Life History Evolution in Amphicarpic Plants

Abstract Plants with dimorphic flowers or seeds provide excellent material for the study of life history evolution because the dimorphism often involves measurable differences in morphology, size, number, or genetic relatedness. For amphicarpic plants, the proportion of aerial: subterranean morphs produced is highly variable (from 0 to > 100) and related to both environmental and genetic factors. Plants from aerial seeds produce lower ratios of aerial: subterranean morphs than those from subterranean seeds. Despite substantial variation, subterranean seeds are generally heavier than aerial seeds (but fewer) and produce vigorous seedlings with high survivorship and high fitness. Adaptive advantages of subterranean seeds include retention of offspring in favorable parental microhabitats, protection of seeds from herbivory, predation, or fire, and avoidance of desiccating conditions on the soil surface; potential disadvantages include lack of gene exchange, high energy costs, limited dispersal, and sibling competition. For the few species studied, aerial reproduction is more plastic than subterranean reproduction and more likely to be affected by environmental conditions. Quantitative genetic analyses of a population of the annual grass Amphicarpum purshii have revealed lower heritabilites for subterranean relative to aerial reproductive traits. Subterranean seed number and mass show genetic correlations with shoot mass while aerial seed number and mass do not; seed set percentages of both seed types as well as percentage allocation to both reproductive morphs show negative genetic correlations with shoot mass. In this Amphicarpum population, directional selection on shoot mass may indirectly select for increased subterranean (but not aerial) seed output.     

The ecology of amphicarpic plants

Amphicarpic plants, which produce both aerial and subterranean flowers and seeds, provide evolutionary ecologists with insight into the evolution of breeding systems involving self-fertilization, seed dimorphisms and multiple dispersal strategies. The subterranean flowers of amphicarpic species do not open, are self-fertile, and produce large seeds with a limited dispersal potential. In contrast, the aerial flowers usually open, can cross-pollinate, and produce smaller seeds with a greater potential for long-distance dispersal. The eco-genetic consequences of this reproductive system are a function of these common features of amphicarpic species, and must be considered in an ecological context when attempting to determine the selective basis of subterranean fruit and seed production.     

REPRODUCTIVE BEHAVIOR OF AMPHICARPAEA BRACTEATA (LEGUMINOSAE), AN AMPHICARPIC ANNUAL

Amphicarpaea bracteata, an annual legume common in woodland communities in the eastern United States, produces three distinct types of flower: subterranean cleistogamous (SCL), aerial cleistogamous (ACL), and aerial chasmogamous (ACH). We sought to quantitatively describe the growth and reproduction of four diverse A. bracteata populations in an effort to explain the adaptive significance of this species’ variable reproductive modes. Virtually all plants develop 1 to 3 SCL seeds on subterranean cotyledonary shoots, starting in late July. Larger plants produce additional SCL seeds later from the tips of axillary shoots which bury. Seeds produced by SCL flowers are large (39 to 134 mg), have restricted dispersal, lack dormancy, have high germination , and produce relatively vigorous seedlings. ACL flowers develop from early August through plant senescence in early October, while ACH flowers appear in a pulse in late August. The number of each aerial flower type was positively correlated with plant size. The ACL flowers take significantly less time to develop mature fruits than do ACH flowers. Both aerial seeds are smaller than the subterranean (mean weights: ACL 12.1, ACH 8.7 mg), have lower germination (ACL 20.2%, ACH 15.3%), appear relatively resistant to environmental extremes, and have the potential for more widespread dispersal. Plants derived from subterranean seeds are much larger than plants derived from aerial seeds, which makes them more likely to produce axillary SCL and aerial seeds. Only larger plants derived from subterranean seeds and growing in favored sites produce ACH flowers. This imposes an alternation of selfing with outcrossing generations. This pattern of reproductive behavior in A. bracteata is similar to that found in several other amphicarpic species.     

Differences in seed dormancy and germination in amphicarpic legumes: manifold bet-hedging in space and time

两型结实豆科植物种子休眠和萌发的差异：空间和时间上多样性的两头下注策略 通过休眠而实现的在空间或时间上的传播是生物体对它们所经历的环境施加影响的主要过程之一。在植物中，由于这两种传播都是通过种子进行的，而且两者在适应性方面发挥的作用也是类似的，因此预测它们之间存在较强的进化相关性。在本研究中，我们使用了两型结实的植株来研究这些进化相关性，这类植株能同时产生具有高度空间传播力的种子以及不会传播的地下种子。我们对经不同组合的休眠过程破坏处理(即干燥后熟、冷积层和物理划伤)后的种子的萌发百分比进行了评估，以研究两种两型结实豆科植物——野豌豆(Vicia amphicarpa L.)和山黧豆(Lathyrus amphicarpos L.)，以及同它们亲缘关系很近的两种单型结实类群——救荒野豌豆(Vicia sativa L.)和红山黧豆(Lathyrus cicera L.)的飞播种子和地下种子在休眠和萌发方面的变化情况。研究结果表明，空间传播和时间传播之间存在着复杂的相互作用。在刚完成传播时，空播种子比地下种子更具休眠性，但当种子经后熟处理而开始物理休眠时，这种趋势也随之逆转。单型结实植株种子的萌发百分比高于其两型结实的同属植株，并在后熟处理后都同样失去了休眠性。相反，两型结实植株的种子则表现出同时受生理休眠和物理休眠调节的不同休眠性策略，预计这可能使出苗时间发生变化，从而提供了多层次多样化的两头下注策略(bet-hedging)。这一策略能够使植株依赖于丰产季中的历史有利区域而不阻碍空间和时间上的迁移，从而有可能在不可预测性很高的条件下具有适应性。     

Amphicarpum purshii and the “pessimistic strategy” in amphicarpic annuals with subterranean fruit

Summary Amphicarpum purshii Kunth is an annual amphicarpic grass of recently disturbed sandy areas in the Coastal Plain of eastern North America, producing small aerial and larger subterranean seeds. At study sites on the eastern edge of the Pine Barrens of New Jersey, the temporal aspects of reproductive allocation were investigated through biweekly whole-plant field harvests of 25 plants each throughout the 1980 growing season, and the survivorship of plants arising from aerial and subterranean seeds was monitored in a total of 10 high and 10 low density quadrats at two sites differeing in soil moisture. Plants arising from subterranean propagules began to allocate early (July 16) considerable energy to subterranean reproduction (ca 40% of whole-plant dry weight by the last half of August); allocation to aerial culms and flowers did not begin until mid-August and never exceeded 3% on a population basis. Plants arising from aerial propagules (aerial plants) produced only subterranean flowers, and these flowers first appeared 2 wk later than they did on subterranean plants. Survivorship was greater for the subterranean seedlings at both the dry and wet sites and at low and high densities, and aerial plants showed significantly less total growth and seed production than subterranean plants. The pessimistic strategy (early allocation of energy to large subterranean propagules) in the annual Amphicarpum has its selective basis in the relative vigor, survival, and timing and amount of reproduction of the two types of seedlings, and appears comparable to the allocation strategies of at least eight other amphicarpic annuals in at least five other families of plants.     

荒漠植物角果藜的地上地下结果性

对分布于准噶尔荒漠中角果藜(Ceratocarpus arenarius)果实的形态特征、空间位置、发育特性及散布特性进行了比较研究,结果表明:角果藜具有地上地下结果性,地上果实和地下果实在颜色、形状、大小、质量、数量、空间位置、成熟期和散布特性上均有显著差异。角果藜地上地下结果性是植物适应荒漠多变环境所具有的一种特殊的繁殖方式。这种独特的繁殖方式增加了物种在荒漠极端环境中成功生存的机率,保证了物种的顺利繁衍。这是首次在藜科植物中发现的地上地下结果性现象。     

Consequences of a mixed reproductive system in the hog peanut,Amphicarpaea bracteata, (Fabaceae)

Summary The forest annual, Amphicarpaea bracteata L. can reproduce via aerial chasmogamous, aerial cleistogamous, and subterranean cleistogamous flowers. Both plant size and light intensity influenced the utilization of the three modes of reproduction. chasmogamous and aerial cleistogamous flower number and the ratio of chasmogamous flowers to the total number of aerial flowers increased with plant size. The latter demonstrated a shift to xenogamy and outbreeding in larger plants. Light intensity indirectly influenced reproductive modes through its infuence on plant size. Seed set by both types of aerial flowers was low and unrelated to plant size. Subterranean seed number and the total dry weight of subterranean seeds per plant increased with size. The subterranean seeds of Amphicarpaea bracteata are thirty-four times larger than the aerial seeds (fresh weight). Under field conditions, subterranean seeds had greater germination after one year than acrial seeds. The plants arising from subterranean seeds were significantly larger and more fecund than those from aerial seeds. Seeds produced by aerial cleistogamous, hand selfpollinated chasmogamous, and naturally pollinated chasmogamous flowers had equivalent germination rates and produced plants of equal size and fecundity. This suggests that the outbred progeny from chasmogamous flowers have no advantage over the inbred progeny from aerial cleistogamous flowers.     

黄土丘陵沟壑区主要物种植冠种子库动态及其生态策略

植冠种子库是植物适应环境并应对外界干扰的种子生态策略之一,研究了黄土丘陵沟壑区12种主要植物植冠种子库动态,结果表明:杠柳不具有植冠种子库,其他11种植物均具有植冠种子库;除了黄刺玫种子在翌年5月达到脱落高峰,其他植物大部分种子在冬季脱落,其中杠柳、达乌里胡枝子、茭蒿、黄柏刺和水栒子的大部分种子脱落集中偏早,铁杆蒿和土庄绣线菊的大部分种子脱落集中偏晚;植冠宿存对大部分植物种子的萌发特性表现为促进作用;但不同植物种子的萌发时滞对植冠宿存响应差异较大;9种植物种子在植冠上宿存至翌年2月底,其种子活力仍能维持达60%以上;该区植物表现出不同的植冠种子库策略,通过不同的方式来减少干扰的威胁,提高成功萌发与更新的几率,它们或具有较大规模的宿存量、或调控种子萌发特性、或提高种子维持活力的百分比。此外,全面了解该区植物形成植冠种子库的机理及对应的生态策略还有待于全面、深入的研究。     

Differences in life history traits of relatedEpilobium species: Clonality, seed size and seed number

Small changes in morphology can affect the performance and functions of organisms and hence their ecological success. In modular constructed plants, contrasting growth strategies may be realized by differences in the spatial arrangement and size of shoots. Such differences change the way in which meristems and resources are assigned to various functions during the lifespan of a plant. If such changes include the capacity to spread clonally, sexual reproduction may also be affected. I compare patterns in vegetative growth and sexual reproductive traits in four allopatric species ofEpilobium which are sometimes considered as subspecies of a single polymorphic taxon. The four species differ in the location of the buds which annually renew the aerial shoot system.E. dodonaei andE. steveni do not spread clonally and are characterized by a shrub-like habit.E. fleischeri, a species occurring only in the Alps, andE. colchicum, which occurs in the upper region of the Caucasus mountains, both produce buds on horizontal roots or plagiotropic shoots. Both alpine species exhibiting clonal growth have smaller shoots, fewer fruits and smaller seeds than the lowland species. An intraspecific trade-off between seed number per fruit and seed mass is realized. Both alpine species produce more seeds per fruit at the expense of seed mass. The morphological relationship between the four species and their geographical distribution suggest that clonal growth inE. fleischeri (restricted to the Alps) andE. colchicum (restricted to the Caucasus) is adaptively associated with the stressful conditions of alpine habitats. Our results suggest that clonal growth is not necessarily correlated with reduced reproduction by seeds. The success of plants which are already established may largely depend on clonal spread, but the colonization of new habitats depends on the production of a large number of small seeds with high dispersability.     

QUANTITATIVE VARIATION OF LIFE HISTORY TRAITS IN AMPHICARPIC PEANUTGRASS (AMPHICARPUM PURSHII) AND ITS EVOLUTIONARY SIGNIFICANCE

Peanutgrass, Amphicarpum purshii, is a predominantly selling annual that exhibits an amphicarpic reproductive strategy, producing spikelets (and seeds) both above and below the soil surface. Both aerial and subterranean spikelets are self-fertile, but only the aerial spikelets are chasmogamous and capable of cross-pollination. This species mostly grows in disturbed areas of the New Jersey Pine Barrens. To examine life history variation, 60 quantitative characters were measured on twelve families raised from seeds collected from the aerial panicles of twelve parents grown in the greenhouse. Only 19 (= 31.7%) of the traits showed significant between-family phenotypic variation, and the mean percentage of the total variation due to family was 14.9 (N = 60 characters). Percentage biomass allocation and vegetative characters showed the highest narrow-sense heritabilities. Traits directly relevant to fitness such as subterranean seed set and seed weight of both seed types showed the least genetic variation. This low variation could reflect genetic fixation and/or developmental canalization of those fitness components important to survival in disturbed, early-successional habitats.     

The role of seed depth,litter, and fire in the seedling establishment of amphicarpic peanutgrass (Amphicarpum purshii)

Summary Amphicarpum purshii is an annual grass which mostly grows in disturbed areas of the New Jersey Pine Barrens, USA. It is amphicarpic, producing spikelets (and seeds) both above and below the soil surface. Previous research has shown that subterranean seed production ensures reproduction in the event of a major disturbance such as fire and results in rapid post-burn colonization of these sandy habitats. The effects of fire, litter, and seed depth were further examined by planting subterranean seeds at four depths in 16 litter-covered flats buried at ground level and comparing plants arising from burned flats with those in undisturbed litter-covered flats. At 0 and 1 cm depth, rates of seedling emergence were lowest in burned flats. Surface-sown seeds produced seedlings more likely to desiccate. Sowing depth had a greater influence on most measured characters than burning treatments. The mean depth of subterranean seed placement by Amphicarpum is 3.5 cm and this coincides with the seed depth from which plants showed the greatest height growth, shoot biomass, and reproductive output. In a second experiment, subterranean seeds on the bare soil surface in clay pots were more likely to lose viability and less likely to germinate than seeds protected by litter or burial in soil. In addition to providing protection from fire, placement of seeds below ground in the sandy habitat of peanutgrass provides conditions more suitable for seed survival and subsequent seedling establishment.     

INFLUENCE OF ENVIRONMENT AND POPULATION ORIGIN ON SURVIVORSHIP AND REPRODUCTION IN RECIPROCAL TRANSPLANTS OF AMPHICARPIC PEANUTGRASS (AMPHICARPUM PURSHII)

Reciprocal transplants of both seeds and seedlings were utilized to determine whether populations of the annual grass Amphicarpum purshii have become locally adapted to specific habitats due to the consistent production of cleistogamous subterranean seeds from year to year. The hypothesis was that subterranean seeds placed in the same habitat as the parents will produce seedlings of greater vigor and adults of higher reproductive capacity than plants from seeds transplanted to a different habitat far removed from the parents. For both seed and seedling transplant experiments involving three sites in the Pine Barrens of New Jersey, the effects of site on shoot dry weight and production of aerial spikelets, subterranean spikelets, and seeds were generally much more significant than the effects of population origin. With one exception, there was no tendency for seedlings (or plants from seeds) replanted into their home sites to outperform alien seedlings (or plants from seeds) transplanted into these same sites. The overriding importance of environmental factors (relative to genetic differences among populations) in determining the phenotypic expression of life history characters, and selection occurring during succession at a site may retard the evolution of genetic adaptation to local habitat conditions in this species.     

Genetic diversity of an amphicarpic species, Amphicarpaea edgeworthii Benth. (Leguminosae) based on RAPD markers

Amphicarpaea edgeworthii Benth. is an amphicarpic legume widespread in China. Amphicarpy describes the phenomenon that a plant produces aerial as well as subterranean fruits. A. edgeworthii can reproduce via three kinds of flowers: aerial chasmogamous flowers, aerial cleistogamous flowers, and subterranean cleistogamous flowers. Although there are some studies on the population genetic structure of species with both chasmogamous and cleistogamous flowers, none has been done for that of an amphicarpic species so far. The present study uses random amplified polymorphic DNA (RAPD) to assess level and pattern of genetic variation in 15 natural populations of A. edgeworthii. A total of 131 stable and clearly scored RAPD bands were achieved from 13 primers. The average genetic diversity within populations estimated by Shannon's information index was 0.218 at the population level, but ranged from 0.119 to 0.302, which was significantly different (P < 0.01). Different statistical analyses revealed a high level of genetic differentiation among populations (G_ST = 0.473–0.527). Thus, the pattern of genetic structure of A. edgeworthii is consistent with that of an inbreeding species.     

On the ecology and evolution of annual plants in disturbed environments

This paper is concerned with the effect of disturbance on some crucial characteristics of annual plants. The theoretically optimal life-history traits that maximize individual fitness in disturbed environments are described and critically evaluated. It seems that none of them holds for all annual species.Self-pollination and especially seed polymorphism are considered important adaptations to life in unpredictable environments. The thesis is put forward that amphicarpic annuals, which exhibit both self-pollination and extreme seed polymorphism, are best adapted to life in hazardous habitats. The hypothetical course of the evolution of amphicarpy is demonstrated on the grounds of the comparison of contemporary annual species producing chasmogamous and cleistogamous flowers on a single individual.     

Plastic bet-hedging in an amphicarpic annual: an integrated strategy under variable conditions

Amphicarpy is a form of diversified bet-hedging expressed mostly in annual plants, where two types of offspring are produced with two distinct ecological roles: long-range aerial dispersers and highly competitive subterranean, sedentary fruit. Emex spinosa is a semi-arid, amphicarpic annual, inhabiting habitats with different levels of environmental variation. We tested the hypothesis that, in E. spinosa, bet-hedging may be “fine-tuned” by plasticity in the phenotype ratio (aerial/subterranean fruit mass) as a function of environmental conditions. We conducted a greenhouse experiment, manipulating nutrient availability and intraspecific density, to determine the pattern of ratio shifts. In order to determine whether the integrated strategy is an adaptation to variable habitats, a similar common garden experiment was conducted, comparing two natural populations differing in environmental variability. The offspring ratio shifted in response to both nutrient availability and plant density. In pots containing single plants the ratio increased steeply with nutrient availability, while in pots containing eight plants a more moderate increase occurred. These shifts were the result of plasticity in allocation to both achene types, as well as ontogenetic effects on aerial achene production. The degree of response increased with the heterogeneity of the habitat of origin. We found evidence for an adaptive integrated strategy, with bet-hedging “fine-tuned” by phenotypic plasticity. Strenuous conditions tended to shift the offspring ratio towards securing subterranean reproductive success, while favorable conditions resulted in a shift towards dispersible achenes. The authors Asaf Sadeh and Hagai Guterman contributed equally to this study.     

Reproductive versatility in legumes: the case of amphicarpy in Trifolium polymorphum

Amphicarpy is a fascinating reproductive strategy, defined as fruit produced both below the soil surface and as aerial fruit on the same plant. Trifolium polymorphum is a grassland species subject to herbivory that combines amphicarpy with vegetative reproduction through stolons. Underground flowers have been described as obligate autogamous and aerial ones as self‐compatible allogamous, with aerial floral traits favouring cross‐pollination. In the present work we performed different pollination treatments on aerial flowers to analyse rates of pollen tube development and offspring fitness, measured as fruit set, seed production and germination percentage. This last variable was compared to that of seeds produced underground. No significant differences were found between fruit set in self‐ and cross‐pollinations. Seed production was higher in self‐pollinations, which is consistent with the higher rate of pollen tube development observed in self‐crosses. Spontaneous self‐pollination is limited in aerial flowers; thus pollen transfer by means of a vector is required even within the same flower. Germination tests showed that aerial seeds produced after self‐ and cross‐pollination did not differ in fitness, but underground seeds had higher germination percentage than aerial ones. Thus, we conclude that T. polymorphum has a mixed mating system. In grasslands with heavy grazing pressure, clonal propagation and underground seed production ensure persistence in the field. An intermediate level of selfing in aerial flowers ensures offspring, but morphological (herkogamy) and functional (dicogamy) floral traits maintain a window to incorporate genetic variability, allowing the species to tolerate temporal and spatial pressures.     

Germination,reproduction and interference in the amphicarpic annual Emex spinosa (L.) Campd

Summary A comparison was made of the dimorphic subterranean and aerial achenes of the annual Emex spinosa (L.) Campd. Subterranean achenes were less dormant, had a higher percentage of viability, germinated at a faster rate, were less temperature-dependent in germination and produced larger seedlings than aerial achenes. Subterranean achenes germinated, equally well in light or dark but aerial achenes had a strong light requirement. There was a linear relationship between numbers of weight of aerial achenes and plant size in the field. More resources were allocated to reproduction in plants restricted in size because of environmental conditions. Subterranean achene production was less affected than aerial by density, nitrogen levels, varying field conditions and interference between plants grown, from subterranean and aerial achenes. In mixtures of such plants, those from subterranean achenes had larger leaf area and stems and more aerial achenes. These differences were not apparent in monocultures by the time of harvest. Seed dimorphism is more likely in short-lived fugitive species and the different roles associated with dimorphism (persistence in situ versus dispersal in E. spinosa) are seen as an ecological advantage in such species.     

Breeding systems and pollination inVigna minima (Leguminosae,Papilionoideae)

Four types of floral breeding systems—(i) chasmogamy, (ii) aerial pseudocleistogamy, (iii) subterranean pseudocleistogamy and (iv) obligate subterranean true cleistogamy—are observed in the populations ofVigna minima inhabiting the Western Ghats (India). Five categories of phenotypes are recognized based on the number and kinds of floral breeding systems found in a given individual. The frequencies of different categories of phenotypes not only show intra- and interpopulation variation, but also fluctuate from generation to generation suggesting differences in the genetic structure of populations. This polymorphism in the breeding system of a single species is unique and may be adaptive. Obligate subterranean true cleistogamy and amphicarpy appear to be adaptations to jungle fires and soil erosion.—The flowers are of the flag-blossom type and insect visitors act as tripping agents. The tripping mechanism together with the polymorphic floral breeding system result in a balanced mixture of selfing and outcrossing. Such a recombination system may enhance the fitness ofV. minima which is essentially a colonizing species.     

Patterns of wing size variation in seeds of the lily Cardiocrinum cordatum (Liliaceae)

We examined the patterns of variation in wing-loading and its related characteristics in Cardiocrinum cordatum to clarify the factors that determine the variation in seed dispersal ability in this species. The square root of wing-loading of a seed of a plant was not significantly correlated with basal stem diameter of a plant, indicating that large plants did not necessarily produce seeds with high dispersal ability. This result was inconsistent with the hypothesis that large plants produce seeds with high dispersal ability to avoid high mortality of seeds and seedlings in the vicinity of the parents. On the other hand, the square root of wing-loading of a seed of a fruit was negatively dependent on seed number of a fruit. Thus, many-seeded fruits produced seeds with high dispersal ability. This was because the projected surface area per seed was large in large fruits and large fruits contained large numbers of seeds. The cost per seed of producing fruit structures was small for many-seeded fruits. Thus, high dispersal ability of seeds in many-seeded fruits may be a result of an effective resource allocation pattern in which a high proportion of resources are allocated to those many-seeded fruits, enabling seeds to develop large wings and thus reducing the structural cost of fruits per seed.     

Reproductive Biology of an Amphicarpic Annual, Polygonum thunbergii (Polygonaceae): Spatio-temporal Changes in Growth, Structure and Reproductive Components of a Population over an Environmental Gradient

Abstract The process and mechanisms of spatio-temporal changes in growth, population structure, as well as various yield and reproductive components of a population of an amphicarpic annual, Polygonum thunbergii (Polygonaceae), with two reproductive systems (aerial chasmogamous flowers and subterranean cleistogamous flowers) along an environmental gradient (light, moisture and soil nitrogen levels) were investigated in the field.
The results clearly demonstrate that growth and allocation patterns, population structure, and reproductive output of individuals changed sharply along the environmental gradient in response to seasonal and spatial changes in resource availability. Models predicted that light conditions bring about one-sided competition, whereas nutrient conditions in the soil engender two-sided competition. As expected, the degree of one-sided competition was prominent in the case of a planophile, Polygonum thunbergii. Allocation patterns, seed outputs, individual seed size as well as relative energy costs of chasmogamous and cleistogamous seed as affected by light and nutrient levels were also critically analyzed. The most noteworthy finding was that the size of chasmogamous seeds sharply decreased in response to a decrease in the light regime, while cleistogamous seed size remained constant along the gradient. However, relative cost of both chasmogamous and cleistogamous seeds sharply increased with decrease in the light level, reflecting different degrees of environmental stress, biotic interference, or both.