PHENOTYPIC PLASTICITY EARLY IN LIFE CONSTRAINS DEVELOPMENTAL RESPONSES LATER

Abstract.— Plastic stem‐elongation responses to the ratio of red:far‐red (R:FR) wavelengths enable plants to match their phenotype to local competitive conditions. However, elongation responses early in the life history may occur at the cost of reduced plasticity later in the life history, because elongation influences both allocation patterns and structural integrity. A common‐garden experiment was performed to test whether seedling responses to R:FR affect biomass allocation, biomass accumulation, and subsequent plasticity to the cue. Seedlings of Abutilon theophrasti were stimulated to elongate by low R:FR treatments, and subsequent growth and plasticity was compared with nonelongated individuals. Elongated seedlings were less responsive than nonelongated ones to a second bout of low R:FR. Thus, seedling plasticity to R:FR reduces subsequent responsiveness to this cue. This negative association across life‐history stages suggests an important constraint on the evolution of plastic stem responses, because selection in A. theophrasti has previously been shown to favor increases in early elongation in combination with increased later elongation. The reduced responsiveness of elongated seedlings to R:FR appeared to result from a structural feedback mechanism, indicating that the opportunity cost of early responses may be lower in environments providing structural support.     

PHYSIOLOGICAL STRESS AND COLOR POLYMORPHISM IN THE INTERTIDAL SNAIL NUCELLA LAPILLUS

The intertidal snail Nucella lapillus exhibits considerable variation in shell color both within and between populations differentially exposed to wave action. Populations from high-wave-energy shores tended to be highly polymorphic and were dominated by pigmented morphs (especially brown), while those at more sheltered locations exhibited less polymorphism and were predominantly white. Field and laboratory experiments were conducted to determine the role of physiological stress and selective predation in maintaining the observed distribution of color morphs. The results demonstrated that 1) physiological stress from high temperature and desiccation during periods of tidal emersion was greater on protected shores, 2) under similar natural conditions, brown morphs heated up faster, attained higher temperatures, desiccated more rapidly, and suffered greater mortality than did white morphs, and 3) when pairs of brown and white morphs were tethered intertidally there was virtually no mortality of either morph on the exposed shore or in shaded microhabitats on the protected shore, but brown morphs suffered much greater mortality in sunny microhabitats on the protected shore. These findings demonstrate that the interpopulation variation in shell color of N. lapillus is in part a response to a selective gradient in physiological stress. Selection for crypsis by visually hunting predators did not appear to play a prominent role; however, only adults were considered, and the predation experiments were conducted in the fall before shorebirds that prey on whelks had arrived from their summer feeding grounds. Further experimentation to quantify the effects of visual predators such as birds and fish, particularly on juvenile snails, is necessary to assess adequately the importance of predation.     

DEVELOPMENTAL NOISE,PHENOTYPIC PLASTICITY,AND ALLOZYME HETEROZYGOSITY IN DAPHNIA

Previous theories and studies have postulated negative correlations between allozyme heterozygosity and developmental noise and between heterozygosity and phenotypic plasticity. We examined these relationships for morphological and life-history traits of Daphnia magna in four independent experiments using two different Moscow populations and one German population. Clones were raised under a range of food levels or individual densities. Heterozygosity was scored at five allozyme loci in two experiments and at three loci in two others. Relative differences in developmental noise among clones with different heterozygosity levels were estimated as the pooled residual variation from an analysis of variation that removed the effects of macroenvironment, clones, and their interaction. Plasticity was measured as the amount of macroenvironmental variation plus genotype-by-environment interaction variation. We found a positive correlation between developmental noise and heterozygosity, although this correlation varied among traits and experiments. This result contradicts most previous claims about these relationships. In contrast, we found that phenotypic plasticity and heterozygosity were negatively correlated for some traits. Developmental noise and phenotypic plasticity were correlated for only two traits in two different experiments. This trait-specific relationship is in concordance with previous studies. Our results could not be explained by effects of developmental time, a previously hypothesized mechanism. We propose several explanations for our results and the disparate results of others that do not require that heterozygosity be the actual cause of variation in developmental noise.     

QUANTITATIVE GENETICS OF SHELL FORM OF AN INTERTIDAL SNAIL: CONSTRAINTS ON SHORT-TERM RESPONSE TO SELECTION

We investigated the genetic and environmental determinants of shell form in an intertidal snail (Prosobranchia: Littorina sp.) to identify constraints on the short-term response to selection. Our quantitative genetic parameters were estimated from a half-sib experimental design using 288 broods of snails. Each brood was divided into two treatments differing in snail population density, and therefore in grazing area per snail. Differences in population density induced marked differences in shell form. Snails in the low density treatment grew faster and had lighter shells with narrower whorls and narrower apertures than their siblings at high density. Despite this environmental plasticity in shell shape we found significant additive genetic variance for components of shell shape. We discuss two mechanisms that may maintain additive genetic variance for shell shape in intertidal snail populations: migration between environments with different selective pressures and migration between environments with different mean growth rates. We also estimated a genetic variance-covariance matrix for shell form traits and used the matrix to identify constraints on the short-term response to selection. We predict the rate of response to selection for predator-resistant morphology such as would occur upon invasion of predatory crabs. The large negative genetic correlation between relative spire height and shell weight would facilitate simultaneous selection for a lower spire and a heavier shell, both of which would increase resistance to predatory crabs.     

DEVELOPMENTAL ANALYSIS OF LEAF PLASTICITY IN THE HETEROPHYLLOUS AQUATIC PLANT HIPPURIS VULGARIS

Leaf development was studied in the heterophyllous aquatic plant Hippuris vulgaris in order to characterize the developmental events that lead to the formation of aerial- vs. submerged-type leaves. Recent evidence that abscisic acid regulates leaf development in this species provided a basis for using abscisic acid as a developmental tool to accurately control leaf development. We found that leaf primordia were fully competent to develop into either aerial- or submerged-type leaves until the 10th plastochron, when they were ca. 300 μm long. Also, leaves between about the 10th and 21st plastochron formed sectored transition leaves (i.e., the basipetal portion was composed of aerial-type tissue and the apical portion was composed of submerged-type tissue, or vice versa), indicating that tissue determination as one or the other leaf type occurred on a local, as opposed to whole-leaf, level. Finally, no significant difference was observed between the apical dimensions of aerial or submerged-type shoots. These results indicate that the final determination of Hippuris vulgaris leaves occurs a) relatively late in leaf development, and b) independently of the shoot apex, and provide a basis for using this plant in further studies concerning leaf determination and pattern formation (e.g., stomates, lateral venation) in plants.     

SURVIVAL OF FUCOID EMBRYOS IN THE INTERTIDAL ZONE DEPENDS UPON DEVELOPMENTAL STAGE AND MICROHABITAT1

Embryos of the fucoid alga Pelvetia fastigiata (J. Ag.) DeToni were outplanted into the intertidal zone to assess survival during the physical stress brought about by emersion during a single low tide. Survival varied among microhabitats. Under the adult Pelvetia canopy, survival of 6-h-, 24-h-, 48-h-, and 1-wk-old embryos was nearly 100%. Almost all embryos of all ages died in exposed habitats on bare rock or within habitats where the Pelvetia canopy was removed experimentally. However, within red algal turfs, where most juvenile Pelvetia occur, survival was unusually age specific: 24- to 48-h-old embryos survived poorly compared to younger (6 h old) or older embryos (1 wk old). Survival patterns reflected microhabitat temperatures during the experiments. The fate of young post-settlement stages must be studied at these fine temporal and spatial scales to understand the organization of intertidal communities.     

BASAL TISSUE STRUCTURE IN THE EARLIEST EUCONODONTS: TESTING HYPOTHESES OF DEVELOPMENTAL PLASTICITY IN EUCONODONT PHYLOGENY

Abstract:  The hypothesis that conodonts are vertebrates rests solely on evidence of soft tissue anatomy. This has been corroborated by microstructural, topological and developmental evidence of homology between conodont and vertebrate hard tissues. However, these conclusions have been reached on the basis of evidence from highly derived euconodont taxa and the degree to which they are representative of plesiomorphic euconodonts remains an open question. Furthermore, the range of variation in tissue types comprising the euconodont basal body has been used to establish a hypothesis of developmental plasticity early in the phylogeny of the clade, and a model of diminishing potentiality in the evolution of development systems. The microstructural fabrics of the basal tissues of the earliest euconodonts (presumed to be the most plesiomorphic) are examined to test these two hypotheses. It is found that the range of microstructural variation observed hitherto was already apparent among plesiomorphic euconodonts. Thus, established histological data are representative of the most plesiomorphic euconodonts. However, although there is evidence of a range in microstructural fabrics, these are compatible with the dentine tissue system alone, and the degree of variation is compatible with that seen in clades of comparable diversity.     

HETEROCHRONIC DEVELOPMENTAL PLASTICITY IN LARVAL SEA URCHINS AND ITS IMPLICATIONS FOR EVOLUTION OF NONFEEDING LARVAE

Preexisting developmental plasticity in feeding larvae may contribute to the evolutionary transition from development with a feeding larva to nonfeeding larval development. Differences in timing of development of larval and juvenile structures (heterochronic shifts) and differences in the size of the larval body (shifts in allocation) were produced in sea urchin larvae exposed to different amounts of food in the laboratory and in the field. The changes in larval form in response to food appear to be adaptive, with increased allocation of growth to the larval apparatus for catching food when food is scarce and earlier allocation to juvenile structures when food is abundant. This phenotypic plasticity among full siblings is similar in direction to the heterochronic evolutionary changes in species that have greater nutrient reserves within the ova and do not depend on particulate planktonic food. This similarity suggests that developmental plasticity that is adaptive for feeding larvae also contributes to correlated and adaptive evolutionary changes in the transition to nonfeeding larval development. If endogenous food supplies have the same effect on morphogenesis as exogenous food supplies, then changes in genes that act during oogenesis to affect nutrient stores may be sufficient to produce correlated adaptive changes in larval development.     

AN INTERPRETATION OF PHENOTYPIC PLASTICITY IN AGROPYRON REPENS (GRAMINAE)

Phenotypic plasticity and genotypic variation were studied in Agropyron repens L. (Beauv.) collected from populations in two grassland communities which differed in the length of time since the last major disturbance. Twenty genotypes were collected from each population. Each genotype was vegetatively propagated, and subjected to six different treatments in a greenhouse. Phenotypic plasticity and genotypic variability were measured as across- and within-treatment standardized variances respectively. Patterns of plasticity were measured by genotype correlations across treatments. The results were presented graphically by the regression method of Garbutt and Zangerl (1983). Analysis of variance revealed significant population, genotype and treatment effects. Significant positive correlations between magnitude and variability of performance were found for all characters. Phenotypic plasticity and magnitude of performance were generally greater in plants collected from the older established field. Evidence for greater specialization in the older population was suggested by negative correlations between performance in the most favorable and least favorable treatments and by greater dissimilarity of genotype response across treatments. A more variable phenotypic response across treatments (i.e., higher plasticity) for plants from the older population may therefore be a consequence of specialization and not an adaptive trait per se.     

木槿的发育可塑性及种下分类研究

对紫花单瓣木槿、紫花重瓣木槿和牡丹木槿在叶和花部性状上的发育可塑性研究表明,三个种下类群,特别是紫花单瓣木槿和牡丹木槿的叶片性状具有很大的发育可塑性,但花部性状的发育可塑性则相对很小,暗示着花部性状较叶片性状具有更大的分类价值。通过种下类群间表型性状的比较,发现牡丹木槿在叶缘、叶柄长度、花色、花冠直径、花梗长度、果实长宽比等性状上都与其它两个类群存在显著差异,从而建议将牡丹木槿确立为亚种(H. syriacus Linn. subsp. paeoniflorus (Gagnep.)G. R. Shi)     

DEVELOPMENTAL CONSEQUENCES OF AN EVOLUTIONARY CHANGE IN EGG SIZE: AN EXPERIMENTAL TEST

Larvae of two species of sea urchins (Strongylocentrotus droebachiensis and S. purpuratus) differ in initial form and in the rate of development. To determine whether these differences are attributable to the large interspecific difference in egg size, we experimentally reduced egg size by isolating blastomeres from embryos. The rate of development of feeding larvae derived from isolated blastomeres was quantified using a novel morphometric method. If the differences early in the life histories of these two species are due strictly to differences in egg size, then experimental reduction of the size of S. droebachiensis eggs should yield an initial larval form and rate of development similar to that of S. purpuratus. Our experimental manipulations of egg size produced three clear results: 1) smaller eggs yielded larvae that were smaller and had simpler body forms, 2) smaller eggs resulted in slower development through the early feeding larval stages, and 3) effects of egg size were restricted to early larval stages. Larvae from experimentally reduced eggs of the larger species had rates of development similar to those of the smaller species. Thus, cytoplasmic volumes of the eggs, not genetic differences expressed during development, account for differences in larval form and the rate of form change. This is the first definitive demonstration of the causal relationship between egg size (parental investment per offspring) and life-history characteristics in marine benthic invertebrates. Because larval form influences feeding capability, the epigenetic effects of egg size on larval form are likely to have important functional consequences. Adaptive evolution of egg size may be constrained by the developmental relationships between egg size and larval form: evolutionary changes in egg size alone can result in concerted changes in larval form and function; likewise evolutionary changes in larval form and function can be achieved through changes in egg size. These findings may have broader implications for other taxa in which larval morphology and, consequently, performance may be influenced by changes in egg size.     

INTRASPECIFIC LIFE HISTORY VARIATION IN A POND SNAIL: THE ROLES OF POPULATION DIVERGENCE AND PHENOTYPIC PLASTICITY

Two approaches were used to determine the degree of divergence in life histories among populations of the pond snail, Lymnaea elodes. Juvenile snails were reciprocally transferred between ponds differing in permanence and productivity, and the resulting variation in life history traits was recorded. In a second experiment, parents and their offspring from both a vernal and a permanent pond population were reared in the same pond. Proximal factors had by far the greatest effects on life history traits in the transfer experiment, with snails reared in a more productive pond showing earlier reproduction at a larger size, higher fecundity, and longer life cycle length. Snails from the more uncertain pond in terms of drying date did reproduce at an earlier age and smaller size and grew less in each pond. However, these population differences, for the most part, disappeared when snails were reared for two generations in the same environment. Much of the intraspecific variation in life histories seen in this species must therefore be considered the result of phenotypic plasticity. I argue that the plasticity in life histories itself may be adaptive to this inhabitant of unpredictable, vernal ponds.     

INCIPIENT REPRODUCTIVE ISOLATION BETWEEN TWO SYMPATRIC MORPHS OF THE INTERTIDAL SNAIL LITTORINA SAXATILIS

The study of speciation in recent populations is essentially a study of the evolution of reproductive isolation mechanisms between sub-groups of a species. Prezygotic isolation can be of central importance to models of speciation, either being a consequence of reinforcement of assortative mating in hybrid zones, or a pleiotropic effect of morphological or behavioral adaptation to different environments. To suggest speciation by reinforcement between incipient species one must at least know that gene flow occurs, or have recently occurred, and that assortative mating has been established in the hybrid zone. In Galician populations of the marine snail Littorina saxatilis, two main morphs appear on the same shores, one on the upper-shore barnacle belt and the other in the lower-shore mussel belt. The two morphs overlap in distribution in the midshore where hybrids are found together with pure forms. Allozyme variation indicates that the two parental morphs share a common gene pool, although within shores, gene flow between morphs is less than gene flow within morphs. In this study, we observed mating behavior in the field, and we found that mating was not random in midshore sites, with a deficiency of heterotypic pairs. Habitat selection, assortative mating, and possibly sexual selection among females contributed to the partial reproductive isolation between the pure morphs. Sizes of mates were often positively correlated, in particular, in the upper shore, indicating size-assortative mating too. However, this seemed to be a consequence of nonrandom microdistributions of snails of different sizes. Because we also argue that the hybrid zone is of primary rather than secondary origin, this seems to be an example of sympatric reproductive isolation, either established by means of reinforcement or as a by-product to divergent selection acting on other characters.     

DEVELOPMENTAL PLASTICITY,GENETIC VARIATION,AND THE EVOLUTION OF ANDROMONOECY IN SOLANUM HIRTUM (SOLANACEAE)

Studies of andromonoecious species have shown that sex expression (proportions of hermaphrodite and staminate flowers) is quite variable. It is not known, however, whether this variation is due to variation among individuals for genetically fixed patterns of allocation to staminate and hermaphrodite flowers (population level variation) and/or to developmental plasticity of individuals in a heterogeneous environment (organismal level variation). Distinguishing between these two levels of variation is important for understanding the evolution of andromonoecy. This study investigates levels of variation in sex expression in the andromonoecious Solanum hirlum. Sex expression in this species is shown to be plastic among individuals of the same genotype (organismal level variation) and determined, in part, by the resource status of the individual. Among the genotypes examined there is also genetic variation for developmental plasticity. Thus, developmental plasticity can potentially respond to selection, and the evolution of this developmental system may have been instrumental in the establishment and maintenance of andromonoecy in S. hirtum.     

PLASTICITY, CANALIZATION, AND DEVELOPMENTAL STABILITY OF THE DROSOPHILA WING: JOINT EFFECTS OF MUTATIONS AND DEVELOPMENTAL TEMPERATURE

The phenotypic effects of genetic and environmental manipulations have been rarely investigated simultaneously. In addition to phenotypic plasticity, their effect on the amount and directions of genetic and phenotypic variation is of particular evolutionary importance because these constitute the material for natural selection. Here, we used heterozygous insertional mutations of 16 genes involved in the formation of the Drosophila wing. The flies were raised at two developmental temperatures (18°C and 28°C). Landmark-based geometric morphometrics was used to analyze the variation of the wing size and shape at different hierarchical levels: among genotypes and temperatures; among individuals within group; and fluctuating asymmetry (FA). Our results show that (1) the phenotypic effects of the mutations depend on temperature; (2) reciprocally, most mutations affect wing plasticity; (3) both temperature and mutations modify the levels of FA and of among individuals variation within lines. Remarkably, the patterns of shape FA seem unaffected by temperature whereas those associated with individual variation are systematically altered. By modifying the direction of available phenotypic variation, temperature might thus directly affect the potential for further evolution. It suggests as well that the developmental processes responsible for developmental stability and environmental canalization might be partially distinct.     

A DEVELOPMENTAL ANALYSIS OF AN EVOLUTIONARY TREND: DIGITAL REDUCTION IN AMPHIBIANS

In this study, we integrate information from phylogeny, comparative ontogeny, and experimental embryology in an attempt to elucidate the mechanisms controlling evolutionary trends towards digital reduction and loss observed in amphibians. Frogs and salamanders that have lost phalanges and even whole toes have done so in a very ordered manner, i.e., certain skeletal elements are lost prior to others. This pattern of morphological diversity is described and trends elucidated. It is concluded that the process is characterized by striking intraordinal convergences coupled with substantial differences between the trends observed in frogs as compared to urodeles. We argue that this pattern is essentially a reflection of the differences in the ontogenies of the two orders. Similarly, the convergences within urodeles and within anurans can be explained as the result of regulation of developmental parameters in a resilient developmental program. We further explore this hypothesis by experimentally perturbing the number of cells in the embryonic limb primordium to show that reduction in the number of mesenchymal cells secondarily affects the developmental process of pattern formation causing a rearrangement of the skeletal morphology of the foot. The same experimental manipulation has different effects in frogs as compared to salamanders. However, in both cases, the experimentally generated morphologies tend to parallel the phenotypes and trends observed in nature. Our conclusion is that most of the patterns of diversity in the digital morphology of amphibians can be explained as a reflection of developmental properties. In general, we present a methodology that attempts to empirically address the issue of identifying developmental constraint in morphological evolution.     

PLASTICITY OF THE LIFE CYCLE OF XEROPICTA DERBENTINA (KRYNICKI, 1836), A RECENTLY INTRODUCED SNAIL IN MEDITERRANEAN FRANCE

Xeropicta derbentina (Krynicki, 1836), a native of Eastern MediterraneanEurope, was introduced to southeastern France during the 1940sand is now widely spread across Provence. In summer it aggregateson plants, making its populations clearly visible. However,its life cycle within the Mediterranean basin is poorly documented.While X. derbentina in its native area exhibits an annual lifecycle, this species has been found in Provence to have a bienniallife cycle. Moreover, in southeastern France, field studieswithin a restricted area show variations in demographic structure.In consequence, the life cycle of X. derbentina and the demographicpatterns observed require clarification. Five populations withvarious demographic structures were studied over 1 year in thesame location, i.e. under the same climatic conditions. Thefield study was complemented by laboratory observations on mating,egg-laying and hatching. Xeropicta derbentina appears to bea semelparous species, with an annual life cycle being foundon four plots. The reproductive period begins at the end ofsummer and lasts until the beginning of winter. First egg-layingoccurs within 1 week after mating and lasts up to 30 days. Hatchingtakes place 15–20 days after egg-laying. Xeropicta derbentinapossesses multiple mating and egg-laying sessions, involvingsuccessive hatching. Populations are mainly characterized bytwo growth stages, the first in spring when newly-hatched snailsevolve into juveniles, and the second in late summer when theyreach maturity. However, on the highest density plot, a bienniallife cycle is observed for some newly-hatched snails that showan interrupted growth during summer and evolve into juvenilesonly in the second autumn. Moreover, this life cycle not onlyvaries among plots but also at a 1-year interval within plots.Hence, the life span of X. derbentina is between 12 and 20 months,but can be extended up to 30 months according to whether hatchingoccurs early or late and whether they survive the first andsecond winters. Xeropicta derbentina is thus able to have variousgrowth speeds and life spans, and appears to switch from anannual life cycle to a biennial cycle in response to populationdensity or climatic conditions. (Received 8 October 2004; accepted 15 December 2004)