Kari Lehtilä

Costs and benefits of genetic heterogeneity within organisms

An increasing number of studies have recently detected within‐organism genetic heterogeneity suggesting that genetically homogeneous organisms may be rare. In this review, we examine the potential costs and benefits of such intraorganismal genetic heterogeneity (IGH) on the fitness of the individual. The costs of IGH include cancerous growth, parasitism, competitive interactions and developmental instability, all of which threaten the integrity of the individual while the potential benefits are increased genetic variability, size‐specific processes, and synergistic interactions between genetic variants. The particular cost or benefit of IGH in a specific case depends on the organism type and the origin of the IGH. While mosaicism easily arise by genetic changes in an individual, and will be the more common type of IGH, chimerism originates by the fusion of genetically distinct entities, and is expected to be substantially rare in most organisms. Potential conflicts and synergistic effects between different genetic lineages within an individual provide an interesting example for theoretical and empirical studies of multilevel selection.

The Use and Usefulness of Artificial Herbivory in Plant-Herbivore Studies

Artificial damage is a popular method in plant-herbivore studies, because the use of real herbivores is often laborious and because it may be virtually impossible to use herbivores in many experimental setups. We made a literature search of studies that tested whether natural and artificial damage have similar effects on plants. Of 46 studies found, 33 (72%) reported a significant difference between responses to artificial and natural herbivore damage in at least one of the statistical tests included. The studies contained 280 statistical tests, of which 99 (35%) showed a significant difference between artificial and natural damage. Phytochemical responses to artificial and natural damage were different in 41% of the statistical tests and 75% of the studies found at least one significant difference. Plant resistance, measured as secondary damage, herbivore performance, fungal growth in damaged tissue or plant attractivity to parasitoids of herbivores, differed in 60% of the statistical tests and 85% of the studies had significant differences. Growth, reproduction and physiological responses to artificial and natural damage differed in 20–30% of statistical tests and 50–83% of studies had significant differences. Thus, studies on plant tolerance (growth and reproduction after damage) more often showed similar effects for artificial and natural damage than studies on plant resistance to herbivory, but even in tolerance studies artificial and natural damage often have different effects. Some studies indicated that application of herbivore saliva and careful imitation of timing and spatial pattern of damage helped in reaching the same effect with simulations and natural damage.

Positive Effects of Pollination on Subsequent Size, Reproduction, and Survival of Primula Veris

We conducted three experiments in which we applied additional hand pol- lination, flower removal, and leaf removal treatments in various combinations to Primula veris, a perennial spring-flowering rosette species. The purpose of the study was to determine whether the seed set of Primula veris was limited by pollen availability or by other resources, and whether there were measurable costs of reproduction. Hand pollination in the beginning of experiments significantly increased current seed set in only one of the three experiments. It also increased the next-year fruiting probability in that first experiment. In the second experiment, hand pollination did not significantly affect current seed set, but we nevertheless observed enhanced leaf growth in the treatment year and the two following years, and increased flowering frequency, fruiting frequency, and survival in the two following years. In the third experiment, after hand pollination we observed a higher net photosynthetic capacity of the leaves and, again, increased leaf growth in the treatment year and a higher flowering probability in the following year. The positive effect of hand pollination was even clearer when the leaves of the plants were removed at the beginning of the experiment. However, the treatment in which all the flowers were removed had effects on subsequent performance similar to those of the hand-pollination treatment, suggesting trade-offs. Thus, we did not observe any costs associated with reproduction after supplemental hand pollination; on the contrary, hand pollination resulted in increased survival, size, and reproduction of the plants in the subsequent years.

The cost of reproduction in Primula veris: differences between two adjacent populations

The effect of flower and leaf removal on Primula veris was studied in two populations close to each other. Removal of both flowers and leaves resulted in decreased growth, flowering and reproduction in the next two years in both populations; there was no change in survival. In one population, removal of all flowers increased the flower number, the flower stalk length and the leaf area, and doubled the seed set in the year following the treatment. In the other population flower removal slightly decreased the seed set in the next year, while plant size did not differ from the control group. There were no significant differences in seed germinability between any of the experimental groups

Modelling compensatory regrowth with bud dormancy and gradual activation of buds

Many plants show compensatory regrowth after herbivory and dormant buds often have an important role in compensatory responses. Theoretical models have shown that herbivore damage may select for a bud bank, i.e., a pool of dormant buds that are protected from herbivory and that are activated after herbivore damage. Earlier models assumed that undamaged plants cannot activate their dormant buds without damage, although they apparently have sufficient resources for successful seed production through the additional shoots dormant buds could produce. However, many plants are able to gradually activate buds over an extended period of time without any cue from damage. The aim of this study was to analyze how herbivory imposes selection for gradual mobilization of the bud bank. I assume that selection pressures that affect the fraction of buds active at each time point include damage by herbivores, time left to the end of season, and the opportunity costs of dormant buds. I modelled bud dynamics with gradual activation when there is a single damage event and (i) when the seed set of a shoot is not dependent on the time it is active, or (ii) when the seed set of a shoot diminishes with later activation. In addition, I analyzed how (iii) risk of repeated herbivory affects selection for gradual activation. Under these models, gradual activation is optimal over a wide range of herbivory pressures. Selection appears to favour activation of all buds at the beginning of the season only when herbivore pressure is weak and when early shoots have a higher seed set than late shoots. Alternatively, strong herbivore pressure and late damage may select for a large bud bank throughout the growing season, without gradual activation; the bud bank is only mobilized after damage. In this case, damaged plants can overcompensate, i.e. they have a higher seed set than undamaged plants with the same bud activation pattern. Selection for overcompensation demands a stronger herbivore pressure in this current model than in earlier bud bank models. The model never predicts selection for overcompensation when there is a risk of repeated herbivory.

PRECISION OF HERBIVORE TOLERANCE EXPERIMENTS WITH IMPOSED AND NATURAL DAMAGE

Abstract Tiffin and Inouye (2000) discussed the use of natural and imposed (controlled) damage in experiments of herbivore tolerance. They constructed a statistical model of the effect of herbivory on plant fitness, including damage level and an environmental factor as the independent factors, in which tolerance is defined as a slope of the regression line when damage level is regressed with plant fitness. They claim that while experiments with imposed damage are more accurate (i.e., they give a more correct estimate of tolerance), experiments with natural damage are more precise under a wide range of parameter values (i.e., tolerance estimates explain a larger part of variation in fitness). I show, however, that experiments with imposed damage are less precise only when an experimenter uses an experimental design that has weaker statistical power than in experiments with natural herbivory. The experimenter can nevertheless control the damage levels to optimize the experimental designs. For instance, when half of the experimental plants are left undamaged and the other half treated with maximal relevant damage level, experiments with imposed damage are almost always much more precise than experiments with natural damage.

The association among herbivory tolerance, ploidy level, and herbivory pressure in cardamine pratensis

We tested whether differences in ploidy level and previous exposure to herbivory can affect plant tolerance to herbivory. We conducted a common garden experiment with 12 populations of two ploidy levels of the perennial herb Cardaminepratensis (five populations of tetraploid ssp. pratensis and seven populations of octoploid ssp. paludosa). Earlier studies have shown that attack rates by the main herbivore, the orange tip butterfly Anthocharis cardamines, are lower in populations of octoploids than in populations of tetraploids, and vary among populations. In the common garden experiment, a combination of natural and artificial damage significantly reduced seed and flower production. We measured tolerance based on four plant-performance metrics: survival, growth, seed production and clonal reproduction. For three of these measurements, tolerance of damage did not differ between ploidy levels. For clonal reproduction, the octoploids had a higher tolerance than the tetraploids, although they experience lower herbivore attack rates in natural populations. Populations from sites with high levels of herbivory had higher tolerance, measured by seed production, than populations with low levels of herbivory. We did not detect any significant costs of tolerance. We conclude that high intensity of herbivory has selected for high tolerance measured by seed production in C. pratensis.

Meristem Allocation as a Means of Assessing Reproductive Allocation

Publisher Summary The principle of resource allocation states that resources are not sufficient to fully supply the demands of all plant functions. If resources are limited, allocation to reproduction must decrease the allocation to some other plant functions. Allocation of resources to reproduction (reproductive allocation) has implications for several study fields in biology. Early studies discussed allocation patterns in light of the evolution of life-history traits and interaction between life-history traits and population dynamics. Initial studies considered animals, but the idea was soon applied to plant ecology to explain how allocation affects plant life-history strategies and plant community dynamics. To test the principle of allocation, biologists have tried to measure the resource use of different plant functions. This task has turned out to be difficult. It is not clear which currency should be used to measure reproductive allocation. Meristems have been proposed as a currency to measure reproductive allocation. Meristems come as distinct reproductive or vegetative entities. This chapter aims to discuss whether meristem allocation can be used as a supplement or a substitute when studying reproductive allocation. It first describes the structural, developmental, and physiological background of the meristem system. It then uses a modeling approach to show theoretically how meristem allocation may affect fitness. It discusses model assumptions and reviews empirical studies that have tested allocation models and their assumptions.

Challenging the genetically homogeneous individual

A growing number of empirical and theoretical studies suggest that naturally occurring intraorganismal genetic heterogeneity (IGH) may be more common than previously believed (for review see Pineda-Krch & Lehtilä, 2004). That the occurrence of genetically heterogeneous organisms in nature is of deep biological significance was recognized by Williams (1966) in his seminal Adaptation and Natural Selection. Nevertheless, the matter has received little attention in ecological and evolutionary research, and issues such as the frequency, the mechanisms and the potential significance of IGH remain largely unexplored. There seem to be two reasons for this omission and the general lines of argument can be summarized as follows: (i) it is important to maintain genetic homogeneity of an organism in order to avoid intraorganismal conflicts, hence IGH will be rare because there is strong selection against it and (ii) genetically heterogeneous organisms do not qualify as true gene vehicles and do not adhere to the predominantly accepted definition of individuality. Although the potential for IGH is acknowledged its significance is dismissed either because of its assumed rarity or the perceived difficulties in accommodating the idea within contemporary biological concepts. This line of reasoning is at least partially justified. That IGHs will often entail costs at the organism level is probably true, but currently we know little about the true distribution of effect, and as several of the commentaries show there is more to the story than what the statement suggests (Rinkevich, 2004; Santelices, 2004; Strassmann & Queller, 2004). It is also true that it would be difficult to accommodate IGH into the contemporary concept of individuality as, ever since Weismann, individuality has implied genetic homogeneity (Santelices, 1999). While several of the commentaries discuss the need for a revised individuality concept to accommodate situations such as IGH, Hutchings & Booth (2004) also appropriately point out that it is unlikely that any given definition will ever be applicable to all types of organisms. Indeed, the complexity of defining the individuality concept has been addressed on several occasions (Tuomi & Vuorisalo, 1989; Santelices, 1999). Nevertheless, a widely accepted conceptual revision has not yet occurred. Incorporating IGH into a revised concept of individuality will pose interesting challenges to theoretical and empirical research alike.

Trophic transfer of naturally produced brominated aromatic compounds in a Baltic Sea food chain.

Brominated aromatic compounds (BACs) are widely distributed in the marine environment. Some of these compounds are highly toxic, such as certain hydroxylated polybrominated diphenyl ethers (OH-PBDEs). In addition to anthropogenic emissions through use of BACs as e.g. flame retardants, BACs are natural products formed by marine organisms such as algae, sponges, and cyanobacteria. Little is known of the transfer of BACs from natural producers and further up in the trophic food chain. In this study it was observed that total sum of methoxylated polybrominated diphenyl ethers (MeO-PBDEs) and OH-PBDEs increased in concentration from the filamentous red alga Ceramium tenuicorne, via Gammarus sp. and three-spined stickleback (Gasterosteus aculeatus) to perch (Perca fluviatilis). The MeO-PBDEs, which were expected to bioaccumulate, increased in concentration accordingly up to perch, where the levels suddenly dropped dramatically. The opposite pattern was observed for OH-PBDEs, where the concentration exhibited a general trend of decline up the food web, but increased in perch, indicating metabolic demethylation of MeO-PBDEs. Debromination was also indicated to occur when progressing through the food chain resulting in high levels of tetra-brominated MeO-PBDE and OH-PBDE congeners in fish, while some penta- and hexa-brominated congeners were observed to be the dominant products in the alga. As it has been shown that OH-PBDEs are potent disruptors of oxidative phosphorylation and that mixtures of different congener may act synergistically in terms of this toxic mode of action, the high levels of OH-PBDEs detected in perch in this study warrants further investigation into potential effects of these compounds on Baltic wildlife, and monitoring of their levels.