GEOGRAPHIC VARIATION AND PHENOTYPIC PLASTICITY OF NUMBER OF TRUNK VERTEBRAE IN SLENDER SALAMANDERS,BATRACHOSEPS (CAUDATA: PLETHODONTIDAE)

To understand the evolutionary significance of geographic variation, one must identify the factors that generate phenotypic differences among populations. I examined the causes of geographic variation in and evolutionary history of number of trunk vertebrae in slender salamanders, Batrachoseps (Caudata: Plethodontidae). Number of trunk vertebrae varies at many taxonomic levels within Batrachoseps. Parallel clines in number occur along an environmental gradient in three lineages in the Coast Ranges of California. These parallel clines may signal either adaptation or a shared phenotypically plastic response to the environmental gradient. By raising eggs from 10 populations representing four species of Batrachoseps, I demonstrated that number of trunk vertebrae can be altered by the developmental temperature; however, the degree of plasticity is insufficient to account for geographic variation. Thus, the geographic variation results largely from genetic variation. Number of trunk vertebrae covaries with body size and shape in diverse vertebrate taxa, including Batrachoseps. I hypothesize that selection for different degrees of elongation, possibly related to fossoriality, has led to the extensive evolution of number of trunk vertebrae in Batrachoseps. Analysis of intrapopulational variation revealed sexual dimorphism in both body shape and number of trunk vertebrae, but no correlation between these variables in either sex. Females are more elongate than males, a pattern that has been attributed to fecundity selection in other taxa. Patterns of covariation among different classes of vertebrae suggest that some intrapopulational variation in number results from changes in vertebral identity rather than changes in segmentation.     

PHENOTYPIC PLASTICITY IN POLYGONUM PERSICARIA. II. NORMS OF REACTION TO SOIL MOISTURE AND THE MAINTENANCE OF GENETIC DIVERSITY

Adaptive phenotypic plasticity is the predicted evolutionary response to fine-grained fluctuation in major environmental factors, such as soil moisture in plant habitats. This study examines genotypes from two natural populations of Polygonum persicaria, one from a relatively homogeneous, moderately moist site, and one from a site in which severe drought and root flooding occur within single growth seasons. Norms of reaction (phenotypic response curves) were determined for a random sample of eight and ten cloned genotypes, respectively, from each of the populations over a controlled moisture gradient ranging from drought to flooding.     

GENETIC VARIATION AND POLYMORPHISM IN THE INDUCIBLE SPINES OF A MARINE BRYOZOAN

Of particular value in understanding the evolution of genotypes with broad phenotypic ranges (phenotypic plasticity) are the few examples of organisms with adaptive plasticity, such as those that develop a defensive morphology in response to cues from predators. We know little about the heritability of inducible defensive characters or the range of phenotypes available for selection to act on in the field. Membranipora membranacea is a colonial marine bryozoan that produces spines within two days of exposure to waterborne predator extracts. Surveys done in 1993 and 1995 showed that the population at Friday Harbor Labs, Washington, was polymorphic for inducible spine type and was composed of a constitutively spined type that produced spines in the absence of a predator stimulus, an unspined phenotype that did not produce spines irrespective of a stimulus, and an inducibly spined phenotype that would produce spines if exposed to the appropriate cue. In 1995, the frequencies of these types were determined through a laboratory common-garden experiment; 178 colonies were cultured from metamorphosis through approximately 30 days and then exposed to the cue. The inducible type was the dominant, comprising 80.3% of the population. The constitutive type made up 6.2% of the population, and the remaining 13.4 % was the unspined type. The frequency of the three types was similar to a preliminary trial of the experiment run in 1993. Experiments also showed that the lengths of the spines of the inducible type varied continuously among genotypes. To assess causes of variation in the inducible spine response and its clonal heritability, 16 clones were subdivided and grown in a common environment and exposed to a single dosage of spine inducing substance (SIS). Spine length showed high clonal heritability. The range of colony responses from a single environment varied from relatively unresponsive to highly responsive colonies with a very low threshold of response. Norms of reaction were quantified for spine lengths of inducible genotypes originating from two field environments by testing them in a concentration series of SIS. Both spine length and spine type varied with concentration of inducer. Within a clone, colonies were more likely to produce membranous spines than corner spines at higher concentrations. At low concentrations, only straight spines were produced. This study showed that populations of M. membranacea at Friday Harbor are a mix of inducible, nonspined and constitutively spined individuals. Even the inducible individuals showed high heritable variation in the length of spine activated, suggesting that there is considerable scope for the evolution of this character. A norm-of-reaction experiment further showed that the type of spine produced, membranous or corner, varied with the concentration of the cue. Factors maintaining the polymorphism and the broad range of genotypes could include high costs of defending the spined types coupled with a shifting biotic regime.     

ADAPTIVE GENETIC VARIATION IN GROWTH AND DEVELOPMENT OF TADPOLES OF THE HYBRIDOGENETIC RANA ESCULENTA COMPLEX

The distribution and proportion of the sexual species Rana lessonae to the hemiclonal hybrid R. esculenta among natural habitats suggests that these anurans may differ in adaptive abilities. I used a half-sib design to partition phenotypic and quantitative genetic variation in tadpole responses at two food levels into causal variance components. Rana lessonae displays strong phenotypic variation across food levels. Growth rate is strictly determined by environmental factors and includes weak maternal effects. Larval period and body size at metamorphosis both contain moderate levels of additive genetic variance. The sire x food interactions and the lack of environmental correlations indicate that adaptive phenotypic plasticity is present in both of these traits. In contrast, R. esculenta displays less phenotypic variation across food levels, especially for larval period. Variation in body size at metamorphosis is underlain by genetic variation as shown by high levels of additive genetic variance, yet growth rate and larval period are not. Significant environmental correlations between larval period at high food level and growth, larval period, and body size at low food, indicate phenotypic plasticity is absent. A positive phenotypic correlation between body size at metamorphosis and larval period for R. lessonae at both food levels suggests a trade-off between growing large and metamorphosing quickly to escape predation or pond drying. The lack of a similar correlation for R. esculenta at the high food level suggests it may be less constrained. Different levels of adaptive genetic variation among larval traits suggest that the sexual species and the hybridogenetic hemiclone differ in their abilities to cope with temporally and spatially heterogeneous environments.     

ADAPTIVE PHENOTYPIC PLASTICITY IN GROWTH,DEVELOPMENT, AND BODY SIZE IN THE YELLOW DUNG FLY

Life-history theory predicts that age and size at maturity of organisms should be influenced by time and food constraints on development. This study investigated phenotypic plasticity in growth, development, body size, and diapause in the yellow dung fly, Scathophaga stercoraria. Full-sib families were allowed to develop under predator-free field conditions. The time before the onset of winter was varied and each brood was split into three environments differing in the amount of dung a set number of larvae had as a resource. When resources were abundant and competition was minimal, individuals of both sexes grew to larger body sizes, took longer time to mature, and were able to increase their growth rates to attain large body sizes despite shorter effective development periods later in the season. In contrast, limited larval resources and strong competition constrained individuals to mature earlier at a smaller adult size, and growth rates could not be increased but were at least maintained. This outcome is predicted by only two life-history optimality models, which treat mortality due to long development periods and mortality due to fast growth as independent. Elevated preadult mortality indicated physiological costs of fast growth independent of predation. When larval resources were limited, mortality increased with heritable variation in development time for males, and toward the end of the season mortality increased as larval resources became more abundant because this induced longer development periods. Sexual and fecundity selection favoring large body size in this species is thus opposed by larval viability selection favoring slower growth in general and shorter development periods when time and resources are limited; this overall combination of selective pressures is presumably shaping the reaction norms obtained here. Flexible growth rates are facilitated by low genetic correlations between development time and body size, a possible consequence of selection for plasticity. Heritable variation was evident in all traits investigated, as well as in phenotypic plasticity of these traits (genotype X interactions). This is possibly maintained by unpredictable spatiotemporal variation in dung abundance, competition, and hence selection.     

THE RESPONSES OF DROSOPHILA MELANOGASTER TO ARTIFICIAL SELECTION ON BODY WEIGHT AND ITS PHENOTYPIC PLASTICITY IN TWO LARVAL FOOD ENVIRONMENTS

To investigate the potential response to natural selection of reaction norms for age and size at maturity, fresh body weight at eclosion was mass selected under rich and poor larval food conditions in Drosophila melanogaster. The sensitivity of dry weight at eclosion to the difference between rich and poor larval food was selected using differences in sensitivities among families. For both experiments, the correlated response to selection of age at eclosion was examined. The flies were derived from wild populations and had been mass cultured in the lab for more than six months before the experiments started. These flies responded to selection on body weight upwards and downwards on both rich and poor larval food. Selection on increased or decreased sensitivity of body weight was also successful in at least one direction. Sensitivity was reduced by selection upwards in a poor environment and downwards in a rich environment.     

PHENOTYPIC PLASTICITY IN CHRYSOPERLA: GENETIC VARIATION IN THE SENSORY MECHANISM AND IN CORRELATED REPRODUCTIVE TRAITS

A genetically variable sensory mechanism provides phenotypic plasticity in the seasonal cycle of the Chrysoperla carnea species-complex of green lacewings. The mechanism functions as a switch during the pupal and early imaginal stages to determine aestival reproduction versus aestival dormancy, and it has two major components: (1) response to photoperiod and (2) response to a stimulus(i) associated with the prey of the larvae. Ultimately, the switch is based on the response to photoperiod—an all-or-nothing trait whose variation (long-day reproduction versus a short-day/long-day requirement for reproduction) is determined by alleles at two unlinked autosomal loci. In eastern North America, variation in this component of the switch differentiates two reproductively isolated “species” that are sympatric throughout the region: Chrysoperla carnea, in which both loci are homozygous for the dominant alleles that determine long-day, spring and summer reproduction and thus multivoltinism, and C. downesi, which has a very high incidence of the recessive alleles for the short-day/long-day requirement, and thus univoltine spring breeding. In contrast, geographical populations in western North America harbor variable amounts of within-and among-family genetic variation for the photoperiodic responses and also for the switch's second component—adult responsiveness to the prey of the larvae. The geographic pattern of genetic variation in the two components of the switch indicates that it is a highly integrated adaptation to environmental heterogeneity. Expression of among-family variation in the prey component of the switch is highly dependent on photoperiodic conditions and genotype (it requires a constant long daylength and the recessive short-day/long-day genotype). Thus, we infer that responsiveness to prey evolved as a modifier of the photoperiodic trait. The switch has a significant negative effect on a major determinant of fitness; it lengthens the preoviposition period in nondiapausing reproductives. This negative effect may result in temporal variation in the direction of selection, which helps maintain genetic variability in the switch mechanisms of western populations. Also, the photoperiodic and prey components of the switch are positively correlated with fecundity in nondiapausing reproductives; however, the strong influence of environmental factors—presence or absence of prey—leaves open the question whether the correlated effects on fecundity are expressed in nature.     

PHENOTYPIC PLASTICITY IN POLYGONUM PERSICARIA. III. THE EVOLUTION OF ECOLOGICAL BREADTH FOR NUTRIENT ENVIRONMENT

Norms of reaction for a number of growth and reproductive characters were determined for 15 randomly sampled Polygonum persicaria genotypes, from two natural populations originating in sites with very different nutrient availabilities. Under severely limiting nutrient conditions, these genotypes shared not only plastic responses such as increased root-to-shoot ratio, but a surprising constancy in such functionally essential characters as leaf area ratio, leaf nitrogen concentration, and propagule nitrogen content. Because functional homeostasis depends on flexibility in underlying characters, similar homeostatic results can be achieved through different combinations of underlying plastic and fixed responses in genetically different entities. For example, plants in each population maintained a relatively constant propagule nitrogen content under extreme low-nitrogen conditions by varying either the size or the tissue nitrogen concentration of propagules. These genotypes also tolerated excessive nutrient levels toxic to many plants, evidently by storing excess nutrients in shoots. Although development was altered under such circumstances, reproductive fitness was maintained.     

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.     

THE ECOLOGY AND GENETICS OF FITNESS IN CHLAMYDOMONAS III. GENOTYPE-BY-ENVIRONMENT INTERACTION WITHIN STRAINS

The fitness of genotypes created by crossing strains of Chlamydomonas reinhardtii was measured in axenic pure culture in a set of chemically defined environments. There was substantial and highly significant genotype-by-environment interaction, with genetic correlations between environments averaging only about +0.1 for both r and K. Higher-order interactions with combinations of environmental factors appeared to be no less important than simple interactions with single factors. The importance of genotype-by-environment interaction increased with the number of environmental factors manipulated. The linear reaction norms of genotypic score on environmental mean score varied substantially among genotypes and often intersected. There was also some evidence that nonallelic genetic interactions were present, and varied among environments. The genetic correlation of r with K also varied among environments, being significantly negative in some but not in others. These results are similar in all important respects to those previously obtained with different species, and suggest that genotype-by-environment interaction is important at all genetic scales. It is argued that they provide empirical support for a general theory of diversity, the “Tangled Bank,” based on the different response of genotypes to the range of conditions found in heterogeneous natural environments.     

GEOGRAPHIC VARIATION IN THE LIFE HISTORY OF MASTOCARPUS PAPILLATUS (RHODOPHYTA)1

Variation in the geographic distribution of the life histories of Mastocarpus papillatus was investigated. Carpospores were isolated from 377 female gametophytes collected from eight localities on the Pacific coast of Baja California, Mexico, and California, U.S.A., and grown in laboratory culture. All carpospores from a single female gave rise either to basal discs with gametophyte-like uprights or crustose plants formerly referred to the genus Petrocelis. Early stages in the development of each type of germling were observed, and environmental factors affecting development were suggested. Based on carpospore germlings, females from each location were scored as having either the 1) sexual life history (crustose germlings) or 2) direct-development life history (discoid germlings with uprights). All females from the two southernmost locations in Baja California exhibited the sexual life history. In the three locations from the central-southern California coast, 70-95% of the females exhibited the sexual life history and the remainder exhibited the direct-development life history. In two of the three populations from the central-northern California coast, 70-90% of the females exhibited the direct-development life history and the remainder the sexual life history. In the third location from the central-northern California coast, the northernmost location sampled in the current study, 60% of the females exhibited the sexual life history and 40% the direct-development life history. The relative ecological advantages and disadvantages of the life histories are unknown as are the environmental factors that produced the ratios of sexual to direct-development females observed at each location.     

ADAPTATION TO FINE-GRAINED ENVIRONMENTAL VARIATION: AN ANALYSIS OF WITHIN-INDIVIDUAL LEAF VARIATION IN AN ANNUAL PLANT

Recent studies of evolution in heterogeneous environments have concentrated on the role of coarse-grained environmental variation. Here I explore the potential for a modular organism to adapt to fine-grained environmental variation through within-individual variation among modules. I describe the pattern of variation among leaves of single individuals and report results of initial analyses of genetic variation for within-individual variability in leaf traits and of genetic correlations that could influence the rate of further evolution of within-individual variation of these traits. Plants from 24 paternal half-sib families were raised in growth chambers, and five traits were measured for two leaves produced by each plant. Four of the five traits differed significantly between sampling times. Genetic analyses revealed significant additive genetic variation for within-individual variation in several traits. Estimates of family mean correlations between traits expressed at different times suggest few relationships that would be expected to impede response to selection for changes in the pattern of within-individual variation in leaf traits. These results support the possibility that within-individual variation could evolve as an adaptive response to fine-grained environmental variation and suggest a need for further investigation to improve understanding of evolution in heterogeneous environments.     

LOCAL ADAPTATION AND THE EVOLUTION OF PHENOTYPIC PLASTICITY IN TRINIDADIAN GUPPIES (POECILIA RETICULATA)

Divergent selection pressures across environments can result in phenotypic differentiation that is due to local adaptation, phenotypic plasticity, or both. Trinidadian guppies exhibit local adaptation to the presence or absence of predators, but the degree to which predator‐induced plasticity contributes to population differentiation is less clear. We conducted common garden experiments on guppies obtained from two drainages containing populations adapted to high‐ and low‐predation environments. We reared full‐siblings from all populations in treatments simulating the presumed ancestral (predator cues present) and derived (predator cues absent) conditions and measured water column use, head morphology, and size at maturity. When reared in presence of predator cues, all populations had phenotypes that were typical of a high‐predation ecotype. However, when reared in the absence of predator cues, guppies from high‐ and low‐predation regimes differed in head morphology and size at maturity; the qualitative nature of these differences corresponded to those that characterize adaptive phenotypes in high‐ versus low‐predation environments. Thus, divergence in plasticity is due to phenotypic differences between high‐ and low‐predation populations when reared in the absence of predator cues. These results suggest that plasticity might initially play an important role during colonization of novel environments, and then evolve as a by‐product of adaptation to the derived environment.     

PHENOTYPIC PLASTICITY INDUCED IN TRANSPLANT EXPERIMENTS IN A MUTUALISTIC ASSOCIATION BETWEEN THE RED ALGA JANIA ADHAERENS (RHODOPHYTA,CORALLINALES) AND THE SPONGE HALICLONA CAERULEA (PORIFERA: HAPLOSCLERIDA): MORPHOLOGICAL RESPONSES OF THE ALGA1

The association between the red macroalga Jania adhaerens J. V. Lamour. and the sponge Haliclona caerulea is the most successful life‐form between 2 and 4 m depth in Mazatlán Bay (Mexican Pacific). J. adhaerens colonizes the rocky intertidal area and penetrates into deeper areas only when it lives in association with H. caerulea. The aposymbiotic form of the sponge has not been reported in the bay. To understand the ecological success of this association, we examined the capacity of J. adhaerens to acclimate in Mazatlán Bay using transplant experiments. The transplanted aposymbiotic J. adhaerens did not survive the first 2 weeks; however, J. adhaerens when living in association with H. caerulea, acclimated easily to depth, showing no sign of mortality during the 103 d of the experiment. We conclude that the ability of J. adhaerens to colonize in deeper areas in this hydrodynamic environment may in part rely on the protection provided by the sponge to the algal canopy. Both species contribute to the shape of the associated form. Nevertheless, the morphological variation in the association appears to be dominated by the variation in J. adhaerens canopy to regulate pigment self‐shading under light‐limited conditions and/or tissue resistance under high hydrodynamics. Consequently, our results are consistent with light as the abiotic controlling factor, which regulates the lower depth distribution of the association in Mazatlán Bay, through limiting the growth rate of J. adhaerens. Hydrodynamics may determine the upper limit of the association by imposing high mass losses.     

MEASURING THE PLASTICITY OF DEVELOPMENTAL RATE ACROSS INSECT POPULATIONS: COMMENT ON ROCHA AND KLACZKO (2012)

Rocha and Klaczko emphasize the general complexity of reaction norm shape and caution that ignoring such complexity can be misleading when forcing nonlinear reaction norms into linear shapes. They refer to our article on differences in plasticity of Drosophila serrata populations along a latitudinal gradient as an example of a misleading simplifying approach. However, their claim that an artifact is introduced into our analyses by calculating developmental rate as the reciprocal of development time (rate = time^?1) is based on a misunderstanding of the mathematical properties of the thermal developmental rate reaction norm. Here we discuss why developmental rate is a suitable measure for our study and under which circumstances it is appropriate to describe developmental rate by a linear model.     

NO EFFECT OF ENVIRONMENTAL HETEROGENEITY ON THE MAINTENANCE OF GENETIC VARIATION IN WING SHAPE IN DROSOPHILA MELANOGASTER

Theory suggests that heterogeneous environments should maintain more genetic variation within populations than homogeneous environments, yet experimental evidence for this effect in quantitative traits has been inconsistent. To examine the effect of heterogeneity on quantitative genetic variation, we maintained replicate populations of Drosophila melanogaster under treatments with constant temperatures, temporally variable temperature, or spatially variable temperature with either panmictic or limited migration. Despite observing differences in fitness and divergence in several wing traits between the environments, we did not find any differences in the additive genetic variance for any wing traits among any of the treatments. Although we found an effect of gene flow constraining adaptive divergence between cages in the limited migration treatment, it did not tend to increase within‐population genetic variance relative to any of the other treatments. The lack of any clear and repeatable patterns of response to heterogeneous versus homogeneous environments across several empirical studies suggests that a single general mechanism for the maintenance of standing genetic variation is unlikely; rather, the relative importance of putative mechanisms likely varies considerably from one trait and ecological context to another.