Erik I. Svensson

On the adaptive significance of stress-induced immunosuppression

We approach the field of stress immunology from an ecological point of view and ask: why should a heavy physical workload, for example as a result of a high reproductive effort, compromise immune function? We argue that immunosuppression by neuroendocrine mechanisms, such as stress hormones, during heavy physical workload is adaptive, and consider two different ultimate explanations of such immunosuppression. First, several authors have suggested that the immune system is suppressed to reallocate resources to other metabolic demands. In our view, this hypothesis assumes that considerable amounts of energy or nutrients can be saved by suppressing the immune system; however, this assumption requires further investigation. Second, we suggest an alternative explanation based on the idea that the immune system is tightly regulated by neuroendocrine mechanisms to avoid hyperactivation and ensuing autoimmune responses. We hypothesize that the risk of autoimmune responses increases during heavy physical workload and that the immune system is suppressed to counteract this.

Density cycles and an offspring quantity and quality game driven by natural selection.

A long-standing hypothesis posits that natural selection can favour two female strategies when density cycles. At low density, females producing many smaller progeny are favoured when the intrinsic rate of increase, r, governs population growth. At peak density, females producing fewer, high-quality, progeny are favoured when the carrying capacity, K, is exceeded and the population crashes. Here we report on the first example of a genetic r versus K selection game that promotes stable population cycles in lizards. Decade-long fitness studies and game theory demonstrated that two throat-colour morphs were refined by selection in which the strength of natural selection varied with density. Orange-throated females, r strategists, produced many eggs and were favoured at low density. Conversely, yellow-throated females, K strategists, produced large eggs and were favoured at high density. Progeny size should also be under negative frequency-dependent selection in that large progeny will have a survival advantage when rare, but the advantage disappears when they become common. We confirmed this prediction by seeding field plots with rare and common giant hatchlings. Thus, intrinsic causes of frequency- and density-dependent selection promotes an evolutionary game with two-generation oscillations.

Correlational selection and the evolution of genomic architecture

We review and discuss the importance of correlational selection (selection for optimal character combinations) in natural populations. If two or more traits subject to multivariate selection are heritable, correlational selection builds favourable genetic correlations through the formation of linkage disequilibrium at underlying loci governing the traits. However, linkage disequilibria built up by correlational selection are expected to decay rapidly (ie, within a few generations), unless correlational selection is strong and chronic. We argue that frequency-dependent biotic interactions that have ‘Red Queen dynamics’ (eg, host-parasite interactions, predator-prey relationships or intraspecific arms races) often fuel chronic correlational selection, which is strong enough to maintain adaptive genetic correlations of the kind we describe. We illustrate these processes and phenomena using empirical examples from various plant and animal systems, including our own recent work on the evolutionary dynamics of a heritable throat colour polymorphism in the side-blotched lizard Uta stansburiana. In particular, male and female colour morphs of side-blotched lizards cycle on five- and two-generation (year) timescales under the force of strong frequency-dependent selection. Each morph refines the other morph in a Red Queen dynamic. Strong correlational selection gradients among life history, immunological and morphological traits shape the genetic correlations of the side-blotched lizard polymorphism. We discuss the broader evolutionary consequences of the buildup of co-adapted trait complexes within species, such as the implications for speciation processes.

The cost of reproduction: a new link between current reproductive effort and future reproductive success

Although a negative trade-off between current reproductive effort and future reproductive output has for long been hypothesized and in some cases empirically shown, no mechanism with the potential to mediate such a reproductive cost from one season to another has been demonstrated. Here we suggest such a mechanism : the time and / or energy constraints during moult. We manipulated current reproduction of blue tits (Parus caeruls) by delaying their breeding attempts. This resulted in reproductive costs both in terms of decreased survival and lower subsequent reproductive success in the form of delayed start of breeding (females) or a smaller clutch (males). We found that delayed birds expended about 15% more energy in thermoregulation during the subsequent winter than did control birds. Thus, more time and / or energy directed to reproduction, may constrain moult which results in the production of feathers with low insulating capacity. These feathers are retained during the following winter and breeding season. Thus, this mechanism has the potential to link reproductive activities in one season to future reproductive success.

The impact of learning on sexual selection and speciation

Learning is widespread in nature, occurring in most animal taxa and in several different ecological contexts and, thus, might play a key role in evolutionary processes. Here, we review the accumulating empirical evidence for the involvement of learning in mate choice and the consequences for sexual selection and reproductive isolation. We distinguish two broad categories: learned mate preferences and learned traits under mate selection (such as bird song). We point out that the context of learning, namely how and when learning takes place, often makes a crucial difference to the predicted evolutionary outcome. Factors causing biases in learning and when one should expect the evolution of learning itself are also explored.

Female Polymorphism, Frequency Dependence, and Rapid Evolutionary Dynamics in Natural Populations

Rapid evolutionary change over a few generations has been documented in natural populations. Such changes are observed as organisms invade new environments, and they are often triggered by changed interspecific interactions, such as differences in predation regimes. However, in spite of increased recognition of antagonistic male‐female mating interactions, there is very limited evidence that such intraspecific interactions could cause rapid evolutionary dynamics in nature. This is because ecological and longitudinal data from natural populations have been lacking. Here we show that in a color‐polymorphic damselfly species, male‐female mating interactions lead to rapid evolutionary change in morph frequencies between generations. Field data and computer simulations indicate that these changes are driven by sexual conflict, in which morph fecundities are negatively affected by frequency‐ and density‐dependent male mating harassment. These frequency‐dependent processes prevent population divergence by maintaining a female polymorphism in most populations. Although these results contrast with the traditional view of how sexual conflict enhances the rate of population divergence, they are consistent with a recent theoretical model of how females may form discrete genetic clusters in response to male mating harassment.

Food Supply, Territory Quality, and Reproductive Timing in the Blue Tit (Parus Caeruleus)

We performed supplemental feeding experiments during three breeding seasons of the Blue Tit (Parus caeruleus L.) in order to establish the importance of food in reproductive timing. In particular, we addressed the question of why the response to supplemental food is restricted to 3—6 d in many bird species. Supplemental food advanced the start of egg—laying in all three breeding seasons. The mean difference between fed and control pairs was 4 d in two years and 6 d in another. The amount and quality of the supplemental food used in the experiment were not limiting, since pairs receiving a further increase in amount and quality of food did not start laying earlier than pairs with a standard feeding regime. The amount of food that was consumed increased during the period from 15 d before egg formation until the beginning of egg formation and then remained at a high utilization rate until clutch completion. Although fed pairs, on average, started egg—laying earlier than control pairs, the earliest control females started to lay eggs as early as the first females. Fed pairs were also relatively late in a year when control pairs were late. In 1992, fed pairs did not produce larger clutches or more fledglings, but had nestlings with lower mass at 13 d post—hatching than those of control pairs. Analysis at the territory level revealed that supplemental food affected laying date to a greater extent in low—quality territories, in which laying could be advanced by up to 9—10 d, compared to high—quality territories in which laying was not advanced at all. We conclude that laying date in most Blue Tit females is limited by low food supply early in spring, but some females, occupying high—quality territories, will not advance laying in response to food. Thus, above a certain critical limit, laying date is unrelated to food supply, and birds use other cues in their decision to commence breeding. Such cues are probably also responsible for the between—year variation in laying dates of food—supplemented pairs, since these were provided with the same amount of food during the different years.

Density-dependent competition and selection on immune function in genetic lizard morphs

Density-dependent territorial interactions have been suggested to cause immunosuppression and thereby decrease fitness, but empirical support from natural populations is lacking. Data from a natural lizard population (Uta stansburiana) showed that breeding females surrounded by many territorial neighbors had suppressed immune function. Furthermore, variation in immunological condition had different effects on the fitness of the two heritable female throat-color morphs in this population. These interactive fitness effects caused correlational selection between female throat color and immune responsiveness. Population genetic theory predicts that this should have lead to the buildup and preservation of a genetic correlation between female morphotype and immunological condition. Accordingly, the throat color of a female was genetically correlated (rA = −1.36; SE = 0.55) with her daughters immune responsiveness.

Effects of natural and sexual selection on adaptive population divergence and premating isolation in a damselfly.

Abstract The relative strength of different types of directional selection has seldom been compared directly in natural populations. A recent meta-analysis of phenotypic selection studies in natural populations suggested that directional sexual selection may be stronger in magnitude than directional natural selection, although this pattern may have partly been confounded by the different time scales over which selection was estimated. Knowledge about the strength of different types of selection is of general interest for understanding how selective forces affect adaptive population divergence and how they may influence speciation. We studied divergent selection on morphology in parapatric, natural damselfly (Calopteryx splendens) populations. Sexual selection was stronger than natural selection measured on the same traits, irrespective of the time scale over which sexual selection was measured. Visualization of the fitness surfaces indicated that population divergence in overall morphology is more strongly influenced by divergent sexual selection rather than natural selection. Courtship success of experimental immigrant males was lower than that of resident males, indicating incipient sexual isolation between these populations. We conclude that current and strong sexual selection promotes adaptive population divergence in this species and that premating sexual isolation may have arisen as a correlated response to divergent sexual selection. Our results highlight the importance of sexual selection, rather than natural selection in the adaptive radiation of odonates, and supports previous suggestions that divergent sexual selection promotes speciation in this group.

Gender Differences in Species Recognition and the Evolution of Asymmetric Sexual Isolation

Closely related sympatric species are expected to evolve strong species discrimination because of the reinforcement of mate preferences. Fitness costs of heterospecific matings are thought to be higher in females than in males, and females are therefore expected to show stronger species discrimination than males. Here, we investigated gender and species differences in sexual isolation in a sympatric species pair of Calopteryx damselflies. The genus Calopteryx is one of the classic examples of reproductive character displacement in evolutionary biology, with exaggerated interspecific differences in the amount of dark wing coloration when species become sympatric. Experimental manipulation of the extent of dark wing coloration revealed that sexual isolation results from both female and male mate discrimination and that wing melanization functions as a species recognition character. Female choice of conspecific males is entirely based on wing coloration, whereas males in one species also use other species recognition cues in addition to wing color. Stronger species discrimination ability in males is presumably an evolutionary response to an elevated male predation risk caused by conspicuous wing coloration. Gender differences in species discrimination and fitness costs of male courtship can thus shed new light on the evolution of asymmetric sexual isolation and the reinforcement of mate preferences.