Adaptation and constraint in the evolution of environmental sex determination

When environments differentially influence male and female performance, environmental sex determination (ESD) might evolve. The conclusion from several previous theoretical models was that reaction norms for sex determination should have a single, sharp threshold, with only females being produced in some environments and only males in others. These reaction norms can be disadvantageous in fluctuating environments, however, because they lead to sex-ratio fluctuations. We analysed the evolution of ESD, looking for equilibrium strategies in unconstrained as well as constrained strategy spaces. We identified situations where a single-threshold reaction norm is not evolutionarily stable. In these cases, we found stable strategies in the form of complex reaction norms, showing an oscillatory pattern of sex determination with respect to variation in an environmental variable. Considering that constraints could prevent such phenotypes from being realized, we found that certain randomized reaction norms, with probabilistic sex determination for a range of environments, would achieve nearly the same fitness. We also investigated reaction norms constrained to have a single threshold and found that genetic polymorphism in the environmental threshold value could evolve, producing a similar effect as a randomized reaction norm. We argue that the appearance of genetic variation can be regarded as an alternative outcome when constraints prevent the evolution of a more complex or a randomized strategy.     

The role of migration in the evolution of phenotypic switching

Stochastic switching is an example of phenotypic bet hedging, where an individual can switch between different phenotypic states in a fluctuating environment. Although the evolution of stochastic switching has been studied when the environment varies temporally, there has been little theoretical work on the evolution of phenotypic switching under both spatially and temporally fluctuating selection pressures. Here, we explore the interaction of temporal and spatial change in determining the evolutionary dynamics of phenotypic switching. We find that spatial variation in selection is important; when selection pressures are similar across space, migration can decrease the rate of switching, but when selection pressures differ spatially, increasing migration between demes can facilitate the evolution of higher rates of switching. These results may help explain the diverse array of non-genetic contributions to phenotypic variability and phenotypic inheritance observed in both wild and experimental populations.     

Melanic through nature or nurture: genetic polymorphism and phenotypic plasticity in Harmonia axyridis

Abstract Individuals can adapt to heterogeneity in their environment through either local adaptation or phenotypic plasticity. Colour forms of the ladybird Harmonia axyridis are a classic example of local adaptation, in which the frequency of melanic forms varies greatly between populations. In some populations, there are also large seasonal changes in allele frequency, with melanism being costly in summer and beneficial in winter. We report that the non‐melanic morph of H. axyridis dramatically increases its degree of melanization at cold temperatures. Furthermore, there is genetic variation in reaction norms, with different families responding to temperature in different ways. Variation at different spatial and temporal scales appears to have selected for either genetic or phenotypically plastic adaptations, which may be important in thermoregulation. As melanism is known to have a large effect on fitness in H. axyridis, this plasticity of melanization may have hastened its spread as an invasive species.     

Genetic differences and phenotypic plasticity as causes of variation in oviposition preference in Battus philenor

Summary Bradshaw (1965) proposed that phenotypic plasticity would be more common than adaptive genetic variability in species for which environmental fluctuations occur over periods roughly equal to that species' generation time. In an effort to examine this notion, sources of seasonal variation in two components of oviposition behavior in an east Texas population of pipevine swallowtail butterflies (Battus philenor) were investigated under natural and seminatural conditions. Variability in a visually-based prealighting component involving orientation to leaf shape was primarily due to phenotypic plasticity in the form of adult learning; no seasonally-based genotypic differences in leaf-shape discrimination behavior were observed. By contrast, a chemotactile post-alighting component involving elicitation of oviposition after landing on the host plant was not phenotypically plastic, i.e., not susceptible to learning. In addition, only slight and nonsignificant seasonally-based differences in post-alighting responses to different host species were observed.     

Egg size and the evolution of phenotypic plasticity in larvae of the echinoid genus Strongylocentrotus

Planktotrophic larvae grow by utilizing energy obtained from food gathered in the plankton. Morphological plasticity of feeding structures has been demonstrated in multiple phyla, in which food-limited larvae increase feeding structure size to increase feeding rates. However, before larvae can feed exogenously they depend largely on material contained within the egg to build larval structures and to fuel larval metabolism. Thus, the capacity for plasticity of feeding structures early in development may depend on egg size. Using the congeneric sea urchins Strongylocentrotus franciscanus and S. purpuratus, which differ in egg volume by 5-fold, I tested whether the degree of expression of feeding structure (larval arm length) plasticity is correlated with differences in the size of the egg. I experimentally manipulated egg size of S. franciscanus (the larger-egged species) by separating blastomeres at the 2-cell stage to produce half-sized larvae. I reared half-size and normal-size larvae under high and low food treatments for 20 days. I measured arm and body lengths at multiple ages during development and calculated the degree of plasticity expressed by larvae from all treatments. Control and unmanipulated S. franciscanus larvae (from ∼ 1.0 nl eggs) had significantly longer arms relative to body size and a significantly greater degree of plasticity than half-sized S. franciscanus larvae (from < 0.18 nl eggs), which in turn expressed a significantly greater degree of plasticity than S. purpuratus larvae (from ∼ 0.3 nl eggs). These results indicate that egg size affects larval arm length plasticity in the genus Strongylocentrotus; larger eggs produce more-plastic larvae both in an experimental and a comparative context. However, changes in egg size alone are not sufficient to account for evolved differences in the pattern of plasticity expressed by each species over time and may not be sufficient for the evolutionary transition from feeding to non-feeding.     

Constraints on the evolution of adaptive phenotypic plasticity in plants

The high potential fitness benefit of phenotypic plasticity tempts us to expect phenotypic plasticity as a frequent adaptation to environmental heterogeneity. Examples of proven adaptive plasticity in plants, however, are scarce and most plastic responses actually may be 'passive' rather than adaptive. This suggests that frequently requirements for the evolution of adaptive plasticity are not met or that such evolution is impeded by constraints. Here we outline requirements and potential constraints for the evolution of adaptive phenotypic plasticity, identify open questions, and propose new research approaches. Important open questions concern the genetic background of plasticity, genetic variation in plasticity, selection for plasticity in natural habitats, and the nature and occurrence of costs and limits of plasticity. Especially promising tools to address these questions are selection gradient analysis, meta-analysis of studies on genotype-by-environment interactions, QTL analysis, cDNA-microarray scanning and quantitative PCR to quantify gene expression, and two-dimensional gel electrophoresis to quantify protein expression. Studying plasticity along the pathway from gene expression to the phenotype and its relationship with fitness will help us to better understand why adaptive plasticity is not more universal, and to more realistically predict the evolution of plastic responses to environmental change.     

The evolution, maintenance and adaptive function of genetic colour polymorphism in birds

The hypothesis that ornaments can honestly signal quality only if their expression is condition-dependent has dominated the study of the evolution and function of colour traits. Much less interest has been devoted to the adaptive function of colour traits for which the expression is not, or is to a low extent, sensitive to body condition and the environment in which individuals live. The aim of the present paper is to review the current theoretical and empirical knowledge of the evolution, maintenance and adaptive function of colour plumage traits for which the expression is mainly under genetic control. The finding that in many bird species the inheritance of colour morphs follows the laws of Mendel indicates that genetic colour polymorphism is frequent. Polymorphism may have evolved or be maintained because each colour morph facilitates the exploitation of alternative ecological niches as suggested by the observation that individuals are not randomly distributed among habitats with respect to coloration. Consistent with the hypothesis that different colour morphs are linked to alternative strategies is the finding that in a majority of species polymorphism is associated with reproductive parameters, and behavioural, life-history and physiological traits. Experimental studies showed that such covariations can have a genetic basis. These observations suggest that colour polymorphism has an adaptive function. Aviary and field experiments demonstrated that colour polymorphism is used as a criterion in mate-choice decisions and dominance interactions confirming the claim that conspecifics assess each other's colour morphs. The factors favouring the evolution and maintenance of genetic variation in coloration are reviewed, but empirical data are virtually lacking to assess their importance. Although current theory predicts that only condition-dependent traits can signal quality, the present review shows that genetically inherited morphs can reveal the same qualities. The study of genetic colour polymorphism will provide important and original insights on the adaptive function of conspicuous traits.     

Environmental stress and the costs of whole-organism phenotypic plasticity in tadpoles

Costs of phenotypic plasticity are important for the evolution of plasticity because they prevent organisms from shaping themselves at will to match heterogeneous environments. These costs occur when plastic genotypes have relatively low fitness regardless of the trait value expressed. We report two experiments in which we measured selection on predator-induced plasticity in the behaviour and external morphology of frog tadpoles (Rana temporaria). We assessed costs under stressful and benign conditions, measured fitness as larval growth rate or competitive ability and focused analysis on aggregate measures of whole-organism plasticity. There was little convincing evidence for a cost of phenotypic plasticity in our experiments, and costs of canalization were nearly as frequent as costs of plasticity. Neither the magnitude of the cost nor the variation around the estimate (detectability) was sensitive to environmental stress.     

Environmental effects on adult growth patterns in the male sailfin molly,Poecilia latipinna (Poeciliidae)

Synopsis Widespread male body size variation in P. latipinna appears to be attributable to genetic variation in the size at maturation. The contribution of adult growth needs to be assessed because adult growth rates may vary with size at maturation and local environment. In our laboratory study we examined adult growth patterns as a function of size at maturation and juvenile experience (favorable or unfavorable conditions). In our field study we assessed adult growth as a function of initial size and environmental condition (using males in enclosures in contrasting habitats). Adult growth rates in the laboratory were an order of magnitude higher than rates observed in field enclosures. Growth rates varied with male size, increasing with increasing male size in the laboratory study but decreasing with increasing male size in the field study. The laboratory results alone would have cast considerable doubt on the ability to interpret size distributions of field-collected males, but the field results indicate that adult growth is sufficiently low that it can be ignored as a source of body size variation within and among populations.     

Plasticity of seed output in response to soil nutrients and density in Abutilon theophrasti: implications for maintenance of genetic variation

 Seed output is determined by two processes: resource acquisition and the allocation of resources to seeds. In order to clarify how the reaction norm of seed output is controlled by the phenotypic expression of its two components, we examined the genetic components of plasticity of seed dry mass, plant size, and reproductive allocation under different conditions of soil nutrient availability and conspecific competition among eight families of Abutilon theophrasti. Without competition, the reaction norm of seed mass of the families crossed between the lowest and other nutrient levels, although neither of its components, plant size and reproductive allocation, showed such a response. The crossing reaction norm (i.e., reversal of relative fitnesses of different genotypes along the environmental gradient) of seed mass resulted from (1) a trade-off between plant size and reproductive allocation, and (2) changes in the relative magnitude of genetic variances in plant size and reproductive allocation with soil nutrient availability. While allocation was more important in determining seed mass under limiting nutrient conditions, plant size became more important under high-nutrient conditions. There were no significant genetic variances in seed mass, plant size, and reproductive allocation in the competition treatment, except at the highest nutrient level. The results show that plant competition mitigated the effects of genetic differences in plant performance among the families. We discuss the results in relation to maintenance of genetic variation within a population. Received: 16 August 1996 / Accepted 26 April 1997     

Environmental effects on variation and covariation in reproductive traits of Western Bluebirds

Summary Environmental conditions can influence the expression and correlations of phenotypic traits. I studied phenotypic plasticity in reproductive traits of Western Bluebirds breeding in northern Arizona. Data collected over 4 years on two contrasting habitats identified significant spatial and temporal variation in bluebird reproduction. Clutch size was similar over different environmental conditions whereas timing of clutch initiation, percent fledging success, and frequency of second nest attempts were flexible. Correlations between traits varied widely—often changing sign—among samples from different years or habitats. Correlations of traits with reproductive success were also dependent on environmental conditions. Variation in traits reflected behavioral responses by nesting adults to differences in time for breeding and feeding conditions. Density of trees differed between habitats and had opposing effects on these environmental variables; breeding seasons were generally longer, but feeding rates to nestlings were lower on the more open habitat. Late Spring snows delayed reproduction and increased the importance of limited time for breeding; feeding conditions were more influential following a dry Spring. This and other studies illustrate that data on phenotypic plasticity are important when evaluating the ecological and evolutionary forces underlying life histories.     

Revisiting the homoiology hypothesis: the impact of phenotypic plasticity on the reconstruction of human population history from craniometric data

Homoiologies are homoplasies that are caused by nongenetic environmental factors. The homoiology hypothesis predicts that osseous regions subject to repeated biomechanical stress during growth should be more variable and, therefore, less reliable for the reconstruction of phylogeny compared with osseous regions relatively unaffected by stress. Previous studies based on the analysis of multiple primate species found that regions of the cranium subject to masticatory-induced stress were significantly more variable than non-masticatory regions, as predicted by the homoiology hypothesis. However, these studies also found that the masticatory regions were no less reliable for reconstructing primate phylogenetic relationships when subjected to parsimony analysis. It was suggested, therefore, that homoiology may be a more potent problem for the reconstruction of phylogeny at the intraspecific level rather than interspecific phylogenetics. This suggestion was tested here using matched molecular and craniometric data for 12 modern human populations. The results show that, as predicted by the homoiology hypothesis, regions of the human cranium related to mastication were more variable than non-masticatory regions. However, masticatory regions were no less reliable for inferring human population history. Therefore, the results match those found from the interspecific analysis of primate species and do not support the suggestion that homoiology is a greater problem for the analysis of intraspecific taxa. The results also suggest that within-taxon variability cannot be relied upon to predict the phylogenetic efficacy of morphometric characters.     

Reproductive system and pattern of genetic variation in two Limnanthes species

Summary Several populations of two species of the genus Limnanthes, (L. alba, an outbreeder and L. floccosa, an inbreeder) were examined with respect to variability of fifteen quantitative characters, allozyme variation at 11 loci, and response to different pollination conditions and moisture stress. Nearly equal amounts of phenotypic variability were found in the two species. L. alba had higher within-family variability than L. floccosa, but this result was highly heterogeneous among characters. A study of between- and within-population variance estimates did not reject the null hypothesis that L. alba and L. floccosa are similar with regard to the partitioning and amount of variability for quantitative characters. However, allozyme variation at 11 loci in a large number of populations showed L. alba to be highly polymorphic in contrast to the virtual monomorphism within L. floccosa populations. The average number of alleles per locus in L. alba and L. floccosa was 1.97 and 1.02, respectively, and on an average, L. alba and L. floccosa populations had 63% and 3% loci with polymorphism, respectively. Three groups of allozyme allelic combinations emerged which correlated well with the taxonomic delineation of allogamous L. alba, three semi-autogamous L. floccosa forms and two autogamous L. floccosa forms.All taxa showed a significant reduction in the seed output per plant due to moisture stress. L. alba suffered a further loss of fecundity under the paucity of pollinators, L. floccosa ssp. floccosa showed no significant effect from this factor, whereas L. floccosa ssp. grandiflora exhibited a curvilinear response which peaked at partial pollination and decreased to a lower level at full pollination.The geographic distribution of the two species with regard to the temperature and rainfall distribution did not suggest L. floccosa to be living in drier marginal areas. Patterns of variation in flowering time showed L. alba to be less variable than L. floccosa. Overall, there seemed to be little direct support for the thesis that inbreeding species originated from outcrossing taxa in marginal environments as a direct adaptation to a shortened growing season of xeric environments and to the lack of pollinators. Alternative hypotheses suggest that autogamy in L. floccosa might have evolved as a reproductive isolating barrier acting through either cleistogamy or divergence in flowering times.     

Habitat range and phenotypic variation in salt marsh plants

Ecologists have long speculated that species with wider environmental ranges would have broader ranges in phenotype; however, most tests of this hypothesis have involved small numbers of species and/or closely related taxa. We related phenotypic variation in twelve salt marsh plant species from six families to variation in four environmental variables using multiple regression. Within species, plant phenotype was predictably related to environmental variation. Salinity was the most common predictor of plant traits, followed by organic content, water content and elevation. Across species, regressions of single plant trait CVs on range (2 × SD) of single environmental variables were not significant and did not support the hypothesis that species occupying broad environmental ranges would have broad ranges in phenotypes. However, regression of a composite phenotypic PCA1 on a composite environmental PCA1 showed a marginally significant (P = 0.054). linear relationship for 10 species. Considering the different patterns of response across species, the lack of a relationship between variation in single phenotypic traits and single environmental variables is likely because the distantly-related taxa employed fundamentally different morphological and physiological strategies to respond to environmental stress gradients. The significant relationship between composite environmental and phenotypic variables reflects the complex nature of species phenotypic response to multivariate environmental gradients. Specifically, in this system, species increase variation in the number of leaves, but decrease variation in leaf size in response to an increase in range of salinity and decrease in range of water and organic content.     

The adaptive significance of an environmentally-cued developmental switch in an anuran tadpole

Summary This study investigated the proximate basis of bimodally-distributed, environmentally-induced variation that occurs in natural populations of spade-foot toad tadpoles (Scaphiopus multiplicatus). Most individuals in most populations occur as a small, slowly-developing omnivore morph. In some of these same populations, a varying number of individuals occur as a large, rapidly-developing carnivore morph (Pfennig 1989). Censuses of 37 different natural ponds revealed that the frequency of the faster-developing carnivore morph correlated significantly positively with fairy shrimp density (their chief prey) and pond drying rate. By simultaneously varying two diet components and pond drying regime in artificial pools I found that only fairy shrimp density significantly affected the proportion of carnivores. Separate experiments established that the extent to which tadpoles developed the carnivore morphology correlated with shrimp density, and that morph determination depended on the ingestion of shrimp, not simply their presence. If a critical number of shrimp were ingested, the tadpole developed into a carnivore; if not, the tadpole developed by default into an omnivore. Thus a single cue — shrimp ingestion — triggers alternative ontogenetic trajectories. Using shrimp density to induce morph differentiation enables tadpoles to respond to their environment adaptively as shrimp are most abundant in highly ephemeral ponds, where the faster developing carnivores are favored.     

Selection in a fluctuating environment leads to decreased genetic variation and facilitates the evolution of phenotypic plasticity

Changes in the environment are expected to induce changes in the quantitative genetic variation, which influences the ability of a population to adapt to environmental change. Furthermore, environmental changes are not constant in time, but fluctuate. Here, we investigate the effect of rapid, continuous and/or fluctuating temperature changes in the seed beetle Callosobruchus maculatus, using an evolution experiment followed by a split-brood experiment. In line with expectations, individuals responded in a plastic way and had an overall higher potential to respond to selection after a rapid change in the environment. After selection in an environment with increasing temperature, plasticity remained unchanged (or decreased) and environmental variation decreased, especially when fluctuations were added; these results were unexpected. As expected, the genetic variation decreased after fluctuating selection. Our results suggest that fluctuations in the environment have major impact on the response of a population to environmental change; in a highly variable environment with low predictability, a plastic response might not be beneficial and the response is genetically and environmentally canalized resulting in a low potential to respond to selection and low environmental sensitivity. Interestingly, we found greater variation for phenotypic plasticity after selection, suggesting that the potential for plasticity to evolve is facilitated after exposure to environmental fluctuations. Our study highlights that environmental fluctuations should be considered when investigating the response of a population to environmental change.     

Larval feeding structure plasticity during pre-feeding stages of echinoids: Not all species respond to the same cues

Much of the work on phenotypic plasticity has focused on inducible defenses. As a result, little is known about induced phenotypes that improve the acquisition of resources (i.e. inducible offenses). Feeding larvae of several marine invertebrate species, gastropods and echinoderms, have inducible offenses, and produce larger feeding structures when given less food. To better understand inducible offenses, I investigated when in development sea urchin and sand dollar larvae can first alter their feeding morphology in response to different concentrations of food. Food induced feeding structure changes in both sea urchin and sand dollar larvae before larvae were able to ingest food. This suggests that the nervous system and a regulator gene, orthopedia, play a mechanistic role. In addition, larvae of the two species, Strongylocentrotus purpuratus and Dendraster excentricus, responded to different cues. Pre-feeding larvae of both species developed relatively shorter arms when given algal cells (i.e. chemical and physical stimuli), whereas only pre-feeding larvae of D. excentricus developed shorter arms when exposed to algal exudates (i.e. chemical stimuli). Larvae of neither species responded morphologically to the presence of polystyrene beads (i.e. physical stimuli).     

Within-population variability in morphology and life history of Plantago major L. ssp. pleiosperma Pilger in relation to environmental heterogeneity

Summary An attempt was made to relate variation in life-history characteristics within a population of Plantago major ssp. pleiosperma to small-scale environmental variability. At a beach plain, embanked in 1966, a mosaic environment was distinguished with spatial variability in vegetation structure as well as in nutrient availability and water content of the soil. Differences between three subsites in comtemporary selection were demonstrated, e.g. in shoot morphology and allocation to reproductive tissue. The effects of nutrient supply and waterlogging on morphology and life history were studied on lines from the three subsites in a greenhouse. For most of the traits high levels of phenotypic plasticity were observed, covering almost entirely the observed phenotypic variability at the beach plain. In all treatments lines from the shrubs had, however, a higher leaf-area ratio as well as delayed flowering when compared to lines from more open subsites. In addition, in a reciprocal transplant experiment it was demonstrated that lines from the shrubs had larger shoots with e.g. broader leaves in the shady environment of the shrubs than other lines.From the experiments no indications were obtained that lines from any subsite were especially adapted to specific levels of nutrient supply or water content of the soil. With respect to these environmental factors P. major ssp. pleisoperma might occur and reproduce at all subsites by means of phenotypic plasticity, e.g. in plant form. However, it is suggested that spatial variability in vegetation structure caused a population subdivision in allocation patterns, leaf form and life history at the beach plain, over distances of about 15–25 m. This differentation occurred during primary succession over a period of twenty years.