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Predator-induced phenotypic plasticity in tadpoles: extension or innovation?

Phenotypic plasticity, the ability of a trait to change as a function of the environment, is central to many ideas in evolutionary biology. A special case of phenotypic plasticity observed in many organisms is mediated by their natural predators. Here, we used a predator-prey system of dragonfly larvae and tadpoles to determine if predator-mediated phenotypic plasticity provides a novel way of surviving in the presence of predators (an innovation) or if it represents a simple extension of the way noninduced tadpoles survive predation. Tadpoles of Limnodynastes peronii were raised in the presence and absence of predation, which then entered a survival experiment. Induced morphological traits, primarily tail height and tail muscle height, were found to be under selection, indicating that predator-mediated phenotypic plasticity may be adaptive. Although predator-induced animals survived better, the multivariate linear selection gradients were similar between the two tadpole groups, suggesting that predator-mediated phenotypic plasticity is an extension of existing survival strategies. In addition, nonlinear selection gradients indicated a cost of predator-induced plasticity that may limit the ability of phenotypic plasticity to enhance survival in the presence of predators.

Animals↗

Physiology of BDNF: focus on hypothalamic function.

Brain-derived neurotrophic factor (BDNF) belongs to the neurotrophin family which interacts with high-affinity protein kinase receptors (Trk) and the unselective p75(NGFR) receptor. The BDNF gene has a complex structure with multiple regulatory elements and four promoters that are differentially expressed in central or peripheral tissue. BDNF expression is regulated by neuronal activity or peripheral hormones. Neurotrophins regulate the survival and differentiation of neurons during development but growing evidence indicates that they are also involved in several functions in adulthood, including plasticity processes. BDNF expression in the central nervous system (CNS) is modified by various kinds of brain insult (stress, ischemia, seizure activity, hypoglycemia, etc.) and alterations in its expression may contribute to some pathologies such as depression, epilepsy, Alzheimer's, and Parkinson's disease. Apart from very traumatic situations, the brain functioning is resilient to stress and capable of adaptive plasticity. Neurotrophins might act as plasticity mediators enhancing this trait which seems to be crucial in adaptive processes. In addition to documenting all of the topics mentioned above in the CNS, we review the state of the art concerning neurotrophins and their receptors, including our personal contribution which is essentially focused on the stress response.

Animals↗

Life history and the competitive environment: trajectories of growth, maturation, and reproductive output among chacma baboons.

The social environment is a key feature influencing primate life histories. Chacma baboons (Papio hamadryas ursinus) are a female-bonded species with a strict linear dominance hierarchy. In this species, the allocation of energy to competing demands of growth and reproduction is hypothesized to vary as a function of competitive ability, which in turn increases with social rank. Since growth rate is a major component of life history models, measures of age-specific growth were used to analyze variation in life history traits across social ranks. Weights of 42 immature baboons were obtained without sedation or baiting from a troop of well-habituated chacma baboons in the Okavango Delta, Botswana. Using demographic and weight data from this wild population, five main findings emerged: 1) Weight for age and growth rate of infant and juvenile females are positively associated with maternal rank. 2) Male growth is not influenced by maternal rank. 3) Female growth shows smaller variation across feeding conditions than male growth. 4) Low-ranking adult females continue investment in offspring through prolonged lactation until they reach a weight comparable to that of high-ranking infants. 5) The benefit of rank to reproductive success shown in this study is 0.83 additional offspring. Reproductive span determined predominantly by age at maturation contributes 27-38% to the difference in expected number of offspring by rank, vs. 62-73% due to reproductive rate. These findings have major implications for understanding the role of social environment in phenotypic plasticity of life history traits, and in the evolution of primate life histories.

Animals↗

Myelin mosaicism and brain plasticity in heterozygous females of a canine X-linked trait.

The shaking (sh) pup, an animal model of Pelizaeus-Merzbacher disease, is characterized by severe central nervous system dysmyelination in affected males, and myelin mosaicism in some female heterozygotes as a result of X-linked inactivation. Heterozygous females develop a tremor of varying severity that usually disappears at 4 to 6 weeks, whereas male hemizygotes have severe, generalized tremor that persists throughout life. We have used these two myelin-deficient models to study the potential for recovery with time as reflected by brainstem auditory evoked responses (BAERs). At set time points, the state of myelination in the trapezoid body was studied microscopically. Sequential BAERs demonstrated consistently prolonged interpeak latencies during the period of gross tremor in heterozygotes, with the trend continuing to a lesser extent after tremor cessation. The random nature of X-linked inactivation resulted in variable myelin mosaicism that was reflected in variations in BAER changes within animals in the same litter. In most heterozygotes, the tremor resolved with time, the BAERs returned to near normal, and myelin mosaicism was lost. In contrast, in the affected males, the severity of tremor and lack of recovery was demonstrated by consistent abnormalities in BAER waves at all times studied, and severe and persistent myelin deficiency in the trapezoid body. These findings show that despite the normal tightly programmed temporal development of myelin in the brain in the heterozygous mosaic state, sufficient plasticity persists during the neonatal period for late-stage myelination to occur.

Animals↗

Phenotypic lability and the evolution of predator-induced plasticity in tadpoles.

The hypothesis that predator-induced defenses in anuran larvae are maintained by divergent selection across multiple predation environments has not been fully supported by empirical results. One reason may be that traits that respond slowly to environmental variation experience a fitness cost not incorporated in the standard adaptive model, due to a time lag between detecting the state of the environment and expressing the phenotypic response. I measured the rate at which behavior and morphology of Rana temporaria tadpoles change when confronted with a switch in the predation environment at two points in development. Hatchling tadpoles that had been exposed during the egg stage to Aeshna dragonfly larvae were not phenotypically different from those exposed as eggs to predator-free conditions, and both responded similarly to post-hatching predator treatments. When 25-day-old tadpoles from treatments with and without dragonflies were subjected to a switch in the environment, their activity budgets reversed completely within 24-36 h, and their body and tail shape began changing significantly within 4 days. The behavioral response was conservative: Tadpoles switched from high-risk to predator-free treatments were slower to adjust their activity. The study confirmed that behavioral traits are relatively labile and exhibit strong plasticity, but it did not reveal such a pattern at the level of individual traits: Morphological traits that developed slowly did not show the least plasticity. Thus, I found that differences in lability of traits were useful for predicting the magnitude of plasticity only for fundamentally different kinds of characters.

Aging↗

Genotypic variation in drought response of silver birch (Betula pendula): leaf water status and carbon gain.

To assess genotypic variation in drought response of silver birch (Betula pendula Roth), we studied the plasticity of 16 physiological traits in response to a 12-14-week summer drought imposed on four clones in two consecutive years. In a common garden experiment, 1-year-old clonal trees from regions with low (550 mm year(-1)) to high rainfall (1270 mm year(-1)) were grown in 45-l pots, and leaf gas exchange parameters, leaf water potentials, leaf osmotic potentials and leaf carbon isotope signatures were repeatedly measured. There were no clonal differences in leaf water potential, but stomatal conductance (gs), net photosynthesis at ambient carbon dioxide concentration, photosynthetic water-use efficiency, leaf carbon isotope composition (delta13C) and leaf osmotic potentials at saturation (Pi0) and at incipient plasmolysis (Pip) were markedly influenced by genotype, especially gs and osmotic adjustment. Genotypes of low-rainfall origin displayed larger osmotic adjustment than genotypes of high-rainfall origin, although their Pi0 and Pip values were similar or higher with ample water supply. Genotypes of low-rainfall origin had higher gs than genotypes of high-rainfall origin under both ample and limited water supply, indicating a higher water consumption that might increase competitiveness in drought-prone habitats. Although most parameters tested were significantly influenced by genotype and treatment, the genotype x treatment interactions were not significant. The genotypes differed in plasticity of the tested parameters and in their apparent adaptation to drought; however, among genotypes, physiological plasticity and drought adaptation were not related to each other. Reduction of gs was the first and most plastic response to drought in all genotypes, and allowed the maintenance of high predawn leaf water potentials during the drought. None of the clones exhibited non-stomatal limitation of photosynthesis. Leaf gs, photosynthetic capacity, magnitude of osmotic adjustment and delta13C were all markedly lower in 2000 than in 1999, indicating root limitation in the containers in the second year.

Betula↗

Inheritance of an oviposition behavior by an egg parasitoid.

A quantitative genetic study revealed genetic and environmental sources of variance in percentage parasitism of European corn borer egg masses and secondary sex ratios by Trichogramma nubilale. Full and half-sib groups of T. nubilale were obtained from a nested mating design, which permitted the partitioning of the variance of T. nubilale parasitism of European corn borer egg masses into additive genetic variance, maternal/dominant variance and environmental variance. A mother-daughter regression of the percentage of an egg mass parasitized allowed a determination of the direction of a potential response to selection in the event of maternal effects. No or very little additive genetic effects were associated with the percentage of eggs within a mass parasitized and secondary sex ratios, but a significant amount of the variance for both traits had a maternal and/or dominant genetic source. The relationship between mothers and daughters in egg mass parasitism was positive, and 55.4% of the progeny of a given mother had behaviors that resemble their mother. Most of the variance had an environmental and/or unknown genetic source implying potentially high phenotypic plasticity associated with all these traits. The presence of maternal effects and phenotypic plasticity could have multiple and complex effects on progeny characters and potential responses to selection.

Animals↗

Rapid temporal change in the expression and age-related information content of a sexually selected trait.

The expression of sexual signals is often phenotypically plastic and also evolves rapidly. Few studies have considered the possibility that proximate determination -- the pathway between genes and trait expression -- may also be subject to both phenotypic plasticity and evolutionary change. We examined long-term patterns in size, condition- and age-dependence, repeatability and heritability of forehead patch size, a sexually selected plumage trait in male collared flycatchers. We also estimated survival and sexual selection on the phenotypic value of the trait. Forehead patch size linearly declined during the 15 years, probably due to the significantly negative survival selection. In addition, the expression of genetic variation for the ornament apparently underwent an age-limited change, which implies a change in the information content of the signal to receivers. The persistent lack of condition-dependence makes phenotypic plasticity an unlikely explanation to our results. This raises the possibility of a microevolutionary change of both expression and proximate determination during the study period.

Age Factors↗

Phenotypic plasticity of reproductive effort in a colonial ascidian, Botryllus schlosseri.

Phenotypic plasticity is the capability of a genotype to produce different phenotypes in different environments. Previous studies have indicated phenotypic variability in asexual, male, and female reproduction in Botryllus schlosseri, a hermaphroditic, colonial ascidian, but not explicitly tested for genotype by environment interactions that indicate genetic variation in plastic responses. Consequently, clones derived from an estuarine population were deployed at their native site and a warmer, higher productivity site 10 km up-river. Male reproduction was assayed by testis size, female reproduction by the number of eggs produced, and asexual reproduction by colony growth rate. To test for ontogenetic effects, data were collected from two different generations of zooids born in the field. Analyses of variance indicated plasticity in asexual and female reproduction during the first zooid generation and plasticity in all three traits during the third zooid generation. Reaction norms varied significantly among genotypes in direction and magnitude for asexual reproduction at both times, implying that selection on asexual reproduction is weak. Sperm production during the third zooid generation was significantly lower at the nonnative site, but there was no genotype by environment interaction. The reaction norms for female reproduction varied significantly among genotypes in direction and magnitude during the first zooid generation, but only varied in magnitude during the third generation, with egg production being higher in all genotypes at the nonnative site. Comparisons of weighted frequency distributions between sites demonstrated that differences in egg production in the third generation were due to increases in the proportion of reproductive zooids within a colony. The greater emphasis on female reproduction at a site associated with higher food availability and temperature, and the greater emphasis on male reproduction at a colder, food-limited site, supports predictions from sex allocation theory.

Adaptation, Physiological↗

Molecular basis of evolutionary adaptation at the lactate dehydrogenase-B locus in the fish Fundulus heteroclitus.

At the extremes of its natural distribution, populations of the common killifish Fundulus heteroclitus experience a difference of more than 15 degrees C in mean annual temperature. These populations are virtually fixed for two different codominant alleles at the heart-type lactate dehydrogenase locus (Ldh-B) which code for allozymes with different and adaptive kinetic responses to temperature. Two populations near the extremes of the species range (i.e., Maine and Georgia) were further studied for thermal adaptation at this locus. In the absence of any kinetic differences one would predict that to maintain a constant reaction velocity, 2 to 3 times as much enzyme would be required for each 10 degrees C decrease in environmental temperature. Consistent with this adaptive strategy and in addition to the adaptive kinetic characteristics, the LDH-B4 enzyme (EC 1.1.1.27) concentration and its mRNA concentration were approximately twice as great in the northern population as in the southern population. Acclimation experiments allow us to conclude that these differences are due to a combination of fixed genetic traits (evolutionary adaptation) and plastic responses to temperature (physiological acclimation). Furthermore, our calculations show that the LDH-B4 reaction velocities are essentially equivalent for these two populations, even though they live in significantly different thermal environments.

Adaptation, Physiological↗

Cyclic variation in seasonal recruitment and the evolution of the seasonal decline in Ural owl clutch size.

Plastic life-history traits can be viewed as adaptive responses to environmental conditions, described by a reaction norm. In birds, the decline in clutch size with advancing laying date has been viewed as a reaction norm in response to the parent's own (somatic or local environmental) condition and the seasonal decline in its offspring's reproductive value. Theory predicts that differences in the seasonal recruitment are mirrored in the seasonal decrease in clutch size. We tested this prediction in the Ural owl. The owl's main prey, voles, show a cycle of low, increase and peak phases. Recruitment probability had a humped distribution in both increase and peak phases. Average recruitment probability was two to three times higher in the increase phase and declined faster in the latter part of the season when compared with the peak phase. Clutch size decreased twice as steep in the peak (0.1 eggs day-1) as in the increase phase (0.05 eggs day-1). This result appears to refute theoretical predictions of seasonal clutch size declines. However, a re-examination of current theory shows that the predictions of modelling are less robust to details of seasonal condition accumulation in birds than originally thought. The observed pattern can be predicted, assuming specifically shaped seasonal increases in condition across individuals.

Adaptation, Physiological↗

Evolution of development in the sea star genus Patiriella: clade-specific alterations in cleavage.

Examination of early development in five species of the Patiriella sea star species complex indicates that the ancestral-type radial holoblastic cleavage (Type I) is characteristic of P. regularis and P. exigua, whereas cleavage in species from the calcar clade followed multiple alternatives (Types II-IV) from holoblastic to meroblastic. Considering that invariant radial cleavage is thought to play a role in embryonic axis formation in echinoderms, we documented the details of blastomere formation in Patiriella sp. and followed development of the embryos. In Type II cleavage, the first and second cleavage planes appeared simultaneously at one pole of the embryo, dividing it directly into four equally sized blastomeres. In Type III cleavage, the first and second cleavage planes appeared simultaneously, followed promptly by the third cleavage plane, dividing the embryo directly into eight equally sized blastomeres. In Type IV cleavage, numerous furrows appeared simultaneously at one end of the embryo, dividing it into 32-40 equally sized blastomeres. Confocal sections revealed that embryos with cleavage Types II-IV were initially syncytial. The timing of karyokinesis in embryos with Types II and III cleavage was similar to that seen in clutch mates with Type I cleavage. Karyokinesis in embryos with Type IV cleavage, however, differed in timing compared with Type I clutch mates. Alteration in cleavage was not associated with polarized distribution of maternally provided nutrients. For each cleavage type, development was normal to the competent larval stage. Although variable blastomere configuration in the calcar clade may be linked to possession of a lecithotrophic development, other Patiriella species with this mode of development have typical cleavage. The presence of variable cleavage in all calcar clade species indicates that phylogenetic history has played a role in the distribution of this embryonic trait in Patiriella. The plasticity in early cleavage in these sea stars indicates that this aspect of early development is not constrained against change and that there are many ways to achieve multicellularity.

Animals↗

Assortative mating as a mechanism for rapid evolution of a migratory divide.

There have been numerous recent observations of changes in the behavior and dynamics of migratory bird populations, but the plasticity of the migratory trait and our inability to track small animals over large distances have hindered investigation of the mechanisms behind migratory change. We used habitat-specific stable isotope signatures to show that recently evolved allopatric wintering populations of European blackcaps Sylvia atricapilla pair assortatively on their sympatric breeding grounds. Birds wintering further north also produce larger clutches and fledge more young. These findings describe an important process in the evolution of migratory divides, new migration routes, and wintering quarters. Temporal segregation of breeding is a way in which subpopulations of vertebrates may become isolated in sympatry.

Animal Migration↗

The Multiple Roles of Genetics on Freshwater Macrophyte Functional Traits in the Interplay With the Environment: A Review.

The study of functional trait variation is increasingly used to understand macrophyte adaptation, as traits reflect organismal performance under different ecosystem conditions. Phenotypic expression results from the interplay of genetic and environmental factors: genetics provides the molecular basis for heritable traits and constrains potential phenotypes, while the environment acts as a selective and modulatory force. However, the genetic insight into traits has rarely been addressed in freshwater macrophyte studies. This review examines the different ways in which the DNA of macrophytes interplays with the environment and contributes to the variation in their functional traits, outlining main approaches, gaps, and future challenges. Only 21 studies explicitly combined genetics with functional traits and environment in the last fifteen years. The most common approach was the use of common garden experiments to explore acclimation and adaptation in a few model species. Current studies mainly focus on morphological and growth traits that best describe macrophytes' economic strategies, with limited attention to other trait categories, while the genetic and DNA traits studied are more variable. Across studies, environmental factors generally explained a larger proportion of functional trait variation, highlighting the dominant role of phenotypic plasticity for macrophyte acclimatation, whereas genetic contribution increased under experimentally manipulated conditions. Genome size and epigenetic variation influenced phenotypic plasticity; however, the effect was different and inconsistent on traits and depended on phylogenetic relationships and geographical environment variation. In field studies of natural populations, life history traits and hydrology had a strong effect on the geographic distribution of genetic diversity and the response to selection, as well as on our ability to distinguish selection from genetic drift. Future research should enhance molecular analyses, adopt multifactorial and long-term experimental designs, develop conceptual frameworks to address the relationships between genomics, environment and functional traits and integrate emerging tools to capture macrophyte adaptation better.

adaptation↗

Mapping of QTLs for lateral root branching and length in maize (Zea mays L.) under differential phosphorus supply.

Low phosphorus availability is a primary constraint for plant growth in terrestrial ecosystems. Lateral root initiation and elongation may play an important role in the uptake of immobile nutrients such as phosphorus by increasing soil exploration and phosphorus acquisition. The objective of this study was to identify quantitative trait loci (QTLs) controlling lateral root length (LRL), number (LRN), and plasticity of the primary seedling root of maize under varying phosphorus availability. Using a cigar roll culture in a controlled environment, we evaluated primary root LRL and LRN at low and high phosphorus availability in 160 recombinant inbred lines (RILs) derived from a cross between maize genotypes B73 and Mo17, which have contrasting adaptation to low phosphorus availability in the field. Low phosphorus availability increased LRL by 19% in Mo17, the phosphorus-efficient parent, but significantly decreased LRL in B73, the phosphorus-inefficient genotype. Substantial genetic variation and transgressive segregation for LRL and LRN existed in the population. The plasticity of LRL ranged from -100% to 146.3%, with a mean of 30.4%, and the plasticity of LRN ranged from -82.2% to 164.1%, with a mean of 18.5%. On the basis of composite interval mapping with a LOD threshold of 3.27, one QTL was associated with LRN plasticity, five QTLs were associated with LRL and one QTL was associated with LRN under high fertility. Under low fertility, six QTLs were associated with LRL and one QTL with LRN. No QTLs were detected for plasticity of LRL. A number of RILs exceeded Mo17, the phosphorus-efficient parent, for LRL, LRN, and plasticity. The detection of QTLs for these traits, in combination with the observation of transgressive segregants in our population, indicates that favorable alleles can be combined to increase seedling lateral root growth in maize.

Breeding↗

Constraints on plastic responses to climate variation in red deer.

Influences of climate on life history traits in natural populations are well documented. However, the implications of between-individual variation in phenotypic plasticity underlying observed trait-environment relationships are rarely considered due to the large, long-term datasets required for such analysis. Studies typically present correlations of annual trait means with climate or assume that individual phenotypic responses are constant. Here, we examine this additional level of variation and show that, in a red deer population on the Isle of Rum, Scotland, changes in climate generate changes in phenotype only amongst individuals who have experienced favourable ecological conditions. Examination of relationships between offspring birth weight and spring temperature within the lifetimes of individual females revealed that the tendency to respond to climate declined as the population density experienced early in life increased. The presence of such systematic variation in individual plasticity is rarely documented in the wild, and has important implications for our understanding of the environmental dependencies of traits under varying ecological conditions.

Acclimatization↗

Growth temperature and reaction norms of morphometrical traits in a tropical drosophilid: Zaprionus indianus.

Ten isofemale lines of Zaprionus indianus were analysed to study the reaction norms of five morphometrical traits (wing and thorax length, body weight, sternopleural bristle and ovariole number) in relation to growth temperature. All these traits exhibited nonlinear concave reaction norms and were characterized by the coordinates of their maximum: MV (maximum value), and TMV (temperature of maximum value). Wing/thorax ratio, which is related to flight capacity, was also calculated and exhibited a monotonically decreasing reaction norm. Intraclass correlations were on average quite low, with no significant differences between traits, temperature or sex; a highly significant trait-temperature interaction was, however, observed. Sex dimorphism was very low in Zaprionus, contrasting with data previously obtained in other species. MVs among lines were positively correlated for the three size-related traits, whereas sternopleural bristle and ovariole number were genetically independent. TMVs were different between the traits, but higher than in D. melanogaster and other cold-adapted species, in agreement with the hypothesis that the norm shape evolves according to species thermal adaptation. MVs and TMVs were never correlated, indicating that mean values and plasticity are genetically independent. Some positive correlations were observed among TMVs of different traits, suggesting that the same genetic system might regulate plasticity of different traits.

Animals↗

Individual and combined effects of Ca/Mg ratio and water on trait expression in Mimulus guttatus.

Low Ca/Mg ratios (a defining component of serpentine soils) and low water environmental conditions often co-occur in nature and are thought to exert strong selection pressures on natural populations. However, few studies test the individual and combined effects of these environmental factors. We investigated the effects of low Ca/Mg ratio and low water availability on plant leaf, stem, stolon, and floral traits of Mimulus guttatus, a bodenvag species, i.e., a species that occurs in serpentine and non-serpentine areas. We quantified genetic variation and genetic variation for plasticity for these leaf, stem, stolon, and floral traits at three hierarchical levels: field-habitat type, population, and family, and we evaluated the relative importance of local adaptation and plasticity. We chose two populations and 10 families per population from four distinct field "habitat types" in northern California: high Ca/Mg ratio (non-serpentine) and season-long water availability, high Ca/Mg ratio and seasonally drying, low Ca/Mg ratio (serpentine) and season-long water availability, and low Ca/Mg ratio and seasonally drying. Seedlings were planted into greenhouse treatments that mimicked the four field conditions. We only detected genetic variation for stem diameter and length of longest leaf at the field-habitat level, but we detected genetic variation at the family level for nearly all traits. Soil chemistry and water availability had strong phenotypic effects, alone and in combination. Our hypothesis of an association between responses to low water levels and low Ca/Mg ratio was upheld for length of longest leaf, stem diameter, corolla width, and total number of reproductive units, whereas for other traits, responses to Ca/Mg ratio and low water were clearly independent. Our results suggest that traits may evolve independently from Ca/Mg ratios and water availability and that our focal traits were not simple alternative measures of vigor. We found genetic variation for plasticity both at the field-habitat type and family levels for half of the traits studied. Phenotypic plasticity and genetic variation for plasticity appear to be more important than local adaptation in the success of these M. guttatus populations found across a heterogeneous landscape in northern California. Phenotypic plasticity is an important mechanism maintaining the broad ecological breadth of native populations of M. guttatus.

Adaptation, Physiological↗