LIFE-HISTORY EVOLUTION IN GUPPIES (POECILIA RETICULATA) 6. DIFFERENTIAL MORTALITY AS A MECHANISM FOR NATURAL SELECTION

We have previously reported a correlation between the life-history patterns of guppies and the types of predators with which they coexist. Guppies from localities with an abundance of large predators (high predation localities) mature at an earlier age and devote more resources to reproduction than those found in localities with only a single, small species of predator (low predation localities). We also found that when guppies were introduced from a high to low predation locality, the guppy life history evolved to resemble what was normally found in this low predation locality. The presumed mechanism of natural selection is differences among localities in age/size-specific mortality (the age/size-specific mortality hypothesis); in high predation localities we assumed that guppies experienced high adult mortality rates while in the low predation localities we assumed that guppies experienced high juvenile mortality rates. These assumptions were based on stomach content analyses of wild-caught predators and on laboratory experiments. Here, we evaluate these assumptions by directly estimating the mortality rates of guppies in natural populations. We found that guppies from high predation localities experience significantly higher mortality rates than their counterparts from low predation localities, but that these higher mortality rates are uniformly distributed across all size classes, rather than being concentrated in the larger size classes. This result appears to contradict the predictions of the age/size-specific predation hypothesis. However, we argue, using additional data on growth rates and the probabilities of survival to maturity in each type of locality, that the age-specific mortality hypothesis remains plausible. This is because the probability of survival to first reproduction is very similar in each type of locality, but the guppies from high predation localities have a much lower probability of survival per unit time after maturity. We also argue for the plausibility of two other mechanisms of natural selection. These results thus reveal mortality patterns that provide a potential cause of natural selection, but expand, rather than narrow, the number of possible mechanisms responsible for life-history evolution in guppies.     

LIFE-HISTORY EVOLUTION IN GUPPIES: 2. REPEATABILITY OF HELD OBSERVATIONS AND THE EFFECTS OF SEASON ON LIFE HISTORIES

Natural populations of guppies that co-occur with the pike cichlid Crenicichla alta and associated predators mature at smaller body sizes, produce more and smaller offspring per litter reproduce more frequently, and have higher reproductive allotments (weight of developing embryos/total body weight) than guppies that co-occur with just the killifish Rivulus harti (Reznick and Endler, 1982). I here consider three forms of repeatability in these life-history patterns: i) among replicate samples collected on the same day from the same locality, ii) between Crenicichla and Rivulus communities among a new series of localities, and iii) among a smaller series of Crenicichla and Rivulus localities sampled in two wet and two dry seasons. In the analysis of replicate collections from two localities, seven of eight statistical comparisons revealed no significant difference. The usual methodology for estimating these variables therefore accurately represents guppy life-history patterns at a given locality. Differences among guppies from Rivulus and Crenicichla localities, covering a wider geographical area than considered by Reznick and Endler (1982), were virtually identical to the previous comparison. Wet-season samples were associated with significant decreases in reproductive allotment and fecundity and significant increases in the size of mature males and the minimum size of reproducing females. Differences between guppies from Rivulus and Crenicichla localities persisted across all samples and were consistent with all other observations, although they tended to be smaller during the wet season. Discriminant analyses on female reproductive traits showed that fecundity and offspring size made strong, independent contributions to discriminating between guppies from the two types of localities. The contribution from reproductive allotment was considerably smaller. There was more overlap between predator treatments during the wet season. Only 8.5% of the individuals were misclassified during the dry season, but 19.5% were misclassified during the wet season.     

PHENOTYPIC PLASTICITY IN THE SAILFIN MOLLY,POECILIA LATIPINNA (PISCES: POECILIIDAE). II. LABORATORY EXPERIMENT

Field studies indicate that the influence of environmental factors on growth rate and size and age at maturity in sailfin mollies (Poecilia latipinna) is inconsistent over time and suggest that the marked interdemic variation in male body size in this species is the result of genetic variation. However, the role of specific environmental factors in generating phenotypic variation must be studied under controlled conditions unattainable in nature. We raised newborn sailfin mollies from four populations in laboratory aquaria under all possible combinations of two temperatures, three salinities, and two food levels to examine explicitly the influence of these environmental factors. Males were much less susceptible than females to temperature variation and were generally less plastic than females in terms of all three traits. Members of both sexes matured at larger sizes and at later ages in less saline and in cooler environments. Food levels were not sufficiently different to affect the traits we studied. The effects of temperature and salinity were not synergistic. Males from different populations exhibited different average ages and sizes at maturity, but females did not. The magnitudes of the effects we found were not substantial enough to account for the consistent interdemic differences in male and female body size that have been observed previously. Our results also indicate that no single environmental factor is solely responsible for the environmental effects observed in field experiments on growth and development. These studies, together with other work, indicate that the strongest sources of interdemic variation are genetic differences in males and differences in postmaturation growth and survivorship in females.     

QUANTITATIVE GENETICS OF BRYOZOAN PHENOTYPIC EVOLUTION. III. PHENOTYPIC PLASTICITY AND THE MAINTENANCE OF GENETIC VARIATION

Cheilostome bryozoan species show long-term morphologic stasis, implying stabilizing selection sustained for millions of years, but nevertheless retain significant heritable variation in traits of skeletal morphology. The possible role of within-genotype (within-colony) phenotypic variability in preserving genetic diversity was analyzed using breeding data for two species of Stylopoma from sites along 110 km of the Caribbean coast of Panama. Variation among zooids within colonies accounts for nearly two-thirds of the phenotypic variance on average, increases with environmental heterogeneity, and includes significant genotype-environment interaction. Thus, within-colony variability apparently represents phenotypic plasticity, at least some of which is heritable, rather than random “developmental noise.” Almost all of the among-colonies component of phenotypic variance is accounted for by additive genetic differences in trait means, suggesting that within-colony plasticity includes virtually all of the environmental component of phenotypic variance in these populations of Stylopoma. Thus, heritable within-colony plasticity could play a significant part in maintaining genetic diversity in cheilostomes, but it is also possible that rates of polygenic mutation alone are sufficient to balance the effects of selection.     

THE EVOLUTION OF PHENOTYPIC PLASTICITY IN LIFE-HISTORY TRAITS: PREDICTIONS OF REACTION NORMS FOR AGE AND SIZE AT MATURITY

We used life-history theory to predict reaction norms for age and size at maturation. We assumed that fecundity increases with size and that juvenile mortality rates of offspring decrease as ages-at-maturity of parents increase, then calculated the reaction norm by varying growth rate and calculating an optimal age at maturity for each growth rate. The reaction norm for maturation should take one of at least four shapes that depend on specific relations between changes in growth rates and changes in adult mortality rates, juvenile mortality rates, or both. Most organisms should mature neither at a fixed size nor at a fixed age, but along an age-size trajectory. The model makes possible a clear distinction between the genetic and phenotypic components of variation. The evolved response to selection is reflected in the shape and position of the reaction norm. The phenotypic response of a single organism to rapid or slow growth is defined by the location of its maturation event as a point on the reaction norm. A quantitative test with data from 19 populations and species of fish showed that predictions were in good agreement with observations (r = 0.93, P < 0.0001). The predictions of the model also agreed qualitatively with observed phenotypic variation in age and size at maturity in humans, platyfish, fruit flies, and red deer. This preliminary success suggests that experiments designed to test the predictions directly will be worthwhile.     

GENETICS OF BRASSICA CAMPESTRIS. 1. GENETIC CONSTRAINTS ON EVOLUTION OF LIFE-HISTORY CHARACTERS

Energy allocation arguments suggest a possible tradeoff between timing and magnitude of reproduction: plants that postpone reproduction may accumulate greater resources and consequently produce more offspring. However, early reproduction may be favored when adult mortality is high. Tradeoffs among life-history characters may be a consequence of constraints imposed by genetic and environmental covariation among traits. In this paper we examine the genetic basis of the relationship between timing and magnitude of reproduction in an annual plant, Brassica campestris, by selecting to change flowering date and plant size in each of four directions (early and large, late and large, early and small, or late and small). There is a strong positive relationship between flowering date and flowering height. The response to selection was greatest along the axis of positive genetic covariation. Populations may evolve to become early flowering and small or late flowering and tall, but there is little response for the alternative combinations of characters. In this instance, the constraints imposed by quantitative genetics are in striking accord with predictions that might be made on physiological, energetic, or ecological grounds.     

GEOGRAPHICAL AND GENETIC STRUCTURE OF LIFE-HISTORY VARIATION IN MILKWEED BUGS (HEMIPTERA: LYGAEIDAE: ONCOPELTUS)

Life-history variation was investigated using crosses within and among the laboratory-bred descendants of six geographic samples of the large milkweed bug, Oncopeltus fasciatus. These samples spanned the species' range, from permanent (year-round) populations on tropical islands to seasonal middle-latitude populations found in temperate North America. The seasonal populations must be refounded each year by colonists from more southern populations. Marked differences in life-history traits (particularly in age at first reproduction, clutch size, and rate of egg production) were observed among the six population samples, with tropical-island and west-coast populations being the most distinct. In the eastern and central United States, there was a marked north-south difference in life history. Crossing experiments demonstrated a genetic basis for these differences. F₁ and F₂ hybrids from crosses between continental populations tended to have intermediate phenotypes. The similarity of the seasonal middle-latitude populations' life histories and the consistency of the distribution of life-history characteristics among populations (across years) may indicate that the north-south difference in life history is due to selection on these traits during the annual northward movement or that migrants represent a distinct genetic form of this species.     

COST OF REPRODUCTION IN POLEMONIUM VISCOSUM: PHENOTYPIC AND GENETIC APPROACHES

I measured the effect of early reproduction on subsequent growth and survival in the alpine perennial wildflower, Polemonium viscosum. Measurements were made over 4 yr on 34 maternal sibships under natural conditions. A significant phenotypic cost of early reproduction characterized the study population. Plants that flowered after only one year's growth had twice as many leaves and 25% more shoots than nonflowering individuals of equal age. However, early flowering decreased leaf number by 18% in the subsequent year and survivorship by 20% after two years relative to changes in leaf number and survival of nonflowering plants. For such trade-offs to shape the further evolution of reproductive schedules, flowering probability and those age-specific components of plant size that represent the energetic currency for reproductive costs must be heritable. Although families showed significant heterogeneity in the probability of early flowering, most (62%) entirely failed to flower. Moreover, phenotypic variation in vegetative size components at ages 1 and 2 had little genetic basis. Only at ages 3 and 4, after vegetative and demographic costs of early reproduction had been incurred, did vegetative size components (leaf length and number, and shoot number) vary significantly among families. Results of this study provide little evidence of a genetically based trade-off between early reproduction and subsequent survival in P. viscosum.     

PHENOTYPIC PLASTICITY IN LIFE-HISTORY TRAITS OF FEMALE THALASSOMA BIFASCIATUM (PISCES: LABRIDAE). 1. MANIPULATIONS OF SOCIAL STRUCTURE IN TESTS FOR ADAPTIVE SHIFTS OF LIFE-HISTORY ALLOCATIONS

Optimal-life-history theory is based on the relative benefit of immediate versus future reproduction. We apply this theory to the life-history tactics of female Thalassoma bifasciatum, a sex-changing coral-reef fish. Local social structure varies in this species and influences a female's chances of achieving high future reproductive success as a territorial terminal-phase male. We predicted that female life-history allocations would be flexible and responsive to variation in future reproductive prospects. We altered population size structure on four reefs, removing large fish and adding small fish. These alterations enhanced the residual reproductive value of the remaining larger female residents. The predicted response to the manipulation was a reduction in reproductive activity and an increase in growth. Our results do not support this hypothesis. Possible interpretations are that: 1) the theory, or our application of the theory, is flawed; 2) female Thalassoma are unresponsive to changes in future reproductive prospects; or 3) the design of our study was ineffectual at detecting a response. We report here an approach to the study of adaptive life-history strategies that deserves implementation in other systems.     

PHENOTYPIC PLASTICITY IN THE SAILFIN MOLLY,POECILIA LATIPINNA (PISCES: POECILIIDAE). I. FIELD EXPERIMENTS

Sailfin mollies (Poecilia latipinna) display marked interdemic variation in body size. We employed “common-garden” experiments in field enclosures to explore the potential role of environmental factors in determining the interdemic phenotypic variation in growth rate, age at maturity, and size at maturity. The largest single, consistent source of variation for all traits was family identity within populations. Environmental effects acted predominantly through family x environment interactions. There was little evidence for any intrinsic variation among populations once family heterogeneity had been accounted for. In general, when statistically significant differences existed, fish raised in a saltwater pond grew faster than their broodmates raised in a freshwater pond. Both males and females tended to mature at a smaller size and later in the freshwater pond than in the saltwater pond. The effects of the environmental conditions differed among the three years in which we performed these studies. In only one year was there a substantial difference between fish raised under the two environmental conditions. These results indicate that direct environmental effects are not strong enough to account for the differences in body size among natural populations and that intrinsic differences among natural populations are due to different frequency distributions of genotypes that are present in all populations.