomeria exigua and Polygala tweedyi were more abundant on ungrazed plots. Three additional species, Eriastrum diffusum and Cryptantha micrantha in winter, and Mollugo cerviana (summer), approached statistical significance. Differences in the effect of cattle grazing on annual plants between our results and those at other sites in the arid southwest most likely reflect differences in the speed of response by annuals in different areas. Comparisons of this with other studies underscores recent calls for studies at broader spatial and greater temporal scales.     

Empirical patterns of environmental variation favor adaptive transgenerational plasticity

Effects of parental environment on offspring traits have been well known for decades. Interest in this transgenerational form of phenotypic plasticity has recently surged due to advances in our understanding of its mechanistic basis. Theoretical research has simultaneously advanced by predicting the environmental conditions that should favor the adaptive evolution of transgenerational plasticity. Yet whether such conditions actually exist in nature remains largely unexplored. Here, using long‐term climate data, we modeled optimal levels of transgenerational plasticity for an organism with a one‐year life cycle at a spatial resolution of 4 km² across the continental United States. Both annual temperature and precipitation levels were often autocorrelated, but the strength and direction of these autocorrelations varied considerably even among nearby sites. When present, such environmental autocorrelations render offspring environments statistically predictable based on the parental environment, a key condition for the adaptive evolution of transgenerational plasticity. Results of our optimality models were consistent with this prediction: High levels of transgenerational plasticity were favored at sites with strong environmental autocorrelations, and little‐to‐no transgenerational plasticity was favored at sites with weak or nonexistent autocorrelations. These results are among the first to show that natural patterns of environmental variation favor the evolution of adaptive transgenerational plasticity. Furthermore, these findings suggest that transgenerational plasticity is likely variable in nature, depending on site‐specific patterns of environmental variation.     

Abronione, a rotenoid from the desert annual Abronia villosa

A high-throughput phytochemical investigation of Abronia villosa afforded a new rotenoid designated abronione (1) along with the known compounds boeravinone C and lupeol. The structure of 1 was determined using NMR, MS, and optical analysis with < 400 μg of material. Compound 1 displayed moderate cytotoxicity against NCI-H460 and HL-60 human cancer cell lines with IC(50) values of 14 and 36 μM, respectively.     

Fever and phenotype: transgenerational effect of disease on desert locust phase state

Natural enemy attack can cause transgenerational shifts in phenotype such that offspring are less vulnerable to future attack. Desert locusts (Schistocerca gregaria) show density‐dependent variation in their resistance to pathogens, such that they are less vulnerable to pathogens when in the high‐density gregarious phase state (when they would probably be more exposed to pathogens) than when in the solitarious phase state. We therefore hypothesized that infected gregarious parents would maintain this phenotype in their offspring. We infected gregarious desert locust nymphs with the fungal pathogen Metarhizium anisopliae var. acridum, and allowed them to survive to reproduction by means of behavioural fever. The phase state of the locust offspring was assessed by their colouration and behavioural assays. Contrary to our hypothesis, we found an increase in solitarization in the infected population (14.6% solitarious offspring from infected parents, vs. <2% from uninfected counterparts at equivalent density). In a second experiment, we simulated behavioural fever temperatures and obtained a similar result (13.6% solitarious offspring vs. 4.4% from controls), implying that the phenomenon is probably a side‐effect of the hosts’ fever response. Identification of this novel environmental factor affecting locust phase state could have important implications for the biological control of these major pests.     

Niche opportunities and invasion dynamics in a desert annual community

Although many factors influence the ability of exotics to invade successfully, most studies focus on only a few variables to explain invasion; attempts at theoretical synthesis are largely untested. The niche opportunities framework proposes that the demographic success of an invader is largely affected by the availability of resources and the abundance of its enemies. Here, we use a 31‐year study from a desert ecosystem to examine the niche opportunities framework via the invasion of the annual plant Erodium cicutarium. While the invader remained rare for two decades, a decline in granivory combined with an ideal climate window created an opportunity for E. cicutarium to escape control and become the dominant annual plant in the community. We show that fluctuations in consumption and resources can create niche opportunities for invaders and highlight the need for additional long‐term studies to track the influence of changing climate and community dynamics on invasions.     

The carbon gain benefits of solar tracking in a desert annual

Abstract. A comparison between two sympatric winter desert annuals, Camissonia claviformis and Malvastrum rotundi folium showed that both gained similar amounts of carbon during a spring day, although by very different means. Camissonia has horizontally fixed leaves which have a very high photosynthetic capacity. The temperature optimum of photosynthesis for this species is near 20°C. Malvastrum has leaves with a lower photosynthetic capacity and a photosynthetic temperature optimum near 30°C. Leaves of the latter species remain normal to the sun throughout the course of the day. The tracking response and high temperature optimum for photosynthesis of Malvastrum result in a high daily carbon gain and also a high water-use efficiency.     

Grandparental effects in marine sticklebacks: transgenerational plasticity across multiple generations

Nongenetic inheritance mechanisms such as transgenerational plasticity (TGP) can buffer populations against rapid environmental change such as ocean warming. Yet, little is known about how long these effects persist and whether they are cumulative over generations. Here, we tested for adaptive TGP in response to simulated ocean warming across parental and grandparental generations of marine sticklebacks. Grandparents were acclimated for two months during reproductive conditioning, whereas parents experienced developmental acclimation, allowing us to compare the fitness consequences of short‐term vs. prolonged exposure to elevated temperature across multiple generations. We found that reproductive output of F1 adults was primarily determined by maternal developmental temperature, but carry‐over effects from grandparental acclimation environments resulted in cumulative negative effects of elevated temperature on hatching success. In very early stages of growth, F2 offspring reached larger sizes in their respective paternal and grandparental environment down the paternal line, suggesting that other factors than just the paternal genome may be transferred between generations. In later growth stages, maternal and maternal granddam environments strongly influenced offspring body size, but in opposing directions, indicating that the mechanism(s) underlying the transfer of environmental information may have differed between acute and developmental acclimation experienced by the two generations. Taken together, our results suggest that the fitness consequences of parental and grandparental TGP are highly context dependent, but will play an important role in mediating some of the impacts of rapid climate change in this system.     

Fruit and seed heteromorphism in the cold desert annual ephemeral Diptychocarpus strictus (Brassicaceae) and possible adaptive significance

Background and Aims

Diptychocarpus strictus is an annual ephemeral in the cold desert of northwest China that produces heteromorphic fruits and seeds. The primary aims of this study were to characterize the morphology and anatomy of fruits and seeds of this species and compare the role of fruit and seed hetermorphism in dispersal and germination.

Methods

Shape, size, mass and dispersal of siliques and seeds and the thickness of the mucilage layer on seeds were measured, and the anatomy of siliques and seeds, the role of seed mucilage in water absorption/dehydration, germination and adherence of seeds to soil particles, the role of pericarp of lower siliques in seed dormancy and seed after-ripening and germination phenology were studied using standard procedures.

Key Results

Plants produce dehiscent upper siliques with a thin pericarp containing seeds with large wings and a thick mucilage layer and indehiscent lower siliques with a thick pericarp containing nearly wingless seeds with a thin mucilage layer. The dispersal ability of seeds from the upper siliques was much greater than that of intact lower siliques. Mucilage increased the amount of water absorbed by seeds and decreased the rate of dehydration. Seeds with a thick mucilage layer adhered to soil particles much better than those with a thin mucilage layer or those from which mucilage had been removed. Fresh seeds were physiologically dormant and after-ripened during summer. Non-dormant seeds germinated to high percentages in light and in darkness. Germination of seeds from upper siliques is delayed until spring primarily by drought in summer and autumn, whereas the thick, indehiscent pericarp prevents germination for >1 year of seeds retained in lower siliques.

Conclusions

The life cycle of D. strictus is morphologically and physiologically adapted to the cold desert environment in time and space via a combination of characters associated with fruit and seed heteromorphism.     

荒漠草原土壤相对湿度对猪毛蒿表型可塑性的影响

猪毛蒿(Artemisia scoparia)为菊科蒿属草本植物,是一种适应性较强的广幅种。研究荒漠草原不同土壤相对湿度条件下猪毛蒿的表型可塑性,对认识异质生境下猪毛蒿的生存适应策略具有重要的生态学意义。结果表明:株高、茎粗、根长、根重和单株生物量均表现出随土壤相对湿度的增大而增加的趋势,对异质生境具有较强的可塑性,而根冠比则表现出相对的稳定性。植株不同部位生物量大小排序为:上部中部下部,且植株下部显著大于上部生物量(P0.05)。土壤相对湿度40%生境下的头状花序数量和重量显著高于土壤相对湿度30%和30%—40%生境。繁殖器官绝对投入量(lg R)随着个体大小(lg V)的增大呈极显著的增加(P0.001),繁殖阈值介于1.868—2.006 g。随着土壤相对湿度的增加,繁殖分配比例极显著增大(P0.001)。营养器官和繁殖器官生物量、头状花序重量和数量、地下生物量和地上生物量均呈极显著线性正相关关系(P0.001),存在正向权衡。单个头状花序重量并不随个体大小和头状花序数量的增加而发生显著变化(P0.05),且在不同土壤相对湿度和不同部位间均无显著差异(P0.05)。由此可见,猪毛蒿在异质生境下产生的可塑性是其生存繁殖的重要反应机制之一。     

Monosoonal precipitation responses of shrubs in a cold desert community on the Colorado Plateau

South-eastern Utah forms a northern border for the region currently influenced by the Arizona monosoonal system, which feeds moisture and summer precipitation into western North America. One major consequence predicted by global climate change scenarios is an intensification of monosoonal (summer) precipitation in the aridland areas of the western United States. We examined the capacity of dominant perennial shrubs in a Colorado Plateau cold desert ecosystem of southern Utah, United States, to use summer moisture inputs. We simulated increases of 25 and 50 mm summer rain events on Atriplex canescens, Artemisia filifolia, Chrysothamnus nauseosus, Coleogyne ramosissima, and Vanclevea stylosa, in July and September with an isotopically enriched water (enriched in deuterium but not ¹⁸O). The uptake of this artificial water source was estimated by analyzing hydrogen and oxygen isotope ratios of stem water. The predawn and midday xylem water potentials and foliar carbon isotope discrimination were measured to estimate changes in water status and water-use efficiency. At. canescens and Ch. nauseosus showed little if any uptake of summer rains in either July or September. The predawn and midday xylem water potentials for control and treatment plants of these two species were not significantly different from each other. For A. filifolia and V. stylosa, up to 50% of xylem water was from the simulated summer rain, but the predawn and midday xylem water potentials were not significantly affected by the additional summer moisture input. In contrast, C. ramosissima showed significant uptake of the simulated summer rain (>50% of xylem water was from the artificial summer rain) and an increase in both predawn and midday water potentials. The percent uptake of simulated summer rain was greater when those rains were applied in September than in July, implying that high soil temperature in midsummer may in some way inhibit water uptake. Foliar carbon isotope discrimination increased significantly in the three shrubs taking up simulated summer rain, but pre-treatment differences in the absolute discrimination values were maintained among species. The ecological implications of our results are discussed in terms of the dynamics of this desert community in response to changes in the frequency and dependability of summer rains that might be associated with a northward shift in the Arizona monsoon boundary.