Important Selective Agent Research Articles

Density-dependent natural selection in Drosophila: correlations between feeding rate, development time and viability

Abstract We have previously hypothesized that density-dependent natural selection is responsible for a genetic polymorphism in crowded cultures of Drosophila. This genetic polymorphism entails two alternative phenotypes for dealing with crowded Drosophila larval cultures. The first phenotype is associated with rapid development, fast larval feeding rates but reduced absolute viability, especially in the presence of nitrogenous wastes like ammonia. The second phenotype has associated with it the opposite set of traits, slow development, slow feeding rates and higher viability. We suggested that these traits are associated due to genetic correlations and that an important selective agent in crowded larval cultures was high levels of ammonia. To test this hypothesis we have examined viability and larval feeding rates in populations kept at low larval densities but selected directly for (i) rapid egg-to-adult development, (ii) tolerance of ammonia in the larval environment and (iii) tolerance of urea in the larval environment. Consistent with our hypothesis we found that (i) larvae selected for rapid development exhibited increased feeding rates, and decreased viability in food laced with ammonia or urea relative to controls, and (ii) larvae selected to tolerate either ammonia or urea in their larval environment show reduced feeding rates but elevated survival in toxin-laced food relative to controls. It would appear that development time and larval feeding rate are important characters for larvae adapting to crowded cultures. The correlated fitness effects of these characters provide important insights into the nature of density-dependent natural selection.

The protective action of tannins against glasshouse whitefly in tomato seedlings

The synthesis and accumulation of tannins on tomato seedlings are regulated by environmental factors. The variation in the content of tannins was sufficiently important to bring about the occurrence of significant differences in the numbers of glasshouse whitefly on the seedlings. During a 2-week experiment, the treatments included mechanical wounding (20 prickings per cm2), spraying with kinetin solutions of 10−4 mol/dm3, plant growth regulators, and the atmosphere enrichment to 680 μmol CO2/mol air, the content of tannins being increased by c. 40, 70, 10–45 and 25% above the values obtained in the control. These results were correlated with a decrease in the numbers of insects occurring on the seedlings by c. 35, 45, 8–29 and 18%, respectively. Contrary to the above results the spraying with solutions of abscisic acid, gibberellic acid, and the incubation of plants in an atmosphere containing 170 μmol CO2/mol air, reduced the content of tannins by c. 69, 22 and 25%, respectively. This was reflected in the respective increases by c. 70, 40 and 35% in the numbers of insects occurring on the seedlings. The obtained results suggest that tannins seem to have a dosage-dependent effect on glasshouse whitefly. Decreasing the host plant quality by increasing tannin content may act as an important selective agent limiting the losses brought about by glasshouse whitefly in tomato cultivation.

DOES “ENEMY-FREE SPACE” EXIST? EXPERIMENTAL HOST SHIFTS OF AN HERBIVOROUS FLY

Natural enemies have been proposed as important agents of natural selection on herbivorous insects that may facilitate host plant shifts and increases in diet breadth. However, there is little experimental field work to support claims of host-shifting via escape from natural enemies, i.e., to enemy-free space. In this study, we took the unique approach of experimentally creating a host shift for a specialized leafmining fly, Liriomyza helianthi (Diptera: Agromyzidae). We manually transferred leafminer larvae from their normal host plant, Helianthus annuus (Asteraceae), to a variety of novel plants: Helianthus maximilianii, Ambrosia artemisiifolia, Taraxacum officinale, and Centaurea solstitialis. By exposing transferred larvae on normal and novel plants to natural enemy attack under field conditions, we were able to examine whether host-shifting can provide an herbivore with enemy-free space. Our data show that enemy-free space does exist for L. helianthi immediately following a host shift, as mortality in novel plants averaged 17% less than in the normal host. Nevertheless, there was significant within- and between-year heterogeneity in results over the 3-yr period of the study. We found that escape from natural enemies was related to annual variation in the diversity and abundance of parasitoid species. In years when parasitoid assemblages were dominated by endoparasitoids, mortality of larvae averaged 22% lower in novel hosts. However, when generalist ectoparasitoids, Diglyphus spp. (Hymenoptera: Eulophidae), were present, there was no advantage of developing in novel plants, a result that could be explained by the less discriminating nature of the ectoparasitoids. When overall levels of mortality from natural enemies were high, the benefit of novel plants was also reduced. This pattern suggests that, as available larval hosts become scarce, parasitoids may be more likely to forage on novel host plants in search for prey, thus diminishing the opportunity for enemy-free space. Nevertheless, our study showed that enemy-free space can exist for an herbivorous insect utilizing a novel host plant, and that natural enemies may, in some cases, offset physiological fitness costs often associated with developing in novel plants. If all else is equal, the balance of these factors may facilitate the inclusion of novel host plants into the feeding repertoire of an herbivore.

EXPERIMENTAL EVOLUTION OF HSP70 EXPRESSION AND THERMOTOLERANCE IN DROSOPHILA MELANOGASTER.

To examine whether recent evolutionary history affects the expression of Hsp70, the major heat-induced-heat shock protein in Drosophila melanogaster, we measured Hsp70 expression, thermotolerance, and hsp70 gene number in replicate populations undergoing laboratory evolution at different temperatures. Despite Hsp70's ancient and highly conserved nature, experimental evolution effectively and replicably modified its expression and phenotype (thermotolerance). Among five D. melanogaster populations founded from a common ancestral population and raised at three different temperatures (one at 18°C, two each at 25°C and 28°C) for twenty years, Hsp70 expression varies in a consistent pattern: the replicate 28°C lines expressed 30-50% less Hsp70 than the other lines at a range of inducing temperatures. This modification was refractory to acclimation, and correlated with thermotolerance: the 28°C lines had significantly lower inducible tolerance of 38.5°C and 39°C. We verified the presence of five hsp70 genes in the genome of each line, excluding copy number variation as a candidate molecular basis of the evolved difference in expression. These findings support the ability of Hsp70 levels in D. melanogaster populations to change over microevolutionary time scales and implicate constancy of environmental temperature as a potentially important selective agent.

THE MAINTENANCE OF A CLINE IN THE MARINE SNAIL LITTORINA SAXATILIS: THE ROLE OF HOME SITE ADVANTAGE AND HYBRID FITNESS.

Steep clinal transitions in one or several inherited characters between genetically distinct populations are usually referred to as hybrid zones. Essentially two different mechanisms may maintain steep genetic clines. Either selection acts against hybrids that are unfit over the entire zone due to their mixed genetic origin (endogenous selection), or hybrids and parental types attain different fitness values in different parts of the cline (exogenous selection). Survival rate estimates of hybrids and parental forms in different regions of the cline may be used to distinguish between these models to assess how the cline is maintained. We used reciprocal transplants to test the relative survival rates of two parental ecotypes and their hybrids over microscale hybrid zones in the direct-developing marine snail Littorina saxatilis (Olivi) on the rocky shores of Galicia, Spain. One of the parental forms occupies upper and the other lower shores, and the hybrids are found at various proportions (1-38%) along with both parental forms in a midshore zone a few meters wide. The survival rate over one month was 39-52% of the native ecotype on upper shores, but only 2-8% for the lower-shore ecotype. In contrast, only 4-8% of the upper-shore ecotype but 53% of large (> 6 mm) and 8% of small (3-6 mm) native lower-shore ecotype survived in the lower shores. In the midshores, both the two parental ecotypes and the hybrids survived about equally well. Thus there is a considerable advantage for the native ecotypes in the upper and lower shores, while in the hybrid zone none of the morphs, hybrids included, are favored. This indicates that the dimorphism of L. saxatilis is maintained by steep cross-shore selection gradients, thus supporting the selection-gradient model of hybrid zones. We performed field and laboratory experiments that suggest physical factors and predation as important selective agents. Earlier studies indicate assortative mating between the two ecotypes in the midshore. This is unexpected in a hybrid zone maintained by selection gradients, and it seems as if the reproductive barrier compresses the hybrid zone considerably.

AN INTERACTION BETWEEN ENVIRONMENTAL TEMPERATURE AND GENETIC VARIATION FOR BODY SIZE FOR THE FITNESS OF ADULT FEMALE DROSOPHILA MELANOGASTER.

- Drosophila and other ectotherms show geographic genetic variation in body size, with larger individuals at higher latitudes and altitudes. Temperature is implicated as an important selective agent because long-term laboratory culture of Drosophila leads to the evolution of larger body size at lower temperatures. In this paper, we tested the hypothesis that, in Drosophila melanogaster, larger size is favored at lower temperatures in part because of selection on adult females. We used replicated lines of D. melanogaster artificially selected for increased and decreased wing area with constant cell area. The resulting size differences between the selected lines were due solely to differences in cell number, and thereby were similar to the cellular basis of clinal variation in body size in nature. We examined life-history traits of adult females at 18 and 25°C. Rearing for two generations at the two temperatures did not affect the extent of the size differences between lines from the different selection regimes. There was a strong interaction between temperature and size selection for both survival and lifetime reproductive success, with larger females living significantly longer and producing more offspring over their lifetime only when reared and tested in the colder environment. There was also an increase in average daily progeny production in large-line females relative to the control and small lines again, only in the colder environment. Thus, the females from the large selection lines were relatively fitter at the colder temperature. At both experimental temperatures, especially the lower one, the small- line females rescheduled their progeny production to later ages. Larger body size may have evolved at higher latitudes and altitudes because of the advantages to the adult female of being larger at lower temperatures.

THERMAL EVOLUTION OF EGG SIZE IN DROSOPHILA MELANOGASTER.

We measured the size of eggs produced by populations of Drosophila melanogaster that had been collected along latitudinal gradients in different continents or that had undergone several years of culture at different temperatures in the laboratory. Australian and South American populations from higher latitudes produced larger eggs when all were compared at a standard temperature. Laboratory populations that had been evolving at 16.5°C produced larger eggs than populations that had evolved at 25°C or 29°C, suggesting that temperature may be an important selective agent in producing the latitudinal clines. Flies from laboratory populations produced larger eggs at an experimental temperature of 16.5°C than at 25°C, and there was no indication of genotype-environment interaction for egg size. Evolution of egg size in response to temperature cannot be accounted for by differences in adult body size between populations. It is not clear which life-history traits are direct targets of thermal selection and which are showing correlated responses, and disentangling these is a task for the future.

The Composition and Foraging Ecology of Mixed-Species Flocks in Pine Forests of Hispaniola

We determined the flocking propensity of 48 species of birds occurring in native pine forest in the Cordillera Central of the Dominican Republic, and the species composition of 180 mixed-species flocks. Flocks were unusually ubiquitous, with 46 species occurring in at least one flock, 11 species regularly present, and all insectivorous species and all migrant species participating. Most birds encountered were permanent residents, but winter residents (Nearctic migrants) were an important component of the flocks and, as a group, had the highest flocking propensity. Flocks were cohesive and the resident insectivore, the Black-crowned Palm Tanager (Phaenicophilus palmarum) often served as the nuclear species. Censuses suggest species richness within flocks reflects the species present in the habitat, but agonistic interactions indicate that intraspecific aggression may limit the number of individuals of a species in these flocks. Species co-occurrence data indicate that species do not occur independently of one another in flocks. Positive associations were far more common than negative co-occurrences, suggesting mutual habitat dependencies or species interactions within flocks. A non-random association of nearest neighbors also indicated that species may be gaining feeding benefits from flocking by associating as close neighbors with an individual of another species, but we were not able to rule out the possibility that predation is an important selective agent. Intraspecific comparisons of foraging behavior between flocking and solitary birds provides some evidence that individuals modify foraging locations and foraging tactics upon joining mixed-species flocks, and that their foraging behavior tends to converge with the feeding behavior of the nuclear species. An increase in the feeding rate was recorded for one species. These data suggest that at least some species may accrue feeding advantages as flock participants.

Antimicrobial activity of extracts of Caribbean gorgonian corals

Extracts of 39 species of Caribbean gorgonians were tested for antimicrobial activity against 15 strains of marine bacteria. The bacteria consisted of three opportunistic pathogens, Vibrio parahaemolyticus, Leucothrix mucor, and Aerococcus viridans, and 12 strains isolated from either healthy or decayed gorgonians. Overall, only 15% (79 out of 544) of the tests resulted in antibacterial activity with 33% (13 out of 39) of the gorgonians inhibiting only one bacterial strain and 23% (9 out of 39) showing no activity. The extracts of four Pseudopterogorgia species showed relatively high levels of activity, inhibiting 43 to 86% of the bacterial strains. The potency of the active Pseudopterogorgia species was variable, however, and three additional Pseudopterogorgia species were inactive against all bacterial strains. With the exception of one sensitive strain, Vibrio species were resistant to gorgonian metabolites. Our results indicate that organic extracts of most Caribbean gorgonians do not possess potent, broad-spectrum antibacterial activity inhibitory to the growth of opportunistic marine pathogens and bacteria associated with healthy and decayed gorgonian surfaces. These findings suggest that the inhibition of bacterial growth is not the primary ecological function of gorgonian secondary metabolites and that bacteria may not be important selective agents in the evolution of gorgonian secondary chemistry.

Host‐Plant Selection and Predation Risk for Offspring of the Parent Bug

Herbivores, especially specialists, must adapt to characteristics of their host to survive and reproduce successfully (Hardin and Tallamy1992). If offspring survival among different hosts varies, natural selection should lead females to choose egg-laying sites where performance of the progeny will be highest. This is especially true when newly hatched larvae cannot move to another host (Singer 1986), or when searching for new hosts would cause heavy mortality (Singer and Mandracchia 1982). A number of studies have shown that females that search for oviposition sites respond to plant characteristics that are correlated with the nutritional quality of plants for their offspring (e.g., Myers 1985, Damman and Feeny 1988). Also, secondary chemicals of plants play an essential part in determining whether the plant is suitable for oviposition (e.g., Feeny et al. 1985). Furthermore, females may detect visually or chemically the presence of other conspecific and nonconspecific competitors already on a potential host (Rothschild and Schoonhoven 1977, Rausher 1979, Mappes and Makela 1993). However, one of the most important selective agents driving the evolution of behavioral adaptations of prey animals is predation (Endler 1991), and for herbivorous insects, natural enemies commonly represent the major source of mortality (Myers 1981, Feeny et al. 1985). Thus, predation as well as plant characteristics could influence both oviposition behavior and offspring performance on the host (Bernays and Graham 1988). At the moment, however, there is very little empirical ev-

Selection by Parasites on Components of Fitness in Tribolium Beetles: The Effect of Intraspecific Competition

In the past decade, parasites have been widely recognized by population biologists as important selective agents on host populations. Little is known, however, about the mechanisms of parasite-imposed selective processes. We examine the effects of the tapeworm, Hymenolepis diminuta, on the fitness of the flour beetle host, Tribolium castaneum, under high and low intraspecific competition environments. We further identify the components of fitness that contribute to the overall parasite-induced reduction of fitness. The fitness components studied include female fecundity, adult cannibalism of eggs, egg-to-adult viability, and male sperm precedence. Under high intraspecific competition, parasite infection significantly reduced the fitness of both male and female beetles; infected beetles showed increased adult cannibalism rate of eggs. Such a parasite-induced behavioral alteration may contribute to the observed reduction in net fecundity. In contrast, under low intraspecific competition, male fitness was not significantly changed, reductions in fecundity were not significant, and second-male sperm precedence was significantly decreased by the tapeworm infection. The egg-to-adult viability of eggs from infected beetles was not significantly changed in either environment. These results provide evidence that parasitism can affect host fitness through both fecundity and sexual selection, and they suggest that the consequences of parasite infection on host fitness and the components of fitness can be mediated by host density.

Selective Grazing of Hairless Silene dioica Plants by Land Gastropods

Silene dioica (Caryophyllaceae) has evolved different morphotypes that vary in hairiness in different habitats in the Swedish mountains. A hairy form, var. serpentinicola and a hairless (glabrous) form, var. smithii grow on serpentine, i.e. a dry soil rich in heavy metals. Var. lapponica is a densely hairy morphotype on subalpine meadows. Crosses between these varieties showed that glabrousness has a simple Mendelian inheritance and that glabrousness is determined by a recessive allele. The crosses further suggested that the recessive allele has been present in the original population that invaded the mountain area. Glabrous plants have, however, never been found on subalpine meadows, even though an earlier study has shown that gene flow is relatively common among serpentine and nearby meadow populations. In addition to the genetic background of glabrousness, we studied the grazing on glabrous smithii and hairy serpentinicola and lapponica plants by the slugs Arion fasciatus and Arion subfuscus and the snail Arianta arbustorum in greenhouse and in nature. Arion slugs, abundant on subalpine meadows, preferred glabrous plants and, in particular, A. fasciatus consumed high amounts of S. dioica. Arianta snails, however, consumed irrespective of morphotype. The selective behaviour was seen both at the seedling stage and the adult plant stage. Arion slugs were more choosy when they were given a choice of glabrous smithii and densely hairy lapponica plants then when they were served smithii and the less hairy variety serpentinicola. This study implies that the Arion slugs are important agents of selection on subalpine meadows. The selective grazing seems to counteract the flow of the recessive allele that determines glabrousness, from serpentine into meadow populations. Gastropods are rare in the dry serpentine habitat. The evolution of a distinct glabrous morphotype on serpentine is therefore rather due to relaxation of selection than to adaptation to serpentine stress.

THE IMPACT OF TREE SQUIRRELS (TAMIASCIURUS) ON LIMBER PINE SEED DISPERSAL ADAPTATIONS.

Tree squirrels (Tamiasciurus) are important selective agents on conifer reproductive strategies (Smith 1970, 1975). Although this is well established for wind-dispersed pines, the impact of tree squirrels on bird-dispersed pines has been largely ignored. I assessed the impact of tree squirrels on the allocation of reproductive energy in the bird-dispersed limber pine (Pinus flexilis) by comparing its cone and seed traits from three sites in the Rocky Mountains where tree squirrels (Tamiasciurus) are present to those from three mountain ranges in the Great Basin where tree squirrels are absent. As predicted, differences between the two regions in individual cone and seed traits are consistent with the hypothesis that tree squirrels are important selective agents on these traits. In the absence of tree squirrels, limber pine allocates more than twice as much energy to kernel compared with that invested in putative seed defenses (cone, resin, and seed coat) as does limber pine where tree squirrels are present. Such a large difference is particularly striking, because tree squirrels may have become extinct in the Great Basin in only the last 12,000 yr. Although many factors influence the allocation of energy to cones and seeds, no single factor other than the presence of tree squirrels is compatible with the large and consistent differences between limber pine in the Rocky Mountains and Great Basin. These results show that tree squirrels are an important constraint on the evolution of cone and seed traits that promote the dispersal of seeds by birds.

THE EVOLUTIONARY INTERACTION AMONG SPECIES: Selection, Escalation, and Coevolution

The hypothesis of escalation states that enemies-competitors, predators, and dangerous prey-are the most important agents of natural selection among individual organisms, and that enemy-related adaptation and responses brought about long-term evolutionary trends in the morphology, behavior, and distribution of organisms over the course of the Phanerozoic. In contrast to this top-down view of the role of organisms in determining the directions of evolution, the hypothesis of coevolution holds that two interacting species or groups of species change in response to each other. I review and evaluate these hypotheses in the light of criticisms about the existence of evolutionary trends and the role of interactions of species in evolution. Models describing the evolutionary effects organisms have on each other have been based largely on population dynamics and on cost-benefit analyses of the net outcome of interactions between species. Yet, the hypotheses of escalation and coevolution are statements about the nature, frequency, causes, and role of selection. Although these models have provided valuable insights and have forced some modifications in the hypotheses of escalation, studies seeking to distinguish between escalation and coevolution will require empirical observations and cost-benefit evaluations of the discrete events of interaction that collectively constitute organism-caused selection.

Active tectonics and human survival strategies

Tectonic movements continuously remould the surface of Earth in response to plate motion. Yet such deformation is rarely taken into account when assessing landscape change and its impact on human land use, except perhaps as an occasional hazard to human life or a temporary disruption in the longer term patterns of human history. However, active tectonics also create and sustain landscapes that can be beneficial to human survival, forming a complex topography of potentially fertile sedimentary basins enclosed by mountain barriers that can facilitate the control and exploitation of food resources, especially animal prey. We discuss the tectonic history of northwest Greece and show how the Paleolithic sites of the region are located to take advantage of tectonically created features at both a local and a regional scale. We suggest that the association of significant concentrations of early Paleolithic sites with tectonically active regions is not coincidental and that on the longer time spans of human biological evolution, active tectonics has been an important selective agent contributing to the development of the human species as an intelligent predator.

Interactions between Abert's Squirrel and Ponderosa Pine: The Relationship between Selective Herbivory and Host Plant Fitness

Abert's squirrels are highly specialized and selective herbivores and are ecologically dependent on their host species, ponderosa pine. Ponderosa pine trees defoliated as a result of inner bark feeding by Abert's squirrels (target trees) suffered significant reductions in several fitness components including incremental growth, male strobilus production, female cone production, and seed quality. Reproductive output was also depressed in trees defoliated experimentally to mimic squirrel herbivory. In previous work, I have shown that target tree selection is mediated by a suite of host characteristics, some of which are under genetic control. Abert's squirrels may be important agents of natural selection in host ponderosa pine populations because they preferentially attack trees with specific genetically determined traits and because target trees suffer significant reductions in several fitness components.

Hidden preferences and the evolution of signals

Mechanisms concerned with the recognition of biological signals act as important agents of selection on the appearance or ‘form’ of signals. Recognition of a given signal form can be achieved by many equally efficient alternative mechanisms. These alternative mechanisms will be selectively neutral and subject to change by genetic drift, thus preventing the fixation of a signal form that is optimal in releasing the receiver’s behaviour. Because signal form is a multidimensional trait with an almost infinite potential to vary, it is expected that some novel forms of signals always exist that elicit responses more readily than any of those signals that the receiver has experienced during its evolutionary history. The existence of such ‘hidden preferences’ is illustrated in simple models of recognition mechanisms based on artificial neural networks. The fundamental evolutionary instability of recognition mechanisms perhaps explains why biological signals are so variable in form, and why, in experiments, animals sometimes show greater responses to novel forms of signals than they do to familiar forms.

Testing hypotheses of adaptive variation in cricket ovipositor lengths.

We experimentally tested a series of hypotheses proposed by Masaki (1979, 1986) for the evolution of ovipositor length in crickets. Female crickets use the ovipositor to bury eggs in the soil, where it was hypothesized to protect their eggs from desiccation, cold and other disturbance. However, we found no effect of depth on the overwinter survival of eggs of three species of Nemobiinae. The probability of hatchlings reaching the soil surface was negatively correlated with depth documenting a significant cost to females laying eggs deep in the soil. Hatchling survival may be an important agent of selection on ovipositor length in habitats of different soil moistures. Hatchling survival in the soil was also correlated with body size, which may impose a constraint on egg-size fecundity trade-offs. Females of a bivoltine population of Allonemobius socius lay eggs at shallower depths when reared under summer compared to fall conditions and, therefore, may be able to respond to selection through behavioral plasticity when morphological adaptation is constrained by allometry.

Selection of exaggerated male traits by female aesthetic senses.

Darwin suggested that many apparently deleterious secondary sexual characters in males, such as bright colours, elaborate ornaments and conspicuous displays, evolved as a result of female choice. Darwin never tried to explain the crucial agent of selection, that females have preferences for exaggerated male traits. Rather, he took it for granted that females of many species possess a 'sense of the beautiful', akin to the aesthetic sense in humans. The question of why such preferences evolve remains a controversial issue. Here we report that mechanisms concerned with signal recognition possess inevitable biases in response that act as important agents of selection on signal form. The existence of such biases may be sufficient to explain the evolution of exaggerated male secondary sexual traits, and elaborate signals in general.

The effects of fire on scarlet gilia: an alternative selection pressure to herbivory?

The primary goals of this paper were to experimentally assess the relative importance of fire, a potentially important selective agent involved in shaping scarlet gilia's compensatory response and, in general, determine scarlet gilia's response to fire. Burn treatment results demonstrated that fire was not an important selective agent involved in shaping scarlet gilia's compensatory response. The most common response to fire was the production of one or more new clonally derived rosettes. This was an unexpected result; this typically monocarpic herb rarely produces clonal offspring. Although rosette production lessened the detrimental effects of fire by giving plants that cloned a second chance to flower, these newly formed rosettes delayed flowering for at least one year and had significantly higher overwinter mortality rates than rosettes from unburned control plots. In addition, significantly fewer individuals from the burn treatments flowered and there was significantly higher immediate mortality. There was, however, no detrimental effect on the reproductive success (seed production) of individuals that flowered following the burn. Overall, cumulative estimates of plant performance suggest that at the population level fire results in a 4.5-fold decrease in relative plant fitness. However, fire-induced seed germination could negate the detrimental effects of fire on the population dynamics of scarlet gilia. In the year of the burn there was a 116-fold increase in the number of germinating seeds and by the second year this translated into an approximate 6-fold difference in the number of surviving rosettes. Two alternative candidates, frost damage and ungulate trampling, can cause the removal of apical dominance and a response similar to that generated by ungulate and insect herbivores. However, they are probably minor factors favoring selection toward growth compensation; experimental and observational results deomonstrate that apical dominance was removed in only 3% of plants exposed to freezing temperatures and ungulate trampling caused breakage and release of apical dominance in only 0.2% of plants.